Stem Cell Reviews and Reports

, Volume 7, Issue 1, pp 1–16 | Cite as

Human Wharton’s Jelly Stem Cells Have Unique Transcriptome Profiles Compared to Human Embryonic Stem Cells and Other Mesenchymal Stem Cells

  • Chui-Yee Fong
  • Li-Ling Chak
  • Arijit Biswas
  • Jee-Hian Tan
  • Kalamegam Gauthaman
  • Woon-Khiong Chan
  • Ariff Bongso


The human umbilical cord that originates from the embryo is an extra-embryonic membrane and the Wharton’s jelly within it is a rich source of stem cells (hWJSCs). It is not definitely known whether these cells behave as human embryonic stem cells (hESCs), human mesenchymal stem cells (hMSC) or both. They have the unique properties of high proliferation rates, wide multipotency, hypoimmunogenicity, do not induce teratomas and have anticancer properties. These advantages are important considerations for their use in cell based therapies and treatment of cancers. In a search for properties that confer these advantages we compared a detailed transcriptome profiling of hWJSCs using DNA microarrays with that of a panel of known hESCs, hMSCs and stromal cells. hWJSCs expressed low levels of the pluripotent embryonic stem cell markers including POUF1, NANOG, SOX2 and LIN28, thus explaining why they do not produce teratomas. Several cytokines were significantly upregulated in hWJSCs including IL12A which is associated with the induction of apoptosis, thus explaining their anticancer properties. When GO Biological Process analysis was compared between the various stem cell types, hWJSCs showed an increased expression of genes associated with the immune system, chemotaxis and cell death. The ability to modulate immune responses makes hWJSCs an important compatible stem cell source for transplantation therapy in allogeneic settings without immunorejection. The data in the present study which is the first detailed report on hWJSC transcriptomes provide a foundation for future functional studies where the exact mechanisms of these unique properties of hWJSCs can be confirmed.


DNA microarray Human Wharton’s jelly stem cells Stem cells Transcriptome 



We acknowledge the financial support provided to Woon Khiong Chan by the Singapore Stem Cell Consortium (SSCC) and Singapore Ministry of Education Academic Research Fund (MOE-AcRF) and to Ariff Bongso by the Singapore National Medical Research Council (R-174-000-103-213). Chak LiLing was supported by a National University of Singapore postgraduate research scholarship.

Supplementary material

12015_2010_9166_MOESM1_ESM.pdf (55 kb)
Supplementary Table 1 NCBI GEO accession numbers of samples used in the DNA microarray analyses (PDF 55 kb)
12015_2010_9166_MOESM2_ESM.pdf (199 kb)
Supplementary Table 2 Pearson’s correlation coefficient results for hESCs, hECCs, hWJSCs and hFCs. (PDF 199 kb)
12015_2010_9166_MOESM3_ESM.pdf (779 kb)
Supplementary Table 3 Genes significantly upregulated in hWJSCs compared to the sample classes in the analyses performed in Fig. 1b. (PDF 778 kb)
12015_2010_9166_MOESM4_ESM.pdf (186 kb)
Supplementary Table 4 Genes significantly upregulated and shared between hESCs and hECCs compared to hWJSCs in Fig. 1b. (PDF 186 kb)
12015_2010_9166_MOESM5_ESM.pdf (39 kb)
Supplementary Table 5 Gene Ontology Biological Process analysis as performed with DAVID for Fig. 1d. (PDF 38 kb)
12015_2010_9166_MOESM6_ESM.pdf (35 kb)
Supplementary Table 6 Gene Ontology Biological Process analysis as performed with DAVID for Fig. 2d. (PDF 35 kb)


  1. 1.
    Bongso, A., Fong, C. Y., Ng, S. C., & Ratnam, S. (1994). Isolation and culture of inner cell mass cells from human blastocysts. Hum Reprod, 9, 2110–2117.PubMedGoogle Scholar
  2. 2.
    Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145–1147.CrossRefPubMedGoogle Scholar
  3. 3.
    Reubinoff, B. E., Pera, M. F., Fong, C. Y., Trounson, A., & Bongso, A. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol, 18, 399–404.CrossRefPubMedGoogle Scholar
  4. 4.
