Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2011 (2011), Article ID 368192, 9 pages
http://dx.doi.org/10.4061/2011/368192
Research Article

Comparison of Gene Expression in Human Embryonic Stem Cells, hESC-Derived Mesenchymal Stem Cells and Human Mesenchymal Stem Cells

1Centre National de la Recherche Scientifique, Institut André Lwoff, 7, Rue Guy Moquet, 94800 Villejuif, France
2CNRS, Institut de Chimie des Substances Naturelles (ICSN), Avenue de la Terrasse, 91190 Gif Sur Yvette, France
3CNRS, Institut de Génétique Humaine (IGH), 141, Rue Cardonille, 34396 Montpellier, France
4Institut National de la Santé et Recherche Médicale U972, and University Paris 11, Hôpital de Bicêtre, 80 Avenue du Général Leclerc, 94276 Kremlin Bicêtre Cedex, France

Received 4 April 2011; Accepted 22 May 2011

Academic Editor: Jackie R. Bickenbach

Copyright © 2011 Romain Barbet et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. Charbord, “Bone marrow mesenchymal stem cells: historical overview and concepts,” Human Gene Therapy, vol. 21, no. 9, pp. 1045–1056, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Short, N. Brouard, T. Occhiodoro-Scott, A. Ramakrishnan, and P. J. Simmons, “Mesenchymal stem cells,” Archives of Medical Research, vol. 34, no. 6, pp. 565–571, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Pontikoglou, B. Delorme, and P. Charbord, “Human bone marrow native mesenchymal stem cells,” Regenerative Medicine, vol. 3, no. 5, pp. 731–741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Deschaseaux, F. Gindraux, R. Saadi, L. Obert, D. Chalmers, and P. Herve, “Direct selection of human bone marrow mesenchymal stem cells using an anti-CD49a antibody reveals their CD45med,low phenotype,” British Journal of Haematology, vol. 122, no. 3, pp. 506–517, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. M. A. Lagar'kova, A. V. Lyakisheva, E. S. Filonenko et al., “Characteristics of human bone marrow mesenchymal stem cells isolated by immunomagnetic selection,” Bulletin of Experimental Biology and Medicine, vol. 141, no. 1, pp. 112–116, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Méndez-Ferrer, T. V. Michurina, F. Ferraro et al., “Mesenchymal and haematopoietic stem cells form a unique bone marrow niche,” Nature, vol. 466, no. 7308, pp. 829–834, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. I. Peiffer, P. Eid, R. Barbet et al., “A sub-population of high proliferative potential-quiescent human mesenchymal stem cells is under the reversible control of interferon alpha/beta,” Leukemia, vol. 21, no. 4, pp. 714–724, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. R. A. Kopher, V. R. Penchev, M. S. Islam, K. L. Hill, S. Khosla, and D. S. Kaufman, “Human embryonic stem cell-derived CD34(+) cells function as MSC progenitor cells,” Bone, vol. 47, no. 4, pp. 718–728, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. E. N. Olivier, A. C. Rybicki, and E. E. Bouhassira, “Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells,” Stem Cells, vol. 24, no. 8, pp. 1914–1922, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. M. E. Stavropoulos, I. Mengarelli, and T. Barberi, “Differentiation of multipotent mesenchymal precursors and skeletal myoblasts from human embryonic stem cells,” in Current Protocols in Stem Cell Biology, chapter 1, unit 1F 8, John Wiley & Sons, New York, NY, USA, 2009. View at Google Scholar
