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Stem Cells International
Volume 2016, Article ID 1947157, 13 pages
http://dx.doi.org/10.1155/2016/1947157
Research Article

Investigation of the Cell Surface Proteome of Human Periodontal Ligament Stem Cells

1Colgate Australian Clinical Dental Research Centre, School of Dentistry, University of Adelaide, Adelaide, SA 50052, Australia
2Laboratory of Tissue Regeneration and Immunology and Department of Periodontics, Beijing Key Laboratory of Tooth Regeneration and Function Reconstruction, School of Stomatology, Capital Medical University, Beijing 1000443, China
3School of Medicine, Faculty of Health Sciences, University of Adelaide, Adelaide, SA 50054, Australia
4Oral Microbiology, School of Dentistry, University of Adelaide, Adelaide, SA 50055, Australia
5Mesenchymal Stem Cell Laboratory, School of Medicine, Faculty of Health Sciences, University of Adelaide, Adelaide, SA 50056, Australia
6South Australian Health and Medical Research Institute, Adelaide, SA 5000, Australia

Received 27 May 2016; Accepted 3 July 2016

Academic Editor: Athina Bakopoulou

Copyright © 2016 Jimin Xiong 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. T. Graf and M. Stadtfeld, “Heterogeneity of embryonic and adult stem cells,” Cell Stem Cell, vol. 3, no. 5, pp. 480–483, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Owen and A. J. Friedenstein, “Stromal stem cells: marrow-derived osteogenic precursors,” Ciba Foundation Symposium, vol. 136, pp. 42–60, 1988. View at Google Scholar · View at Scopus
  3. S. Gronthos, A. C. W. Zannettino, S. E. Graves, S. Ohta, S. J. Hay, and P. J. Simmons, “Differential cell surface expression of the STRO-1 and alkaline phosphatase antigens on discrete developmental stages in primary cultures of human bone cells,” Journal of Bone and Mineral Research, vol. 14, no. 1, pp. 47–56, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. B.-M. Seo, M. Miura, S. Gronthos et al., “Investigation of multipotent postnatal stem cells from human periodontal ligament,” The Lancet, vol. 364, no. 9429, pp. 149–155, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. D. Menicanin, K. M. Mrozik, N. Wada et al., “Periodontal-ligament-derived stem cells exhibit the capacity for long-term survival, self-renewal, and regeneration of multiple tissue types in vivo,” Stem Cells and Development, vol. 23, no. 9, pp. 1001–1011, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. S. C. Chen, V. Marino, S. Gronthos, and P. M. Bartold, “Location of putative stem cells in human periodontal ligament,” Journal of Periodontal Research, vol. 41, no. 6, pp. 547–553, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. C. Rincon, W. G. Young, and P. M. Bartold, “The epithelial cell rests of Malassez—a role in periodontal regeneration?” Journal of Periodontal Research, vol. 41, no. 4, pp. 245–252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Iwata, M. Yamato, H. Tsuchioka et al., “Periodontal regeneration with multi-layered periodontal ligament-derived cell sheets in a canine model,” Biomaterials, vol. 30, no. 14, pp. 2716–2723, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. P. M. Bartold, S. Shi, and S. Gronthos, “Stem cells and periodontal regeneration,” Periodontology 2000, vol. 40, no. 1, pp. 164–172, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. C. A. G. McCulloch, “Progenitor cell populations in the periodontal ligament of mice,” Anatomical Record, vol. 211, no. 3, pp. 258–262, 1985. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. G. McCulloch, E. Nemeth, B. Lowenberg, and A. H. Melcher, “Paravascular cells in endosteal spaces of alveolar bone contribute to periodontal ligament cell populations,” Anatomical Record, vol. 219, no. 3, pp. 233–242, 1987. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Yamada, S. Murakami, R. Matoba et al., “Expression profile of active genes in human periodontal ligament and isolation of PLAP-1, a novel SLRP family gene,” Gene, vol. 275, no. 2, pp. 279–286, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Saito, T. Yoshizawa, F. Takizawa et al., “A cell line with characteristics of the periodontal ligament fibroblasts is negatively regulated for mineralization and Runx2/Cbfa1/Osf2 activity, part of which can be overcome by bone morphogenetic protein-2,” Journal of Cell Science, vol. 115, no. 21, pp. 4191–4200, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Morsczeck, G. Schmalz, T. E. Reichert, F. Völlner, K. Galler, and O. Driemel, “Somatic stem cells for regenerative dentistry,” Clinical Oral Investigations, vol. 12, no. 2, pp. 113–118, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. C. A. McCulloch, “Proteomics for the periodontium: current strategies and future promise,” Periodontology 2000, vol. 40, no. 1, pp. 173–183, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Zhang, T. Wang, W. Chen et al., “Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components,” Proteomics, vol. 5, no. 1, pp. 198–211, 2005. View at Publisher · View at Google Scholar · View at Scopus