    Laflamme, M. A., Chen, K. Y., Naumova, A. V., et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol, 25, 1015–1024.CrossRefPubMedGoogle Scholar
  5. 5.
    Shim, J. H., Kim, S. E., Woo, D. H., et al. (2007). Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia, 50, 1228–1238.CrossRefPubMedGoogle Scholar
  6. 6.
    Yang, D., Zhang, Z. J., Oldenburg, M., Ayala, M., & Zhang, S. C. (2008). Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells, 26, 55–63.CrossRefPubMedGoogle Scholar
  7. 7.
    Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663–676.CrossRefPubMedGoogle Scholar
  8. 8.
    Yu, J., Vodyanik, M. A., Smuga-Otto, K., et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917–1920.CrossRefPubMedGoogle Scholar
  9. 9.
    French, A. J., Adams, C. A., Anderson, L. S., Kitchen, J. R., Hughes, M. R., & Wood, S. H. (2008). Development of human cloned blastocysts following somatic cell nuclear transfer with adult fibroblasts. Stem Cells, 26, 485–493.CrossRefPubMedGoogle Scholar
  10. 10.
    Aleckovic, M., & Simon, C. (2008). Is teratoma formation in stem cell research a characterization tool or a window to developmental biology? Reprod Biomed Online, 17, 270–280.CrossRefPubMedGoogle Scholar
  11. 11.
    Lensch, M. W., Schlaeger, T. M., Zon, L. I., et al. (2007). Teratoma formation assays with human embryonic stem cells: a rationale for one type of human-animal chimera. Cell Stem Cell, 1, 253–258.CrossRefPubMedGoogle Scholar
  12. 12.
    Blum, B., & Benvenisty, N. (2008). The tumorigenecity of human embryonic stem cells. Advances in Cancer Res, 100, 133–158.CrossRefGoogle Scholar
  13. 13.
    Bongso, A., Fong, C. Y., & Gauthaman, K. (2008). Taking stem cells to the clinic: major challenges. J Cell Biochem, 105, 1352–1360.CrossRefPubMedGoogle Scholar
  14. 14.
    Pappa, K. I., & Anagnou, N. P. (2009). Novel sources of fetal stem cells: where do they fit on the developmental continuum? Regen Med, 4, 423–433.CrossRefPubMedGoogle Scholar
  15. 15.
    Jones, E., & McGonagle, D. (2008). Human bone marrow mesenchymal stem cells in vivo. Rheumatology, 47, 126–131.CrossRefPubMedGoogle Scholar
  16. 16.
    Fong, C. Y., Richards, M., Manasi, N., Biswas, A., & Bongso, A. (2007). Comparative growth behaviour and characterization of stem cells from human Wharton’s jelly. Reprod Biomed Online, 15, 708–718.CrossRefPubMedGoogle Scholar
  17. 17.
    De Miguel, M. P., Montiel, F. A., Iglesias, P. L., Blazquez Martinez, A. B., & Nistal, M. (2009). Epiblast-derived stem cells in embryonic and adult tissues. Int J Dev Bio, 53, 1529–1540.CrossRefGoogle Scholar
  18. 18.
    Karahuseyinoglu, S., Cinar, O., Kilic, E., et al. (2007). Biology of stem cells in human umbilical cord stroma: in situ and in vitro surveys. Stem Cells, 25, 319–331.CrossRefPubMedGoogle Scholar
  19. 19.
    Chao, K. C., Chao, K. F., Fu, Y. S., & Liu, S. H. (2008). Islet-like clusters derived from mesenchymal stem cells in Wharton’s Jelly of the human umbilical cord for transplantation to control type 1 diabetes. PLoS One, 3, e1451.CrossRefPubMedGoogle Scholar
  20. 20.
    Wang, L., Tran, I., Seshareddy, K., Weiss, M. L., & Detamore, M. S. (2009). A comparison of human bone marrow-derived mesenchymal stem cells and human umbilical cord-derived mesenchymal stromal cells for cartilage tissue engineering. Tissue Eng Part A, 15, 2259–2266.CrossRefPubMedGoogle Scholar
  21. 21.
