From: Subject: Transmembrane Protein 18 Enhances the Tropism of Neural Stem Cells for Glioma Cells -- Jurvansuu et al. 68 (12): 4614 -- Cancer Research Date: Tue, 8 Jul 2008 19:58:40 +0200 MIME-Version: 1.0 Content-Type: multipart/related; type="text/html"; boundary="----=_NextPart_000_0014_01C8E135.04708B60" X-MimeOLE: Produced By Microsoft MimeOLE V6.00.2900.5512 This is a multi-part message in MIME format. ------=_NextPart_000_0014_01C8E135.04708B60 Content-Type: text/html; charset="iso-8859-1" Content-Transfer-Encoding: quoted-printable Content-Location: http://cancerres.aacrjournals.org/cgi/content/full/68/12/4614 Transmembrane Protein 18 Enhances the Tropism of = Neural Stem Cells for Glioma Cells -- Jurvansuu et al. 68 (12): 4614 -- = Cancer Research 3D"Cancer 3D"
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Cell, Tumor, and Stem Cell = Biology

Transmembrane Protein 18 Enhances the Tropism of Neural Stem Cells = for=20 Glioma Cells

Jaana = Jurvansuu1,=20 Ying Zhao1,2, Doreen S.Y.=20 Leung1, Jerome Boulaire1, = Yuan=20 Hong Yu3,4, Sohail=20 Ahmed3,4 and Shu=20 Wang1,2

1 Institute of Bioengineering and = Nanotechnology;=20 Departments of 2 Biological Sciences and 3 = Physiology,=20 National University of Singapore; 4 Institute of Medical = Biology,=20 Singapore, Singapore

Requests for reprints: Shu Wang, Institute of=20 Bioengineering and Nanotechnology, Singapore 138669, Singapore. Phone:=20 65-6824-7105; Fax: 65-6478-9083; E-mail: swang{at}ibn.a-star.edu.sg .


3D"   =20 Abstract
Top
3D"Abstract
Introduction
Materials and Methods
Results
Discussion
Disclosure of Potential...
References
 
T= he=20 failure of current glioma therapies is mainly due to the = ability of=20 the tumor cells to invade extensively the surrounding healthy = brain=20 tissue, hence escaping localized treatments. Neural stem = cells (NSC)=20 are able to home in on tumor foci at sites distant from the = main=20 tumor mass, possibly enabling treatment of scattered glioma = clusters.=20 To make the strategy more effective, we performed a cDNA = expression=20 library screening to identify the candidate genes that once=20 overexpressed would enhance the tropism of NSCs for gliomas. = Here, we=20 show that a previously unannotated gene, the one encoding=20 transmembrane protein 18 (TMEM18), is one such gene. = Overexpression=20 of TMEM18 was seen in the current study to provide NSCs and = neural=20 precursors an increased migration capacity toward = glioblastoma cells=20 in vitro and in the rat brain. Functional inactivation = of the=20 TMEM18 gene resulted in almost complete loss of the = migration=20 activity of these cells. Thus, TMEM18 is a novel cell = migration=20 modulator. Overexpression of this protein could be favorably = used in=20 NSC-based glioma therapy. [Cancer Res = 2008;68(12):4614=9622]=20


3D"   =20 Introduction
Top
Abstract
3D"Introduction
Materials and Methods
Results
Discussion
Disclosure of Potential...
References
 
G= lioma=20 cells misregulate the expression of growth factors, proteases, = and=20 extracellular matrix and cell surface proteins to gain their=20 devastating invasion capacity (1,=20 2).=20 Localized treatments are thus inefficient and comprehensive=20 treatments are too damaging to the delicate brain. A solution = is to=20 find a treatment that can specifically locate the tumor = cells. Neural=20 stem cells (NSC) and neural precursor cells (NPC) have an = intrinsic=20 tropism for sites of brain injuries, including gliomas, and = as shown=20 first by Benedetti and colleagues (3)=20 and Aboody and colleagues (4),=20 engrafted primary and immortalized NSCs can be used in gene=20 therapy of gliomas in animal models. These engrafted stem = cells=20 have been shown to spread through the existing migratory = pathways=20 in healthy brain as well as nontypical routes when gliomas = are=20 present (4,=20 5).=20 Besides primary and immortalized NSCs/NPCs, embryonic stem=20 cell=96derived NPCs seem to have the same aptitude for glioma = cell=20 tracking (6).=20 Moreover, NSCs are able to locate not only gliomas but also = tumors of=20 a nonneural origin, suggesting that there exist common = regulators of=20 cell trafficking probably composed of secreted factors from a = tumor=20 site and receptors present on NSCs (7,=20 8).=20

Candidate signals to attract NSCs to the sites of brain injuries = and tumors have been studied. Among them are cytokines = released=20 from the immunoreactive microglial cells of the brain during=20 inflammation (9),=20 which also provide cues for NSC migration in brain = development (10).=20 Stromal cell=96derived factor-1 (SDF-1) chemokine can attract = NSCs too.=20 When its receptor CX chemokine receptor 4 (CXCR4) is blocked, = SDF-1=20 hinders the NSC migration to the site of injury (9,=20 11,=20 12).=20 In addition, chemokine monocyte chemoattractant protein-1, = the=20 expression of which can be induced by tumor necrosis = factor-,=20 can activate migration of NSCs (13).=20 Cytokine stem cell factor, expressed by glioma cell lines and = overexpressed in neurons at the sites of brain injury, is = another=20 possible contributing attractant for NSCs (14=9616).=20 Similar to cytokines and chemokines, growth factor=96mediated = signaling=20 [e.g., vascular endothelial growth factor and epidermal = growth factor=20 (EGF) receptor] has been shown to regulate NSC and NPC = migration (17,=20 18).=20 Glioma invasion depends largely on the ability of the cell to = modify=20 the extracellular matrix, and interestingly, the = extracellular matrix=20 secreted from glioma cell lines is able to promote NSC = motility (19).=20