  12. A. Mahmood, L. Harkness, H. D. Schrøder, B. M. Abdallah, and M. Kassem, “Enhanced differentiation of human embryonic stem cells to mesenchymal progenitors by inhibition of TGF-beta/activin/nodal signaling using SB-431542,” Journal of Bone and Mineral Research, vol. 25, no. 6, pp. 1216–1233, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. T. Barberi, L. M. Willis, N. D. Socci, and L. Studer, “Derivation of multipotent mesenchymal precursors from human embryonic stem cells,” PLoS Medicine, vol. 2, no. 6, p. e161, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Delorme, J. Ringe, N. Gallay et al., “Specific plasma membrane protein phenotype of culture-amplified and native human bone marrow mesenchymal stem cells,” Blood, vol. 111, no. 5, pp. 2631–2635, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Kaps, A. Hoffmann, Y. Zilberman et al., “Distinct roles of BMP receptors type IA and IB in osteo-/chondrogenic differentiation in mesenchymal progenitors (C3H10T1/2),” BioFactors, vol. 20, no. 2, pp. 71–84, 2004. View at Google Scholar · View at Scopus
  16. K. Lavery, P. Swain, D. Falb, and M. H. Alaoui-Ismaili, “BMP-2/4 and BMP-6/7 differentially utilize cell surface receptors to induce osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells,” Journal of Biological Chemistry, vol. 283, no. 30, pp. 20948–20958, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. B. Delorme, J. Ringe, C. Pontikoglou et al., “Specific lineage-priming of bone marrow mesenchymal stem cells provides the molecular framework for their plasticity,” Stem Cells, vol. 27, no. 5, pp. 1142–1151, 2009. View at Publisher · View at Google Scholar
  18. F. Ulloa-Montoya, B. L. Kidder, K. A. Pauwelyn et al., “Comparative transcriptome analysis of embryonic and adult stem cells with extended and limited differentiation capacity,” Genome Biology, vol. 8, no. 8, p. R163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. J. Greco and P. Rameshwar, “Enhancing effect of IL-1alpha on neurogenesis from adult human mesenchymal stem cells: implication for inflammatory mediators in regenerative medicine,” Journal of Immunology, vol. 179, no. 5, pp. 3342–3350, 2007. View at Google Scholar · View at Scopus
  20. L. C. van den Berk, B. J. Jansen, K. G. Siebers-Vermeulen et al., “Mesenchymal stem cells respond to TNF but do not produce TNF,” Journal of Leukocyte Biology, vol. 87, no. 2, pp. 283–289, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. P. Batard, M. N. Monier, N. Fortunel et al., “TGF-(beta)1 maintains hematopoietic immaturity by a reversible negative control of cell cycle and induces CD34 antigen up-modulation,” Journal of Cell Science, vol. 113, no. 3, pp. 383–390, 2000. View at Google Scholar · View at Scopus
  22. N. Fortunel, J. Hatzfeld, S. Kisselev et al., “Release from quiescence of primitive human hematopoietic stem/progenitor cells by blocking their cell-surface TGF-beta type II receptor in a short-term in vitro assay,” Stem Cells, vol. 18, no. 2, pp. 102–111, 2000. View at Google Scholar · View at Scopus
  23. N. O. Fortunel, A. Hatzfeld, and J. A. Hatzfeld, “Transforming growth factor-beta: pleiotropic role in the regulation of hematopoiesis,” Blood, vol. 96, no. 6, pp. 2022–2036, 2000. View at Google Scholar · View at Scopus
  24. P. Sansilvestri, A. A. Cardoso, P. Batard et al., “Early CD34(high) cells can be separated into KIT(high) cells in which transforming growth factor-beta (TGF-beta) downmodulates c-kit and KIT(low) cells in which anti-TGF-beta upmodulates c-kit,” Blood, vol. 86, no. 5, pp. 1729–1735, 1995. View at Google Scholar · View at Scopus
  25. Y. Gunji, M. Nakamura, H. Osawa et al., “Human primitive hematopoietic progenitor cells are more enriched in KIT(low) cells than in KIT(high) cells,” Blood, vol. 82, no. 11, pp. 3283–3289, 1993. View at Google Scholar · View at Scopus
  26. I. Kawashima, E. D. Zanjani, G. Almaida-Porada, A. W. Flake, H. Zeng, and M. Ogawa, “CD34+ human marrow cells that express low levels of Kit protein are enriched for long-term marrow-engrafting cells,” Blood, vol. 87, no. 10, pp. 4136–4142, 1996. View at Google Scholar · View at Scopus
