From: Subject: Side Population Is Enriched in Tumorigenic, Stem-Like Cancer Cells, whereas ABCG2+ and ABCG2- Cancer Cells Are Similarly Tumorigenic -- Patrawala et al. 65 (14): 6207 -- Cancer Research Date: Sat, 23 Feb 2008 11:38:52 +0100 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_004B_01C87610.AA478FB0" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.3198 This is a multi-part message in MIME format. ------=_NextPart_000_004B_01C87610.AA478FB0 Content-Type: text/html; charset="Windows-1252" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/65/14/6207 Side Population Is Enriched in Tumorigenic, Stem-Like = Cancer Cells, whereas ABCG2+ and ABCG2- Cancer Cells Are Similarly = Tumorigenic -- Patrawala et al. 65 (14): 6207 -- Cancer Research 3D"Cancer 3D"
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[Cancer Research 65, 6207-6219, July 15, 2005]
=A9 = 2005 American = Association=20 for Cancer Research

Cell and Tumor Biology

Side Population Is Enriched in Tumorigenic, Stem-Like Cancer Cells, = whereas=20 ABCG2+ and ABCG2=96 Cancer Cells Are Similarly = Tumorigenic=20

Lubna Patrawala1, = Tammy=20 Calhoun1, Robin = Schneider-Broussard1,=20 Jianjun Zhou1, Kent = Claypool1=20 and Dean G. Tang1,2

1 Department of Carcinogenesis, Science=20 Park-Research Division, The University of Texas M.D. Anderson Cancer = Center,=20 Smithville, Texas and 2 Program in Environmental and = Molecular=20 Carcinogenesis, Graduate School of Biomedical Sciences, Houston, Texas =

Requests for reprints: Dean Tang, Department = of=20 Carcinogenesis, Science Park-Research Division, The University of Texas = M.D.=20 Anderson Cancer Center, 1808 Park Road 1C, Smithville, TX 78957. Phone:=20 512-237-9575; Fax: 512-237-2475; E-mail: dtang{at}mdanderson.org .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
R= ecently,=20 several human cancers including leukemia and breast and brain = tumors=20 were found to contain stem-like cancer cells called cancer = stem cells=20 (CSC). Most of these CSCs were identified using markers that = identify=20 putative normal stem cells. In some cases, stem-like cancer = cells=20 were identified using the flow cytometry-based side = population=20 technique. In this study, we first show that 3D~=2030% of = cultured=20 human cancer cells and xenograft tumors examined (3D~=2030 in = total)=20 possess a detectable side population. Purified side = population cells=20 from two cell lines (U373 glioma and MCF7 breast cancer) and = a=20 xenograft prostate tumor (LAPC-9) are more tumorigenic than = the=20 corresponding non=96side population cells. These side = population cells=20 also possess some intrinsic stem cell properties as they = generate=20 non=96side population cells in vivo, can be further=20 transplanted, and preferentially express some "stemness" = genes,=20 including Notch-1 and =DF-catenin. Because the = side=20 population phenotype is mainly mediated by ABCG2, an = ATP-binding=20 cassette half-transporter associated with multidrug = resistance, we=20 subsequently studied ABCG2+ and ABCG2=96 = cancer=20 cells with respect to their tumorigenicity in vivo. Although = side population cells show increased ABCG2 mRNA expression = relative=20 to the non=96side population cells and all cancer cells = and=20 xenograft tumors examined express ABCG2 in a small fraction = (0.5-3%)=20 of the cells, highly purified ABCG2+ cancer cells,=20 surprisingly, have very similar tumorigenicity to the=20 ABCG2=96 cancer cells. Mechanistic studies = indicate that=20 ABCG2 expression is associated with proliferation and=20 ABCG2+ cancer cells can generate = ABCG2=96 cells.=20 However, ABCG2=96 cancer cells can also generate=20 ABCG2+ cells. Furthermore, the ABCG2=96 = cancer=20 cells form more and larger clones in the long-term clonal = analyses=20 and the ABCG2=96 population preferentially expresses = several=20 "stemness" genes. Taken together, our results suggest that = (a) the=20 side population is enriched with tumorigenic stem-like cancer = cells,=20 (b) ABCG2 expression identifies mainly fast-cycling tumor=20 progenitors, and (c) the ABCG2=96 population contains=20 primitive stem-like cancer cells.


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
References
 
S= tem=20 cells, which have now been found in multiple adult tissues = and=20 organs, have several fundamental properties. First, they are=20 generally very rare. For example, the long-term hematopoietic = stem=20 cells (LT-HSC) in mouse bone marrow constitute 3D~=200.02% = and=20 the short-term HCSs (ST-HSC) 3D~=200.1% = of the total=20 cells (1).=20 Second, stem cells in their normal microenvironment (i.e., = niche)=20 rarely divide, although they possess tremendous proliferative = potential (2).=20 Third, stem cells can self-renew; that is, they can regenerate=20 themselves when they divide to give rise to progenitor cells=20 (2).=20 Fourth, stem cells possess multipotential, oligopotential, or = unipotential differentiation ability (3).=20 Many adult stem cells also seem to have the ability to=20 trans-differentiate into other cell types, although = this=20 phenomenon is still being hotly debated (3,=20 4).=20 Finally, stem cells may express unique markers or properties = that can=20 allow their enrichment and identification.

Indeed, many stem cells are identified by their expression of=20 unique markers. For example, mouse LT-HSCs, ST-HSCs, and = multipotent=20 progenitors can be identified and separated by their marker=20 phenotypes,=20 c-kithiSca-1hiThy1.1loLin=96/loFlk=96,=20 c-kithiSca-1hiThy1.1loLin=96/loFlk+,=20 and=20 c-kithiSca-1hiThy1.1=96Lin=96/loFlk+,=20 respectively (1).=20 Unfortunately, most organ-restricted stem cells or progenitors = lack=20 unique and specific markers. One way to identify them relies = on the=20 slow-cycling properties of stem cells. When pulsed by=20 bromodeoxyuridine (BrdU) for a period of time followed by = "chasing"=20 for longer time intervals, slow-dividing stem cells will be=20 identified as label-retaining cells (LRC; refs. 2,=20 5).=20 The LRCs purified from the stem cell niche (i.e., the bulge = in the=20 hair follicle) in transgenic animals possess many of the=20 expected stem cell properties (2,=20 5).=20 Another way to identify putative adult stem cells was = pioneered by=20 Goodell et al. (6),=20 who observed that when bone marrow=96derived cells are = incubated=20 with Hoechst dye 33342 and then analyzed by dual-wavelength = flow=20 cytometry, a small population of cells does not accumulate an = appreciable amount of dye and is thus identified as a=20 Hoechstlo side population. Remarkably, the side = population=20 is highly enriched in HSCs (6).=20 Since its initial application in bone marrow HSCs, the side=20 population technique has been adapted to identify putative = stem cells=20 and progenitors in multiple tissues/organs including = umbilical cord=20 blood (7),=20 skeletal muscle (8=9610),=20 mammary glands (11,=20 12),=20 lung (13=9615),=20 liver (16),=20 epidermis (17,=20 18),=20 forebrain (19),=20 testis (20,=20 21),=20 heart (22),=20 kidney (23),=20 limbal epithelium (24),=20 and prostate (25).=20

The side population=96enriched stem cells are rare (3D~=200.01-5%;=20 refs. 18,=20 23,=20 26)=20 and heterogeneous, varying with tissue types, stages of = development,=20 and methods of preparation (10,=20 27,=20 28).=20 For example, the bone marrow side population cells contain = not=20 only HSCs but also mesenchymal stem cells (29)=20 and do not capture all HSCs (30)=20 but only a subset of long-term repopulating HSCs (31).=20 The skeletal muscle side population cells are composed of = mostly bone=20 marrow=96derived cells (8,=20 9)=20 with only a minor population of resident muscle = stem/progenitor cells=20 (i.e., satellite cells). The lung side population cells are = also=20 heterogeneous comprising both CD45+ (i.e., bone = marrow=20 derived) and CD45=96 cells (13=9615).=20 Similarly, the testis side population cells may be enriched = in=20 spermatogonial, germinal, as well as mesenchymal (i.e., = Leydig) stem=20 cells (20,=20 21).=20 Although the side population cells in most cases seem = enriched in=20 primitive stem cells, there are also reports that suggest = that the=20 side population cells do not identify stem cells (17,=20 18,=20 32).=20

The side population phenotype is mediated by the ABC family = of=20 transporter proteins. One of the major mediators seems to be = ABCG2 or=20 BCRP (33),=20 which was initially identified in drug-selected MCF7 breast = cancer=20 cells and later found to efflux multiple chemotherapeutic = drugs and=20 xenobiotics (34).=20 The strongest evidence linking ABCG2 and the side population=20 phenotype comes from the nearly complete loss of the bone = marrow side=20 population phenotype in abcg=96/=96 mice = (35).=20 Other supporting evidence is that side population cells=20 preferentially express ABCG2 (13,=20 16,=20 18,=20 20,=20 22,=20 24,=20 36,=20 37)=20 and that ABCG2 expression is detected in known = stem/progenitor cells=20 such as HSCs (33),=20 nestin-positive islet-derived progenitors (36),=20 hepatic oval cells (16),=20 limbal basal cells (24),=20 and neural stem cell (38).=20 On the other hand, it should be noted that only a fraction of = the=20 side population cells expresses ABCG2 (e.g., ref. 24)=20 and that both side population and known stem/progenitor cells = also=20 express other ABC transporters such as MDR-1 (i.e., ABCB1 or=20 P-glycoprotein), MRP-1 (ABCC1), and ABCA2 (36,=20 37,=20 39),=20 suggesting that these latter molecules may also be involved = in=20 mediating the side population phenotype. In support, enforced = expression of MDR-1 in murine bone marrow cells leads to the=20 expansion of the side population (40).=20

Recently, several human cancers including leukemia (1,=20 41)=20 and breast (42)=20 and brain (37,=20 43=9646)=20 tumors were found to contain stem-like cells (SLC) called = cancer stem=20 cell (CSCs; ref. 47).=20 Most of these tumorigenic SLCs were identified using markers = that=20 identify putative normal stem cells. Interestingly, SLCs have = also=20 been identified in immortalized cell lines (39),=20 long-term cultured cancer cells (37,=20 48),=20 or patient tumor samples (37)=20 using the side population technique. These observations = suggest that=20 even long-term cultured (cancer) cells may retain SLCs and = that the=20 side population approach represents a valid = marker-independent method=20 to identify such cells. In a recent study,3=20 we have also provided independent evidence for the existence = of SLCs=20 in multiple human tumor cell cultures as well as xenograft = tumors. In=20 the current study, we first seek to confirm the utility of = the side=20 population technique to identify tumorigenic SLCs in cultured = human=20 cancer cells and xenograft tumors. Then we focus on the = question=20 whether the higher tumorigenicity associated with the side = population=20 might be related to the expression of ABCG2, a major mediator = of the=20 side population phenotype in bone marrow cells. Our results=20 surprisingly show that in contrast to the tumorigenic = differences=20 between the side population and non=96side population cells, = the=20 ABCG2+ and ABCG2=96 cancer cells show = very=20 similar tumorigenicities in vivo.