The picture emerging from the above studies seems to support = a=20 model of the complex interaction of several factors in regulating = NSC=20 migration toward tumors. We hypothesized that other regulators = are=20 likely to exist and their genes can be identified through = expression=20 cloning based on gene function in influencing the tropism of = NSCs=20 toward glioma cells. We were particularly interested in the = molecules=20 that once overexpressed in NSCs and NPCs are able to enhance = cell=20 migration toward gliomas, as the manipulation of the = expression of=20 these molecules could then facilitate the use of NSCs/NPCs as = gene=20 therapy vectors to reach scattered glioma cells. We used = Boyden=20 chambers in the current study to select the cells that were = primed by=20 gene transfer of a tumor cDNA expression library. A novel = gene=20 encoding transmembrane protein 18 (TMEM18) emerged from the = screen=20 and was selected for extensive characterizations.


3D"   =20 Materials and Methods
Top
Abstract
Introduction
3D"Materials and = Methods
Results
Discussion
Disclosure of Potential...
References
 
<= B>Cells.=20 NT2, U87MG, H4, and NIH3T3 cell lines were purchased from the = American Type Culture Collection and HEK293FT cells were = purchased=20 from Invitrogen. All the cell lines were maintained in DMEM=20 supplemented with 10% FCS (Life Technologies), = penicillin-streptomycin=20 (Life Technologies), normoxin (Invivogen), and nonessential=20 amino acids (Life Technologies). C17.2 cells were kindly = provided=20 by Prof. E. Arenas (Department of Medical Biochemistry and=20 Biophysics, Karolinska Institute, Stockholm, Sweden) and = maintained=20 in DMEM supplemented with 10% FCS, 5% horse serum (Life=20 Technologies), penicillin-streptomycin, normoxin, and = nonessential=20 amino acids. The NIH Human Embryonic Stem Cell Registry = listed human=20 embryonic stem (hES) cell line, HES-1, and its feeder cell=20 K4 mouse embryonic fibroblasts were obtained from = ES Cell=20 International (ESI), Singapore. The hES cells were amplified = and=20 maintained according to the protocol provided by ESI. = Embryoid bodies=20 and neural spheres from hES cells were generated as = previously=20 described (20).=20

Primary murine NSCs and NPCs were isolated from the embryonic=20 forebrain of C57BL/6 mice. The treatment of animals was = performed=20 in accordance with the Guidelines for the Care and Use of = Laboratory=20 Animals of our institution. Pregnant C57BL/6 mice at the = specified=20 gestational age of 14 d (E14) were killed via cervical = dislocation=20 and the uteri were aseptically removed. Fetuses were removed=20 from the amniotic sac and transferred to a Petri dish = containing=20 ice-cold HBSS. Cortices were rapidly excised from the fetuses = and mechanically dissociated by pipetting into a single-cell=20 suspension. Cells were plated at a density of 2 x 105/mL into 10-cm = culture=20 dishes (Nunc) in DMEM/nutrient mixture F-12 (1:1) mixture = medium=20 (Invitrogen) containing B27 supplement (Invitrogen), 20 ng/mL = basic=20 fibroblast growth factor (Sigma-Aldrich), 20 ng/mL EGF = (Invitrogen),=20 and 1% penicillin-streptomycin (Invitrogen). Floating = neurospheres=20 with diameter range between 150 and 250 =B5m were passaged = every 6 to 7=20 d. The multipotency of the cells was confirmed by = immunocytochemical=20 analysis after differentiation into three fundamental = lineages in=20 central nervous system (neurons, astrocytes, and=20 oligodendrocytes).

cDNA expression library screening. Human Daudi cell cDNA = library=20 containing retrovirus supernatants was purchased from = Stratagene=20 and used as recommended by the supplier. One million of NT2=20 cells were infected with the cDNA library retrovirus = supernatants=20 to yield 20% infection efficiency to ensure a proper = presentation=20 of all the cDNAs in the library. Cells were allowed to = recover=20 for 4 d, after which they were selected in Transwell = migration=20 assays using Boyden chambers as described below. Migrating = cells=20 were collected and let to recover for 5 d before the next = migration=20 assay. After three rounds of the migration assays, both = nonmigrating=20 and migrating cells were collected.

For analysis of virus-imported cDNAs, chromosomal DNA was = purified=20 from nonmigrating or migrating cells using DNeasy kit = (Qiagen)=20 as recommended by the manufacturer. Retrovirus-imported = sequences=20 were recovered according to a PCR protocol suggested in = ViraPort=20 manual (Stratagene). Same amount of chromosomal DNA was used = in=20 PCR for nonmigrating and migrating cells. The success of the = PCR was=20 verified by running aliquots of the reactions on an agarose = gel. PCR=20 products were subsequently cloned into pDrive using TA = Cloning kit=20 (Qiagen). DH53D{alpha}=20 = Escherichia=20 coli cells were transformed with the cloning products and = plated.=20 After overnight incubation, bacterial clones were picked and = plasmid=20 DNA was isolated and then subsequently used in PCR using the = same=20 conditions as previously described to isolate individual = sequences=20 for sequencing.