    Sarugaser, R., Lickorish, D., Baksh, D., et al. (2005). Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors. Stem Cells, 23, 220–229.CrossRefPubMedGoogle Scholar
  22. 22.
    Troyer, D. L., & Weiss, M. L. (2008). Wharton’s jelly-derived cells are a primitive stromal cell population. Stem Cells, 26, 591–599.CrossRefPubMedGoogle Scholar
  23. 23.
    Weiss, M. L., Medicetty, S., Bledsoe, A. R., et al. (2006). Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells, 24, 781–792.CrossRefPubMedGoogle Scholar
  24. 24.
    Hou, T., Xu, J., Wu, X., et al. (2009). Umbilical cord Wharton’s Jelly: a new potential cell source of mesenchymal stromal cells for bone tissue engineering. Tissue Eng Part A, 15, 2325–2334.CrossRefPubMedGoogle Scholar
  25. 25.
    Ganta, C., Chiyo, D., Ayuzawa, R., et al. (2009). Rat umbilical cord stem cells completely abolish rat mammary carcinomas with no evidence of metastasis or recurrence 100 days post-tumor cell inoculation. Cancer Res, 69, 1815–1820.CrossRefPubMedGoogle Scholar
  26. 26.
    Ayuzawa, R., Doi, C., Rachakatla, R. S., et al. (2009). Naive human umbilical cord matrix derived stem cells significantly attenuate growth of human breast cancer cells in vitro and in vivo. Cancer Lett, 280, 31–37.CrossRefPubMedGoogle Scholar
  27. 27.
    Fong CY, Subramanian A, Biswas A, et al. Derivation efficiency, cell proliferation, freeze-thaw survival, stem-cell properties and differentiation of human Wharton’s jelly stem cells. Reprod BioMed. 2010. Online doi: 10.1016/j.rbmo.2010.04.010.
  28. 28.
    Reich, M., Liefeld, T., Gould, J., Lerner, J., Tamayo, P., & Mesirov, J. P. (2006). GenePattern 2.0. Nat Genet, 38, 500–501.CrossRefPubMedGoogle Scholar
  29. 29.
    Gould, J., Getz, G., Monti, S., Reich, M., & Mesirov, J. P. (2006). Comparative gene marker selection suite. Bioinformatics, 22, 1924–1925.CrossRefPubMedGoogle Scholar
  30. 30.
    Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B (Methodological), 57, 289–300.Google Scholar
  31. 31.
    Corram, T. E., Settles, M. L., & Chen, X. (2009). Large-scale analysis of antisense transcription in wheat using the Affymetrix GeneChip Wheat Genome Array. BMC Genomics, 10, 253.CrossRefGoogle Scholar
  32. 32.
    Maisel, M., Herr, A., Milosevic, J., et al. (2007). Transcription profiling of adult and fetal human neuroprogenitors identifies divergent paths to maintain the neuroprogenitor cell state. Stem Cells, 25, 1231–1240.CrossRefPubMedGoogle Scholar
  33. 33.
    Subramanian, A., Tamayo, P., Mootha, V. K., et al. (2005). Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA, 102, 15545–15550.CrossRefPubMedGoogle Scholar
  34. 34.
    Cai, J., Chen, J., Liu, Y., et al. (2006). Assessing self-renewal and differentiation in human embryonic stem cell lines. Stem Cells, 24, 516–530.CrossRefPubMedGoogle Scholar
  35. 35.
    Richards, M., Tan, S. P., Tan, J. H., Chan, W. K., & Bongso, A. (2002). The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells, 22, 51–64.CrossRefGoogle Scholar
  36. 36.
    Anzalone, R., Iacono, M. L., Corrao, S., et al. (2009). New emerging potentials for human Wharton’s jelly mesenchymal stem cells: immunological features and hepatocyte-like differentiative capacity. Stem Cells Dev, 19, 423–438.CrossRefGoogle Scholar
  37. 37.
    La Rocca, G., Anzalone, R., Corrao, S., et al. (2009). Isolation and characterization of Oct-4+/HLA-G + mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markers. Histochem Cell Biol, 131, 267–282.CrossRefPubMedGoogle Scholar
  38. 38.
    Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc, 4, 44–57.CrossRefGoogle Scholar
  39. 39.
    The International Stem Cell Initiative. (2007). Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol, 25, 803–816.CrossRefGoogle Scholar
  40. 40.
    Nekanti, U., Rao, V. B., Bahirvani, A. G., Jan, M., Totey, S., & Ta, M. (2010). Long-term expansion and pluripotent marker array analysis of Wharton’s jelly-derived mesenchymal stem cells. Stem Cells Dev, 19, 117–30.CrossRefPubMedGoogle Scholar
  41. 41.
    Alaminos, M., Pérez-Köhler, B., Garzón, I., et al. (2010). Transdifferentiation potentiality of human Wharton’s jelly stem cells towards vascular endothelial cells. J Cell Physiol, 223, 640–647.PubMedGoogle Scholar
  42. 42.
    Kim, J. S., Romero, R., Tarca, A. L., et al. (2008). Gene expression profiling demonstrates a novel role for foetal fibrocytes and the umbilical vessels in human fetoplacental development. J Cell Mol Med, 12, 1317–1330.CrossRefPubMedGoogle Scholar
  43. 43.
    Blum, B., Bar-Nur, O., Golan-Lev, T., & Benvenisty, N. (2009). The anti-apoptotic gene survivin contributes to teratoma formation by human embryonic stem cells. Nat Biotechnol, 27, 281–287.CrossRefPubMedGoogle Scholar
  44. 44.
    Muller, F., Laurent, L., Kostka, D., et al. (2008). Regulatory networks define phenotypic classes of human stem cell lines. Nature, 455, 401–405.CrossRefPubMedGoogle Scholar
  45. 45.
    Chin, M. H., Mason, M. J., Xie, W., et al. (2009). Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell, 5, 111–123.CrossRefPubMedGoogle Scholar
  46. 46.
    Carlin, R., Davis, D., Weiss, M., Schultz, B., & Troyer, D. (2006). Expression of early transcription factors Oct-4, Sox-2 and Nanog by porcine umbilical cord (PUC) matrix cells. Reprod Biol Endocrinol, 4, 8.CrossRefPubMedGoogle Scholar
  47. 47.
    Jansen BJ, Gilissen C, Roelofs H, et al. Functional differences between mesenchymal stem cell population are reflected by their transcriptome. Stem Cell Dev (in press). 2010.Google Scholar
  48. 48.
    Ben, I., Thomson, M. W., Carey, V. J., et al. (2008). An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet, 40, 499–507.CrossRefGoogle Scholar
  49. 49.
    Knoepfler, P. S. (2009). Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine. Stem Cells, 27, 1050–1056.CrossRefPubMedGoogle Scholar
  50. 50.
    Takeda, J., Seino, S., & Bell, G. I. (1992). Human Oct3 gene family: cDNA sequences, alternative splicing, gene organization, chromosomal location, and expression at low levels in adult tissues. Nucleic Acids Res, 20, 4613–4620.CrossRefPubMedGoogle Scholar
  51. 51.
    Lee, J., Kim, H. K., Rho, J. Y., Han, Y. M., & Kim, J. (2006). The human OCT-4 isoforms differ in their ability to confer self-renewal. J Biol Chem, 281, 33554–33565.CrossRefPubMedGoogle Scholar
  52. 52.
    Pain, D., Chirn, G. W., Strassel, C., & Kemp, D. M. (2005). Multiple retropseudogenes from pluripotent cell-specific gene expression indicates a potential signature for novel gene identification. J Biol Chem, 280, 6265–6268.CrossRefPubMedGoogle Scholar
  53. 53.
    Liedtke, S., Stephan, M., & Kogler, G. (2008). Oct4 expression revisited: potential pitfalls for data misinterpretation in stem cell research. Biol Chem, 389, 845–850.CrossRefPubMedGoogle Scholar
  54. 54.
    Niwa, H., Miyazaki, J., & Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet, 24, 37237–6.CrossRefGoogle Scholar
  55. 55.
    Lengner, C. J., Camargo, F. D., Hochedlinger, K., et al. (2007). Oct4 expression is not required for mouse somatic stem cell self-renewal. Cell Stem Cell, 1, 403–415.CrossRefPubMedGoogle Scholar
  56. 56.
