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PLoS One. 2009; 4(12):=20 e8314.
Published online 2009 = December 15.=20 doi:=20 10.1371/journal.pone.0008314.
PMCID:=20 = PMC2789379
Copyright=20 Frank et al. This is an open-access article distributed under the = terms of=20 the Creative Commons Attribution License, which permits = unrestricted use,=20 distribution, and reproduction in any medium, provided the = original author=20 and source are credited.
Neural Stem Cells as a Novel Platform for=20 Tumor-Specific Delivery of Therapeutic Antibodies
Richard T.=20 Frank,1* Marissa Edmiston,1 = Stephen E.=20 Kendall,2 Joseph Najbauer,1 Chia-Wei=20 Cheung,3 Thewodros Kassa,3 Marianne Z.=20 Metz,1 Seung U. Kim,6,7 Carlotta = A.=20 Glackin,2 Anna M. Wu,5 Paul J. = Yazaki,3=20 and Karen S. Aboody1,4*
1Divisions of Hematology and = Hematopoietic=20 Cell Transplantation, City of Hope National Medical Center and = Beckman=20 Research Institute, Duarte, California, United States of = America
2Department of Molecular Medicine, = City of=20 Hope National Medical Center and Beckman Research Institute, = Duarte,=20 California, United States of America
3Department of Cancer = Immunotherapy and=20 Tumor Immunology, City of Hope National Medical Center and Beckman = Research Institute, Duarte, California, United States of = America
4Department of Neurosciences, City = of Hope=20 National Medical Center and Beckman Research Institute, Duarte,=20 California, United States of America
5Department of Molecular and = Medical=20 Pharmacology, David Geffen School of Medicine, University of = California=20 Los Angeles, Los Angeles, California, United States of = America
6Division of Neurology, Department = of=20 Medicine, UBC Hospital, University of British Columbia, Vancouver, = British=20 Columbia, Canada
7Institute for Regenerative = Medicine, Gachon=20 University Gil Hospital, Inchon, Korea
Mikhail V. Blagosklonny, = Editor
Roswell Park Cancer Institute, United States = of=20 America
* E-mail: rikfrank/at/gmail.com (RTF); Email: kaboody/at/coh.org=20 (KSA) (KA)
Conceived and = designed the=20 experiments: RTF SEK JN CWC TK MM CG AMW PJY KSA. Performed the=20 experiments: RTF ME CWC. Analyzed the data: RTF JN CWC TK AMW PJY. = Contributed reagents/materials/analysis tools: RTF SEK CWC TK MM = SUK AMW=20 PJY KSA. Wrote the paper: RTF JN.
Received July 10, 2009; Accepted November = 20,=20 2009.
3D"Small = This=20 article has been cit= ed=20 by other articles in PMC.
Abstract
Background
Recombinant = monoclonal=20 antibodies have emerged as important tools for cancer therapy. = Despite the=20 promise shown by antibody-based therapies, the large molecular = size of=20 antibodies limits their ability to efficiently penetrate solid = tumors and=20 precludes efficient crossing of the blood-brain-barrier into the = central=20 nervous system (CNS). Consequently, poorly vascularized solid = tumors and=20 CNS metastases cannot be effectively treated by = intravenously-injected=20 antibodies. The inherent tumor-tropic properties of human neural = stem=20 cells (NSCs) can potentially be harnessed to overcome these = obstacles and=20 significantly improve cancer immunotherapy. = Intravenously-delivered NSCs=20 preferentially migrate to primary and metastatic tumor sites = within and=20 outside the CNS. Therefore, we hypothesized that NSCs could serve = as an=20 ideal cellular delivery platform for targeting antibodies to = malignant=20 tumors.
Methods and Findings
As = proof-of-concept, we=20 selected Herceptin=E2=84=A2 (trastuzumab), a monoclonal antibody = widely used to=20 treat HER2-overexpressing breast cancer. HER2 overexpression in = breast=20 cancer is highly correlated with CNS metastases, which are = inaccessible to=20 trastuzumab therapy. Therefore, NSC-mediated delivery of = trastuzumab may=20 improve its therapeutic efficacy. Here we report, for the first = time, that=20 human NSCs can be genetically modified to secrete anti-HER2 = immunoglobulin=20 molecules. These NSC-secreted antibodies assemble properly, = possess tumor=20 cell-binding affinity and specificity, and can effectively inhibit = the=20 proliferation of HER2-overexpressing breast cancer cells in=20 vitro. We also demonstrate that immunoglobulin-secreting NSCs = exhibit=20 preferential tropism to tumor cells in vivo, and can = deliver=20 antibodies to human breast cancer xenografts in mice.
Conclusions
Taken together, = these results=20 suggest that NSCs modified to secrete HER2-targeting antibodies = constitute=20 a promising novel platform for targeted cancer immunotherapy.=20 Specifically, this NSC-mediated antibody delivery system has the = potential=20 to significantly improve clinical outcome for patients with=20 HER2-overexpressing breast cancer.
Recombinant monoclonal = antibodies=20 offer a targeted approach to cancer therapy and have substantially = lower=20 toxicity to normal cells than chemotherapy. However, their large = molecular=20 size and high affinity to antigens at the tumor border limit the = ability=20 of antibodies to deeply penetrate tumor foci [1]. Central nervous system (CNS) = tumors=20 pose a particular challenge for antibody therapeutics, because the = blood-brain barrier (BBB) prevents intravenously-injected = antibodies from=20 reaching CNS metastases.
The unique tumor-tropic properties = of neural=20 stem cells (NSCs) may provide the means to significantly improve = antibody=20 distribution within metastatic tumor sites throughout the body [2], [3], [4], [5], [6]. NSCs localize to infiltrative = tumor=20 cells and hypoxic tumor regions, which are inaccessible to = intravenously=20 administered drugs [7]. NSCs are also able to cross = the BBB,=20 making them a potential platform for therapeutic antibody delivery = to the=20 brain. Previous studies have demonstrated that HB1.F3 cells, a = clonal,=20 well-characterized human NSC line [8], can effectively express and = deliver a=20 variety of therapeutic agents to primary and metastatic tumor = sites,=20 including metastases to the brain [2], [4], [5], [6], [9]. Therefore, we hypothesized that = NSCs=20 could be used to enhance antibody-based therapies by delivering = antibodies=20 to previously inaccessible tumor foci, while minimizing the = exposure of=20 normal tissue to the therapeutic agent.
As a model system, we chose = Herceptin=E2=84=A2=20 (trastuzumab), a well characterized antibody therapy for=20 HER2-overexpressing breast carcinoma, because HER2-overexpression = is=20 correlated with a poor prognosis and an increased incidence of CNS = metastases [10]. Trastuzumab is a = humanized=20 monoclonal antibody that targets the HER2 receptor, which is = overexpressed=20 in approximately 20=E2=80=9330% of human breast carcinomas [11]. Although the clinical use = of=20 trastuzumab has made measurable improvements in the prognosis of = patients=20 with HER2-overexpressing breast cancer, its effectiveness is = limited [12], [13]. In addition, HER2 is = expressed in many=20 normal tissues, giving systemic HER2-targeted antibody therapy the = potential to cause toxicity in a subset of patients, including = cardiac=20 myopathy, congestive heart failure, and pulmonary toxicity [14], [15].