Overexpression and gene silencing. TMEM18 was cloned = from=20 Human Daudi cell cDNA library infected cells by PCR using=20 primers 5'-caccatgccgtccgccttctctg and=20 5'-aaagtcttctttccttctccttttc into pLenti6/V5-TOPO vector = (Invitrogen)=20 followed by sequencing to ensure that the cloned sequence was = correct. TMEM18A virus contained one amino acid mutation from = alanine=20 to threonine at position 103, which did not seem to have any = effect=20 in later experiments. Empty and TMEM18 lentiviruses were = produced=20 using ViraPower Lentiviral Directional TOPO Expression kit=20 (Invitrogen). Virus transduction in NT2 and C17.2 cells to = express=20 TMEM18, cell selection for stable expression, and cell = maintenance=20 were carried out as recommended by the manufacturer=20 (Invitrogen). The titer of lentivirus infection was = controlled to=20 have one virus per cell. For TMEM18 overexpression in primary = murine NSCs/NPCs, neural spheres were dissociated on the day = of=20 transfection, and plasmid DNA pLenti/V5-TMEM18 was = transfected into=20 the cells with Lipofectamine 2000 (Invitrogen) according to = the=20 manufacturer's protocol. pLenti/V5-eGFP plasmid was used as a = vector=20 control. Thirty hours after the transfection, cells were = collected=20 for the migration assay and reverse transcription-PCR = (RT-PCR)=20 study described below.

For short interfering RNA (siRNA)-mediated TMEM18 gene = silencing,=20 two sequences, 5'-tcatcttagtctactgtgctgaata and=20 5'-tgctcacgcagacggactggactga, were cloned into = double-promoter siRNA=20 expression vector pFIV-H1/U6-PURO (System Biosciences) as = recommended=20 by the manufacturer's protocol. A siRNA sequence against=20 luciferase provided in pFIV Vector cloning kit (System = Biosciences) was used as a control. Cells were plated to = reach 90%=20 confluence on the day of transfection of the siRNA expression = plasmids, and plasmid DNA was transfected with Lipofectamine = 2000=20 according to the manufacturer's protocol. Puromycin-resistant = cells=20 were selected for 4 d, after which cells were used for = migration=20 assay and for RT-PCR study.

Reverse transcription-PCR. Cytoplasmic RNA was collected = with=20 RNeasy kit (Qiagen) as recommended by the manufacturer. The=20 concentration and purity was verified before equal amounts of = RNAs from all the samples were used to produce cDNAs by = reverse=20 transcription using oligo(T) priming of SuperScript III = First-Strand=20 Synthesis System (Invitrogen). PCR amplification for the = produced=20 cDNAs was carried out using HotStart Taq system (Qiagen) as=20 suggested by the HotStart Taq manual. Real-time PCR was done=20 using Power SYBR Green PCR master mix and protocol (Applied=20 Biosystems), with primers for TMEM18 (5'-atgccgtccgccttctctg=20 and 5'-gtcttctttccttctccttttc) and β-actin = (5'-tcatgtttgagaccttcaa=20 and 5'-gtctttgcggatgtccacg). Opticon 2 real-time PCR machine=20 (Applied Biosystems) was used to run the PCRs. The program = for=20 TMEM18 PCR was 10 min at 95=B0C followed by 45 cycles of 15 = s at=20 95=B0C followed by 1 min at 68=B0C; the program for = β-actin was 10 min at=20 95=B0C followed by 40 cycles of 10 s at 95=B0C, 20 s at = 55=B0C, and 20 s at=20 68=B0C. Real-time PCR results were presented as a ratio of = TMEM18 mRNA=20 to β-actin mRNA. CXCR4 fragment was PCR amplified using = the following=20 primers: CXCR4, 5'-CCCGATAGCCTGTGGATGGTGGTGT-3' (forward) and = 5'-AGCTTTTGAACTTGGCCCCGAGGAA-3' (reverse). PCR products were=20 separated by electrophoresis on a 2% agarose gel.

Immunostaining and Western blot analysis. Antibody against = TMEM18=20 was produced in rabbits against peptides 122 to 135: = C-DLKNAQERRKEKKR=20 (BioGenes GmbH). This peptide is unique to TMEM18 based on = BLAST=20 search. The anti-TMEM18 serum was tested using Western = blotting=20 and detected one band with molecular mass of 18 kDa, which = was=20 blocked when the serum was incubated in the presence of the=20 immunizing peptide. The serum was used in 1:200 for = immunostaining=20 and Western blot analysis. Antibody against β-actin was=20 purchased from Sigma-Aldrich and used in 1:200. Secondary = horseradish=20 peroxidase=96linked antibodies were purchased from Bio-Rad.=20 Primary antibody anti-β-III-tubulin (1:200; Promega), = anti-GFAP=20 (1:200; Sigma-Aldrich), and anti-O4 (1:100; Chemicon) were = used=20 in immunostaining of cells derived from NSCs/NPCs.=20 4',6-Diamidino-2-phenylindole (DAPI; Invitrogen-Molecular = Probes) was=20 used in concentration of 2 nmol/L.

