Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for Stem Cells International, enter your email address in the box below.

Stem Cells International
Volume 2015, Article ID 362753, 8 pages
http://dx.doi.org/10.1155/2015/362753
Review Article

Platelet-Derived Growth Factor Receptor Alpha as a Marker of Mesenchymal Stem Cells in Development and Stem Cell Biology

Ramin M. Farahani1 and Munira Xaymardan2

1Institute of Dental Research, Department of Life Science, Faculty of Dentistry, University of Sydney, Sydney, NSW 2006, Australia
2Bioengineering Unit, Department of Life Science, Faculty of Dentistry, University of Sydney, Sydney, NSW 2006, Australia

Received 15 February 2015; Revised 24 May 2015; Accepted 17 June 2015

Academic Editor: Renke Li

Copyright © 2015 Ramin M. Farahani and Munira Xaymardan. 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. A. J. Friedenstein, S. Piatetzky II, and K. V. Petrakova, “Osteogenesis in transplants of bone marrow cells,” Journal of Embryology and Experimental Morphology, vol. 16, no. 3, pp. 381–390, 1966. View at Google Scholar · View at Scopus
  2. A. J. Friedenstein, A. A. Ivanov-Smolenski, R. K. Chajlakjan et al., “Origin of bone marrow stromal mechanocytes in radiochimeras and heterotopic transplants,” Experimental Hematology, vol. 6, no. 5, pp. 440–444, 1978. View at Google Scholar · View at Scopus
  3. M. Xaymardan, M. Cimini, R. Weisel, and R. Li, “Bone marrow stem cells: properties and pluripotency,” in Principles of Regenerative Medicine, R. L. A. Atala, R. Nerem, and J. A. Thomso, Eds., pp. 268–283, Elsevier, 2008. View at Google Scholar
  4. D. D. Houlihan, Y. Mabuchi, S. Morikawa et al., “Isolation of mouse mesenchymal stem cells on the basis of expression of Sca-1 and PDGFR-α,” Nature Protocols, vol. 7, no. 12, pp. 2103–2111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Morikawa, Y. Mabuchi, Y. Kubota et al., “Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow,” Journal of Experimental Medicine, vol. 206, no. 11, pp. 2483–2496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. J. J. H. Chong, V. Chandrakanthan, M. Xaymardan et al., “Adult cardiac-resident MSC-like stem cells with a proepicardial origin,” Cell Stem Cell, vol. 9, no. 6, pp. 527–540, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. J. J. H. Chong, H. Reinecke, M. Iwata, B. Torok-Storb, A. Stempien-Otero, and C. E. Murry, “Progenitor cells identified by PDGFR-alpha expression in the developing and diseased human heart,” Stem Cells and Development, vol. 22, no. 13, pp. 1932–1943, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Uezumi, S. Fukada, N. Yamamoto et al., “Identification and characterization of PDGFRα+ mesenchymal progenitors in human skeletal muscle,” Cell Death & Disease, vol. 5, no. 4, Article ID e1186, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Morikawa, Y. Mabuchi, K. Niibe et al., “Development of mesenchymal stem cells partially originate from the neural crest,” Biochemical and Biophysical Research Communications, vol. 379, no. 4, pp. 1114–1119, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Chen, T. Acciani, T. Le Cras, C. Lutzko, and A.-K. T. Perl, “Dynamic regulation of platelet-derived growth factor receptor α expression in alveolar fibroblasts during realveolarization,” American Journal of Respiratory Cell and Molecular Biology, vol. 47, no. 4, pp. 517–527, 2012. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Artus, J.-J. Panthier, and A.-K. Hadjantonakis, “A role for PDGF signaling in expansion of the extra-embryonic endoderm lineage of the mouse blastocyst,” Development, vol. 137, no. 20, pp. 3361–3372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. R. V. Hoch and P. Soriano, “Roles of PDGF in animal development,” Development, vol. 130, no. 20, pp. 4769–4784, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Kohler and A. Lipton, “Platelets as a source of fibroblast growth-promoting activity,” Experimental Cell Research, vol. 87, no. 2, pp. 297–301, 1974. View at Publisher · View at Google Scholar · View at Scopus