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
References
 
<= B>Cells,=20 reagents, and animals. Various cancer cell lines including = those=20 of prostate (PPC-1, Du145, LNCaP, and PC3 cells), breast = (T47D,=20 MCF-7, MDA-MB231, MDA-MB435, and MDA-MB468), colon (COLO 320, = DLD-1,=20 RKO, and HCT116), bladder (RT4, UC14, UC1, and UC3), glioma = (D54,=20 U87, U251, and U373), melanoma (WM266-4 and WM562-4), cervix = (HeLa),=20 and ovary (SKOV-3) were obtained from American Type Culture=20 Collection (Manassas, MA) or collaborators and cultured in = the=20 recommended medium containing 5% to 10% of heat-inactivated = fetal=20 bovine serum (FBS). Xenograft human prostate tumors LAPC-4 = and LAPC-9=20 were kindly provided by C. Sawyers (Department of Medicine,=20 University of California, Los Angeles, CA) (49)=20 and maintained in nonobese diabetic/severe combined=20 immunodeficiency (NOD/SCID) mice. Du145 xenograft tumors were = established in our lab using early-passage cells and = maintained in=20 NOD/SCID mice. All animals were obtained from The Jackson=20 Laboratory (Bar Harbor, ME) and maintained in standard = conditions=20 according to the Institutional guidelines. The monoclonal=20 anti-ABCG2, FITC-, and PE-conjugated anti-ABCG2 monoclonal=20 antibodies, isotype control antibody, and secondary = antibodies were=20 all obtained from Chemicon (Temecula, CA). Monoclonal = antibodies=20 against Ber-EP4 and CD31 were obtained from DakoCytomation, = Inc.=20 (Carpinteria, CA) and BD PharMingen (San Diego, CA), = respectively.=20 All chemicals were obtained from Sigma (St. Louis, MO) unless = specified otherwise.

Side population analysis. The protocol was based on = Goodell=20 et al. (6)=20 with slight modifications. Briefly, cells (1 x=20 106 cells/mL) were incubated in prewarmed DMEM/5% = FBS=20 containing freshly added Hoechst 33342 (5 =B5g/mL final=20 concentration) for 90 minutes at 37=B0C with intermittent = mixing. In=20 some experiments, cells were incubated with the Hoechst dye = in=20 the presence of verapamil (50 =B5mol/L) or reserpine (100 = =B5mol/L).=20 At the end of incubation, cells were spun down in the cold = and=20 resuspended in ice-cold PBS. 7-AAD (2 =B5g/mL final = concentration)=20 was added for 5 minutes before fluorescence-activated cell = sorting=20 (FACS) analysis, which allows for the discrimination of dead=20 versus live cells. As positive controls, we used HL60 = promyelocytic=20 leukemia cells selected by chronic exposure to doxorubicin.=20 Samples were analyzed on a Coulter Epics flow cytometer. The=20 Hoechst dye was excited with the UV laser at 351 to 364 nm = and=20 its fluorescence measured with a 515-nm side population = filter=20 (Hoechst blue) and a 608 EFLP optical filter (Hoechst red). = A=20 540 DSP filter was used to separate the emission wavelengths. =

Indirect immunofluorescence, flow cytometry analysis of ABCG2 = expression, and fluorescence-activated cell sorting of=20 ABCG2+ cells. For fluorescence microscopy (50),=20 3 to 10 x 103 cells = were=20 plated on glass coverslips. Next day, cells were fixed in 4%=20 paraformaldehyde (10 minutes at room temperature) and blocked = in 10%=20 goat whole serum. Coverslips were incubated sequentially with = monoclonal antibody anti-ABCG2, biotinylated goat anti-mouse = IgG, and=20 FITC-conjugated streptavidin with washings in between. = Generally=20 1,200 to 1,500 cells were counted for each cell type to = quantify the=20 ABCG2+ cells. For flow cytometry, cells were = gently=20 dissociated with Accutase (Innovative Cell Technologies, = Inc., San=20 Diego, CA) and washed (twice) in serum-free medium. Cells = were=20 stained live in the staining solution containing bovine serum = albumin=20 and insulin and FITC- or PE-conjugated monoclonal anti-ABCG2 = (15=20 minutes at 4=B0C). Samples were analyzed on a Coulter flow = cytometer. A=20 minimum of 500,000 viable cells was measured per sample, and = cell=20 debris and cell aggregates were electronically gated out. For = FACS, 2=20 to 4 x 107 cells = were=20 similarly stained for ABCG2 and used to sort out ABCG2+=20 and ABCG2=96 cells. For the positive population, only = the=20 top 10% most brightly stained cells were selected. For the = negative=20 population, only the bottom 5% to 10% most dimly stained = cells=20 were selected. The purity of ABCG2+ cells, as = determined=20 by both post-sorting flow analyses as well as restaining=20 followed by fluorescence microscopy analyses, was 3D≥=2098% and = the=20 purity of the ABCG2=96 cells was 3D≥=2099%.

Xenograft tumor experiments and in vivo tumorigenicity. = Xenograft prostate (Du145, LAPC-4, and LAPC-9) and glioma = (U373)=20 tumors were aseptically dissected out from animals and minced = into 3D~1 mm3 pieces in DMEM supplemented with 10% FBS. = After=20 rinsing in the same medium (twice) followed by PBS to wash = out=20 serum, tumor tissues were incubated with 1x Accumax (1,200-2,000 units/mL=20 proteolytic activity containing collagenase and DNase; = Innovative=20 Cell Technologies) at 10 mL/1 g tissue in DPBS for 20 minutes = at 37=B0C under rotating conditions. At the end, residual = tissues=20 were allowed to precipitate to the bottom of tubes and = dissociated=20 cells collected from the supernatant. When necessary, the = residual=20 tumor pieces were subjected to one or more rounds of Accumax=20 digestion and dissociated cells pooled. A single cell = suspension was=20 obtained by filtering the supernatant through a 40-=B5m cell = strainer=20 (BD Falcon, Bedford, MA). Upon viability count using = erythrosin B=20 (American Type Culture Collection), cell suspension was = gently loaded=20 onto a layer of Histopaque-1077 gradient (Sigma-Aldrich, St. = Louis,=20 MO) and centrifuged at 400 x=20 g for 30 minutes at room temperature. RBC, dead cells, and=20 debris were removed from the bottom of the tube and live = nucleated=20 cells collected at the interface. Then the cell mixture was=20 depleted of lineage-positive host cells using the MACS = Lineage=20 Cell Depletion Kit (Miltenyi Biotec, Auburn, CA). Briefly, = cells=20 were first incubated (10 minutes at 4=B0C) in the staining=20 solution [PBS (pH 7.2), 0.5% FBS, 0.5 =B5g/mL insulin] = containing=20 biotinylated antibodies against a panel of lineage antigens=20 (CD5, CD45R, CD11b, anti-Ly-6G, 7-4, and Ter-119). Cells were = then incubated with the anti-biotin Microbeads (15 minutes at = 4=B0C) and the Lin=96 cells were eluted using the MS = columns.=20 The eluted prostate cancer cells were all human epithelial = cells=20 as confirmed by their expression of Ber-EP4, a surface marker = unique to human epithelial cells, indicating that we had = obtained=20 highly purified human tumor cells using this protocol.

For tumor experiments, various numbers of cells, either unsorted = or sorted populations (i.e., side population, non=96side=20 population, ABCG2+, and ABCG2=96) were = injected in 40=20 =B5L of medium/Matrigel (1:1) s.c. into either male or female = NOD/SCID mice (4-8 weeks old). MCF7 cells were injected into = female=20 mice. Tumor development was monitored starting from the = second=20 week. The primary tumor sizes were measured with a caliper on = a=20 weekly basis and approximate tumor weights determined using = the=20 formula 0.5ab2, where b is the = smaller of=20 the two perpendicular diameters. Tumorigenicity was measured = mainly=20 by tumor incidence (i.e., the number of tumors/number of = injections)=20 and latency (i.e., time from injection to detection of = palpable=20 tumors). All animals were terminated at 6 to 9 months after = tumor=20 cell injection. Tumors harvested were fixed in formalin and = paraffin=20 sections were made for H&E staining or = immunohistochemistry for=20 CD31.

Relationship between ABCG2 expression and cell = proliferation.=20 Two sets of experiments were done. In one, cells undergoing=20 mitotic division were determined in ABCG2+ and=20 ABCG2=96 populations of cells. In the other, = purified=20 ABCG2+ and ABCG2=96 cancer cells, = cultured for=20 various time intervals, were pulsed with BrdU (2.5 =B5mol/L = x 3 hours) and processed for BrdUrd=20 staining (50).=20

In vitro and in vivo self-renewal and clonal = analyses.=20 Purified ABCG2+ and ABCG2=96 cancer = cells were=20 plated at clonal density (i.e., 100-400 cells per well; = depending on=20 cell type) in the flat-bottomed 6-well culture dishes. Cells = were=20 cultured for different time periods. The percentage of cells = that=20 initiated a clone was presented as cloning efficiency. The = clone=20 sizes (i.e., the number of cells/clone) were determined for = some=20 time points. Triplicate samples were run for each cell type = and=20 experiments repeated when feasible. For in vivo = self-renewal=20 experiments, tumor cells purified from the tumors derived = from=20 unsorted, ABCG2+, or ABCG2=96 cells = were stained=20 for ABCG2 and used to quantify the ABCG2-expressing cells by = flow=20 cytometry.