Here we report that = HB1.F3 NSCs can=20 be engineered to express and secrete functional full-length = HER2-specific=20 human immunoglobulin molecules that can selectively bind to and = inhibit=20 the proliferation of HER2-positive breast carcinoma cells. = Furthermore,=20 these antibody-secreting NSCs retain tropism to tumor cells in = vitro and can deliver anti-HER2 antibody to tumor foci in = vivo. Our data suggest that NSCs may represent a novel = platform for=20 delivery of therapeutic antibodies to metastatic breast=20 carcinoma.
NSCs Can Express and Secrete = Anti-HER2=20 Antibody
To determine whether = NSCs can=20 express immunoglobulins, HB1.F3 NSCs were transiently = co-transfected with=20 plasmids encoding the heavy and light chains of an anti-HER2 = antibody=20 (HB1.F3.H2IgG) identical in sequence to trastuzumab. Intracellular = expression of human immunoglobulin in HB1.F3.H2IgG NSCs was = visualized=20 using immunocytochemistry. In contrast to parental HB1.F3 NSCs (Fig. 1A3D"Figure),=20 HB1.F3.H2IgG NSCs displayed a clear intracellular signal when = stained with=20 FITC-conjugated anti-human IgG (Fig. 1B3D"Figure).=20 This signal was often punctate and localized to the cytoplasm, = which is=20 consistent with expected cellular localization within the = endoplasmic=20 reticulum and secretory vesicles. We next explored viral = expression of=20 anti-HER2 antibody in NSCs in order to prolong antibody = expression.=20 Trastuzumab heavy and light chains were reformatted into a = bicistronic=20 expression cassette and cloned into adenoviral and lentiviral = vectors for=20 transient and stable expression, respectively. Expression of human = immunoglobulin within adenovirally-transduced HB1.F3 NSCs=20 (HB1.F3.Ad-H2IgG; Fig. 1C3D"Figure)=20 and HB1.F3.Lenti-H2IgG, a stable cell line generated by lentiviral = transduction of HB1.F3 NSCs (Fig. 1D3D"Figure),=20 was visualized using immunocytochemistry. These results were = confirmed by=20 intracellular flow cytometry (Fig. 1E3D"Figure).=20 Both transient transfection with Lipofectamine and transduction = with=20 adenovirus resulted in a subpopulation of cells that experessed = human IgG,=20 as shown by the increased fluorescence intensity. In contrast, the = stable=20 HB1.F3.Lenti-H2IgG cell line showed a shift in green fluorescence=20 intensity for the entire cell population, albeit at lower levels = than with=20 the transient expression methods. This is consistent with a stable = cell=20 line.
To determine whether the = NSC-secreted=20 anti-HER2 antibody binds specifically to the HER2 receptor, = HB1.F3-H2IgG=20 cells were co-cultured overnight with either MCF7 human breast = cancer=20 cells that express low levels of HER2, or MCF7/HER2 cells, an MCF7 = line=20 stably transfected to overexpress HER2 [16]. Breast cancer cells were = pre-labeled=20 with CM-DiI to visually distinguish them from NSCs in co-culture.=20 MCF7/HER2 cells in the vicinity of transfected NSCs were strongly = labeled=20 with human IgG (Fig. 2B3D"Figure).=20 In contrast, we did not detect any human immunoglobulin bound to = the=20 surface of neighboring MCF7 cells (Fig. 2A3D"Figure).=20 To confirm specificity, supernatant from transfected or transduced = HB1.F3=20 cells was incubated with MCF7, MCF7/HER2, or BT474, a human breast = cancer=20 cell line that endogenously overexpresses HER2. Antibody bound to = breast=20 cancer cells was detected by flow cytometry (Fig. 2C3D"Figure),=20 and significant quantities of human IgG were detected on the = surface of=20 both HER2-overexpressing cell lines following incubation with = supernatant=20 from HB1.F3-H2IgG and HB1.F3.Ad-H2IgG NSCs. Supernatant from = stable=20 HB1.F3.Lenti-H2IgG NSCs also labeled HER2-overexpressing breast = cancer=20 cells, but to a lesser extent. This result is consistent with the = lower=20 expression levels observed by intracellular flow cytometry of=20 HB1.F3.Lenti-H2IgG cells. Importantly, each supernatant labeled = MCF7 cells=20 between one and two logs less than either of the = HER2-overexpressing=20 breast cancer cell lines. These findings demonstrate the = NSC-secreted=20 antibody is specific for HER2.
3D"Figure
Figure=20 1
Expression of human=20 IgG in NSCs.
NSC-Secreted IgG Is = Functionally=20 Equivalent to Trastuzumab
To directly compare = trastuzumab and=20 NSC-secreted anti-HER2 antibody (F3-IgG), F3-IgG was purified from = the=20 supernatant of transfected HB1.F3 cells. Trastuzumab and F3-IgG = were=20 analyzed by SDS-PAGE under reducing and non-reducing conditions. = Both=20 antibodies showed an apparent molecular mass of 150 kDa under = non-reducing=20 conditions and two major bands indicative of the heavy (50 kDa) = and light=20 (25 kDa) chains under reducing conditions (data not shown). This = suggests=20 the two antibodies have a similar molecular composition.
To confirm the specificity of = F3-IgG, purified=20 F3-IgG was added directly to target cells and binding was detected = by flow=20 cytometry. At all concentrations tested, trastuzumab and purified = F3-IgG=20 bound equally well to MCF7/HER2 and BT474, as indicated by similar = mean=20 fluorescence intensities of assayed target cells (Fig. 3A3D"Figure).=20 A non-specific isotype control antibody (human IgG1) showed no = reactivity.=20 Minimal labeling of MCF7 cells was observed for both trastuzumab = and=20 F3-IgG. This indicates that F3-IgG binds to HER2 protein = specifically and=20 with an affinity comparable to that of trastuzumab, which suggests = that it=20 should have similar anti-tumor efficacy.
3D"Figure
Figure=20 2
NSC-secreted human=20 IgG specifically binds HER2.
To assess the ability of = F3-IgG to=20 inhibit the proliferation of HER2-overexpressing breast carcinoma = cells,=20 we measured the proliferation of BT474, MCF7/HER2 and MCF7 breast = cancer=20 cell lines in the presence of trastuzumab, F3-IgG, or an = isotype-matched=20 control antibody. F3-IgG significantly inhibited the proliferation = of=20 BT474 cells in a dose-dependent manner, comparable to the = trastuzumab (Fig. 3B3D"Figure).=20 As expected, MCF7 cells were not affected by treatment with either = trastuzumab or F3-IgG. F3-IgG did not inhibit the proliferation of = MCF7/HER2 cells, which is consistent with previously published = reports for=20 trastuzumab [16], [17].