  14. X. Li, A. Pontén, K. Aase et al., “PDGF-C is a new protease-activated ligand for the PDGF α-receptor,” Nature Cell Biology, vol. 2, no. 5, pp. 302–307, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. W. J. LaRochelle, M. Jeffers, W. F. McDonald et al., “PDGF-D, a new protease-activated growth factor,” Nature Cell Biology, vol. 3, no. 5, pp. 517–521, 2001. View at Google Scholar
  16. T. F. Deuel, J. S. Huang, S. S. Huang, P. Stroobant, and M. D. Waterfield, “Expression of a platelet-derived growth factor-like protein in simian sarcoma virus transformed cells,” Science, vol. 221, no. 4618, pp. 1348–1350, 1983. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Rozengurt, P. Stroobant, M. D. Waterfield, T. F. Deuel, and M. Keehan, “Platelet-derived growth factor elicits cyclic AMP accumulation in Swiss 3T3 cells: role of prostaglandin production,” Cell, vol. 34, no. 1, pp. 265–272, 1983. View at Publisher · View at Google Scholar · View at Scopus
  18. C.-H. Heldin and B. Westermark, “Mechanism of action and in vivo role of platelet-derived growth factor,” Physiological Reviews, vol. 79, no. 4, pp. 1283–1316, 1999. View at Google Scholar · View at Scopus
  19. P. Ataliotis and M. Mercola, “Distribution and functions of platelet-derived growth factors and their receptors during embryogenesis,” International Review of Cytology, vol. 172, pp. 95–127, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Ross, D. F. Bowen-Pope, and E. W. Raines, “Platelet-derived growth factor: its potential roles in wound healing, atherosclerosis, neoplasia, and growth and development,” Ciba Foundation Symposium, vol. 116, pp. 98–112, 1985. View at Google Scholar · View at Scopus
  21. L. Liu, S.-W. Chong, N. V. Balasubramaniyan, V. Korzh, and R. Ge, “Platelet-derived growth factor receptor alpha (pdgfr-α) gene in zebrafish embryonic development,” Mechanisms of Development, vol. 116, no. 1-2, pp. 227–230, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. S. L. Palmieri, J. Payne, C. D. Stiles, J. D. Biggers, and M. Mercola, “Expression of mouse PDGF-A and PDGF alpha-receptor genes during pre- and post-implantation development: evidence for a developmental shift from an autocrine to a paracrine mode of action,” Mechanisms of Development, vol. 39, no. 3, pp. 181–191, 1992. View at Publisher · View at Google Scholar · View at Scopus
  23. D. A. Rappolee, C. A. Brenner, R. Schultz, D. Mark, and Z. Werb, “Developmental expression of PDGF, TGF-α, and TGF-β genes in preimplantation mouse embryos,” Science, vol. 241, no. 4874, pp. 1823–1825, 1988. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Ataliotis, K. Symes, M. M. Chou, L. Ho, and M. Mercola, “PDGF signalling is required for gastrulation of Xenopus laevis,” Development, vol. 121, no. 9, pp. 3099–3110, 1995. View at Google Scholar · View at Scopus
  25. M. Jechlinger, A. Sommer, R. Moriggl et al., “Autocrine PDGFR signaling promotes mammary cancer metastasis,” The Journal of Clinical Investigation, vol. 116, no. 6, pp. 1561–1570, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Orr-Urtreger and P. Lonai, “Platelet-derived growth factor-A and its receptor are expressed in separate, but adjacent cell layers of the mouse embryo,” Development, vol. 115, no. 4, pp. 1045–1058, 1992. View at Google Scholar · View at Scopus
  27. N. Takakura, H. Yoshida, Y. Ogura, H. Kataoka, S. Nishikawa, and S.-I. Nishikawa, “PDGFRα expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFRα antibody APA5,” Journal of Histochemistry and Cytochemistry, vol. 45, no. 6, pp. 883–893, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. G. C. Schatteman, K. Morrison-Graham, A. Van Koppen, J. A. Weston, and D. F. Bowen-Pope, “Regulation and role of PDGF receptor α-subunit expression during embryogenesis,” Development, vol. 115, no. 1, pp. 123–131, 1992. View at Google Scholar · View at Scopus