Preparation of mouse bone marrow and newborn mouse = keratinocytes.=20 To prepare bone marrow, we sacrificed C57BL/6 mice (6-8 weeks = old) by cervical dislocation and removed the skin covering = the=20 femurs. The bones were removed by cutting below the knee and=20 cutting at the hip. The muscle was then cleaned from both = femurs.=20 The bone marrow cells were flushed out of the femur using a=20 27-gauge needle in 50 mL of PBS, washed once, and used in the = side population analysis. For keratinocytes, newborn pups = were=20 cleaned and anesthetized on ice for at least 30 minutes. The=20 tail and limbs were removed and discarded. The skin was = removed=20 and floated on 2 mL trypsin (0.25%) solution with dermal side = down overnight at 4=B0C. Epidermis was removed from dermis,=20 placed in Waymouth's Medium (Life Technologies, Gaithersburg, = MD) containing 10% FBS and 1% penicillin-streptomycin and = minced.=20 The minced epidermis was gently stirred for 20 minutes in a=20 sterile glass beaker. The resulting solution was filtered = through=20 a 30-=B5m mesh and plated at 3 x=20 106 cells per 35-mm dish for 2.5 hours. The medium = was=20 changed to Keratinocyte Growth Medium - 2 (KGM-2; Cambrex = BioScience=20 Walkersville, Inc., Walkersville, MD) with 0.5 mmol/L = calcium. Cells=20 were either used freshly or cultured for a short period of = time (to=20 expand) and used in the side population analysis.

Reverse transcription-PCR analysis. Total RNA was isolated = using=20 the Absolutely RNA Nanoprep Kit (Stratagene, La Jolla, CA) = and=20 used in semiquantitative reverse transcription-PCR (RT-PCR)=20 analysis (50).=20 The PCR primers included ABCG2 (sense, 5'-CTGAGATCCTGAGCCTTTGG-3';=20 antisense, 5'-TGCCCATCACAACATCATCT-3'); Notch-1 (sense,=20 5'-ATCGGGCACCTGAACGTGGCG-3; antisense, 5'-CACGTCTGCCTGGCTCGG = CTC-3');=20 =DF-catenin (sense, 5'-ACTGGCAGCAACAGTCTTACC-3'; antisense,=20 5'-TTTGAAGGCAGTCTGTC GTAAT-3'); SMO (sense,=20 5'-ATCTCCACAGGAGAGACTGGTTCGG-3'; antisense, 5'-AAAGTGGG=20 GCCTTGGGAACATG-3'); Oct-4 (sense, 5'-GTGGAGGAAGCTGCAAACAATGAAA-3';=20 antisense, 5'-GACCGAGGAGTTACAGTGCAGTGAAG-3'); and=20 glyceraldehyde-3-phosphate dehydrogenase (sense, = 5'-ACCACAGTCCATGC=20 CATCAC-3'; antisense, 5'-TCCACCACCCTGTTGCTGTA-3'). =


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
References
 
<= B>Some=20 cultured human cancer cells and xenograft tumors have a side=20 population. Several articles have recently reported the = presence=20 of stem cell=96enriched side population in long-term cultured = mouse=20 C2C12 myogenic cells (39),=20 rat C6 glioma cells (48),=20 or human brain tumor (i.e., glioma and medulloblastoma; ref. = 37)=20 cells. We first sought to determine whether this phenomenon = is=20 generally applicable to other human tumor cells in culture, = in=20 particular, the human epithelial cancer cells. To that end, = we first=20 established the side population protocol on our flow = cytometer using=20 as experimental controls the HL60-Dox cells (courtesy of Dr. = M.=20 Andreef, Department of Blood and Marrow Transplantation, UT = MD=20 Anderson Cancer Center, Houston, TX); i.e., HL60 leukemia = cells=20 chronically exposed to a low concentration of doxorubicin. = The=20 HL60-Dox cells overexpressed the multidrug resistance = proteins that=20 allowed them to efflux various drugs and xenobiotics = including the=20 Hoechst 33342 dye.4=20 As shown in Fig.=20 1, unselected HL60 cells did not show a side population=20 (A) whereas >90% of the HL60-Dox cells were in the side=20 population (B), which presented as a distinct "tail" = on the=20 histogram and was completely inhibited by either verapamil = (C)=20 or reserpine (D), chemicals previously shown to block = the side=20 population phenotype (e.g., refs. 6,=20 33).=20 To determine the sensitivity of our system, we titrated the = HL60-Dox=20 cells into HL60 cultures and then did side population = analysis. The=20 results (Fig.=20 1E-H) revealed that our system could reliably = detect a=20 side population of 3D~=200.01%. = Indeed,=20 using these experimental conditions, we reliably detected = 3D~=200.01% = and 0.5%=20 side population in mouse bone marrow cells (Fig.=20 1I) and newborn mouse keratinocytes (Fig.=20 1L), respectively, and the side population = phenotypes in=20 these cells could also be blocked by verapamil or reserpine = (Fig.=20 1J and K; data not shown).



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  		Figure 1. Side population = (SP) analysis. A-H, determination of the = sensitivity=20 of the side population protocol using HL60-Dox cells. = Vera,=20 verapamil; Res, reserpine. E-H, HL60-Dox cells = were=20 added to HL60 cells at the concentrations indicated. = I-K,=20 mouse bone marrow (BM) cells were used in side = population=20 analysis in the absence (I) or presence of verapamil=20 (J) or reserpine (K). L, newborn mouse=20 keratinocytes were used in side population analysis. =

 = ;
Using=20 the above protocol, we surveyed 3D~=2030 = cultured human=20 tumor cell lines of the prostate, breast, colon, glioma,=20 bladder, ovary, cervix, glioma, and melanoma and we reliably=20 detected a side population (0.04-0.2%) in 3D~=2030% of = the cell=20 lines (Table=20 1; data not shown). We also analyzed side population in=20 tumor cells freshly purified from three xenograft human = prostate=20 tumors (i.e., Du145, LAPC-4, and LAPC-9), and we only = detected a=20 distinct side population (0.07%) in the LAPC-9 tumor (Table=20 1; data not shown). These results suggest that only some = cultured=20 human cancer cells and tumors cells freshly purified from=20 xenograft tumors contain a detectable side population and = that most=20 cultured human cancer cells may have a side population too = small=20 (i.e., <0.01%) to be reliably detected.


View = this=20 table:
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  		Table 1. Side population = and ABCG2=20 in human tumor cells =

 = ;
Side=20 population cells are more tumorigenic than the non=96side = population=20 cells. The side population cells isolated from the rat C6 = glioma=20 have been shown to be more tumorigenic than the non=96side = population=20 cells (48).=20 To determine whether the side population cells we identified = in human=20 cancer cells might also be more tumorigenic, we did several=20 small-scale tumor experiments. We first purified the side = population=20 cells from the U373 glioma cells, which had 3D~=200.1% = side=20 population (Table=20 1; Fig.=20 2A, a-b). When 1,000 U373 side population = cells=20 were injected into the NOD/SCID mice, a prominent tumor arose = within=20 about 1 month (Table=20 2; Fig.=20 2A, c). The side population tumor histologically = resembled=20 clinical samples in that it had palisades-like structures (Fig.=20 2A, d) and was highly vascularized (Fig.=20 2A, e). In contrast, no tumor was observed in 7 = months=20 when 50,000 non=96side population U373 cells were injected = (Table=20 2).



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  		Figure 2. Side population = (SP) cells are more tumorigenic and have some stem = cell=20 properties. A, U373 side population analysis = (a-b) and=20 the side population cell-initiated tumor (c) analyzed = for=20 histology (d; x100) or CD31=20 staining (e; x100).=20 Clonogenic assays using side population and non=96side = population=20 cells (f). B, MCF7 side population analysis = (a)=20 or RT-PCR assays (b). C, LAPC-9 side = population=20 analysis (a-b) and RT-PCR assays (c). =

 = ;

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  		Table 2. Side population = is=20 enriched with tumorigenic cells =

 = ;
We=20 similarly isolated side population cells from MCF7 breast = cancer=20 cells, which had 3D~0.2% side population (Table=20 1; Fig.=20 2B, a). When injected into the NOD/SCID mice, we = observed=20 a cell number=96dependent tumor development (Table=20 2). For example, we observed a 17% (one of six) tumor = incidence=20 with 1,000 side population cells injected and 50% (three of = six)=20 tumor incidence with 10,000 side population cells injected (Table=20 2). Tumor latency was also reduced with increased numbers = of=20 side population cells injected (Table=20 2). In contrast to the side population MCF7 cells, the = non=96side=20 population MCF7 at 1,000 cells did not give rise to any = tumors (zero=20 of six). With 10,000 cells injected, we observed one tumor = with six=20 injections (Table=20 2). Even with 250,000 cells injected, we only observed = one of two=20 tumor incidence (Table=20 2). In addition, the tumors from the non=96side = population MCF7=20 cells arose with longer latencies (Table=20 2).