    Riekstina, U., Cakstina, I., Parfejevs, V., et al. (2009). Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis. Stem Cell Rev and Rep, 5, 378–386.CrossRefGoogle Scholar
  57. 57.
    Greco, S. J., Liu, K., & Rameshwar, P. (2007). Functional similarities among genes regulated by OCT4 in human mesenchymal and embryonic stem cells. Stem Cells, 25, 3143–3154.CrossRefPubMedGoogle Scholar
  58. 58.
    Liu, T., Wu, Y., Guo, X., Hui, J., Lee, E., & Lim, B. (2008). Effects of ectopic Nanog and Oct4 overexpression on mesenchymal stem cells. Stem Cell Dev, 18, 1013–1022.CrossRefGoogle Scholar
  59. 59.
    Guillot, P. V., Gotherstrom, C., Chan, J., Kurata, H., & Fisk, N. M. (2007). Human first-trimester fetal MSC express pluripotency markers and grow faster and have longer telomeres than adult MSC. Stem Cells, 25, 646–54.CrossRefPubMedGoogle Scholar
  60. 60.
    Friedman, R., Betancur, M., Boissel, L., Tuncer, H., Cetrulo, C., & Klingemann, H. (2007). Umbilical cord mesenchymal stem cells: adjuvants for human cell transplantation. Biol Blood Marrow Transplant, 13, 1477–1486.CrossRefPubMedGoogle Scholar
  61. 61.
    Le Blanc, K. (2003). Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy, 5, 485–489.CrossRefPubMedGoogle Scholar
  62. 62.
    Tse, W. T., Pendleton, J. D., Beyer, W. M., Egalka, M. C., & Guinan, E. C. (2003). Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation, 75, 389–397.CrossRefPubMedGoogle Scholar
  63. 63.
    Horwitz, E. M., & Dominici, M. (2008). How do mesenchymal stromal cells exert their therapeutic benefit? Cytotherapy, 10, 771–774.CrossRefPubMedGoogle Scholar
  64. 64.
    Weiss, M. L., Anderson, C., Medicetty, S., et al. (2008). Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells, 26, 2865–2874.CrossRefPubMedGoogle Scholar
  65. 65.
    Yoo, K. H., Jang, I. K., Lee, M. W., et al. (2009). Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues. Cell Immunol, 259, 150–156.CrossRefPubMedGoogle Scholar
  66. 66.
    Djouad, F., Charbonnier, L. M., Bouffi, C., et al. (2007). Mesenchymal stem cells inhibit the differentiation of dendritic cells through an interleukin-6-dependent mechanism. Stem Cells, 25, 2025–2032.CrossRefPubMedGoogle Scholar
  67. 67.
    Rabreau, M., Rouas-Freiss, N., Landi, M., Le Danff, C., & Carosella, E. D. (2000). HLA-G expression in trophoblast cells is independent of embryonic development. Hum Immunol, 61, 1108–1112.CrossRefPubMedGoogle Scholar
  68. 68.
    Moffett, A., & Loke, Y. W. (2004). The immunological paradox of pregnancy: a reappraisal. Placenta, 25, 1–8.CrossRefPubMedGoogle Scholar
  69. 69.
    Rouas-Freiss, N., Goncalves, R. M., Menier, C., Dausset, J., & Carosella, E. D. (1997). Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A, 94, 11520–11525.CrossRefPubMedGoogle Scholar
  70. 70.
    Le Bouteiller, P. (2000). HLA-G in the human placenta: expression and potential functions. Biochem Soc Trans, 28, 208–212.PubMedGoogle Scholar
  71. 71.
    Clark, D. A., Yu, G., Levy, G. A., & Gorczynski, R. M. (2001). Procoagulants in fetus rejection: the role of the OX-2 (CD200) tolerance signal. Semin Immunol, 13, 255–263.CrossRefPubMedGoogle Scholar
  72. 72.