In vitro cell migration assay. In vitro = migration of=20 NPCs toward glioma cells was examined using Boyden chamber = assays. A=20 migration kit from BD Falcon with 24-well cell culture plates = was=20 used. Each well of the plates was separated into two chambers = by=20 an insert membrane of 8-=B5m pores. One day before = assays,=20 50,000 glioma cells were seeded into each lower chamber. The=20 next day, cell culture medium in the lower chamber was = removed=20 and replaced with 500 =B5L of nonsupplemented DMEM. NSCs/NPCs = (50,000 in 500 =B5L of nonsupplemented DMEM) were then seeded = into the upper chamber. For the assay using a neutralization=20 antibody to block cell migration, 40 =B5g/mL of anti-CXCR4=20 monoclonal antibodies (R&D Systems) were incubated with=20 NSCs and NPCs for 30 min at room temperature before the cell=20 seeding. After 12 or 24 h of incubation at 37=B0C, migrating=20 cells on the bottom of the insert membrane and nonmigrating=20 cells on the upper side of the membrane were dissociated by=20 trypsination. These cells were subsequently lysed and stained = using a CyQUANT Cell Proliferation Assay kit = (Invitrogen-Molecular=20 Probes). Fluorescence was measured with a fluorescence plate=20 reader (GENios Pro, Tecan). Values from 6 to 12 wells were = expressed=20 as the mean =B1 SD in percentage control. In most of in=20 vitro migration assays, the migration of cells transduced = with=20 a vector control in response to serum-free DMEM was used as = the=20 basal migration rate. In those experiments without the use of = a=20 vector control, cell migration in response to serum-free DMEM = was=20 used as the basal migration rate. Statistical analyses were = done=20 using Student's t test.

In vivo cell migration assay. Rat C6 glioma cells (1=20 million cells in 5 =B5L) were injected into the right = striatum of=20 the rat brain (AP +1.0 mm, ML +2.5 mm, and DV =965.0 mm = from=20 bregma and dura) using a 10 =B5L Hamilton syringe connected = with a=20 30-gauge needle at a speed of 0.5 =B5L/min. Three days later, = 1.25=20 million of green fluorescent DiO dye (Invitrogen)-labeled=20 TMEM18-overexpressing C17.2 cells were mixed with the equal=20 number of red fluorescent Dil dye (Invitrogen)-labeled vector = control C17.2 cells and injected into the contralateral side = of=20 the rat brain. The brain samples were collected 3 wk later = for=20 sectioning and examination. To quantify the number of migrating = cells=20 in the migration front, red and green fluorescent cells were = counted=20 in 10 sections, with dots of yellow color being considered as = comigration of green and red cells. In the handling and care = of=20 animals, the Guidelines on the Care and Use of Animals for = Scientific=20 Purposes issued by the National Advisory Committee for = Laboratory=20 Animal Research, Singapore was followed. The experimental = protocols=20 of the current study were approved by the Institutional = Animal Care=20 and Use Committee, National University of Singapore, and = Biological=20 Resource Center, Agency for Science, Technology and Research=20 (A*STAR), Singapore.

Nuclear localization assay. Green fluorescent protein = (GFP)=20 fusion protein expression plasmids were created as instructed = in NT-GFP Fusion TOPO Expression kit manual (Invitrogen). The = TMEM18 NH2 terminus with 15 amino acid residues was = cloned=20 by PCR using primers 5'-tcagtcttctttccttctcc and=20 5'-aagaatgcacaagagagaag. TAT coding sequence was formed by = annealing=20 oligos 5'-cagcgcaaaaaacgccgccagcgccgctaga and=20 5'-ctagcggcgctggcggcgttttttgcgctga. Plasmid constructs generated = were=20 sequenced to confirm GFP fusion and transfected into U87MG = cell by=20 Lipofectamine.


3D"   =20 Results
Top
Abstract
Introduction
Materials and Methods
3D"Results
Discussion
Disclosure of Potential...
References
 
<= B>TMEM18=20 is a novel modulator identified by cDNA expression library = screening=20 for the genes that promote glioma-directed stem cell = migration.=20 To identify genes that promote the migration of stem cells = toward=20 glioma cells, we performed cDNA expression library screening. = A cDNA=20 library derived from the Daudi Burkitt lymphoma cell line was = used=20 for expression cloning, in view of the capacity of the cells = to=20 invade locally and to metastasize via mechanisms similar to = those=20 developed by solid tumors (21,=20 22).=20 Retrovirus vectors were used to transduce the cDNA library = into human=20 NPC line NT2. The transduced cells were evaluated = subsequently=20 for their glioma-directed migration ability in a Transwell = cell=20 migration assay using Boyden chambers. In the assay, = nonmigrating=20 cells stayed on the top of the membrane, whereas cells that=20 were primed to migrate went through 8-=B5m pores into the=20 opposite site of the Transwell insert membrane. Migrated = cells=20 were isolated and passed through two more rounds of the = migration=20 assay selection, after which virus-imported cDNAs in = migrating=20 cells were cloned by PCR and identified by sequencing. The = protocol=20 is summarized in Supplementary Fig. S1A. Nonmigrating = cells=20 were used as controls for the cDNA analysis.

We sequenced 70 virus-imported cDNA clones from migrating cells=20 and 46 clones from nonmigrating cells and identified several=20 cDNAs that express proteins capable of enhancing the tropism = of=20 NT2 cells for glioma cells. Among the clones collected from = the=20 migrating cells for sequence analysis, two were found to = encode for=20 TMEM18, whereas no clone from the nonmigrating cells had=20 virus-imported TMEM18 gene sequence. TMEM18 was thus a = promising=20 candidate for further analysis for its role in regulating NSC = migration.

Overexpression of TMEM18 enhances the glioma-specific = migration=20 ability of NSCs/NPCs. To verify the above finding, we=20 investigated whether the overexpression of the TMEM18 = cDNA in=20 NT2 human NPCs, C17.2 murine NSCs, and primary NSCs/NPCs = isolated=20 from the mouse embryo forebrains at the 14th day would affect = the=20 migration. We used lentiviral vectors to create stable cell = lines=20 overexpressing TMEM18 in NT2 and C17.2 cells. Two populations = of=20 stable cell lines that express different levels of TMEM18 = were=20 selected from each type of NPCs. We also used transfection to = overexpress TMEM18 in primary NSCs/NPCs. TMEM18 = overexpression was=20 confirmed using RT-PCR (Supplementary Fig. S2).