  17. Q. Xia, T. Wang, F. Taub et al., “Quantitative proteomics of intracellular Porphyromonas gingivalis,” Proteomics, vol. 7, no. 23, pp. 4323–4337, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. P. D. Veith, G. H. Talbo, N. Slakeski, and E. C. Reynolds, “Identification of a novel heterodimeric outer membrane protein of Porphyromonas gingivalis by two-dimensional gel electrophoresis and peptide mass fingerprinting,” European Journal of Biochemistry, vol. 268, no. 17, pp. 4748–4757, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. M. J. Somerman, S. Y. Archer, G. R. Imm, and R. A. Foster, “A comparative study of human periodontal ligament cells and gingival fibroblasts in vitro,” Journal of Dental Research, vol. 67, no. 1, pp. 66–70, 1988. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Mayrhofer, S. Krieger, G. Allmaier, and D. Kerjaschki, “DIGE compatible labelling of surface proteins on vital cells in vitro and in vivo,” Proteomics, vol. 6, no. 2, pp. 579–585, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. P. S. Zilm, A. Mira, C. J. Bagley, and A. H. Rogers, “Effect of alkaline growth pH on the expression of cell envelope proteins in Fusobacterium nucleatum,” Microbiology, vol. 156, part 6, pp. 1783–1794, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. A. Gorg, G. Boguth, C. Obermaier, and W. Weiss, “Two-dimensional electrophoresis of proteins in an immobilized pH 4-12 gradient,” Electrophoresis, vol. 19, no. 8-9, pp. 1516–1519, 1998. View at Publisher · View at Google Scholar · View at Scopus
  23. N. Ancellin, C. Colmont, J. Su et al., “Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation,” The Journal of Biological Chemistry, vol. 277, no. 8, pp. 6667–6675, 2002. View at Publisher · View at Google Scholar · View at Scopus
  24. J. A. Hengst, J. M. Guilford, T. E. Fox, X. Wang, E. J. Conroy, and J. K. Yun, “Sphingosine kinase 1 localized to the plasma membrane lipid raft microdomain overcomes serum deprivation induced growth inhibition,” Archives of Biochemistry and Biophysics, vol. 492, no. 1-2, pp. 62–73, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. K. E. Jarman, P. A. B. Moretti, J. R. Zebol, and S. M. Pitson, “Translocation of sphingosine kinase 1 to the plasma membrane is mediated by calcium- and integrin-binding protein 1,” Journal of Biological Chemistry, vol. 285, no. 1, pp. 483–492, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. S. M. Pitson, P. Xia, T. M. Leclercq et al., “Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling,” The Journal of Experimental Medicine, vol. 201, no. 1, pp. 49–54, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. R. V. Stahelin, J. H. Hwang, J.-H. Kim et al., “The mechanism of membrane targeting of human sphingosine kinase 1,” The Journal of Biological Chemistry, vol. 280, no. 52, pp. 43030–43038, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. B. W. Wattenberg, “Role of sphingosine kinase localization in sphingolipid signaling,” World Journal of Biological Chemistry, vol. 1, no. 12, pp. 362–368, 2010. View at Publisher · View at Google Scholar
  29. K. W. Young, J. M. Willets, M. J. Parkinson et al., “Ca2+/calmodulin-dependent translocation of sphingosine kinase: role in plasma membrane relocation but not activation,” Cell Calcium, vol. 33, no. 2, pp. 119–128, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. E. Reichenberg, M. Redlich, P. Cancemi et al., “Proteomic analysis of protein components in periodontal ligament fibroblasts,” Journal of Periodontology, vol. 76, no. 10, pp. 1645–1653, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. L. Wu, X. Wei, J. Ling et al., “Early osteogenic differential protein profile detected by proteomic analysis in human periodontal ligament cells,” Journal of Periodontal Research, vol. 44, no. 5, pp. 645–656, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. L. J. Foster, P. A. Zeemann, C. Li, M. Mann, O. N. Jensen, and M. Kassem, “Differential expression profiling of membrane proteins by quantitative proteomics in a human mesenchymal stem cell line undergoing osteoblast differentiation,” Stem Cells, vol. 23, no. 9, pp. 1367–1377, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. A.