  27. M. Xiao, B. K. Oppenlander, J. M. Plunkett, and D. C. Dooley, “Expression of Flt3 and c-kit during growth and maturation of human CD34+CD38- cells,” Experimental Hematology, vol. 27, no. 5, pp. 916–927, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. N. O. Fortunel, J. A. Hatzfeld, P. A. Rosemary et al., “Long-term expansion of human functional epidermal precursor cells: promotion of extensive amplification by low TGF-beta1 concentrations,” Journal of Cell Science, vol. 116, no. 19, pp. 4043–4052, 2003. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Li, P. J. Simmons, and P. Kaur, “Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 7, pp. 3902–3907, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Bianco, P. G. Robey, I. Saggio, and M. Riminucci, ““Mesenchymal” stem cells in human bone marrow (Skeletal Stem Cells): a critical discussion of their nature, identity, and significance in incurable skeletal disease,” Human Gene Therapy, vol. 21, no. 9, pp. 1057–1066, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. T. M. Dexter, T. D. Allen, D. Scott, and N. M. Teich, “Isolation and characterisation of a bipotential haematopoietic cell line,” Nature, vol. 277, no. 5696, pp. 471–474, 1979. View at Google Scholar · View at Scopus
  32. M. A. Moore, A. P. Sheridan, T. D. Allen, and T. M. Dexter, “Prolonged hematopoiesis in a primate bone marrow culture system: characteristics of stem cell production and the hematopoietic microenvironment,” Blood, vol. 54, no. 4, pp. 775–793, 1979. View at Google Scholar · View at Scopus
  33. I. Peiffer, D. Belhomme, R. Barbet et al., “Simultaneous differentiation of endothelial and trophoblastic cells derived from human embryonic stem cells,” Stem Cells and Development, vol. 16, no. 3, pp. 393–401, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. J. A. Thomson, J. Itskovitz-Eldor, S. S. Shapiro et al., “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar
  35. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Willems, L. Leyns, and J. Vandesompele, “Standardization of real-time PCR gene expression data from independent biological replicates,” Analytical Biochemistry, vol. 379, no. 1, pp. 127–129, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Weksberg, S. Hughes, L. Moldovan, A. S. Bassett, E. W. Chow, and J. A. Squire, “A method for accurate detection of genomic microdeletions using real-time quantitative PCR,” BMC Genomics, vol. 6, p. 180, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Arpornmaeklong, S. E. Brown, Z. Wang, and P. H. Krebsbach, “Phenotypic characterization, osteoblastic differentiation, and bone regeneration capacity of human embryonic stem cell-derived mesenchymal stem cells,” Stem Cells and Development, vol. 18, no. 7, pp. 955–968, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. N. S. Hwang, S. Varghese, H. J. Lee et al., “In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 52, pp. 20641–20646, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. S. E. Brown, W. Tong, and P. H. Krebsbach, “The derivation of mesenchymal stem cells from human embryonic stem cells,” Cells Tissues Organs, vol. 189, no. 1–4, pp. 256–260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. F. Djouad, C. Bony, F. Canovas et al., “Transcriptomic analysis identifies foxo3a as a novel transcription factor regulating mesenchymal stem cell chrondrogenic differentiation,” Cloning and Stem Cells, vol. 11, no. 3, pp. 407–416, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. L. Zhao, G. Li, K. M. Chan, Y. Wang, and P. F. Tang, “Comparison of multipotent differentiation potentials of murine primary bone marrow stromal cells and mesenchymal stem cell line C3H10T1/2,” Calcified Tissue International, vol. 84, no. 1, pp. 56–64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Aziz, T. Miyake, K. A. Engleka, J. A. Epstein, and J. C. McDermott, “Menin expression modulates mesenchymal cell commitment to the myogenic and osteogenic lineages,” Developmental Biology, vol. 332, no. 1, pp. 116–130, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. I. Peiffer, R. Barbet, Y. P. Zhou et al., “Use of xenofree matrices