Advertisement

Journal of Applied Genetics

, Volume 48, Issue 4, pp 307–319 | Cite as

Bone-marrow-derived stem cells — our key to longevity?

  • Mariusz Z. Ratajczak
  • Ewa K. Zuba-Surma
  • Bogusław Machalinski
  • Magdalena Kucia
Invited Editorial

Abstract

Bone marrow (BM) was for many years primarily regarded as the source of hematopoietic stem cells. In this review we discuss current views of the BM stem cell compartment and present data showing that BM contains not only hematopoietic but also heterogeneous non-hematopoietic stem cells. It is likely that similar or overlapping populations of primitive non-hematopoietic stem cells in BM were detected by different investigators using different experimental strategies and hence were assigned different names (e.g., mesenchymal stem cells, multipotent adult progenitor cells, or marrow-isolated adult multilineage inducible cells). However, the search still continues for true pluripotent stem cells in adult BM, which would fulfill the required criteria (e.g. complementation of blastocyst development). Recently our group has identified in BM a population of very small embryonic-like stem cells (VSELs), which express several markers characteristic for pluripotent stem cells and are found during early embryogenesis in the epiblast of the cylinder-stage embryo.

Keywords

CXCR4 embryonic stem cells Nanog Oct-4 SSEA very small embryonic-like stem cells 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ, 2004. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation 110: 3300–3305PubMedCrossRefGoogle Scholar
  2. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, et al. 1999. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85: 221–228.PubMedGoogle Scholar
  3. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, et al. 1997. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964–967.PubMedCrossRefGoogle Scholar
  4. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, et al. 2004. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 10: 64–71.PubMedCrossRefGoogle Scholar
  5. Boiani M, Schöler HR, 2005. Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Biol 6: 872–884.PubMedCrossRefGoogle Scholar
  6. Bradley A, Evans M, Kaufman MH, Robertson E, 1984. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309: 255–256.PubMedCrossRefGoogle Scholar
  7. Bucala R, Spiegel LA, Chesney J, Hogan M, Cerami A, 1994. Circulating fibrocytes define anew leukocyte subpopulation that mediates tissue repair. Mol Med 1: 71–81.PubMedGoogle Scholar
  8. Bunting KD, Hawley RG, 2003. Integrative molecular and developmental biology of adult stem cells. Biol Cell 95: 563–578.PubMedCrossRefGoogle Scholar
  9. Buzańska L, Machaj EK, Zabłocka B, Pojda Z, Domańska-Janik K, 2002. Human cord blood-derived cells attain neuronal and glial features in vitro. J Cell Sci 115: 2131–2138.PubMedGoogle Scholar
  10. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM, 2001. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 98: 2396–2402.PubMedCrossRefGoogle Scholar
  11. Castro RF, Jackson KA, Goodell MA, Robertson CS, Liu H, Shine HD, 2002. Failure of bone marrow cells to transdifferentiate into neural cells in vivo. Science 297: 1299.PubMedCrossRefGoogle Scholar
  12. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, et al. 2004. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858–864.PubMedCrossRefGoogle Scholar
  13. Corbel SY, Lee A, Yi L, Duenas J, Brazelton TR, Blau HM, et al. 2003. Contribution of hematopoietic stem cells to skeletal muscle. Nat Med 9: 1528–1532.PubMedCrossRefGoogle Scholar
  14. Corti S, Locatelli F, Donadoni C, Strazzer S, Salani S, Del Bo R, et al. 2002a. Neuroectodermal and microglial differentiation of bone marrow cells in the mouse spinal cord and sensory ganglia. J Neurosci Res 70: 721–733.PubMedCrossRefGoogle Scholar
  15. Corti S, Strazzer S, Del Bo R, Salani S, Bossolasco P, Fortunato F, et al. 2002b. A subpopulation of murine bone marrow cells fully differentiates along the myogenic pathway and participates in muscle repair in the mdx dystrophic mouse. Exp Cell Res 277: 74–85.PubMedCrossRefGoogle Scholar
  16. Crane IJ, Wallace CA, McKillop-Smith S, Forrester JV, 2000. CXCR4 receptor expression on human retinal pigment epithelial cells from the blood-retina barrier leads to chemokine secretion and migration in response to stromal cell-derived factor 1 alpha. J Immunol 165: 4372–4378.PubMedGoogle Scholar
  17. D’Ippolito G, Diabira S, Howard GA, Menei P, Roos BA, Schiller PC, 2004. Marrow-isolated adult multilineage inducible (MIAMI) cells, aunique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117: 2971–2981.PubMedCrossRefGoogle Scholar
  18. De Felici M, McLaren A, 1983. In vitro culture of mouse primordial germ cells. Exp Cell Res 144: 417–427.CrossRefGoogle Scholar
  19. Devine SM, Flomenberg N, Vesole DH, Liesveld J, Weisdorf D, Badel K, et al. 2004. Rapid mobilization of CD34+ cells following administration of the CXCR4 antagonist AMD3100 to patients with multiple myeloma and non-Hodgkin’s lymphoma. J Clin Oncol 22: 1095–1102.PubMedCrossRefGoogle Scholar