Finally, we purified from the LAPC-9 prostate xenograft tumors = the=20 side population cells, which constituted 3D~=200.07% = of the=20 total tumor (Table=20 1; Fig.=20 2C, a-b). When injected into the NOD/SCID mice, as = few as=20 100 cells generated a tumor (25% incidence; Table=20 2). With 1,000 side population cells injected, we observed = a=20 tumor incidence of 75% (three of four; Table=20 2). With 1,500 side population cells injected, we = observed two of=20 two tumor formation with shorter latencies (Table=20 2). Tumors derived from the side population cells = histologically=20 resembled the unsorted LAPC-9 tumors (data not shown). In = contrast,=20 no tumor generation was observed with 1,500 (zero of six) or = 15,000=20 (zero of four) non=96side population LAPC-9 cells injected. = Even=20 150,000 non=96side population LAPC-9 cells injected did not = give=20 rise to tumors within 9 months, although tumor did arise with = 300,000 non=96side population cells (Table=20 2). These results suggest that the side population LAPC-9 = tumor=20 cells are probably >100 times more tumorigenic than the = non=96side=20 population LAPC-9 cells.

Side population cells have some stem cell properties. To=20 determine whether the higher tumorigenicity in the side = population=20 cells might be associated with some of the intrinsic stem = cell=20 properties, we first used the purified side population and=20 non=96side population U373 cells in a clonogenic assay, which = partially measures the self-renewal capacity of the cells. As = shown=20 in Fig.=20 2A, f, whereas 3D~=2010% of = the side=20 population U373 cells could sustain a clonal growth, = <0.01% of the=20 non=96side population U373 cells were clonogenic. Then we = asked whether=20 the side population cell-generated tumors contain non=96side = population=20 cells and can be further passaged in vivo. To that = end, we=20 took the U373 side population tumor obtained from the = preceding=20 experiments (above) and purified tumor cells out and did side = population analysis. The results revealed a side population = of 0.1%=20 (data not shown), which was similar to the percentage of side = population cells in the first-generation tumor (Table=20 1; Fig.=20 2A, a). These observations suggest that the side=20 population cells can give rise to non=96side population cells = in=20 vivo. When injected into the NOD/SCID mice, 100 side = population=20 cells generated tumors with 3D~=2060% (7 = of 11)=20 efficiency and 1,000 side population U373 cells also = generated a=20 tumor (Table=20 2). By contrast, no tumors were observed with 1,000 = non=96side=20 population cells injected (zero of six). Even 200,000 = non=96side=20 population U373 cells injected did not generate a tumor (Table=20 2), suggesting that the U373 side population cells = possess=20 self-renewal capacities in vitro and in vivo = and they=20 are probably >200 more tumorigenic than the non=96side = population=20 cells.

To determine whether the side population cells have some other=20 intrinsic properties of stem cells such as preferential = expression=20 of "stemness" genes, which are important for stem cell = self-renewal,=20 proliferative capacity, or fate determination (2,=20 47,=20 51),3=20 we did semiquantitative RT-PCR analysis of Notch-1, = =DF-catenin=20 (a crucial molecule in the Wnt signaling pathway), and = Smoothened=20 (SMO; the activating receptor for the Hedgehog signaling = pathway).=20 As shown in Fig.=20 2B, b, the side population MCF7 cells expressed = higher=20 levels of Notch-1 and =DF-catenin mRNAs than the non=96side = population=20 MCF7 cells although both populations expressed similar levels = of SMO=20 mRNA.

Taken together, these results suggest that the side population=20 cancer cells have some intrinsic properties of stem cells, = similar=20 to observations in various normal stem cell populations (see=20 Introduction).

Expression of ABCG2 in a small subset of cancer cells: = association=20 of ABCG2 with cell proliferation. Three considerations = made=20 us to turn our attention to ABCG2. First, ABCG2 is one of the = primary mediators of the side population phenotype in mouse=20 bone marrow and some other cells (35).=20 Second, the majority of the cancer cells we have studied do = not=20 possess a detectable side population under our experimental=20 conditions therefore an alternate "marker" is needed to = identify the=20 rare tumorigenic cells. Third, one of the potential concerns = in the=20 side population analysis is that the chronic accumulation of = the low=20 levels of the Hoechst dye in the non=96side population cells = might=20 be toxic to these cells, although our post-sort viability = analysis=20 as well as culture of multiple non=96side population cells = did=20 not reveal such cytotoxicities (data not shown). Regardless, = if ABCG2=20 could be used as a surrogate marker for the side population = cells, it=20 would completely avoid the potential cytotoxicity problem. = With these=20 considerations, we first examined the relationship between = side=20 population cells and ABCG2 expression. As expected, the side=20 population MCF7 cells expressed higher levels of ABCG2 mRNA = than the=20 non=96side population cells (Fig.=20 2B, b). We then examined the ABCG2 protein = expression,=20 using both immunofluorescence staining and flow cytometry, in = the=20 same spectrum of human tumor cell lines and xenograft = tumor-derived=20 cells. In every case, we detected ABCG2 expression in a small = percentage (0.1-4%) of the cells (Table=20 1; Fig.=20 3). A similar ABCG2 expression pattern (i.e., 0.1-2%) was = also=20 observed in several bladder cell lines (Fig.=20 3E, d; data not shown) as well as in LAPC-4 and LAPC-9=20 xenograft tumors (data not shown).



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  		Figure 3. ABCG2 = expression in human=20 cancer cells. Cultured glioma (A), or prostate = (B),=20 breast (C), colon (D), or other (E; see = Table=20 1) cancer cells were stained for ABCG2 using a = monoclonal=20 antibody. Original magnifications, x100. =

 = ;
Interestingly,=20 we observed that many of the ABCG2+ cancer cells = were in=20 the process of cell division (Fig.=20 4). Overall, we observed that 3D~=2030% of = the=20 ABCG2+ cancer cells were mitotic, whereas only = 3D~=201% of = the=20 ABCG2=96 cells were mitotic. In clonal analyses, = we found=20 that the majority of divided cells that had completed or were = about=20 to complete cytokinesis equally distributed ABCG2 to both = daughter=20 cells (Fig.=20 4G-I and J-L). However, in 3D~=201% = of=20 the dividing cells undergoing cytokinesis ABCG2 seemed to = segregate=20 asymmetrically to mainly one daughter cell (e.g., Fig.=20 4M-O). These observations suggest that ABCG2 might = preferentially mark proliferating cells and that some=20 ABCG2-expressing cancer cells might be undergoing = asymmetrical cell=20 division, a cardinal feature of stem cells. To determine = whether=20 ABCG2 expression might be associated with cell proliferation = in=20 general, we prospectively purified ABCG2+ and=20 ABCG2=96 cancer cells to near homogeneity and used = them in a=20 BrdU-labeling experiment. As shown in Fig.=20 5, acutely purified ABCG2+ Du145 prostate = (A)=20 and MDA-MB435 breast (B) cancer cells that had been=20 BrdU-pulsed and cultured for only 3 hours showed = significantly more=20 proliferation than the corresponding ABCG2=96 = cells.=20



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  		Figure 4. Association of = ABCG2=20 expression with cell division. B-C and E-F, = cells that=20 have just undergone nuclear division but have not undergone=20 cytokinesis (arrows). By contrast, cells in (G-I, = J-L,=20 and M-O) have just undergone cytokinesis. Cells in=20 (D-O) were clonal cultures. Original magnifications, = x400. =

 = ;


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  		Figure 5. Proliferative = and=20 self-renewal properties of ABCG2+ and = ABCG2-=20 tumor cells. Purified ABCG2+ and = ABCG2- Du145=20 (A) or MDA-MB435 (B) cells were plated for = either 3=20 hours or cultured for the time periods indicated. Cells were = pulsed=20 with BrdUrd for 3 hours before the end of each time point.=20 Columns, mean % BrdUrd+ cells from two = experiments=20 with 500 to 1,200 total cells counted; bars, =B1SE. = *, P=20 < 0.001 (t test). #, P < 0.01 (A) = or=20 <0.05 (B). Purified ABCG2+ and=20 ABCG2- Du145 (C) or MDA-MB435 (D) = cells=20 were plated at clone density (400 cells per well) and = cultured for=20 the times indicated. At the end, the numbers of clones were=20 quantified. % Cloning efficiency. *, P < 0.01. = Purified=20 ABCG2+ and ABCG2- Du145 (E and=20 G) or MDA-MB435 (F and H) cells were = plated at=20 clone density (100 cells per well) and cultured for 7 = (E and=20 F), 14 (G), or 11 (H) days. At the end, = the=20 numbers of cells in each clone were counted and clones were = grouped=20 according to their sizes. On average 100 to 200 clones were = randomly=20 counted for each condition. Representative of two = independent=20 experiments. *, P < 0.05. =

 = ;
ABCG2+=20 and ABCG2=96 tumor cells are similarly tumorigenic.=20 Next, we purified ABCG2+ and ABCG2=96 cells = and did=20 tumor experiments to determine whether the ABCG2+ = cancer=20 cells might be more tumorigenic. Much to our surprise, when = the two=20 populations of U373 cells were injected into the NOD/SCID = mice, we=20 did not observe any major differences with respect to their=20 tumorigenicities (Table=20 3). In fact, the ABCG2=96 cells tended to generate=20 tumors slightly faster than the ABCG2+ or unsorted = cells (Table=20 3).


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  		Table 3. ABCG2 and = tumorigenesis =

 = ;
To=20 determine whether the lack of correlation between ABCG2 expression=20 and tumorigenicity may be a cell type=96restricted = phenomenon, we=20 carried out similar tumor experiments using purified = ABCG2+=20 and ABCG2=96 cells from prostate (Du145), breast=20 (MDA-MB435), and colon (HCT116) cancer cell cultures. In = every case,=20 we failed to observe any significant difference in tumor = incidence=20 or latency periods between the two populations (Table=20 3; data not shown). We also compared the = ABCG2+ and=20 ABCG2=96 cells purified from Du145 xenograft = tumors and=20 again did not observe any major differences in their = tumorigenicities=20 (Table=20 3).