Antibody-Secreting NSCs Display = Tumor=20 Tropism and Deliver Antibody to Breast Cancer Xenografts
In order for stem cell = targeting of=20 antibodies to be clinically relevant, immunoglobulin-secreting = NSCs must=20 retain their migratory tumor-tropic properties. We tested the = migration of=20 transfected NSCs in vitro using a chemotaxis assay in = which cells=20 must actively migrate through a semi-permeable membrane in = response to a=20 cytokine gradient. Both parental HB1.F3 NSCs and NSCs expressing = intact=20 anti-HER2 immunoglobulin showed preferential in vitro = migration=20 to tumor cell-conditioned media. Although we observed fewer = migrated=20 anti-HER2-expressing NSCs than untransfected NSCs, both cell types = showed=20 a statistically significant tropism to MCF7/HER2 conditioned = medium=20 relative to BSA control (Fig. 43D"Figure).=20 This result indicates that immunoglobulin-expressing HB1.F3 NSCs = would=20 likely maintain the in vivo tumor tropism of the parental = NSC=20 line.
3D"Figure
Figure=20 3
NSC-secreted=20 anti-HER2 antibody is functionally equivalent to=20 trastuzumab.
We next tested the ability of=20 antibody-expressing NSCs to deliver anti-HER2 antibodies to tumor = foci=20 in vivo using a xenograft nude-beige mouse model.=20 Intravenously-injected parental and transduced HB1.F3 NSCs were = detected=20 within the tumor mass of each treated animal by = immunohistochemistry.=20 Tumor sections from animals receiving NSCs showed a patchy = distribution of=20 NSCs (CM-DiI labeled, red) within the tumor. In contrast, tumor = sections=20 from mice receiving trastuzumab injections showed no red stained = cells (Fig. 53D"Figure).=20 The presence of NSCs within the tumor mass was confirmed by = detection of=20 v-myc DNA using nested PCR. A 293 bp PCR product was = detected in=20 the tumors of every mouse treated with HB1.F3, HB1.F3.Ad-H2IgG, or = HB1.F3.Lenti-H2IgG. In contrast, no PCR product was detected in = tumors=20 from mice treated with trastuzumab alone. Tumor sections were then = stained=20 with FITC-conjugated anti-human IgG. Tumor sections from=20 trastuzumab-injected animals showed patches of bright green = cobblestone=20 patterns, indicative of antibody bound to tumor cell membranes. As = expected, trastuzumab distribution was heterogeneous and localized = in the=20 vicinity of tumor vasculature. Tumor sections from mice treated = with=20 HB1.F3.Ad-H2IgG and HB1.F3.Lenti-H2IgG also showed patches of = green=20 cobblestone patterns throughout the tumor mass. = Antibody-expressing NSC=20 appear yellow, due to the presence of both CM-DiI and = FITC-conjugated=20 anti-human IgG. Parental HB1.F3 NSCs showed only background levels = of=20 green fluorescence and tumor sections from mice injected with = these NSCs=20 did not exhibit the green cobblestone pattern associated with=20 membrane-bound antibody.
3D"Figure
Figure=20 4
In = vitro=20 migration of NSCs to breast carcinoma conditioned=20 media.
Of note, quantitative = ELISA revealed=20 significant quantities of human IgG in the blood of = trastuzumab-injected=20 mice. In contrast, mice treated with antibody-expressing NSCs = showed=20 anti-HER2 IgG at the tumor site, but no human IgG was detectable = in the=20 blood (data not shown). Taken together, these data indicate that = anti-HER2=20 IgG-expressing NSCs can deliver antibody selectively to tumor foci = in=20 vivo.
Overexpression of HER2 = is a marker=20 for poor prognosis in breast cancer and is often correlated with = increased=20 metastasis, including to the CNS [18], [19]. Trastuzumab directly = inhibits the=20 proliferation of HER2-overexpressing breast cancer cells and = induces=20 immune-mediated killing of target cancer cells through = antibody-dependent=20 cellular cytotoxicity [20]. However, trastuzumab is = unable to=20 cross the BBB, and therefore cannot be used to treat CNS = metastases.=20 Importantly, NSCs can target breast cancer metastasis in the brain = [9] and can penetrate deep and = hypoxic regions=20 of solid tumors [7]. Therefore, we examined the = feasibility=20 of expressing therapeutic antibodies in tumor-tropic human NSCs, = with the=20 ultimate goal of using such NSCs as a platform for delivery of = anti-HER2=20 antibody to otherwise inaccessible tumor foci.
NSCs have been successfully = engineered to=20 express and deliver a broad range of recombinant therapeutic = proteins to=20 tumor foci [3]. However, antibodies are = complex=20 tetrameric molecules, that are normally expressed only by = lymphocytes and=20 a few other specialized cells. Whether NSCs are capable of = expressing and=20 secreting such complex molecules was previously unknown. Here, we = have=20 demonstrated that NSCs can express and secrete intact = immunoglobulin while=20 retaining their inherent tumor tropism. In addition, F3-IgG binds = to HER2=20 specifically and inhibits the proliferation of HER2-overexpressing = breast=20 cancer cells.
In our initial experiments, we = transiently=20 co-transfected trastuzumab heavy and light chains with = Lipofectamine to=20 achieve trastuzumab expression in HB1.F3 NSCs. Although this = method was=20 successful in generating high levels of human IgG in HB1.F3 NSCs,=20 expression was limited to 3=E2=80=934 days and caused = unpredictable toxicity to=20 the NSCs. We therefore chose to pursue two alternative viral = transduction=20 strategies to prolong antibody expression. Our laboratory has = previously=20 used adenoviral expression as a means to transiently express = therapeutic=20 transgenes [2], [6]. We have found that adenoviral = transduction results in high levels of transgene expression for at = least=20 two weeks. We have also generated a stable anti-HER2 = IgG-expressing NSC=20 line (HB1.F3.Lenti-H2IgG). In this stable line, antibody = expression is=20 prolonged, but at significantly lower levels than observed with=20 adenovirally-transduced NSCs (HB1.F3.Ad-H2IgG). Both of these = strategies=20 resulted in antibody-expressing NSCs capable of achieving = tumor-specific=20 antibody delivery in vivo. Our ability to detect = anti-HER2=20 antibody at the tumor site but not in the blood of NSC-treated = mice=20 suggests that this approach could have robust localized anti-tumor = effect,=20 while minimizing the systemic toxicity associated with traditional = trastuzumab therapy.