  29. N. A. M. Bax, S. B. Bleyl, R. Gallini et al., “Cardiac malformations in Pdgfrα mutant embryos are associated with increased expression of WT1 and Nkx2.5 in the second heart field,” Developmental Dynamics, vol. 239, no. 8, pp. 2307–2317, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Orr-Urtreger, M. T. Bedford, M.-S. Do, L. Eisenbach, and P. Lonai, “Developmental expression of the alpha receptor for platelet-derived growth factor, which is deleted in the embryonic lethal Patch mutation,” Development, vol. 115, no. 1, pp. 289–303, 1992. View at Google Scholar · View at Scopus
  31. Y. Hayashi, M. R. Bardsley, Y. Toyomasu et al., “Platelet-derived growth factor receptor-α regulates proliferation of gastrointestinal stromal tumor cells with mutations in KIT by stabilizing ETV1,” Gastroenterology, 2015. View at Publisher · View at Google Scholar
  32. H. Chen, X. Gu, Y. Liu et al., “PDGF signalling controls age-dependent proliferation in pancreatic beta-cells,” Nature, vol. 478, no. 7369, pp. 349–355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Xaymardan, J. Zheng, I. Duignan et al., “Senescent impairment in synergistic cytokine pathways that provide rapid cardioprotection in the rat heart,” The Journal of Experimental Medicine, vol. 199, no. 6, pp. 797–804, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. J. M. Edelberg, S. H. Lee, M. Kaur et al., “Platelet-derived growth factor-AB limits the extent of myocardial infarction in a rat model: feasibility of restoring impaired angiogenic capacity in the aging heart,” Circulation, vol. 105, no. 5, pp. 608–613, 2002. View at Publisher · View at Google Scholar · View at Scopus
  35. P. C. H. Hsieh, C. MacGillivray, J. Gannon, F. U. Cruz, and R. T. Lee, “Local controlled intramyocardial delivery of platelet-derived growth factor improves postinfarction ventricular function without pulmonary toxicity,” Circulation, vol. 114, no. 7, pp. 637–644, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. P. C. H. Hsieh, M. E. Davis, J. Gannon, C. MacGillivray, and R. T. Lee, “Controlled delivery of PDGF-BB for myocardial protection using injectable self-assembling peptide nanofibers,” Journal of Clinical Investigation, vol. 116, no. 1, pp. 237–248, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. H. Qian, K. Le Blanc, and M. Sigvardsson, “Primary mesenchymal stem and progenitor cells from bone marrow lack expression of CD44 protein,” The Journal of Biological Chemistry, vol. 287, no. 31, pp. 25795–25807, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. R. M. Samsonraj, B. Rai, P. Sathiyanathan et al., “Establishing criteria for human mesenchymal stem cell potency,” Stem Cells, vol. 33, no. 6, pp. 1878–1891, 2015. View at Publisher · View at Google Scholar
  39. S. Pinho, J. Lacombe, M. Hanoun et al., “PDGFRalpha and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion,” Journal of Experimental Medicine, vol. 210, no. 7, pp. 1351–1367, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Nagoshi, S. Shibata, Y. Kubota et al., “Ontogeny and multipotency of neural crest-derived stem cells in mouse bone marrow, dorsal root ganglia, and whisker pad,” Cell Stem Cell, vol. 2, no. 4, pp. 392–403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Tamai, T. Yamazaki, T. Chino et al., “PDGFRα-positive cells in bone marrow are mobilized by high mobility group box 1 (HMGB1) to regenerate injured epithelia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 16, pp. 6609–6614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Iinuma, E. Aikawa, K. Tamai et al., “Transplanted bone marrow-derived circulating PDGFRα+ cells restore type VII collagen in recessive dystrophic epidermolysis bullosa mouse skin graft,” Journal of Immunology, vol. 194, no. 4, pp. 1996–2003, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Asli, M. Xaymardan, and R. P. Harvey, “Epicardial origin of resident mesenchymal stem cells in the adult mammalian heart,” Journal of Developmental Biology, vol. 2, no. 2, pp. 117–137, 2014. View at Publisher · View at Google Scholar
  44. K. Morrison-Graham, G. C. Schatteman, T. Bork, D. F. Bowen-Pope, and J. A. Weston, “A PDGF receptor mutation in the mouse (Patch) perturbs the development of a non-neuronal subset of neural crest-derived cells,” Development, vol. 115, no. 1, pp. 133–142, 1992. View at Google Scholar · View at Scopus