We used Boyden chamber assay to examine the movement of the = above=20 TMEM18-overexpressing cells toward human U87MG glioma cells, = the same=20 tumor cell line that was used in the cDNA expression library=20 screening earlier. TMEM18-overexpressing NT2 cells, C17.2 = cells, and=20 primary NSCs/NPCs displayed significantly higher migration = capacities=20 when compared with their parental cells and empty vector = controls (Fig.=20 1 for NT2 and C17.2 cells and Fig.=20 2 for primary NSCs/NPCs). These cells also responded to = other=20 glioma cell lines, H4 and C6, by displaying significant = migration=20 advantage over control cells (Figs.=20 1B and F and 2A).=20 Interestingly, the TMEM18-overexpressing NT2 cells did not = change=20 their migration capacities when nontumor cell lines, mouse = fibroblast=20 cell line NIH3T3 and human kidney cell line HEK293FT, were = seeded=20 in the bottom chamber in the assays (Fig.=20 1C and D). TMEM18 overexpression did not = change the=20 migration of primary NSCs/NPCs toward HEK293FT either. = Moreover, the=20 amount of cells migrating to plain DMEM cell culture medium = remained=20 similar between the TMEM18-overexpressing cells and the = controls (Fig.=20 1). Hence, the preference of TMEM18-overexpressing cells = for=20 glioma cells implies a role for the protein in response to=20 glioma-secreted factors.



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  = 		Figure 1. TMEM18 = overexpression=20 increases the migration activity of NT2 human NPCs = (A) and=20 C17.2 murine NSCs (B) in Boyden chamber assays.=20 Columns, percentage of vector control; bars, = SD.=20 Statistical comparisons are calculated between cells = overexpressing=20 TMEM18 and vector controls using Student's t test. *, = P < 0.05; **, P < 0.01; ***, P = <=20 0.001. =

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  = 		Figure 2. Effects of = TMEM18=20 overexpression on NSCs/NPCs. A, TMEM18 overexpression = increases the migration activity of primary NSCs/NPCs in = Boyden=20 chamber. Columns, percentage of vector control; = bars,=20 SD. Statistical comparisons are calculated between cells=20 overexpressing TMEM18 and vector controls using Student's = t=20 test. *, P < 0.05; **, P < 0.01. = B,=20 glioma-tracking cells of TMEM18-overexpressing NSCs/NPCs in = Boyden=20 chamber assay are mainly astrocytic precursors. Top,=20 phase-contrast and fluorescence images show the transfection = efficiency of control plasmid pLenti/V5-eGFP; bottom, = immunostaining using antibodies against β-tubulin, = GFAP, and O4=20 (green). DAPI (blue) was used to counterstain = nuclei.=20 Note that the cells derived from migrating = TMEM18-overexpressing=20 NSCs/NPCs were stained strongly with anti-GFAP. =

 = ;
Primary=20 NSCs/NPCs isolated from E14 mouse forebrains are a heterogenous=20 population with multipotency, each of subpopulations capable = of=20 giving rise to specific type of neural cells. To understand = whether=20 TMEM overexpression has any specific effect on the migration = of a=20 particular subtype of NSCs/NPCs, we examined the differentiation=20 ability of the primary cells, migrating TMEM18-overexpressing = NSCs/NPCs collected on the bottom of the insert membrane of = the=20 Boyden chamber, and nonmigrating cells on the upper side of = the=20 membrane. Although there was no obvious difference in cell = type=20 distribution between the cells derived from primary NSCs/NPCs = and the=20 cells from nonmigrating TMEM18-overexpressing NSCs/NPCs, the = cells=20 derived from migrating TMEM18-overexpressing NSCs/NPCs = displayed=20 morphologic features typical of astrocytes and were strongly = positive=20 for GFAP, a marker for astroglial precursors and astrocytes = (Fig.=20 2B). The cells derived from migrating NSCs/NPCs = were=20 negative for O4, a marker for oligodendrocytes, and only = weakly=20 stained with anti-β-III-tubulin, a marker for neurons. = These results=20 indicate that glioma-tracking populations of = TMEM18-overexpressing=20 NSCs/NPCs comprise largely of astrocytic precursors, which is = consistent with previous observations from an in vivo = study=20 reporting that the majority of NSCs that migrated along with = glioma=20 outgrowths and satellites were astrocytic precursors (23).=20

Encouraged by the above in vitro results, we moved on to = test=20 whether overexpression of TMEM18 would improve the migration = of=20 C17.2 murine NSCs toward gliomas in the brain. In a rat C6 = glioma=20 xenograft model, green fluorescent dye=96labeled = TMEM18-overexpressing=20 C17.2 cells were injected together with red fluorescent = dye=96labeled=20 vector control C17.2 cells on the side of the brain = contralateral to=20 the tumor inoculation site. Three weeks after the injection, = the=20 brain samples were collected for examination. As shown in Fig.=20 3 , the labeled green and red cells migrated together = (exhibited=20 a yellow color in Fig.=20 3E) toward the tumor site and about half of them had=20 already crossed the middle line of the brain by week 3. At = the=20 front of the migrating cells, many cells with green = fluorescence=20 only were observed. The brain sections around the front = region=20 were evaluated, where 3D~=2060% of = the=20 migrating cells were stained with the green fluorescent dye = and 40%=20 labeled with the red fluorescent dye. These findings suggest = an=20 improved migration of the TMEM18-overexpressing cells toward = gliomas=20 in the brain.