Evidence that ABCG2 expression marks proliferating tumor = progenitors=20 whereas ABCG2=96 population contains primitive cancer = stem=20 cells. If the ABCG2+ cells proliferate faster than = the=20 ABCG2=96 cancer cells, why are they not more = tumorigenic?=20 One possibility is that ABCG2+ cells are mostly = fast=20 proliferating tumor progenitors (i.e., transit amplifying = cells)=20 rather than primitive, slow-cycling CSCs. To test this = possibility,=20 we first determined whether the ABCG2+ tumor cells = could=20 generate ABCG2=96 cells and, more importantly, = whether=20 ABCG2=96 cells could generate ABCG2+ = cells. As=20 shown in Table=20 4, tumors derived from the ABCG2+ cancer cells = all=20 contained only a fraction of ABCG2+ cells (Table=20 4), suggesting that ABCG2+ cells generated=20 ABCG2=96 tumor cells in vivo. Except for = one tumor=20 derived from the 1,000 ABCG2+ Du145 cells, we = detected=20 only small percentages of ABCG2+ cells in all = other tumors=20 derived from the ABCG2+ tumor cells (Table=20 4). On the other hand, tumors derived from the=20 ABCG2=96 cells also contained a small fraction of=20 ABCG2+ cells (Table=20 4), suggesting that some ABCG2=96 cells also = have the=20 ability to generate ABCG2+ tumor cells. =


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  		Table 4. = ABCG2+ and=20 ABCG2=96 cells in tumors =

 = ;
Next,=20 we did a series of clonal analyses to determine the relationship=20 between ABCG2+ and ABCG2=96 cancer cells. = Although=20 freshly purified ABCG2+ Du145 (Fig.=20 5A; 3 hours) or MDA-MB435 (Fig.=20 5B; 3 hours) cells proliferated faster than their=20 corresponding ABCG2=96 counterparts, culture for = as short as=20 1 day eliminated or reduced this proliferative difference. = Continued=20 cultures of these cells revealed increasing proliferating = (i.e.,=20 BrdU+) cells in the ABCG2=96 = populations (Fig.=20 5A-B). These results suggest the possibility that, = with=20 time in culture, the ABCG2+ tumor progenitors = gradually=20 lose their proliferative capacity whereas primitive CSCs in = the=20 ABCG2=96 population give rise to highly = proliferative=20 ABCG2+ tumor progenitors. In support, = immunostaining=20 revealed the emergence of ABCG2+ cells from the = starting=20 ABCG2=96 cancer cells within 1 week (data not shown),=20 consistent with the ability of some ABCG2=96 tumor = cells=20 to generate ABCG2+ cells in vivo (Table=20 4).

Consistent with the BrdU incorporation assays, clonal analyses=20 revealed that at earlier time points the ABCG2+ tumor=20 cells had higher cloning efficiency; that is, more cells had = the=20 ability to establish a clone (Fig.=20 5C-D). However, at later time points, the=20 ABCG2=96 tumor cells picked up and formed similar or = higher=20 (Fig.=20 5C-D) percentages of clones. Subsequently, we carried = out=20 differential clonal analyses in which purified ABCG2+ = and=20 ABCG2=96 tumor cells were plated at clonal density and=20 clonal sizes were quantified at a shorter and a longer time=20 point. As shown in Fig.=20 5E, 7 days after plating, more ABCG2+ Du145=20 cells formed larger clones. However, at 14 days post plating, = there were significantly more large clones derived from the=20 ABCG2=96 Du145 cells (Fig.=20 5G). The average clonal sizes (cells/clone) of the = ABCG2+ versus ABCG2=96 Du145 cells were = 101 and=20 60 cells at 7 days versus 4,716 and 5,658 cells at 14 days,=20 respectively (P < 0.01 in both cases, ANOVA). = Similarly,=20 more ABCG2+ MDA-MB435 cells formed larger clones = than the=20 ABCG2=96 MDA-MB435 cells at 7 days after plating = (Fig.=20 5F). However, by 11 days after plating, there were = significantly=20 more large clones (i.e., >500 cells per clone) derived = from=20 the ABCG2=96 MDA-MB435 cells (Fig.=20 5H). The average clonal sizes of the = ABCG2+=20 versus ABCG2=96 MDA-MB435 cells were 30 and 16 = cells at 7=20 days (P < 0.01) versus 346 and 356 cells at 11 = days,=20 respectively. Together, the proliferation (Fig.=20 5A-B) and clonal (Fig.=20 5C-H) analyses provide strong evidence that the=20 ABCG2+ tumor cells likely represent fast-proliferating=20 tumor progenitor cells, whereas the ABCG2=96 = population=20 contains slow-cycling, primitive CSC cells that, with time,=20 could establish robust clonal growth and also generate = fast-cycling=20 progenitor cells.

Finally, we did RT-PCR analysis to assess the mRNA expression = of=20 several stemness genes (Fig.=20 6A-B). Consistent with the concept that the=20 ABCG2=96 population contains primitive, stem-like = cancer=20 cells, we found that purified ABCG2=96 tumor cells = expressed=20 higher mRNA levels of Notch-1, =DF-catenin, and SMO (Fig.=20 6A-B). Even Oct-4, a transcription factor essential = for=20 embryonic stem cell self-renewal (51)=20 and recently shown to be expressed in some adult stem cells = (52),=20 also showed preferential expression in the = ABCG2=96 cells in=20 three of four cell types (Fig.=20 6A). Interestingly, the Notch-1 mRNA was detected nearly = exclusively in the ABCG2=96 tumor cells (Fig.=20 6A). Similarly, the =DF-catenin mRNA was observed = only in=20 the ABCG2=96 Du145 cells (Fig.=20 6B). These RT-PCR results provide strong support = for the=20 existence of primitive CSC in the ABCG2=96 tumor = cell=20 population.



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  		Figure 6. = ABCG2- cancer=20 cells express higher levels of stemness genes. A-B, = RT-PCR=20 analysis of stemness genes using purified ABCG2+ = (+) and=20 ABCG2- (=96) cancer cells. Negative controls = (Neg.=20 CTL) refer to RT using H2O and positive = control=20 (Pos. CTL) in (H) refers to unsorted Du145 = cells=20 previously shown to express =DF-catenin.3=20 C, a hypothetical model. See text for more = discussion. =

 = ;

3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
References
 
A= =20 long-time puzzle to tumor biologists is the observations that = even=20 with long-term cultured cancer cells, in general sufficient = numbers=20 of cells have to be injected to initiate an orthotopic tumor = in=20 recipient animals (reviewed in refs. 1,=20 47),=20 suggesting that even in long-term tumor cell cultures, not = all cells=20 are equal and only a small population of cells is = tumorigenic.=20 Indeed, when multiple human cancer cells, which have been in=20 culture under different conditions for years or even decades = are=20 assessed for their clonal growth and clonogenic potentials, = we find=20 that only a small percentage of cells possesses such = potentials.3=20 Furthermore, when tumor cell=96derived spheres or xenograft=20 tumors in situ are pulsed with BrdU followed by extended=20 chase, only a very minor population of the cells manifests as = the=20 long-term LRCs,3=20 which are known to preferentially identify stem cells (2,=20 5).=20 In further support, long-term cultured rat C6 glioma cells = (48)=20 and some human brain tumor (i.e., glioma and medulloblastoma; = ref. 37)=20 cells are found to contain a side population, which is known = to be=20 enriched in stem cells (see Introduction). Importantly, the = C6 side=20 population cells are more tumorigenic than and can also = generate the=20 non=96side population cells (48),=20 providing the first direct evidence for a population of more=20 tumorigenic cells in long-term tumor cell cultures. It is = these=20 observations (37,=20 48)3=20 that have prompted us to first determine whether the side = population=20 technique can be generally applied to other cultured human = tumor=20 cells, in particular, the human epithelial cancer cells. =

Our results reveal that 3D~=2030% = cultured human=20 cancer cell lines and xenograft tumor-derived cells possess a = side=20 population that can be reliably detected under the current=20 experimental conditions. Several notable points are worthy of = mention. First, in most literature reports, the side = population is=20 identified on either a MoFlo or FACS Vantage flow cytometer = as a=20 continuous tail of the non=96side population. Therefore, the=20 discrimination of the side population from the non=96side = population=20 is, to a certain extent, arbitrary and can vary significantly = from experiment to experiment. In contrast, using a Coulter=20 Epics flow cytometer and our modified protocol, we have in = most=20 cases identified the side population as a distinct "side"=20 population separate from the main non=96side population. This = could potentially give us relatively pure side population = cells.=20 Second, in support of this possibility, our system seems to=20 identify the side population cells in a more stringent manner = and=20 the percentages of the side population cells may be more=20 representative of putative CSCs in the cultures or xenograft = tumors.=20 Therefore, only 3D~=2030% = cultured human=20 cancer cell lines and xenograft tumor-derived cells possess a = side=20 population of 0.04% to 0.2%. These percentages are similar to = the=20 side population of multiple normal stem cell or progenitor = cell=20 populations [i.e., 0.01-5%; refs. 18,=20 23,=20 26;=20 e.g., mouse bone marrow (0.01%; Fig.=20 1), newborn mouse keratinocyte progenitors (0.5%; Fig.=20 1), and human bone marrow (3D~=200.03%; = ref.=20 8)].=20 The majority of the cancer cell lines or xenograft tumors = examined=20 seems to possess too small a side population to be reliably=20 detected.

Importantly, the side population cells purified from two cell=20 lines and one xenograft tumor are more tumorigenic than the=20 non=96side population counterparts. Furthermore, the side=20 population cells are found to possess several intrinsic = properties=20 of stem cells: self-renewal, preferential expression of some=20 stemness genes, and an ability to give rise to non=96side=20 population cells. These results thus extend the others = studies=20 on rat C6 glioma cells (48)=20 and support the concept that the side population is indeed = enriched=20 in stem-like tumorigenic cells. It should be noted that with = higher=20 numbers of the non=96side population epithelial cancer cells = (i.e.,=20 MCF7 and LAPC-9) injected, we also observed tumor = development. These=20 results may suggest that the non=96side population also = contains a very=20 small percentage of tumorigenic cells, although the results=20 might have stemmed from the contamination of small numbers of = the side population cells in the non=96side population as=20 epithelial cancer cells are very "sticky".