  45. M. Noseda, M. Harada, S. McSweeney et al., “PDGFRα demarcates the cardiogenic clonogenic Sca1+ stem/progenitor cell in adult murine myocardium,” Nature Communications, vol. 6, Article ID 6930, 2015. View at Publisher · View at Google Scholar
  46. M. Masters and P. R. Riley, “The epicardium signals the way towards heart regeneration,” Stem Cell Research, vol. 13, no. 3, pp. 683–692, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. N. P. Pringle, H. S. Mudhar, E. J. Collarini, and W. D. Richardson, “PDGF receptors in the rat CNS: during late neurogenesis, PDGF alpha-receptor expression appears to be restricted to glial cells of the oligodendrocyte lineage,” Development, vol. 115, no. 2, pp. 535–551, 1992. View at Google Scholar · View at Scopus
  48. N. P. Pringle and W. D. Richardson, “A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage,” Development, vol. 117, no. 2, pp. 525–533, 1993. View at Google Scholar · View at Scopus
  49. H.-J. Yeh, I. Silos-Santiago, Y.-X. Wang, R. J. George, W. D. Snider, and T. F. Deuel, “Developmental expression of the platelet-derived growth factor alpha-receptor gene in mammalian central nervous system,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 5, pp. 1952–1956, 1993. View at Publisher · View at Google Scholar · View at Scopus
  50. H. S. Mudhar, R. A. Pollock, C. Wang, C. D. Stiles, and W. D. Richardson, “PDGF and its receptors in the developing rodent retina and optic nerve,” Development, vol. 118, no. 2, pp. 539–552, 1993. View at Google Scholar · View at Scopus
  51. L. E. Rivers, K. M. Young, M. Rizzi et al., “PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice,” Nature Neuroscience, vol. 11, no. 12, pp. 1392–1401, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. E. L. Jackson, J. M. Garcia-Verdugo, S. Gil-Perotin et al., “PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling,” Neuron, vol. 51, no. 2, pp. 187–199, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. F. J. Sim, C. R. McClain, S. J. Schanz, T. L. Protack, M. S. Windrem, and S. A. Goldman, “CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells,” Nature Biotechnology, vol. 29, no. 10, pp. 934–941, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Fruttiger, A. R. Calver, W. H. Krüger et al., “PDGF mediates a neuron-astrocyte interaction in the developing retina,” Neuron, vol. 17, no. 6, pp. 1117–1131, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. A. R. Calver, A. C. Hall, W.-P. Yu et al., “Oligodendrocyte population dynamics and the role of PDGF in vivo,” Neuron, vol. 20, no. 5, pp. 869–882, 1998. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Oishi, A. Uezumi, A. Kanaji et al., “Osteogenic differentiation capacity of human skeletal muscle-derived progenitor cells,” PLoS ONE, vol. 8, no. 2, Article ID e56641, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Berry and M. S. Rodeheffer, “Characterization of the adipocyte cellular lineage in vivo,” Nature Cell Biology, vol. 15, no. 3, pp. 302–308, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Kurahashi, Y. Nakano, L. E. Peri, J. B. Townsend, S. M. Ward, and K. M. Sanders, “novel population of subepithelial platelet-derived growth factor receptor α-positive cells in the mouse and human colon,” American Journal of Physiology - Gastrointestinal and Liver Physiology, vol. 304, no. 9, pp. G823–G834, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Osada, V. J. Singh, K. Wu, D. B. Sant'Angelo, and M. Pezzano, “Label retention identifies a multipotent mesenchymal stem cell-like population in the postnatal thymus,” PLoS ONE, vol. 8, no. 12, Article ID e83024, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. C. E. Barkauskas, M. J. Cronce, C. R. Rackley et al., “Type 2 alveolar cells are stem cells in adult lung,” Journal of Clinical Investigation, vol. 123, no. 7, pp. 3025–3036, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. R. R. Driskell, B. M. Lichtenberger, E. Hoste et al., “Distinct fibroblast lineages determine dermal architecture in skin development and repair,” Nature, vol. 504, no. 7479, pp. 277–281, 2013. View at Publisher · View at Google Scholar · View at Scopus