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  = 		Figure 3. TMEM18 = overexpression=20 increases the migration of C17.2 NSCs toward C6 glioma cells = in the=20 rat brain. Green fluorescent dye=96labeled = TMEM18-overexpressing C17.2=20 cells and red fluorescent dye=96labeled vector control C17.2 = cells=20 were mixed up and injected into the left side of the rat = brain=20 contralateral to a C6 glioma inoculation site = (right). Three=20 weeks later, the brains were sectioned for cell migration=20 examination under a fluorescence microscope. A, = migration of=20 green fluorescent dye=96labeled and red fluorescent = dye=96labeled cells=20 shown at a low magnification. The squares on the right side = in each=20 image indicate the front of cell migration toward the tumor, = which=20 were shown at a high magnification in B. C, merge of = the two=20 images in B. Dots with yellow color present green = fluorescent=20 dye=96labeled and red fluorescent dye=96labeled cells moving = together.=20 Note many of green fluorescent dye=96labeled = TMEM18-overexpressing=20 C17.2 cells (arrows) migrating alone. D,=20 quantification of fluorescent dye=96labeled C17.2 = (red) and=20 C17.2/TMEM18B (green) cells in the front of cell = migration=20 toward the C6 glioma inoculation site. ***, P < = 0.001. =

 = ;
Endogenous=20 TMEM18 is critical for the migration of NSCs/NPCs. To = determine=20 the effect of endogenous TMEM18 in regulating NSC migration, = we used=20 RNA interference approach to reduce the expression of TMEM18 = in NT2=20 cells. Puromycin-resistant siRNA expression vector was = constructed to=20 express siRNA sequences against TMEM18 and against the = luciferase gene (as a siRNA control). Two different=20 transductions with two siRNA constructs against TMEM18 in = NT2=20 cells yielded four populations with different levels of = reduction=20 of TMEM18 mRNA expression, ranging from 31%, 35%, 37% to 65% = of=20 the original endogenous TMEM18 mRNA level (Fig.=20 4A ). In a 24-h Boyden chamber assay, siRNAs = against=20 TMEM18 displayed strong inhibitory effects on the = migration of=20 NT2 cells when compared with cells transfected with plasmids=20 expressing siRNA against the luciferase gene (Fig.=20 4B). Reduction in the amount of TMEM18 mRNA = to 60%=20 of the normal levels lowered the number of cells migrating = toward=20 glioma cells to 3D~50% of the control. Further reduction of = TMEM18 mRNA=20 expression to 31% of the normal level in NT2 cells almost = abolished=20 the cell migration ability completely (Fig.=20 4B). Moreover, down-regulation of TMEM18 comparably=20 reduced cell migration toward plain DMEM as well (Fig.=20 4B), suggesting that TMEM18 is an important factor = regulating general cell motility.



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  = 		Figure 4. Endogenous = TMEM18=20 expression affects cell migration. A, siRNAs against=20 TMEM18 transcripts reduced the expression of = TMEM18=20 transcripts in NT2 cells, as quantified by real-time PCR. = Two=20 different sequences of siRNAs against TMEM18 were = tested in=20 NT2 cells and yielded four different knockdown levels of the = TMEM18 mRNA. siRNA against luciferase was used = as a=20 control. B, silencing endogenous TMEM18 expression = reduced=20 the migration activity of NSCs/NPCs toward both DMEM and = U87MG.=20 C and D, neural differentiation of hES cells = was=20 accompanied by progressive increase in TMEM18 mRNA = expression=20 and cell migration toward glioma cells. Columns, = percentage=20 of control; bars, SD. Statistical comparison is = calculated=20 between cells with down-regulated TMEM18 and controls using=20 Student's t test. *, P < 0.05; **, P = <=20 0.01; ***, P < 0.001. =

 = ;
The=20 effect of endogenous TMEM18 on the movement was also studied = in hES=20 cell-derived NPCs. Along with the differentiation of hES = cells into=20 embryoid body and neural sphere, TMEM18 mRNA = expression=20 increased (Fig.=20 4C). This increase was accompanied with an = enhanced=20 migration of cells in neural sphere toward glioma U87MG cells = (Fig.=20 4D). Taken together, these findings suggest that = the=20 expression of endogenous TMEM18 at a physiologic level is = crucial to=20 the migration capacity of NP/NSCs.

Up-regulation of CXCR4 by TMEM18 mediates the glioma-specific = migration capacity of NSCs/NSCs. In view of the importance = of=20 the CXCR4 that governs the migration of stem cells toward = gliomas=20 (24),=20 we investigated whether TMEM18 would affect its expression in = NSCs/NPCs. We observed that, although weak CXCR4 expression=20 was visible in parental NT2 and C17.2 cells as well as their=20 vector controls, overexpression of TMEM18 seemed to raise its = expression levels in NT2 cells, C17.2 cells, and primary = NSCs/NPCs=20 (Fig.=20 5A ). Using an antibody against CXCR4 to block cell = surface=20 CXCR4 receptors on these cells, we further observed that the=20 tropism of these TMEM18-overexpressing cells toward U87MG = cells=20 was inhibited drastically in Boyden chamber assays and the = number=20 of migrating cells went down to a level close to that of = basal=20 cell migration in response to serum-free DMEM (Fig.=20 5B). These results suggest that up-regulation of = CXCR4 in=20 TMEM18-overexpressing cells might be one possible mechanism=20 underlying the augmented glioma tropism of these cells. =