-X. Zhang, W.-H. Yu, B.-F. Ma et al., “Proteomic identification of differently expressed proteins responsible for osteoblast differentiation from human mesenchymal stem cells,” Molecular and Cellular Biochemistry, vol. 304, no. 1-2, pp. 167–179, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. J. Sun, Y. Y. Bahk, Y. R. Choi, J. H. Shim, S. H. Han, and J. W. Lee, “A proteomic analysis during serial subculture and osteogenic differentiation of human mesenchymal stem cell,” Journal of Orthopaedic Research, vol. 24, no. 11, pp. 2059–2071, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. K. M. Mrozik, P. S. Zilm, C. J. Bagley et al., “Proteomic characterization of mesenchymal stem cell-like populations derived from ovine periodontal ligament, dental pulp, and bone marrow: analysis of differentially expressed proteins,” Stem Cells and Development, vol. 19, no. 10, pp. 1485–1499, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Balcerzak, E. Hamade, L. Zhang et al., “The roles of annexins and alkaline phosphatase in mineralization process,” Acta Biochimica Polonica, vol. 50, no. 4, pp. 1019–1038, 2003. View at Google Scholar · View at Scopus
  37. D. C. Genetos, A. Wong, S. Watari, and C. E. Yellowley, “Hypoxia increases Annexin A2 expression in osteoblastic cells via VEGF and ERK,” Bone, vol. 47, no. 6, pp. 1013–1019, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. J. M. Gillette and S. M. Nielsen-Preiss, “The role of annexin 2 in osteoblastic mineralization,” Journal of Cell Science, vol. 117, no. 3, pp. 441–449, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. T. L. Haut Donahue, D. C. Genetos, C. R. Jacobs, H. J. Donahue, and C. E. Yellowley, “Annexin V disruption impairs mechanically induced calcium signaling in osteoblastic cells,” Bone, vol. 35, no. 3, pp. 656–663, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Kirsch, B. Swoboda, and H.-D. Nah, “Activation of annexin II and V expression, terminal differentiation, mineralization and apoptosis in human osteoarthritic cartilage,” Osteoarthritis and Cartilage, vol. 8, no. 4, pp. 294–302, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Pfander, B. Swoboda, and T. Kirsch, “Expression of early and late differentiation markers (proliferating cell nuclear antigen, syndecan-3, annexin VI, and alkaline phosphatase) by human osteoarthritic chondrocytes,” American Journal of Pathology, vol. 159, no. 5, pp. 1777–1783, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Wang and T. Kirsch, “Retinoic acid stimulates annexin-mediated growth plate chondrocyte mineralization,” The Journal of Cell Biology, vol. 157, no. 6, pp. 1061–1069, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Zhang, C. Niu, L. Ye et al., “Identification of the haematopoietic stem cell niche and control of the niche size,” Nature, vol. 425, no. 6960, pp. 836–841, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Stier, Y. Ko, R. Forkert et al., “Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size,” The Journal of Experimental Medicine, vol. 201, no. 11, pp. 1781–1791, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. S. K. Nilsson, H. M. Johnston, G. A. Whitty et al., “Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells,” Blood, vol. 106, no. 4, pp. 1232–1239, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. L. M. Calvi, G. B. Adams, K. W. Weibrecht et al., “Osteoblastic cells regulate the haematopoietic stem cell niche,” Nature, vol. 425, no. 6960, pp. 841–846, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Arai, A. Hirao, M. Ohmura et al., “Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche,” Cell, vol. 118, no. 2, pp. 149–161, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. S. T. Avecilla, K. Hattori, B. Heissig et al., “Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis,” Nature Medicine, vol. 10, no. 1, pp. 64–71, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. M. J. Kiel, Ö. H. Yilmaz, T. Iwashita, O. H. Yilmaz, C. Terhorst, and