The use of NSCs to target = antibodies=20 specifically to tumor foci has broad implications for the field of = antibody therapy in cancer and other diseases. In addition to = improving=20 distribution of antibodies to the CNS and within malignant solid = tumors,=20 this strategy could expand the number of targets to which = antibodies can=20 be directed. Currently, molecular targets for cancer therapy must = either=20 be exclusively expressed by tumor cells or expressed at = significantly=20 higher levels in tumors than in normal tissues. Because the tumor=20 specificity of NSC-mediated immunotherapy is endowed by the NSCs, = antigens=20 on tumor cells can likely be safely targeted, regardless of = whether they=20 are present in healthy tissues.
We conclude that = tumor-tropic human=20 NSCs can be genetically modified to secrete intact therapeutic = antibodies.=20 The data presented here provide the first fundamental step in the=20 development of a stem cell-based cancer immunotherapy. Such a = therapeutic=20 platform has significant clinical implications for improving the = treatment=20 of metastatic breast carcinoma and other malignant solid=20 tumors.
Vector Construction and=20 Purification
DNA encoding the = trastuzumab=20 scFv molecule (hu4D5v8) was generated as described previously [21]. The genes encoding the = variable=20 domains were individually inserted on to the human IgG1 heavy and = light=20 chains by splice-overlap PCR using the anti-CEA hT84.66-M5A = antibody as a=20 template and cloned into glutamine synthetase vectors (Lonza = Biologics,=20 Slough, UK) as previously described [21]. To create viral expression = vectors, a=20 bicistronic construct was created. Briefly, trastuzumab heavy and = light=20 chain sequences were amplified with PCR and a truncated FMDV 2A = peptide=20 sequence was inserted between them by splice overlap extension. = This=20 expression construct was inserted into the pENTR vector of = Invitrogen's=20 Gateway system using the D-TOPO cloning kit. Entry vector = constructs were=20 recombined into adenoviral (pAd, Invitrogen) or lentiviral = (pCSC-Zeo with=20 Gateway recombination sites cloned into the multiple cloning site) = destination vectors according to manufacturer's instructions. = Adenovirus=20 was produced by transfecting adenoviral expression vector into=20 E1-complemented cell line 293A and performing successive rounds of = amplification until high titer was achieved. Virus was then = purified using=20 ViraBind Adenovirus Purification Kit (Cell Biolabs). Lentivirus = was=20 produced by cotransfecting replication incompetent lentiviral = vector with=20 psPAX2 (Addgene, 12260) and pLP/VSV-G (Invitrogen). Virus was = purified=20 from crude viral supernatant using LentiX Viral concentrator = (Clontech)=20 according to manufacturer's instructions.
Cell Culture
HB1.F3, MCF7, = MCF7/HER2, 293A=20 and 293FT cells were cultured in Dulbecco's Modified Eagle Medium = (DMEM)=20 supplemented with 10% fetal bovine serum (FBS), 100 units = penicillin, 100=20 =C2=B5g/mL streptomycin, and 2 mM L-glutamine. BT474 cells were = cultured in=20 RPMI 1640 supplemented with 10% FBS, 100 units penicillin, 100 = =C2=B5g/mL=20 streptomycin, and 2 mM L-glutamine and 500 =C2=B5g/mL insulin. All = cells were=20 cultured at 37=C2=B0C with 6% CO2.
Transfection and Transduction = of HB1.F3=20 NSCs
Plasmids encoding = the=20 trastuzumab heavy and light chains, pEE6-HER2-Heavy and = pEE12-HER2-Light,=20 were co-transfected in equal concentrations using Lipofectamine = LTX=20 (Invitrogen) according to the manufacturer's instructions. Dishes = (10 cm=20 diameter) were seeded with HB1.F3 NSCs (3=C3=97106) and = transfected=20 with pooled heavy and light chain DNA (6 =C2=B5g). Stable=20 trastuzumab-expressing NSCs (HB1.F3.Lenti-H2IgG) were generated by = incubating HB1.F3 cells with purified lentivirus (MOI 100) for 4 h = in the=20 presence of 8 =C2=B5g/mL polybrene. After 24 h, = trastuzumab-expressing NSC were=20 selected using increasing concentrations of Zeocin (InvivoGen), = beginning=20 at 100 =C2=B5g/mL. For adenoviral transduction, HB1.F3 cells were = incubated=20 with purified adenovirus (13D[ratio]=201000 dilution in DMEM) for 4 h and then cultured = overnight in=20 DMEM.
Mouse Tumor Xenograft = Model
Female 7-week old=20 nude-beige-xid mice (NCI) were injected with MCF7/HER2 cells=20 (5=C3=97106) in the right mammary fat pad. Tumors were = allowed to=20 grow until palpable (3 weeks), then mice were injected = intravenously with=20 trastuzumab (4 mg/kg) or unmodified NSCs (2=C3=97106),=20 adenovirally-transduced NSCs or HB1.F3/H2IgG (3 mice per group). = One=20 additional mouse per group received an intratumoral injection as a = control. Four days later, mice were humanely euthanized and tumors = were=20 harvested and fixed for 48 h in 4% PFA. Blood was collected by = cardiac=20 puncture immediately after euthanasia. All procedures were = approved by=20 City of Hope IACUC.
PCR Detection of = v-myc
Genomic DNA from = tumor sections=20 was purified using DNeasy Blood and Tissue kit (Qiagen). Nested = PCR was=20 performed as described previously [2]. The v-myc amplicon = was=20 detected as a band of 293 bp. Genomic DNA from HB1.F3.H2IgG cells = was used=20 as a positive control.
Quantitative ELISA
Mouse serum was = diluted 100 or=20 1000-fold in PBS and tested by quantitative ELISA using the human = IgG=20 ELISA Kit (Bethyl Laboratories) according to manufacturer's=20 instructions.
Immunocytochemistry and=20 Immunohistochemistry
Parental or=20 transfected/transduced NSCs were seeded into 4-well chamber slides = and=20 allowed to adhere overnight. For co-culture experiments, = CM-DiI-labeled=20 breast cancer cells were seeded one day prior to the addition of = NSCs.=20 Adherent cells were washed once (PBS supplemented with 100 mg/L = calcium=20 chloride and 100 mg/L magnesium chloride), fixed (4% = paraformaldehyde, 10=20 min), then permeabilized (0.3% Triton X-100 in PBS, 30 min). For = tissue=20 sections, PFA-fixed tumors were impregnated with 30% sucrose then = cut into=20 10 =C2=B5m sections using a cryostat. Sections were blocked and = stained=20 overnight with FITC-conjugated donkey anti-human IgG (H+L) = (Jackson=20 ImmunoResearch). Slides were washed, counterstained with=20 4=E2=80=B2,6-diamidino-2-phenylindole (DAPI), mounted in = fluorescent mounting=20 media (DAKO), and imaged using a Nikon Eclipse TE2000-U microscope = equipped with a SPOT RT Slider digital camera or confocal imaging = using a=20 Zeiss LSM 510 confocal microscope (Carl Zeiss = Microimaging).