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  = 		Figure 5. CXCR4 = expression mediates=20 NSC migration toward glioma cells. A, RT-PCR shows = increased=20 levels of CXCR4 mRNA transcripts in TMEM18-overexpressing = NT2 cells,=20 C17.2 cells, and primary NSCs/NPCs. B, addition of an = anti-CXCR4 neutralization antibody significantly decreased = NSC and=20 NPC migration toward U87 glioma cells compared with cells = treated=20 with nonspecific isotype IgG. Columns, percentage of = the DMEM=20 control; bars, SD. **, P < 0.01; ***, = P <=20 0.001. =

 = ;
The=20 NLS sequence of TMEM18 is sufficient for nuclear targeting. = To=20 uncover the cellular localization of TMEM18, a polyclonal = antibody=20 against TMEM18 COOH-terminal peptide was produced. The = activity and=20 specificity of the antibody were examined using cellular=20 immunostaining and Western blot analysis (Supplementary Fig. = S2). In=20 NT2 cells, preimmunization serum produced almost no signal, = whereas=20 the serum against TMEM18 gave a strong immunofluorescence. = Western=20 blot analysis with the serum revealed both endogenous and=20 overexpressed TMEM18 with molecular mass of 18 kDa. The bands = disappeared when the serum was incubated in the presence of = the=20 immunizing peptide (data not shown).

The TMEM18 antibody stained the cytoplasm of NT2 cells, with=20 intensive staining in the perinuclear area (Fig.=20 6A and B ). In comparison with cytoskeletal = structures stained with an 3D{alpha}=20-tubulin=20 antibody (Fig.=20 6B, green), TMEM18 was localized only partly with = the=20 areas of the tubulin network (Fig.=20 6B, yellow). Several structures within the nucleus = were=20 also positively stained (Fig.=20 6B). With a closer look, the TMEM18 antibody = recognized a=20 ring structure superimposed on the nucleus, presumably the = nuclear=20 membrane (Fig.=20 6B). This structure became even clearer when the TMEM18=20 immunofluorescence staining was overlaid with nuclear = staining=20 (Fig.=20 6B, blue).



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  = 		Figure 6. Cellular = localization of=20 TMEM18 and the function of its NLS. A and B, = cellular=20 localization of TMEM18 protein. NT2 cells were stained = against=20 TMEM18 (A and B, red), 3D{alpha}=20-tubulin (B, green), and DNA (B, = blue).=20 B, superimposition of TMEM18, DNA, and 3D{alpha}=20-tubulin. The immunostaining reveals the nuclear = membrane=20 (a ring structure around the nucleus in A and = B)=20 recognized by the TMEM18 antibody. C, GFP fusion = protein with=20 NH2 terminus of TMEM18 is localized to the = nucleus. U87=20 cells were transfected with plasmid vectors expressing GFP, = TMEM18=20 NH2-terminal=96linked GFP (GFP-KED), or = HIV=20 TAT-linked GFP (GFP-TAT). Left, light = microscope=20 pictures of the cells; right, fluorescence microscope = pictures of the cells. =

 = ;
As=20 TMEM18 contains a putative NLS sequence (Supplementary Fig.=20 S1C), we tested whether it was effective in directing = nuclear=20 location in U87MG cells using a GFP fusion protein approach.=20 Transfection of the control GFP plasmid in U87MG cells led to = green fluorescent signals all over the cells, in both the = nucleus=20 and the cytoplasm (Fig.=20 6C, GFP). This was expected because the small size = of GFP=20 (30 kDa) permits diffusion between the nucleus and the = cytoplasm.=20 Noticeably, transfection with a plasmid vector encoding a = hybrid=20 protein composed of GFP linked to the putative NLS at the = COOH=20 terminus of TMEM18 (KED) resulted in significant accumulation = of=20 fluorescent signals in the cell nucleus (Fig.=20 6C, GFP-KED). The TMEM18 KED peptide seemed as = effective=20 as TAT peptide (Fig.=20 6C, GFP-TAT), a well-established nuclear = localization=20 signal peptide, in directing GFP into the nucleus. In = addition,=20 diffuse fluorescence signals were detectable in these U87MG = cells=20 transfected with the fusion genes.


3D"   =20 Discussion
Top
Abstract
Introduction
Materials and Methods
Results
3D"Discussion
Disclosure of Potential...
References
 
W= e have=20 described in this report the identification and characterization = of a=20 novel cell motility modulator TMEM18. TMEM18 was first = identified in=20 a screen to discover membrane spanning proteins (25).=20 There have been no other publications on this protein since. = The=20 functional importance of this protein is highlighted in the = strong=20 amino acid conservation throughout mammalians and even = reaching to=20 lower forms of multicellular eukaryotes. Furthermore, = according to=20 the profile of TMEM18 expressed sequence tags (EST), the = protein is=20 transcribed in embryonic developmental states and in many of = the=20 adult human tissues (National Center for Biotechnology = Information's=20 EST expression profile viewer). Clearly, TMEM18 has a crucial = biological function. Based on our results, this function = would=20 probably be linked to cell mobility. In particular, with = respect to=20 tumor therapy, TMEM18 can be used as a specific enhancer for=20 glioma-directed migration of NSCs.