The major focus of the current study is to address whether the=20 higher tumorigenicity associated with the side population = cells=20 is related to ABCG2 expression. Because the side population=20 phenotype in some cell types is mainly mediated by ABCG2, the = side population cells (e.g., in MCF7) express higher levels = of=20 ABCG2 mRNA, ABCG2 is expressed only in a small subset of = cancer=20 cells, and ABCG2 expression in cancer cells seems associated = with=20 cell proliferation, it stands to reason that the ABCG2+=20 cancer cells might or should be more tumorigenic than the=20 ABCG2=96 tumor cells. Surprisingly, however, = highly purified=20 ABCG2+ cells from several types of tumor cells are = not=20 more tumorigenic than the corresponding ABCG2=96 = cells.=20 Further proliferation assays, clonal analyses, self-renewal, = and=20 molecular studies suggest a model in which the = ABCG2=96=20 population contains primitive stem-like cancer cells with = higher=20 self-renewal (because of higher levels of stemness genes) and = proliferative potentials but are normally slow cycling (Fig.=20 6C). These cells then give rise to = ABCG2+ tumor=20 progenitor cells that are more actively proliferating but = possess=20 reduced self-renewal and long-term proliferative capacities = (Fig.=20 6). The ABCG2+ tumor progenitor cells = eventually give=20 rise to ABCG2=96, partially or even fully = differentiated=20 tumor cells that constitute the bulk of tumor cell mass (Fig.=20 6).

The side population has been shown to be very heterogeneous = (10,=20 27,=20 28).=20 Therefore, the side population detected in cancer cells might = contain=20 several subsets of cells, one of which expresses ABCG2 thus=20 explaining the increased ABCG2 expression in the side = population. The=20 higher tumorigenicity associated with the side population = might be=20 conferred by combined effects of several other subpopulations = of=20 cells in addition to the ABCG2+ cells. For = example, cells=20 expressing other ABC family members might also contribute to = the=20 cancer cell side population phenotype. Indeed, it has been = shown that=20 only a fraction of side population cells expresses ABCG2 (24)=20 and that both side population and known stem/progenitor cells = also=20 express other ABC transporters such as MDR-1 (i.e., ABCB1 or=20 P-glycoprotein), MRP-1 (ABCC1), and ABCA2 (36,=20 37,=20 39).=20 In addition, enforced expression of MDR-1 in murine bone = marrow cells=20 is sufficient to expand the side population (40).=20 We are currently using cultured cancer cells as well as = xenograft and=20 primary human tumor samples to determine the molecular basis = of the=20 higher tumorigenicity associated with the side population = (e.g.,=20 amplification of oncogenes and/or mutations of specific tumor = suppressors), dissect different subpopulations of the side = population=20 with respect to their tumorigenic potentials, and elucidate = the=20 interrelationship between the side population and several = other=20 tumorigenic populations we have identified.


3D"   =20 Acknowledgments =
 
Grant support:=20 NIH grants CA90297, AG023374, and P30 CA16672; NIEHS grant = ES07784;=20 American Cancer Society grant RSG MGO-105961; Department of = Defense=20 grant DAMD17-03-1-0137; Prostate Cancer Foundation; and M.D. = Anderson=20 Cancer Center (PCRP and IRG).

The costs of publication of this article were defrayed in part = by=20 the payment of page charges. This article must therefore be = hereby=20 marked advertisement in accordance with 18 U.S.C. = Section 1734=20 solely to indicate this fact.

We thank C. Conti, T-J. Liu, M. Andreef, and C. Sawyers for=20 providing cells; C. Carter for assistance in preparing mouse=20 bone marrow cells; the Histology Core for excellent = assistance=20 in tissue processing and immunohistochemistry; the Animal = Facility=20 Core for help in tumor experiments; E. Richie for her = insights;=20 and members of the Tang lab for support and helpful = discussion.=20


3D"   =20 Footnotes
 
Note: J. Zhou is currently at the = Dermatology=20 Branch, National Cancer Institute, NIH, Building 10, Room = 12N262, 10=20 Center Drive, MSC 1908, Bethesda, MD 20892-1908.

3 C. Jeter et al. Stem-like = cancer=20 cells in culture and xenograft tumors: expression and roles = of=20 stemness genes, submitted for publication.

4 Unpublished = observations.=20

Received 2/21/05. Revised 4/16/05. Accepted 4/28/05.


3D"   =20 References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
3D"References
&nb= sp;