Purification of Secreted = Antibody
Immunoglobulin-containing=20 HB1.F3.H2IgG NSC culture supernatant was subjected to purification = by=20 protein A affinity chromatography. The NSC-expressed anti-HER2 = antibody=20 and trastuzumab were analyzed by SDS-PAGE as previously described = [21].
Flow Cytometry
The specificity of = purified=20 NSC-secreted antibody (F3-IgG) was compared to trastuzumab by = measuring=20 the binding to HER2 over-expressing target cells. Bound = immunoglobulin on=20 target cells was labeled with FITC-conjugated donkey anti-human = IgG (H+L)=20 (Jackson ImmunoResearch) and detected using a Guava EasyCyte flow=20 cytometer. For intracellular flow cytometry, cells were fixed in = 4% PFA=20 for 20 min, then washed and resuspended in permeabilization buffer = (PBS=20 with 3% FBS and 0.1% Saponin) prior to staining.
Cell Proliferation Assay
Breast carcinoma = cells=20 (5=C3=97103 cells/well) were seeded into a 96-well = plate and treated=20 with trastuzumab, isotype-matched control IgG, or F3-IgG at = concentrations=20 ranging from 0.01 to 10 =C2=B5g/mL. As a negative control, medium = alone (100=20 =C2=B5L) was added. Plates were incubated (37=C2=B0C) for 5 or 6 = days. To quantify=20 cell proliferation, WST-1 reagent (Roche) was used according to=20 manufacturer's instructions. Background absorbance of WST-1 with = media=20 only was subtracted and all concentrations were expressed as a = percentage=20 of control. All experiments were performed in = triplicate.
In Vitro Chemotaxis = Assay
Cell migration = assay was=20 performed as described previously [22]. Briefly, NSCs = (1=C3=97105 in=20 400 =C2=B5L culture media) were seeded into the upper chamber of a = 24-well=20 Boyden chamber with an 8 =C2=B5m pore-size membrane, and tumor = cell-conditioned=20 medium (600 =C2=B5L) was added to the bottom chamber. After 4 h, = the number of=20 migrated cells was quantified using a Guava EasyCyte flow = cytometer. NSCs=20 transfected with anti-HER2 antibody were used 24 h after = transfection, the=20 time-point that correlated with peak antibody expression. All = experiments=20 were performed in triplicate. Student's t-test was used = for=20 statistical analysis. p<0.05 was considered=20 significant.
Acknowledgments
We thank Sridhar Samineni for = assistance with=20 the animal experiments and Dr. Keely L. Walker for critical = reading of the=20 manuscript.
Footnotes
Competing = Interests:=20 The authors have declared that no competing interests=20 exist.
Funding: = This=20 work was supported by the Rosalinde and Arthur Gilbert Foundation, = STOP=20 CANCER, The Jewish Federation's Jeanne Schnitzer Reynolds Fund for = Women's=20 Health, Ziman Family Foundation, the Helen and Morgan Chu Graduate = Student=20 Fellowship, the Irell and Manella Graduate School of Biological = Sciences=20 and the Beckman Research Institute at City of Hope. The funders = had no=20 role in study design, data collection and analysis, decision to = publish or=20 preparation of the manuscript.
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11. Molina MA, Codony-Servat J, Albanell = J, Rojo=20 F, Arribas J, et al. Trastuzumab (herceptin), a humanized = anti-Her2=20 receptor monoclonal antibody, inhibits basal and activated Her2 = ectodomain=20 cleavage in breast cancer cells. Cancer Res.=20 2001;61:4744=E2=80=934749. [PubMed]
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21. Yazaki PJ, Sherman MA, Shively JE, = Ikle D,=20 Williams LE, et al. Humanization of the anti-CEA T84.66 antibody = based on=20 crystal structure data. Protein = Eng Des Sel.=20 2004;17:481=E2=80=93489. [PubMed]
22. Gutova M, Najbauer J, Frank RT, = Kendall SE,=20 Gevorgyan A, et al. Urokinase plasminogen activator and urokinase=20 plasminogen activator receptor mediate human stem cell tropism to=20 malignant solid tumors. Stem = Cells.=20 2008;26:1406=E2=80=931413. [PubMed]
Articles from PLoS = ONE are provided here courtesy of
Public Library of = Science
3D"Figure
Figure=20 5
NSCs = target breast=20 carcinoma and can deliver anti-HER2 antibody in=20 vivo.

PubMed articles by these = authors

  • Frank,=20 R.
  • Edmiston,=20 M.
  • Kendall,=20 S.
  • Aboody,=20 K.

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BUTTON { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/btn-arrow.gif) } .x-toolbar .x-btn-text-icon .x-btn-menu-arrow-wrap .x-btn-center BUTTON = { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/btn-arrow.gif) } .x-toolbar .x-btn-over .x-btn-left { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-over .x-btn-right { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-over .x-btn-center { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-over BUTTON { COLOR: #111 } .x-toolbar .x-btn-click .x-btn-left { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-pressed .x-btn-left { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-menu-active .x-btn-left { BACKGROUND-IMAGE: url(../../img/oldentrez/toolbar/tb-btn-sprite.gif) } .x-toolbar .x-btn-click .x-btn-right { BACKGROUND-IMAGE: 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0px } .issue-block { BORDER-COLLAPSE: collapse } .iss-cell { BORDER-RIGHT: black 1px solid; BORDER-TOP: black 1px solid; = BORDER-LEFT: black 1px solid; BORDER-BOTTOM: black 1px solid } .vol-cell { BORDER-RIGHT: black 1px solid; BORDER-TOP: black 1px solid; = BORDER-LEFT: black 1px solid; BORDER-BOTTOM: black 1px solid } } .nopagesectioncontent { DISPLAY: none } .port { FONT-SIZE: 1em } .port { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port DIV { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port DL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port DT { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port DD { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port UL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port OL { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port LI { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H1 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H2 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H3 