and molecularly-defined media to control human embryonic stem cell pluripotency: effect of low physiological TGF-beta concentrations,” Stem Cells and Development, vol. 17, no. 3, pp. 519–533, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. G. D'Ippolito, S. Diabira, G. A. Howard, P. Menei, B. A. Roos, and P. C. Schiller, “Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential,” Journal of Cell Science, vol. 117, no. 14, pp. 2971–2981, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Stockis, D. Colau, P. G. Coulie, and S. Lucas, “Membrane protein GARP is a receptor for latent TGF-beta on the surface of activated human treg,” European Journal of Immunology, vol. 39, no. 12, pp. 3315–3322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. S. C. Gautam, C. J. Noth, L. M. Niewenhuis, N. Janakiraman, J. S. Kim, and M. Chopp, “Transforming growth factor beta-1 (TGF-beta 1) potentiates IL1 alpha-induced IL6 mRNA and cytokine protein production in a human astrocytoma cell line,” Oncology Research, vol. 5, no. 10-11, pp. 423–432, 1993. View at Google Scholar · View at Scopus
  48. A. Vambutas, J. DeVoti, E. Goldofsky, M. Gordon, M. Lesser, and V. Bonagura, “Alternate splicing of interleukin-1 receptor type II (IL1R2) in vitro correlates with clinical glucocorticoid responsiveness in patients with AIED,” PLoS ONE, vol. 4, no. 4, p. e5293, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Qiu, X. Wu, F. Zhang, T. L. Clemens, M. Wan, and X. Cao, “TGF-beta type II receptor phosphorylates PTH receptor to integrate bone remodelling signalling,” Nature Cell Biology, vol. 12, no. 3, pp. 224–234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Romero, W. B. Sneddon, Y. Yang, D. Wheeler, H. C. Blair, and P. A. Friedman, “Parathyroid hormone receptor directly interacts with dishevelled to regulate beta-catenin signaling and osteoclastogenesis,” Journal of Biological Chemistry, vol. 285, no. 19, pp. 14756–14763, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Weiss, T. Hennig, R. Bock, E. Steck, and W. Richter, “Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells,” Journal of Cellular Physiology, vol. 223, no. 1, pp. 84–93, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. A. E. Nedeau, R. J. Bauer, K. Gallagher, H. Chen, Z. J. Liu, and O. C. Velazquez, “A CXCL5- and bFGF-dependent effect of PDGF-B-activated fibroblasts in promoting trafficking and differentiation of bone marrow-derived mesenchymal stem cells,” Experimental Cell Research, vol. 314, no. 11-12, pp. 2176–2186, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. A. Muley, S. Majumder, G. K. Kolluru et al., “Secreted frizzled-related protein 4: an angiogenesis inhibitor,” American Journal of Pathology, vol. 176, no. 3, pp. 1505–1516, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. W. Si, Q. Kang, H. H. Luu et al., “CCN1/Cyr61 is regulated by the canonical Wnt signal and plays an important role in Wnt3A-induced osteoblast differentiation of mesenchymal stem cells,” Molecular and Cellular Biology, vol. 26, no. 8, pp. 2955–2964, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Baines, H. Mayani, M. Bains, J. Fisher, T. Hoy, and A. Jacobs, “Enrichment of CD34 (My10)-postitive myeloid and erythroid progenitors from human marrow and their growth in cultures supplemented with recombinant human granulocyte-macrophage colony-stimulating factor,” Experimental Hematology, vol. 16, no. 9, pp. 785–789, 1988. View at Google Scholar · View at Scopus
  56. S. Kaiser, B. Hackanson, M. Follo et al., “BM cells giving rise to MSC in culture have a heterogeneous CD34 and CD45 phenotype,” Cytotherapy, vol. 9, no. 5, pp. 439–450, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. P. J. Simmons and B. Torok-Storb, “CD34 expression by stromal precursors in normal human adult bone marrow,” Blood, vol. 78, no. 11, pp. 2848–2853, 1991. View at Google Scholar · View at Scopus