The results that TMEM18-overexpressing cells and control cells=20 migrated at the same rate in plain cell culture medium or = toward=20 nonglioma cells (NIH3T3 mouse fibroblast and 293T human = embryonic=20 kidney cells) suggest that TMEM18 overexpression provided no=20 beneficial effects on the general movement of NSCs. However,=20 knockdown of endogenous TMEM18 expression with RNA = interference=20 had enormous inhibitory effects on the overall movement of = NSCs.=20 The effect seemed much stronger than that induced by TMEM18=20 overexpression. It is worthy of noting that, as determined by = our quantitative real-time PCR experiments, TMEM18 mRNA is=20 low-abundant transcripts and could be functionally sensitive = to=20 siRNA-mediated gene silencing. Furthermore, along with the = increase=20 of TMEM18 expression from an undetectable level to an easily=20 detectable level when hES cells differentiated into NPCs, = these=20 NSCs/NPCs displayed an increased capacity of cell migration = (Fig.=20 4C and D). These findings indicate a = crucial role=20 of the basal, physiologic level expression of TMEM18 for cell = movement, which is well consistent with the highly conserved = and=20 ubiquitously expressed pattern of TMEM18.

Most interestingly, TMEM18 overexpressing cells respond strongly = to glioma cell=96secreted cues in both in vitro = Transwell=20 assays and an in vivo migration experiment. Although both=20 RT-PCR and Western blot yielded unidirectional results in the = increase of TMEM18 expression in the current study, mismatch = in=20 terms of increase level is obvious. A discrepancy between=20 transcription and translation is not an uncommon phenomenon. = A recent=20 article has indicated that the correlation between mRNA and=20 protein expression is moderately or weekly positive, with=20 correlation coefficients ranging from 0.2 to 0.6 (26).=20 This can be most plausibly explained by the observation that = mRNA and=20 protein are synthesized with independent mechanisms and = degraded=20 by different pathways. In Transwell assays, cells will have = to=20 force themselves through holes in Boyden chamber membrane = that=20 are smaller than the normal size of a cell body. It could be=20 even more difficult for cells to migrate to a target site in=20 the brain where cell migration needs to overcome numerous=20 extracellular interactions. We thus conclude that TMEM18=20 overexpression increases the sensitivity of NSCs to = appropriate=20 signals that stimulate cell migration. In other words, = without=20 appropriate cues, TMEM18 overexpression will have = undetectable=20 effects on the movement of NSCs.

TMEM18 is expected to be a transmembrane protein. But it did = not=20 seem to be located to outer cell membrane, as would be expected = for=20 example for chemokine receptors, nor was it spread to cover=20 cytoskeletal structures that would affect cell movement = directly.=20 TMEM18 is predicated to possess a NLS sequence at the COOH = terminus.=20 NLS sequences occur in a subset of soluble nuclear proteins=20 that are imported into the cell nucleus by transport = receptors.=20 Membrane proteins with NLS-like sequences are found in the = majority=20 of mammalian inner nuclear membrane (INM) proteins (27).=20 A recent study in budding yeast shows that NLS sequences are=20 essential for passage of integral membrane proteins through = the=20 nuclear pore complex and receptor-mediated transport of the=20 proteins to the INM (28).=20 Further studies are warranted to assess whether TMEM18 is = really=20 located along the inside of the nuclear envelope.

Cell motility is a highly complex process and involves several=20 factors, from sensing of environmental cues, restructuring = the=20 cytoskeleton, dynamic regulation of cell attachment and = detachment=20 to extracellular matrix, to signaling between all these = processes=20 to coordinate the movements. Hence, there are many steps = downstream=20 of chemoattractant receptor signaling that can affect cell = movement=20 and migration. Bioinformatics searches for protein domains = did=20 not reveal any informative features related to a possible = biochemical=20 function of TMEM18. Our preliminary data on the up-regulation = of CXCR4 in TMEM18-overexpressing cells and inhibiting cell=20 migration by antibodies against CXCR4 suggest an enhanced = effect=20 of the SDF-1/CXCR4 axis by TMEM18. Further research is = necessary=20 to define the basic mechanisms underlying the effects of = endogenous=20 TMEM18 on general cell migration and the effects of = overexpressed=20 TMEM18 to enhance cell response to migration-stimulating = signals.=20 An adequate understanding of these mechanisms could have = important=20 implications for effective cellular delivery of therapeutic=20 agents for brain tumor therapy.


3D"   =20 Disclosure of Potential Conflicts of Interest =
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
3D"Disclosure of = Potential...
References
 
N= o=20 potential conflicts of interest were disclosed.


3D"   =20 Acknowledgments =
 
Grant support:=20 Institute of Bioengineering and Nanotechnology, Agency for = Science,=20 Technology and Research (A*STAR) in Singapore.

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 the lab members for helpful discussion and support. =


3D"   =20 Footnotes
 
Note: Supplementary data for this = article are=20 available at Cancer Research Online (http://cancerres.aacrjournals= .org/).=20

J. Jurvansuu and Y. Zhao contributed = equally to=20 this work.

Received 9/13/07. Revised 3/28/08. Accepted 3/31/08.


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

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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_0014_01C8E135.04708B60 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 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=0A= }=0A= function _uGT() {=0A= var h=3Dlocation.hash, a;=0A= if (h && h!=3D"" && h.indexOf("#gaso=3D")=3D=3D0) {=0A= a=3D_uGC(h,"gaso=3D","&");=0A= } else {=0A= a=3D_uGC(_ubd.cookie,"GASO=3D",";");=0A= }=0A= return a;=0A= }=0A= var _utk=3D_uGT();=0A= if (_utk && _utk!=3D"" && _utk.length>10 && _utk.indexOf("=3D")=3D=3D-1) = {=0A= if (window.addEventListener) {=0A= window.addEventListener('load', _uCO, false); =0A= } else if (window.attachEvent) { =0A= window.attachEvent('onload', _uCO);=0A= }=0A= }=0A= =0A= function _uNx() {=0A= return (new Date((new Date()).getTime()+63072000000)).toGMTString();=0A= }=0A= ------=_NextPart_000_0014_01C8E135.04708B60--