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H4 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H5 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port H6 { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port PRE { PADDING-RIGHT: 0px; PADDING-LEFT: 0px; PADDING-BOTTOM: 0px; MARGIN: = 0px; PADDING-TOP: 0px } .port FORM { PADDING-RIGHT: 0px; 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(moveToY > 0 ? moveToY : moveToYDefault)=0A= }=0A= catch (e) {}=0A= =0A= var wLeftTopCornerOptions =3D ',left=3D' + moveToX + ',top=3D' + = moveToY + ',screenX=3D' + moveToX + ',screenY=3D' + moveToY=0A= =0A= allOptions =3D allOptions + wLeftTopCornerOptions=0A= =0A= w =3D window.open (link, windowname, allOptions)=0A= w.focus()=0A= =0A= link.target=3Dwindowname=0A= =0A= return false;=0A= }=0A= =0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function focuswin(windowname)=0A= {=0A= windowname =3D String(windowname).replace(/-/g, "_")=0A= w =3D = window.open("",windowname,"menubar=3Dyes,scrollbars=3Dyes,toolbar=3Dyes,l= ocation=3Dyes,status=3Dyes,directories=3Dyes,resizable=3Dyes");=0A= w.focus();=0A= =0A= return true;=0A= }=0A= =0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function reverseString (inStr)=0A= {=0A= var outStr =3D ''=0A= =0A= for (i =3D0; i <=3D inStr.length; i++)=0A= {=0A= outStr =3D inStr.charAt(i) + outStr=0A= }=0A= =0A= return outStr=0A= }=0A= =0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function reverseAndReplaceString (inStr, findStr, newStr)=0A= {=0A= return reverseString(inStr).replace(findStr, newStr)=0A= }=0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function initUnObscureEmail (className, innerHTML)=0A= {=0A= =0A= try{=0A= if (window.addEventListener)=0A= window.addEventListener('load', function() {unObscureEmail = (className, innerHTML)}, false)=0A= else if (window.attachEvent)=0A= window.attachEvent('onload', function() {unObscureEmail = (className, innerHTML)})=0A= }catch(e){=0A= }=0A= }=0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function unObscureEmail (className, innerHTML)=0A= {=0A= try {=0A= if (typeof(unObscuredEmails) =3D=3D 'undefined')=0A= unObscuredEmails =3D new Array()=0A= =0A= if (! unObscuredEmails[className])=0A= {=0A= =0A= var elmnts =3D document.getElementsByTagName("span")=0A= for (var i =3D 0, len =3D elmnts.length; i < len; i++)=0A= {=0A= if (elmnts.item(i).className.indexOf(className, " ") = !=3D -1)=0A= {=0A= elmnts.item(i).innerHTML =3D innerHTML;=0A= unObscuredEmails[className] =3D true=0A= =0A= }=0A= }=0A= }=0A= }=0A= catch(e){=0A= }=0A= }=0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= function pubMedDbLinkSubmit(control) {=0A= try{=0A= if (control.pubmedOption)=0A= control =3D control.pubmedOption=0A= if (control.options)=0A= location.href =3D = control.options[control.options.selectedIndex].value;=0A= }=0A= catch(e){}=0A= return false;=0A= }=0A= =0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= // elements "a", "area" with "ref" attribute report to redirect utility = before dereferencing link=0A= //=0A= function initRedirectClicks(report_url) {=0A= =0A= if (report_url && typeof jQuery !=3D 'undefined')=0A= jQuery(document).click(function(e) {=0A= =0A= //=0A= if (!e) return true;=0A= //=0A= if (e.shiftKey || e.altKey || e.ctrlKey) return true;=0A= //=0A= var target =3D jQuery(e.target).closest("a[ref], area[ref]");=0A= if (!target || target.length =3D=3D 0) return true;=0A= //=0A= var ref =3D target.attr("ref");=0A= var href =3D target.attr("href")=0A= =0A= // special processing of href element for pubmed's authors=0A= if (typeof (href) !=3D 'undefined' && = href.indexOf('sites/entrez') && href.indexOf('%5Bauth%5D'))=0A= {=0A= var newHref =3D replacePubMedUnsupportedChars(href);=0A= if (newHref !=3D href)=0A= target.attr("href", newHref)=0A= }=0A= =0A= // append ref with value of href if 'redirect-to-url' is = missing in ref.=0A= if (typeof (ref) !=3D 'undefined' && = ref.indexOf('redirect-to-url') =3D=3D -1)=0A= {=0A= ref =3D ref + '&redirect-to-url=3D' + = encodeURIComponent(href)=0A= //=0A= jQuery.ajax({=0A= type: "HEAD",=0A= url: report_url + '?' + ref,=0A= timeout: 1000,=0A= async: false=0A= });=0A= }=0A= =0A= return true;=0A= });=0A= };=0A= =0A= // function to replace unsupported charachters in author names to be = searchable in PubMed database.=0A= function replacePubMedUnsupportedChars (str)=0A= {=0A= // replace low 128 chars automatically=0A= str =3D str.replace(/%26%23(x000[0-7][0-9a-f])%3b/ig,=0A= function($0, $1){=0A= return (String.fromCharCode('0' + $1))=0A= }=0A= )=0A= // replace others based on map and if it is not in the map replace = with empty string.=0A= str =3D = str.replace(/%26%23(x[0-9a-f][0-9a-f][0-9a-f][0-9a-f][0-9a-f])%3b/ig,=0A= function($0, $1){=0A= return (pubmedUnsupportedCharMap[$1] ? = pubmedUnsupportedCharMap[$1] : '')=0A= }=0A= )=0A= return str;=0A= }=0A= //=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=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=3D=3D=3D=3D=3D=3D=3D=3D= =3D=3D=3D=3D=3D=0A= // Based on script written by Dean Edwards, 2005=0A= // http://dean.edwards.name/=0A= =0A= var pmc_script =3D {=0A= addEvent: function(element, type, handler) {=0A= // assign each event handler a unique ID=0A= if (!handler.$$guid) handler.$$guid =3D this.addEvent_guid++;=0A= // create a hash table of event types for the element=0A= if (!element.events) element.events =3D {};=0A= // create a hash table of event handlers for each element/event pair=0A= var handlers =3D element.events[type];=0A= if (!handlers) {=0A= handlers =3D element.events[type] =3D {};=0A= // store the existing event handler (if there is one)=0A= if (element["on" + type]) {=0A= handlers[0] =3D element["on" + type];=0A= }=0A= }=0A= // store the event handler in the hash table=0A= handlers[handler.$$guid] =3D handler;=0A= // assign a global event handler to do all the work=0A= element["on" + type] =3D handleEvent;=0A= =0A= =0A= function handleEvent(event) {=0A= var returnValue =3D true;=0A= // grab the event object (IE uses a global event object)=0A= event =3D event || fixEvent(window.event);=0A= // get a reference to the hash table of event handlers=0A= var handlers =3D this.events[event.type];=0A= // execute each event handler=0A= for (var i in handlers) {=0A= this.