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=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=3D=3D=3D=0A= =0A= Emulate Gecko 'XMLHttpRequest()' functionality in IE and Opera. Opera = requires=0A= the Sun Java Runtime Environment .=0A= =0A= by Andrew Gregory=0A= http://www.scss.com.au/family/andrew/webdesign/xmlhttprequest/=0A= =0A= This work is licensed under the Creative Commons Attribution License. To = view a=0A= copy of this license, visit = http://creativecommons.org/licenses/by-sa/2.5/ or=0A= send a letter to Creative Commons, 559 Nathan Abbott Way, Stanford, = California=0A= 94305, USA.=0A= =0A= Attribution: Leave my name and web address in this script intact.=0A= =0A= Not Supported in Opera=0A= ----------------------=0A= * user/password authentication=0A= * responseXML data member=0A= =0A= Not Fully Supported in Opera=0A= ----------------------------=0A= * async requests=0A= * abort()=0A= * getAllResponseHeaders(), getAllResponseHeader(header)=0A= =0A= */=0A= // IE support=0A= if (window.ActiveXObject && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= var msxmls =3D new Array(=0A= 'Msxml2.XMLHTTP.5.0',=0A= 'Msxml2.XMLHTTP.4.0',=0A= 'Msxml2.XMLHTTP.3.0',=0A= 'Msxml2.XMLHTTP',=0A= 'Microsoft.XMLHTTP');=0A= for (var i =3D 0; i < msxmls.length; i++) {=0A= try {=0A= return new ActiveXObject(msxmls[i]);=0A= } catch (e) {=0A= }=0A= }=0A= return null;=0A= };=0A= }=0A= // Gecko support=0A= /* ;-) */=0A= // Opera support=0A= if (window.opera && !window.XMLHttpRequest) {=0A= window.XMLHttpRequest =3D function() {=0A= this.readyState =3D 0; // = 0=3Duninitialized,1=3Dloading,2=3Dloaded,3=3Dinteractive,4=3Dcomplete=0A= this.status =3D 0; // HTTP status codes=0A= this.statusText =3D '';=0A= this._headers =3D [];=0A= this._aborted =3D false;=0A= this._async =3D true;=0A= this._defaultCharset =3D 'ISO-8859-1';=0A= this._getCharset =3D function() {=0A= var charset =3D _defaultCharset;=0A= var contentType =3D = this.getResponseHeader('Content-type').toUpperCase();=0A= val =3D contentType.indexOf('CHARSET=3D');=0A= if (val !=3D -1) {=0A= charset =3D contentType.substring(val);=0A= }=0A= val =3D charset.indexOf(';');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= val =3D charset.indexOf(',');=0A= if (val !=3D -1) {=0A= charset =3D charset.substring(0, val);=0A= }=0A= return charset;=0A= };=0A= this.abort =3D function() {=0A= this._aborted =3D true;=0A= };=0A= this.getAllResponseHeaders =3D function() {=0A= return this.getAllResponseHeader('*');=0A= };=0A= this.getAllResponseHeader =3D function(header) {=0A= var ret =3D '';=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= if (header =3D=3D '*' || this._headers[i].h =3D=3D header) {=0A= ret +=3D this._headers[i].h + ': ' + this._headers[i].v + '\n';=0A= }=0A= }=0A= return ret;=0A= };=0A= this.getResponseHeader =3D function(header) {=0A= var ret =3D getAllResponseHeader(header);=0A= var i =3D ret.indexOf('\n');=0A= if (i !=3D -1) {=0A= ret =3D ret.substring(0, i);=0A= }=0A= return ret;=0A= };=0A= this.setRequestHeader =3D function(header, value) {=0A= this._headers[this._headers.length] =3D {h:header, v:value};=0A= };=0A= this.open =3D function(method, url, async, user, password) {=0A= this.method =3D method;=0A= this.url =3D url;=0A= this._async =3D true;=0A= this._aborted =3D false;=0A= this._headers =3D [];=0A= if (arguments.length >=3D 3) {=0A= this._async =3D async;=0A= }=0A= if (arguments.length > 3) {=0A= opera.postError('XMLHttpRequest.open() - user/password not = supported');=0A= }=0A= this.readyState =3D 1;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= };=0A= this.send =3D function(data) {=0A= if (!navigator.javaEnabled()) {=0A= alert("XMLHttpRequest.send() - Java must be installed and = enabled.");=0A= return;=0A= }=0A= if (this._async) {=0A= setTimeout(this._sendasync, 0, this, data);=0A= // this is not really asynchronous and won't execute until the = current=0A= // execution context ends=0A= } else {=0A= this._sendsync(data);=0A= }=0A= }=0A= this._sendasync =3D function(req, data) {=0A= if (!req._aborted) {=0A= req._sendsync(data);=0A= }=0A= };=0A= this._sendsync =3D function(data) {=0A= this.readyState =3D 2;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= // open connection=0A= var url =3D new java.net.URL(new = java.net.URL(window.location.href), this.url);=0A= var conn =3D url.openConnection();=0A= for (var i =3D 0; i < this._headers.length; i++) {=0A= conn.setRequestProperty(this._headers[i].h, this._headers[i].v);=0A= }=0A= this._headers =3D [];=0A= if (this.method =3D=3D 'POST') {=0A= // POST data=0A= conn.setDoOutput(true);=0A= var wr =3D new = java.io.OutputStreamWriter(conn.getOutputStream(), this._getCharset());=0A= wr.write(data);=0A= wr.flush();=0A= wr.close();=0A= }=0A= // read response headers=0A= // NOTE: the getHeaderField() methods always return nulls for me :(=0A= var gotContentEncoding =3D false;=0A= var gotContentLength =3D false;=0A= var gotContentType =3D false;=0A= var gotDate =3D false;=0A= var gotExpiration =3D false;=0A= var gotLastModified =3D false;=0A= for (var i =3D 0; ; i++) {=0A= var hdrName =3D conn.getHeaderFieldKey(i);=0A= var hdrValue =3D conn.getHeaderField(i);=0A= if (hdrName =3D=3D null && hdrValue =3D=3D null) {=0A= break;=0A= }=0A= if (hdrName !=3D null) {=0A= this._headers[this._headers.length] =3D {h:hdrName, = v:hdrValue};=0A= switch (hdrName.toLowerCase()) {=0A= case 'content-encoding': gotContentEncoding =3D true; break;=0A= case 'content-length' : gotContentLength =3D true; break;=0A= case 'content-type' : gotContentType =3D true; break;=0A= case 'date' : gotDate =3D true; break;=0A= case 'expires' : gotExpiration =3D true; break;=0A= case 'last-modified' : gotLastModified =3D true; break;=0A= }=0A= }=0A= }=0A= // try to fill in any missing header information=0A= var val;=0A= val =3D conn.getContentEncoding();=0A= if (val !=3D null && !gotContentEncoding) = this._headers[this._headers.length] =3D {h:'Content-encoding', v:val};=0A= val =3D conn.getContentLength();=0A= if (val !=3D -1 && !gotContentLength) = this._headers[this._headers.length] =3D {h:'Content-length', v:val};=0A= val =3D conn.getContentType();=0A= if (val !=3D null && !gotContentType) = this._headers[this._headers.length] =3D {h:'Content-type', v:val};=0A= val =3D conn.getDate();=0A= if (val !=3D 0 && !gotDate) this._headers[this._headers.length] = =3D {h:'Date', v:(new Date(val)).toUTCString()};=0A= val =3D conn.getExpiration();=0A= if (val !=3D 0 && !gotExpiration) = this._headers[this._headers.length] =3D {h:'Expires', v:(new = Date(val)).toUTCString()};=0A= val =3D conn.getLastModified();=0A= if (val !=3D 0 && !gotLastModified) = this._headers[this._headers.length] =3D {h:'Last-modified', v:(new = Date(val)).toUTCString()};=0A= // read response data=0A= var reqdata =3D '';=0A= var stream =3D conn.getInputStream();=0A= if (stream) {=0A= var reader =3D new java.io.BufferedReader(new = java.io.InputStreamReader(stream, this._getCharset()));=0A= var line;=0A= while ((line =3D reader.readLine()) !=3D null) {=0A= if (this.readyState =3D=3D 2) {=0A= this.readyState =3D 3;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= }=0A= reqdata +=3D line + '\n';=0A= }=0A= reader.close();=0A= this.status =3D 200;=0A= this.statusText =3D 'OK';=0A= this.responseText =3D reqdata;=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onload) {=0A= this.onload();=0A= }=0A= } else {=0A= // error=0A= this.status =3D 404;=0A= this.statusText =3D 'Not Found';=0A= this.responseText =3D '';=0A= this.readyState =3D 4;=0A= if (this.onreadystatechange) {=0A= this.onreadystatechange();=0A= }=0A= if (this.onerror) {=0A= this.onerror();=0A= }=0A= }=0A= };=0A= };=0A= }=0A= // ActiveXObject emulation=0A= if (!window.ActiveXObject && window.XMLHttpRequest) {=0A= window.ActiveXObject =3D function(type) {=0A= switch (type.toLowerCase()) {=0A= case 'microsoft.xmlhttp':=0A= case 'msxml2.xmlhttp':=0A= case 'msxml2.xmlhttp.3.0':=0A= case 'msxml2.xmlhttp.4.0':=0A= case 'msxml2.xmlhttp.5.0':=0A= return new XMLHttpRequest();=0A= }=0A= return null;=0A= };=0A= }=0A= ------=_NextPart_000_004B_01C87610.AA478FB0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/ajax/utility.js /************************************************************************= *****=0A= * javascript/ajax/utility.js=0A= *=0A= * Utility functions for working with XMLHttpRequest data.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Copy XML nodes into an HTMLElement. This effectively=0A= * clones XML markup which uses XHTML naming conventions=0A= * into an HTML DOM.=0A= */=0A= function copy_xml_to_html(src, dst) {=0A= if (src.nodeType =3D=3D 1) { /* Node.ELEMENT_NODE */=0A= var e =3D document.createElement(src.nodeName);=0A= for (var i =3D 0; i < src.childNodes.length; i++) {=0A= copy_xml_to_html(src.childNodes[i], e);=0A= }=0A= for (var i =3D 0; i < src.attributes.length; i++) {=0A= var n =3D src.attributes[i].name;=0A= var v =3D unescape_xml_string(src.attributes[i].value); =0A= e.setAttribute(n, v);=0A= if (n =3D=3D "class") {=0A= e.className =3D v;=0A= }=0A= else if (n =3D=3D "style") {=0A= set_css_style(v, e, "");=0A= }=0A= }=0A= dst.appendChild(e);=0A= }=0A= else if (src.nodeType =3D=3D 3) { /* Node.TEXT_NODE */=0A= dst.appendChild(document.createTextNode(src.nodeValue));=0A= }=0A= }=0A= =0A= /* =0A= * It is unclear that this is the right thing to be calling=0A= * from copy_xml_to_html, but it appears that Safari decides=0A= * to convert & to the NCR #, and then encodes that=0A= * NCR to &%26%2338;. So, I'm going to treat the DOM Attr=0A= * value as a plain string, and run our XML string input=0A= * through the decoding routine below.=0A= */=0A= function unescape_xml_string(s) {=0A= return s.replace(/'/g, "'")=0A= .replace(/'/g, "'")=0A= .replace(/"/g, "\"")=0A= .replace(/"/g, "\"")=0A= .replace(/>/g, ">")=0A= .replace(/>/g, ">")=0A= .replace(/</g, "<")=0A= .replace(/</g, "<")=0A= .replace(/&/g, "&")=0A= .replace(/&/g, "&");=0A= }=0A= =0A= /*=0A= * Parse set of CSS rules and apply them to an element.=0A= * This is quite horrifying, but I'm unable to determine=0A= * how else to handle this with IE 6. FireFox and other=0A= * sane browsers let you simply set the style attribute=0A= * or use e.style.setProperty(rule, value, priority),=0A= * IE 6 appears to have neither of these capabilities..=0A= */=0A= function set_css_style(css, e, priority) {=0A= var rules =3D css.split(";");=0A= for (var i =3D 0; i < rules.length; i++) {=0A= var nvpair =3D rules[i].split(":");=0A= if (nvpair.length =3D=3D 2) {=0A= try {=0A= var name =3D nvpair[0]; /* style attribute */=0A= var value =3D nvpair[1]; /* attribute value */=0A= =0A= /*=0A= * For each possible style attribute, set the=0A= * appropriate style property in the element.