    Clark, D. A., Keil, A., Chen, Z., Markert, U., Manuel, J., & Gorczynski, R. M. (2003). Placental trophoblast from successful human pregnancies expresses the tolerance signaling molecule, CD200 (OX-2). Am J Reprod Immunol, 50, 187–195.CrossRefPubMedGoogle Scholar
  73. 73.
    Chamberlain, G., Fox, J., Ashton, B., & Middleton, J. (2007). Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells, 25, 2739–2749.CrossRefPubMedGoogle Scholar
  74. 74.
    Gorczynski, R. M., Chen, Z., He, W., et al. (2009). Expression of a CD200 transgene is necessary for induction but not maintenance of tolerance to cardiac and skin allografts. J Immunol, 183, 1560–1568.CrossRefPubMedGoogle Scholar
  75. 75.
    Fong, C. Y., Chak, L. L., Subramanian, A., et al. (2009). A three dimensional anchorage independent in vitro system for the prolonged growth of embryoid bodies to study cancer cell behaviour and anticancer agents. Stem Cell Rev Rep, 5, 410–419.CrossRefGoogle Scholar
  76. 76.
    Moser, B., Wolf, M., Walz, A., & Loetscher, P. (2004). Chemokines: multiple levels of leukocyte migration control. Trends Immunol, 25, 75–84.CrossRefPubMedGoogle Scholar
  77. 77.
    Kobayashi, M., Fitz, L., Ryan, M., et al. (1989). Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med, 170, 827–845.CrossRefPubMedGoogle Scholar
  78. 78.
    Wolf, S. F., Temple, P. A., Kobayashi, M., et al. (1991). Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J Immunol, 146, 3074–3081.PubMedGoogle Scholar
  79. 79.
    Colombo, M. P., & Trinchieri, G. (2002). Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev, 13, 155–168.CrossRefPubMedGoogle Scholar
  80. 80.
    Weiss, J. M., Subleski, J. J., Wigginton, J. M., & Wiltrout, R. H. (2007). Immunotherapy of cancer by IL-12-based cytokine combinations. Expert Opin Biol Ther, 7, 1705–1721.CrossRefPubMedGoogle Scholar
  81. 81.
    Herman, J. G., & Meadows, G. G. (2007). Increased class 3 semaphorin expression modulates the invasive and adhesive properties of prostate cancer cells. Int J Oncol, 30, 1231–1238.PubMedGoogle Scholar
  82. 82.
    Esselens, C., Malapeira, J., Colomé, N., et al. (2010). The cleavage of semaphorin 3C induced by ADAMTS1 promotes cell migration. J Biol Chem, 285, 2463–2473.CrossRefPubMedGoogle Scholar
  83. 83.
    Capparuccia, L., & Tamagnone, L. (2009). Semaphorin signaling in cancer cells and in cells of the tumor microenvironment—two sides of a coin. J Cell Sci, 122, 1723–1736.CrossRefPubMedGoogle Scholar
  84. 84.
    Tamm, I., Wang, Y., Sausville, E., et al. (1998). IAP-family protein survivin inhibits caspase activity and apoptosis induced by Fas (CD95), Bax, caspases, and anticancer drugs. Cancer Res, 58, 5315–5320.PubMedGoogle Scholar
  85. 85.
    Baker, D. E., Harrison, N. J., Maltby, E., et al. (2007). Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat Biotechnol, 25, 207–215.CrossRefPubMedGoogle Scholar
  86. 86.
    Angelucci, S., Marchisio, M., Di Giuseppe, F., et al. (2010). Proteome analysis of human Wharton’s jelly cells during in vitro expansion. Proteome Science, 8, 18–25.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Chui-Yee Fong
    • 1
  • Li-Ling Chak
    • 2
  • Arijit Biswas
    • 1
  • Jee-Hian Tan
    • 2
  • Kalamegam Gauthaman
    • 1
  • Woon-Khiong Chan
    • 2
  • Ariff Bongso
    • 1
    • 3
  1. 1.Department of Obstetrics and GynaecologyNational University of SingaporeKent RidgeSingapore
  2. 2.Department of Biological SciencesNational University of SingaporeKent RidgeSingapore
  3. 3.Department of Obstetrics and Gynaecology, Yong Loo Lin School of MedicineNational University of SingaporeKent RidgeSingapore

Personalised recommendations