$$handleEvent =3D handlers[i];=0A= if (this.$$handleEvent(event) =3D=3D=3D false) {=0A= returnValue =3D false;=0A= }=0A= }=0A= return returnValue;=0A= };=0A= =0A= function fixEvent(event) {=0A= // add W3C standard event methods=0A= event.preventDefault =3D fixEvent.preventDefault;=0A= event.stopPropagation =3D fixEvent.stopPropagation;=0A= return event;=0A= };=0A= =0A= fixEvent.preventDefault =3D function() {=0A= this.returnValue =3D false;=0A= };=0A= =0A= fixEvent.stopPropagation =3D function() {=0A= this.cancelBubble =3D true;=0A= };=0A= },=0A= =0A= // a counter used to create unique IDs=0A= addEvent_guid: 1,=0A= =0A= removeEvent: function(element, type, handler) {=0A= // delete the event handler from the hash table=0A= if (element.events && element.events[type]) {=0A= delete element.events[type][handler.$$guid];=0A= }=0A= }=0A= }=0A= =0A= =0A= // = *************************************************************************= ***=0A= // implementation of figure's popup using jQuery and = jQuery.fn.hoverIntent lib=0A= // it set appropriate handlers for all "a" elements with "figpopup" = class name.=0A= // = *************************************************************************= ***=0A= if (typeof jQuery !=3D 'undefined' && typeof jQuery.fn.hoverIntent !=3D = 'undefined') {=0A= (function($j) {=0A= // = =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 hoverHandlers = =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= var hoverHandlers =3D function (opts) {=0A= this.config =3D {}=0A= this.self =3D this;=0A= this.__init(opts)=0A= }=0A= =0A= $j.fn.extend(hoverHandlers.prototype, {=0A= //=0A= __init: function(opts) {=0A= $j.fn.extend(this.config, opts)=0A= },=0A= //=0A= over: function (el) {=0A= var canvas =3D $j('.large-thumb-canvas', el)=0A= var prnt =3D canvas.parent();=0A= var win =3D $j(window)=0A= =0A= //=0A= if (canvas && prnt && win)=0A= {=0A= =0A= // collect necessary coordinates from all = intresting objects=0A= canvas.coords =3D this._x_coords(canvas, = 'canvas')=0A= prnt.coords =3D this._x_coords(prnt, = 'parent')=0A= win.coords =3D this._x_coords(win, = 'window')=0A= =0A= // replace @src with value of @hires, because = href hold high resolution image and src low one.=0A= $j('img', canvas).attr('src',=0A= function(){=0A= var hires =3D $j(this).attr("hires");=0A= return (typeof (hires) !=3D = 'undefined' && hires !=3D this.src)=0A= ? hires : this.src=0A= }=0A= )=0A= =0A= // make arrangement of canvas in the view port = nearby parent element.=0A= var cnvsRltvToPrnt =3D = this._x_arrange_canvas(canvas.coords, prnt.coords, win.coords)=0A= =0A= // visualize the canvas with images.=0A= canvas.css('top', cnvsRltvToPrnt.top + 'px')=0A= canvas.css('left', cnvsRltvToPrnt.left + 'px')=0A= canvas.css('display', 'block')=0A= } // canvas=0A= }, // over=0A= //=0A= out: function (el) {=0A= var canvas =3D $j('.large-thumb-canvas', el)=0A= canvas.css('display', 'none')=0A= },=0A= //=0A= _x_offset: function(el, elname) {=0A= var c =3D {}=0A= if (el[0] =3D=3D window )=0A= c =3D this._x_scroll(el, elname)=0A= else=0A= c =3D el.offset()=0A= //console.info('%s.offset {top,left} =3D {%s, %s}', = elname, c.top, c.left)=0A= return c=0A= },=0A= _x_scroll: function(el, elname) {=0A= var c =3D {top: el.scrollTop(), left: = el.scrollLeft()}=0A= //console.info('%s.scroll {top,left} =3D {%s, %s}', = elname, c.top, c.left)=0A= return c=0A= },=0A= _x_width: function(el, elname) {=0A= var w =3D el.outerWidth() || el.width()=0A= //console.info('%s.width =3D %s; outerWidth =3D = %s; width =3D %s', elname, w, el.outerWidth(), el.width())=0A= //IE: alert(elname + '.width =3D ' + w + '; = outerWidth =3D ' + el.outerWidth() + 'width =3D ' + el.width())=0A= return w=0A= },=0A= _x_height: function(el, elname) {=0A= var h =3D el.outerHeight() || el.height()=0A= // console.info('%s.height =3D %s', elname, h)=0A= return h=0A= },=0A= _x_coords: function(el, elname) {=0A= var size =3D { width: this._x_width (el, elname), = height: this._x_height(el, elname)}=0A= var coords =3D {=0A= scroll: this._x_scroll(el, elname),=0A= width: size.width,=0A= height: size.height,=0A= offset: this._x_offset(el, elname),=0A= size: size=0A= }=0A= return coords=0A= },=0A= _x_get_rltv_coord: function(trgtObj, baseObj, = label) {=0A= var c =3D {top: trgtObj.top - baseObj.top, left: = trgtObj.left - baseObj.left}=0A= //console.info("%s {top: %s, left: %s}", label, = c.top, c.left)=0A= return c=0A= },=0A= //=0A= _x_get_empty_space: function(objCoords, = objSize, viewPortCoords, viewPortSize, label) {=0A= var objRelToViewPort =3D = this._x_get_rltv_coord(objCoords, viewPortCoords, '_x_get_empty_space: = for ' + label);=0A= var c =3D {above: objRelToViewPort.top,=0A= below: viewPortSize.height - = (objRelToViewPort.top + objSize.height),=0A= left: objRelToViewPort.left,=0A= right: viewPortSize.width - = (objRelToViewPort.left + objSize.width)}=0A= $j.each(c, function(k, v){c[k] =3D (v < 0 ? 0 : v)})=0A= //console.info("%s {above: %s, below: %s, left: %s, = right: %s}", label, c.above, c.below, c.left, c.right)=0A= return c=0A= },=0A= //=0A= _x_get_bigest_space_area_name: function(spaces, label) {=0A= var sArr =3D [];=0A= for (k in spaces){ sArr[sArr.length] =3D {k: k, v: = spaces[k]} }=0A= // sort in reverse order=0A= sArr.sort (function(a,b){return ( a.v < b.v ? 1 : ( = a.v > b.v ? - 1 : 0 ) )})=0A= // console.info('%s: %s', label, sArr[0].k)=0A= return sArr[0].k=0A= },=0A= //=0A= _x_get_space_ratios: function(spaces, = viewPortSize, label) {=0A= var ratios =3D {above: 0, left: 0}=0A= if (viewPortSize.height > 0)=0A= ratios.above =3D spaces.above / = viewPortSize.height=0A= if (viewPortSize.width > 0)=0A= ratios.left =3D spaces.left / viewPortSize.width=0A= // console.info('ratio: %s {above: %s, left: %s}', = label, ratios.above, ratios.left)=0A= return ratios=0A= },=0A= _x_arrange_canvas: function(c_c, prnt_c, = viewp_c) {=0A= // then calculate empty space areas around parent = element of the canvas, which is ususally an anchor ("a" element)=0A= var emptySpacesArndPrntInViewPort =3D = this._x_get_empty_space (prnt_c.offset, prnt_c.size, viewp_c.offset, = viewp_c.size, 'emptySpacesArndPrntInWinPort')=0A= =0A= // get the area name, where the most linear space = avaiable=0A= var areaName =3D = this._x_get_bigest_space_area_name(emptySpacesArndPrntInViewPort, = viewp_c.size, 'spacios areaName')=0A= =0A= // calculate the proportions of area to be taken by = canvas in empty space area=0A= // relativly to the parent element.