=0A= */=0A= if (name =3D=3D "background") {=0A= e.style.background =3D value;=0A= }=0A= else if (name =3D=3D "background-attachment") {=0A= e.style.backgroundAttachment =3D value;=0A= }=0A= else if (name =3D=3D "background-color") {=0A= e.style.backgroundColor =3D value;=0A= }=0A= else if (name =3D=3D "background-image") {=0A= e.style.backgroundImage =3D value;=0A= }=0A= else if (name =3D=3D "background-position") {=0A= e.style.backgroundPosition =3D value;=0A= }=0A= else if (name =3D=3D "background-position-x") {=0A= e.style.backgroundPositionX =3D value;=0A= }=0A= else if (name =3D=3D "background-position-y") {=0A= e.style.backgroundPositionY =3D value;=0A= }=0A= else if (name =3D=3D "background-repeat") {=0A= e.style.backgroundRepeat =3D value;=0A= }=0A= else if (name =3D=3D "behavior") {=0A= e.style.behavior =3D value;=0A= }=0A= else if (name =3D=3D "border") {=0A= e.style.border =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom") {=0A= e.style.borderBottom =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-color") {=0A= e.style.borderBottomColor =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-style") {=0A= e.style.borderBottomStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-bottom-width") {=0A= e.style.borderBottomWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-collapse") {=0A= e.style.borderCollapse =3D value;=0A= }=0A= else if (name =3D=3D "border-color") {=0A= e.style.borderColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left") {=0A= e.style.borderLeft =3D value;=0A= }=0A= else if (name =3D=3D "border-left-color") {=0A= e.style.borderLeftColor =3D value;=0A= }=0A= else if (name =3D=3D "border-left-style") {=0A= e.style.borderLeftStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-left-width") {=0A= e.style.borderLeftWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-right") {=0A= e.style.borderRight =3D value;=0A= }=0A= else if (name =3D=3D "border-right-color") {=0A= e.style.borderRightColor =3D value;=0A= }=0A= else if (name =3D=3D "border-right-style") {=0A= e.style.borderRightStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-right-width") {=0A= e.style.borderRightWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-style") {=0A= e.style.borderStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top") {=0A= e.style.borderTop =3D value;=0A= }=0A= else if (name =3D=3D "border-top-color") {=0A= e.style.borderTopColor =3D value;=0A= }=0A= else if (name =3D=3D "border-top-style") {=0A= e.style.borderTopStyle =3D value;=0A= }=0A= else if (name =3D=3D "border-top-width") {=0A= e.style.borderTopWidth =3D value;=0A= }=0A= else if (name =3D=3D "border-width") {=0A= e.style.borderWidth =3D value;=0A= }=0A= else if (name =3D=3D "bottom") {=0A= e.style.bottom =3D value;=0A= }=0A= else if (name =3D=3D "clear") {=0A= e.style.clear =3D value;=0A= }=0A= else if (name =3D=3D "clip") {=0A= e.style.clip =3D value;=0A= }=0A= else if (name =3D=3D "color") {=0A= e.style.color =3D value;=0A= }=0A= else if (name =3D=3D "cssText") {=0A= e.style.Sets =3D value;=0A= }=0A= else if (name =3D=3D "cursor") {=0A= e.style.cursor =3D value;=0A= }=0A= else if (name =3D=3D "direction") {=0A= e.style.direction =3D value;=0A= }=0A= else if (name =3D=3D "display") {=0A= e.style.display =3D value;=0A= }=0A= else if (name =3D=3D "font") {=0A= e.style.font =3D value;=0A= }=0A= else if (name =3D=3D "font-family") {=0A= e.style.fontFamily =3D value;=0A= }=0A= else if (name =3D=3D "font-size") {=0A= e.style.fontSize =3D value;=0A= }=0A= else if (name =3D=3D "font-style") {=0A= e.style.fontStyle =3D value;=0A= }=0A= else if (name =3D=3D "font-variant") {=0A= e.style.fontVariant =3D value;=0A= }=0A= else if (name =3D=3D "font-weight") {=0A= e.style.fontWeight =3D value;=0A= }=0A= else if (name =3D=3D "height") {=0A= e.style.height =3D value;=0A= }=0A= else if (name =3D=3D "ime-mode") {=0A= e.style.imeMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-flow") {=0A= e.style.layoutFlow =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid") {=0A= e.style.layoutGrid =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-char") {=0A= e.style.layoutGridChar =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-line") {=0A= e.style.layoutGridLine =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-mode") {=0A= e.style.layoutGridMode =3D value;=0A= }=0A= else if (name =3D=3D "layout-grid-type") {=0A= e.style.layoutGridType =3D value;=0A= }=0A= else if (name =3D=3D "left") {=0A= e.style.left =3D value;=0A= }=0A= else if (name =3D=3D "letter-spacing") {=0A= e.style.letterSpacing =3D value;=0A= }=0A= else if (name =3D=3D "line-break") {=0A= e.style.lineBreak =3D value;=0A= }=0A= else if (name =3D=3D "line-height") {=0A= e.style.lineHeight =3D value;=0A= }=0A= else if (name =3D=3D "list-style") {=0A= e.style.listStyle =3D value;=0A= }=0A= else if (name =3D=3D "list-style-image") {=0A= e.style.listStyleImage =3D value;=0A= }=0A= else if (name =3D=3D "list-style-position") {=0A= e.style.listStylePosition =3D value;=0A= }=0A= else if (name =3D=3D "list-style-type") {=0A= e.style.listStyleType =3D value;=0A= }=0A= else if (name =3D=3D "margin") {=0A= e.style.margin =3D value;=0A= }=0A= else if (name =3D=3D "margin-bottom") {=0A= e.style.marginBottom =3D value;=0A= }=0A= else if (name =3D=3D "margin-left") {=0A= e.style.marginLeft =3D value;=0A= }=0A= else if (name =3D=3D "margin-right") {=0A= e.style.marginRight =3D value;=0A= }=0A= else if (name =3D=3D "margin-top") {=0A= e.style.marginTop =3D value;=0A= }=0A= else if (name =3D=3D "min-height") {=0A= e.style.minHeight =3D value;=0A= }=0A= else if (name =3D=3D "overflow") {=0A= e.style.overflow =3D value;=0A= }=0A= else if (name =3D=3D "overflow-x") {=0A= e.style.overflowX =3D value;=0A= }=0A= else if (name =3D=3D "overflow-y") {=0A= e.style.overflowY =3D value;=0A= }=0A= else if (name =3D=3D "padding") {=0A= e.style.padding =3D value;=0A= }=0A= else if (name =3D=3D "padding-bottom") {=0A= e.style.paddingBottom =3D value;=0A= }=0A= else if (name =3D=3D "padding-left") {=0A= e.style.paddingLeft =3D value;=0A= }=0A= else if (name =3D=3D "padding-right") {=0A= e.style.paddingRight =3D value;=0A= }=0A= else if (name =3D=3D "padding-top") {=0A= e.style.paddingTop =3D value;=0A= }=0A= else if (name =3D=3D "page-break-after") {=0A= e.style.pageBreakAfter =3D value;=0A= }=0A= else if (name =3D=3D "page-break-before") {=0A= e.style.pageBreakBefore =3D value;=0A= }=0A= else if (name =3D=3D "pixelBottom") {=0A= e.style.pixelBottom =3D value;=0A= }=0A= else if (name =3D=3D "pixelHeight") {=0A= e.style.pixelHeight =3D value;=0A= }=0A= else if (name =3D=3D "pixelLeft") {=0A= e.style.pixelLeft =3D value;=0A= }=0A= else if (name =3D=3D "pixelRight") {=0A= e.style.pixelRight =3D value;=0A= }=0A= else if (name =3D=3D "pixelTop") {=0A= e.style.pixelTop =3D value;=0A= }=0A= else if (name =3D=3D "pixelWidth") {=0A= e.style.pixelWidth =3D value;=0A= }=0A= else if (name =3D=3D "posBottom") {=0A= e.style.posBottom =3D value;=0A= }=0A= else if (name =3D=3D "posHeight") {=0A= e.style.posHeight =3D value;=0A= }=0A= else if (name =3D=3D "position") {=0A= e.style.position =3D value;=0A= }=0A= else if (name =3D=3D "posLeft") {=0A= e.style.posLeft =3D value;=0A= }=0A= else if (name =3D=3D "posRight") {=0A= e.style.posRight =3D value;=0A= }=0A= else if (name =3D=3D "posTop") {=0A= e.style.posTop =3D value;=0A= }=0A= else if (name =3D=3D "posWidth") {=0A= e.style.posWidth =3D value;=0A= }=0A= else if (name =3D=3D "right") {=0A= e.style.right =3D value;=0A= }=0A= else if (name =3D=3D "ruby-align") {=0A= e.style.rubyAlign =3D value;=0A= }=0A= else if (name =3D=3D "ruby-overhang") {=0A= e.style.rubyOverhang =3D value;=0A= }=0A= else if (name =3D=3D "ruby-position") {=0A= e.style.rubyPosition =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-3dlight-color") {=0A= e.style.scrollbar3dLightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-arrow-color") {=0A= e.style.scrollbarArrowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-base-color") {=0A= e.style.scrollbarBaseColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-darkshadow-color") {=0A= e.style.scrollbarDarkShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-face-color") {=0A= e.style.scrollbarFaceColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-highlight-color") {=0A= e.style.scrollbarHighlightColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-shadow-color") {=0A= e.style.scrollbarShadowColor =3D value;=0A= }=0A= else if (name =3D=3D "scrollbar-track-color") {=0A= e.style.scrollbarTrackColor =3D value;=0A= }=0A= else if (name =3D=3D "float") {=0A= e.style.styleFloat =3D value;=0A= }=0A= else if (name =3D=3D "table-layout") {=0A= e.style.tableLayout =3D value;=0A= }=0A= else if (name =3D=3D "text-align") {=0A= e.style.textAlign =3D value;=0A= }=0A= else if (name =3D=3D "text-align-last") {=0A= e.style.textAlignLast =3D value;=0A= }=0A= else if (name =3D=3D "text-autospace") {=0A= e.style.textAutospace =3D value;=0A= }=0A= else if (name =3D=3D "text-decoration") {=0A= e.style.textDecoration =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationBlink") {=0A= e.style.textDecorationBlink =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationLineThrough") {=0A= e.style.textDecorationLineThrough =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationNone") {=0A= e.style.textDecorationNone =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationOverline") {=0A= e.style.textDecorationOverline =3D value;=0A= }=0A= else if (name =3D=3D "textDecorationUnderline") {=0A= e.style.textDecorationUnderline =3D value;=0A= }=0A= else if (name =3D=3D "text-indent") {=0A= e.style.textIndent =3D value;=0A= }=0A= else if (name =3D=3D "text-justify") {=0A= e.style.textJustify =3D value;=0A= }=0A= else if (name =3D=3D "text-kashida-space") {=0A= e.style.textKashidaSpace =3D value;=0A= }=0A= else if (name =3D=3D "text-overflow") {=0A= e.style.textOverflow =3D value;=0A= }=0A= else if (name =3D=3D "text-transform") {=0A= e.style.textTransform =3D value;=0A= }=0A= else if (name =3D=3D "text-underline-position") {=0A= e.style.textUnderlinePosition =3D value;=0A= }=0A= else if (name =3D=3D "top") {=0A= e.style.top =3D value;=0A= }=0A= else if (name =3D=3D "unicode-bidi") {=0A= e.style.unicodeBidi =3D value;=0A= }=0A= else if (name =3D=3D "vertical-align") {=0A= e.style.verticalAlign =3D value;=0A= }=0A= else if (name =3D=3D "visibility") {=0A= e.style.visibility =3D value;=0A= }=0A= else if (name =3D=3D "white-space") {=0A= e.style.whiteSpace =3D value;=0A= }=0A= else if (name =3D=3D "width") {=0A= e.style.width =3D value;=0A= }=0A= else if (name =3D=3D "word-break") {=0A= e.style.wordBreak =3D value;=0A= }=0A= else if (name =3D=3D "word-spacing") {=0A= e.style.wordSpacing =3D value;=0A= }=0A= else if (name =3D=3D "word-wrap") {=0A= e.style.wordWrap =3D value;=0A= }=0A= else if (name =3D=3D "writing-mode") {=0A= e.style.writingMode =3D value;=0A= }=0A= else if (name =3D=3D "z-index") {=0A= e.style.zIndex =3D value;=0A= }=0A= else if (name =3D=3D "zoom") {=0A= e.style.zoom =3D value;=0A= }=0A= }=0A= catch (e) {=0A= /* ignore error on attempt to set e.style.[property] */=0A= }=0A= }=0A= }=0A= }=0A= ------=_NextPart_000_004B_01C87610.AA478FB0 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/javascript/entrez/callback.js /************************************************************************= *****=0A= * javascript/entrez/callback.js=0A= *=0A= * Entrez Linking callback to populate content box.=0A= *=0A= * Copyright 2006 Board of Trustees of the Leland Stanford Junior = University.=0A= = *************************************************************************= ***/=0A= =0A= /*=0A= * Execute callback to fill content box with Entrez Linking information.=0A= */=0A= function entrez_callback(pmid, callback_url) {=0A= /*=0A= * MSIE 5.5 and below have issues with the JavaScript=0A= * used for Entrez Linking. 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