S. J. Morrison, “SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells,” Cell, vol. 121, no. 7, pp. 1109–1121, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. J. M. Barrett, K. A. Parham, J. B. Pippal et al., “Over-expression of sphingosine kinase-1 enhances a progenitor phenotype in human endothelial cells,” Microcirculation, vol. 18, no. 7, pp. 583–597, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. B. Zhang, “CD73: a novel target for cancer immunotherapy,” Cancer Research, vol. 70, no. 16, pp. 6407–6411, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. S. P. Colgan, H. K. Eltzschig, T. Eckle, and L. F. Thompson, “Physiological roles for ecto-5′-nucleotidase (CD73),” Purinergic Signalling, vol. 2, no. 2, pp. 351–360, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. P. A. Beavis, J. Stagg, P. K. Darcy, and M. J. Smyth, “CD73: a potent suppressor of antitumor immune responses,” Trends in Immunology, vol. 33, no. 5, pp. 231–237, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. C. Sattler, M. Steinsdoerfer, M. Offers et al., “Inhibition of T-cell proliferation by murine multipotent mesenchymal stromal cells is mediated by CD39 expression and adenosine generation,” Cell Transplantation, vol. 20, no. 8, pp. 1221–1230, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Saldanha-Araujo, F. I. S. Ferreira, P. V. Palma et al., “Mesenchymal stromal cells up-regulate CD39 and increase adenosine production to suppress activated T-lymphocytes,” Stem Cell Research, vol. 7, no. 1, pp. 66–74, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Wada, D. Menicanin, S. Shi, P. M. Bartold, and S. Gronthos, “Immunomodulatory properties of human periodontal ligament stem cells,” Journal of Cellular Physiology, vol. 219, no. 3, pp. 667–676, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Kato, K. Hattori, T. Deguchi et al., “Osteogenic potential of rat stromal cells derived from periodontal ligament,” Journal of Tissue Engineering and Regenerative Medicine, vol. 5, no. 10, pp. 798–805, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Tomokiyo, H. Maeda, S. Fujii et al., “A multipotent clonal human periodontal ligament cell line with neural crest cell phenotypes promotes neurocytic differentiation, migration, and survival,” Journal of Cellular Physiology, vol. 227, no. 5, pp. 2040–2050, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. O. Trubiani, S. F. Zalzal, R. Paganelli et al., “Expression profile of the embryonic markers nanog, OCT-4, SSEA-1, SSEA-4, and frizzled-9 receptor in human periodontal ligament mesenchymal stem cells,” Journal of Cellular Physiology, vol. 225, no. 1, pp. 123–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. C. M. Baum, I. L. Weissman, A. S. Tsukamoto, A.-M. Buckle, and B. Peault, “Isolation of a candidate human hematopoietic stem-cell population,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 7, pp. 2804–2808, 1992. View at Publisher · View at Google Scholar · View at Scopus
  61. N. M. Masson, I. S. Currie, J. D. Terrace, O. J. Garden, R. W. Parks, and J. A. Ross, “Hepatic progenitor cells in human fetal liver express the oval cell marker Thy-1,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 291, no. 1, pp. G45–G54, 2006. View at Publisher · View at Google Scholar · View at Scopus
  62. Z. F. Yang, D. W. Ho, M. N. Ng et al., “Significance of CD90+ cancer stem cells in human liver cancer,” Cancer Cell, vol. 13, no. 2, pp. 153–166, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. J. E. Bradley, G. Ramirez, and J. S. Hagood, “Roles and regulation of Thy-1, a context-dependent modulator of cell phenotype,” BioFactors, vol. 35, no. 3, pp. 258–265, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. S. M. M. Haeryfar and D. W. Hoskin, “Thy-1: more than a mouse pan-T cell marker,” Journal of Immunology, vol. 173, no. 6, pp. 3581–3588, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Dominici, K. Le Blanc, I. Mueller et al., “Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement,” Cytotherapy, vol. 8, no. 4, pp. 315–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. D. A. Siever and H. P. Erickson, “Extracellular annexin II,” International Journal of Biochemistry and Cell Biology, vol. 29, no. 11, pp. 1219–1223, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. N. Zobiack, V. Gerke, and U. Rescher, “Complex formation and submembranous localization of annexin 2 and S100A10 in live HepG2 cells,” FEBS Letters, vol. 500, no. 3, pp. 137–140, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. J. R. Glenney Jr., “Co-precipitation of intestinal p36 with a 73K protein and a high molecular weight factor,” Experimental Cell Research, vol. 162, no. 1, pp. 183–190, 1986. View at Publisher · View at Google Scholar · View at Scopus