=0A= var ratios =3D = this._x_get_space_ratios(emptySpacesArndPrntInViewPort, viewp_c.size, = 'ratios')=0A= =0A= // calculate parent's coordinates relative to view = port=0A= var prntRltvToViewPort =3D = this._x_get_rltv_coord(prnt_c.offset, viewp_c.offset, = 'prntRltvToViewPort')=0A= =0A= // declare canvas relative coordinates=0A= var cnvsRltvToPrnt =3D {top: 0, left: 0}=0A= =0A= // choose appropriate location for placing canvas.=0A= // and choose the 1st element of an array as the one = with the biggest area around parent of canvas.=0A= // console.info ('place it at the %s', = bigestEmptySpaceAreaName)=0A= // calculations are relative to the left corner of = the parent element of canvas. (it has to have the css property = position:relative)=0A= switch (areaName)=0A= {=0A= case 'above':=0A= cnvsRltvToPrnt.top =3D - c_c.height=0A= cnvsRltvToPrnt.left =3D prnt_c.width * 0.5 - = c_c.width * ratios.left=0A= break;=0A= case 'below':=0A= cnvsRltvToPrnt.top =3D prnt_c.height=0A= cnvsRltvToPrnt.left =3D prnt_c.width * 0.5 - = c_c.width * ratios.left=0A= break;=0A= case 'left':=0A= cnvsRltvToPrnt.left =3D - c_c.width=0A= cnvsRltvToPrnt.top =3D prnt_c.height * 0.5 = - c_c.height * ratios.above=0A= break;=0A= case 'right':=0A= cnvsRltvToPrnt.left =3D prnt_c.width=0A= cnvsRltvToPrnt.top =3D prnt_c.height * 0.5 = - c_c.height * ratios.above=0A= break;=0A= }=0A= =0A= // recalculate canvas' coordinates relative to = parent into coordinates relative to view port.=0A= var cnvsRltvToViewPort =3D {=0A= top: prntRltvToViewPort.top + = cnvsRltvToPrnt.top,=0A= left: prntRltvToViewPort.left + = cnvsRltvToPrnt.left=0A= }=0A= //console.info("cnvsRltvToPrnt {top:%s, left: %s}", = cnvsRltvToPrnt.top, cnvsRltvToPrnt.left)=0A= //console.info("cnvsRltvToViewPort {top:%s, left: = %s}", cnvsRltvToViewPort.top, cnvsRltvToViewPort.left)=0A= =0A= // adjust relative position of canvas to the window = if calculated values=0A= // are forcing canvas go out of view port=0A= // next order should be preserved to keep left top = corner visible always=0A= =0A= // adjust right side and move a bit to the left=0A= if (cnvsRltvToViewPort.left + c_c.width > = viewp_c.width)=0A= {=0A= var horAdj =3D c_c.width - (viewp_c.width - = cnvsRltvToViewPort.left)=0A= cnvsRltvToPrnt.left -=3D horAdj=0A= cnvsRltvToViewPort.left -=3D horAdj=0A= //console.log('adjust right side and move to = the left %spx', horizontalAdjustment)=0A= }=0A= =0A= // adjust below side and move to the top=0A= if (cnvsRltvToViewPort.top + c_c.height > = viewp_c.height)=0A= {=0A= var vertAdj =3D c_c.height - (viewp_c.height - = cnvsRltvToViewPort.top)=0A= cnvsRltvToPrnt.top -=3D vertAdj=0A= cnvsRltvToViewPort.top -=3D vertAdj=0A= // console.log('adjust below side and move to = the top %spx', verticalAdjustment)=0A= }=0A= =0A= // adjust left side and move to the right=0A= if (cnvsRltvToViewPort.left < 0)=0A= {=0A= // console.log('adjust left side and move to the = right %spx', -(cnvsLeftRelativeToWindowPort))=0A= cnvsRltvToPrnt.left -=3D = cnvsRltvToViewPort.left=0A= cnvsRltvToViewPort.left =3D 0=0A= }=0A= // adjust above side and move to the bottom=0A= if (cnvsRltvToViewPort.top < 0)=0A= {=0A= // console.log('adjust above side and move to = the bottom %spx', -(cnvsTopRelativeToWindowPort))=0A= cnvsRltvToPrnt.top -=3D = cnvsRltvToViewPort.top=0A= cnvsRltvToViewPort.top =3D 0=0A= }=0A= // console.info("cnvsRltvToPrnt adjusted {top: %s, = left: %s}", cnvsRltvToPrnt.top, cnvsRltvToPrnt.left)=0A= // console.info("cnvsRltvToViewPort adjusted {top: = %s, left: %s}", cnvsRltvToViewPort.top, cnvsRltvToViewPort.left)=0A= return cnvsRltvToPrnt=0A= }=0A= })=0A= // = =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 end of hoverHandlers = =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= =0A= // = =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 $j.fn.figPopup = =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= function hoverOverHandler () {=0A= var h =3D new hoverHandlers();=0A= h.over(this)=0A= }=0A= =0A= function hoverOutHandler () {=0A= var h =3D new hoverHandlers();=0A= h.out(this)=0A= }=0A= =0A= $j.fn.figPopup =3D function(opts){=0A= var config =3D {=0A= interval: 500,=0A= timeout: 0,=0A= over: hoverOverHandler, // handler onMouseOver=0A= out: hoverOutHandler // handler onMouseOut=0A= }=0A= $j.extend(config, opts)=0A= return config=0A= }=0A= =0A= // = =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 end of $j.fn.figPopup = =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= }) (jQuery) // end of extention of jQuery with figPopup=0A= =0A= =0A= =0A= jQuery(document).ready( function () {=0A= var fp_cfg =3D new jQuery.fn.figPopup()=0A= jQuery('a.figpopup').hoverIntent(fp_cfg)=0A= });=0A= }=0A= =0A= // end of hoverIntent routines for figures' popups=0A= // = *************************************************************************= ***=0A= // implementation of ....=0A= // = *************************************************************************= ***=0A= ------=_NextPart_000_0000_01CB196E.7DC01B70 Content-Type: application/octet-stream Content-Transfer-Encoding: quoted-printable Content-Location: http://www.ncbi.nlm.nih.gov/corehtml/pmc/js/noext.menu.js if (typeof(noext) =3D=3D=3D 'undefined') { noext =3D {};=20 } if (typeof jQuery =3D=3D=3D 'undefined') { throw new Error('noext.Menu: jQuery must be present'); } // Constructor noext.Menu =3D function (n, subMenuStyle) { this.n =3D n; this.subMenuStyle =3D (subMenuStyle =3D=3D=3D 'ext') ? 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