  69. V. Gerke and K. Weber, “Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin,” The EMBO Journal, vol. 3, no. 1, pp. 227–233, 1984. View at Google Scholar · View at Scopus
  70. C. Thiel, M. Osborn, and V. Gerke, “The tight association of the tyrosine kinase substrate annexin II with the submembranous cytoskeleton depends on intact p11- and Ca2+-binding sites,” Journal of Cell Science, vol. 103, no. 3, pp. 733–742, 1992. View at Google Scholar · View at Scopus
  71. H. C. Anderson, “Molecular biology of matrix vesicles,” Clinical Orthopaedics and Related Research, no. 314, pp. 266–280, 1995. View at Google Scholar · View at Scopus
  72. B. Brachvogel, J. Dikschas, H. Moch et al., “Annexin A5 is not essential for skeletal development,” Molecular and Cellular Biology, vol. 23, no. 8, pp. 2907–2913, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. K. Yuan, J.-S. Huang, C.-W. Hsu, and I.-J. Hung, “A mineralization-associated membrane protein plays a role in the biological functions of the peptide-coated bovine hydroxyapatite,” Journal of Periodontal Research, vol. 42, no. 5, pp. 420–428, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. D. Bozic, L. Grgurevic, I. Erjavec et al., “The proteome and gene expression profile of cementoblastic cells treated by bone morphogenetic protein-7 in vitro,” Journal of Clinical Periodontology, vol. 39, no. 1, pp. 80–90, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. Y. Jung, J. Wang, J. Song et al., “Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation,” Blood, vol. 110, no. 1, pp. 82–90, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. A. Pébay, C. S. Bonder, and S. M. Pitson, “Stem cell regulation by lysophospholipids,” Prostaglandins and Other Lipid Mediators, vol. 84, no. 3-4, pp. 83–97, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. H. Chi, “Sphingosine-1-phosphate and immune regulation: trafficking and beyond,” Trends in Pharmacological Sciences, vol. 32, no. 1, pp. 16–24, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Olivera and S. Spiegel, “Sphingosine kinase: a mediator of vital cellular functions,” Prostaglandins and Other Lipid Mediators, vol. 64, no. 1–4, pp. 123–134, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Spiegel, O. Cuvillier, L. C. Edsall et al., “Sphingosine-1-phosphate in cell growth and cell death,” Annals of the New York Academy of Sciences, vol. 845, pp. 11–8, 1998. View at Publisher · View at Google Scholar
  80. V. Limaye, X. Li, C. Hahn et al., “Sphingosine kinase-1 enhances endothelial cell survival through a PECAM-1-dependent activation of PI-3K/Akt and regulation of Bcl-2 family members,” Blood, vol. 105, no. 8, pp. 3169–3177, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. C. S. Bonder, W. Y. Sun, T. Matthews et al., “Sphingosine kinase regulates the rate of endothelial progenitor cell differentiation,” Blood, vol. 113, no. 9, pp. 2108–2117, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. H. Meng, Y. Yuan, and V. M. Lee, “Loss of Sphingosine kinase 1/S1P signaling impairs cell growth and survival of neurons and progenitor cells in the developing sensory ganglia,” PLoS ONE, vol. 6, no. 11, Article ID e27150, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. A. Pébay, R. C. B. Wong, S. M. Pitson et al., “Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells,” Stem Cells, vol. 23, no. 10, pp. 1541–1548, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. Y. Nagata, T. A. Partridge, R. Matsuda, and P. S. Zammit, “Entry of muscle satellite cells into the cell cycle requires sphingolipid signaling,” The Journal of Cell Biology, vol. 174, no. 2, pp. 245–253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. P. Xia, J. R. Gamble, L. Wang et al., “An oncogenic role of sphingosine kinase,” Current Biology, vol. 10, no. 23, pp. 1527–1530, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. D. Shida, K. Takabe, D. Kapitonov, S. Milstien, and S. Spiegel, “Targeting SphK1 as a new strategy against cancer,” Current Drug Targets, vol. 9, no. 8, pp. 662–673, 2008. View at Publisher · View at Google Scholar · View at Scopus