  20. Devine SM, Hoffman R, 2000. Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr Opin Hematol 7: 358–363.PubMedCrossRefGoogle Scholar
  21. Dexter TM, Spooncer E, 1987. Growth and differentiation in the hemopoietic system. Annu Rev Cell Biol 3.Google Scholar
  22. Di Campli C, Piscaglia AC, Pierelli L, Rutella S, Bonanno G, Alison MR, et al. 2004. A human umbilical cord stem cell rescue therapy in a murine model of toxic liver injury. Dig Liver Dis 36: 603–613.PubMedCrossRefGoogle Scholar
  23. Dome B, Timar J, Dobos J, Meszaros L, Raso E, Paku S, et al. 2006. Identification and clinical significance of circulating endothelial progenitor cells in human non-small cell lung cancer. Cancer Res 66: 7341–7347.PubMedCrossRefGoogle Scholar
  24. Donovan PJ, 1994. Growth factor regulation of mouse primordial germ cell development. Curr Top Dev Biol 29.Google Scholar
  25. Donovan PJ, 1998. The germ cell — the mother of all stem cells. Int J Dev Biol 42: 1043–1050.PubMedGoogle Scholar
  26. Eghbali-Fatourechi GZ, Lamsam J, Fraser D, Nagel D, Riggs BL, Khosla S, 2005. Circulating osteoblastlineage cells in humans. N Engl J Med 352: 1959–1966.PubMedCrossRefGoogle Scholar
  27. Evans MJ, Kaufman MH, 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154–156.PubMedCrossRefGoogle Scholar
  28. Gomperts BN, Belperio JA, Rao PN, Randell SH, Fishbein MC, Burdick MD, et al. 2006. Circulating progenitor epithelial cells traffic via CXCR4/CXCL12 in response to airway injury. J Immunol 176: 1916–1927.PubMedGoogle Scholar
  29. Hasegawa T, Kosaki A, Shimizu K, Matsubara H, Mori Y, Masaki H, et al. 2006. Amelioration of diabetic peripheral neuropathy by implantation of hematopoietic mononuclear cells in streptozotocininduced diabetic rats. Exp Neurol 199: 274–280.PubMedCrossRefGoogle Scholar
  30. Hashimoto N, Jin H, Liu T, Chensue SW, Phan SH, 2004. Bone marrow-derived progenitor cells in pulmonary fibrosis. J Clin Invest 113: 243–252.PubMedGoogle Scholar
  31. Hatch HM, Zheng D, Jorgensen ML, Petersen BE, 2002. SDF-1 alpha/CXCR4: a mechanism for hepatic oval cell activation and bone marrow stem cell recruitment to the injured liver of rats. Cloning Stem Cells 4: 339–351.PubMedCrossRefGoogle Scholar
  32. Hess D, Li L, Martin M, Sakano S, Hill D, Strutt B, et al. 2003. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 21: 763–770.PubMedCrossRefGoogle Scholar
  33. Hess DC, Abe T, Hill WD, Studdard AM, Carothers J, Masuya M, et al. 2004. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol 186: 134–144.PubMedCrossRefGoogle Scholar
  34. Hill WD, Hess DC, Martin-Studdard A, Carothers JJ, Zheng J, Hale D, et al. 2004. SDF-1 (CXCL 12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 63: 84–96.PubMedGoogle Scholar
  35. Hitchon C, Wong K, Ma G, Reed J, Lyttle D, El-Gabalawy H, 2002. Hypoxia-induced production of stromal cell-derived factor 1 (CXCL12) and vascular endothelial growth factor by synovial fibroblasts. Arthritis Rheum 46: 2587–2597.PubMedCrossRefGoogle Scholar
  36. Hochedlinger K, Jaenisch R, 2003. Nuclear transplantation, embryonic stem cells, and the potential for cell therapy. N Engl J Med 349: 275–286.PubMedCrossRefGoogle Scholar
  37. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, et al. 2005. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement. Cytotherapy 7: 393–395.PubMedCrossRefGoogle Scholar
  38. Houchen CW, George RJ, Sturmoski MA, Cohn SM, 1999. FGF-2 enhances intestinal stem cell survival and its expression is induced after radiation injury. Am J Physiol 276: G249–258.PubMedGoogle Scholar
  39. Houghton J, Stoicov C, Nomura S, Rogers AB, Carlson J, Li H, et al. 2004. Gastric cancer originating from bone marrow-derived cells. Science 306.Google Scholar
  40. Jackson KA, Majka SM, Wang H, Pocius J, Hartley CJ, Majesky MW, et al. 2001. Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells. J Clin Invest 107: 1395–1402.PubMedCrossRefGoogle Scholar
  41. Ji JF, He BP, Dheen ST and Tay SS, 2004. Expression of chemokine receptors CXCR4, CCR2, CCR5 and CX3CR1 in neural progenitor cells isolated from the subventricular zone of the adult rat brain. Neurosci Lett 355: 236–240.PubMedCrossRefGoogle Scholar
  42. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, et al. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418: 41–49.PubMedCrossRefGoogle Scholar
  43. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, et al. 2006. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 2006 May; 12(5): 12: 557–567.CrossRefGoogle Scholar
  44. Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, et al. 2005. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122: 303–315.PubMedCrossRefGoogle Scholar
  45. Kale S, Karihaloo A, Clark PR, Kashgarian M, Krause DS, Cantley LG, 2003. Bone marrow stem cells contribute to repair of the ischemically injured renal tubule. J Clin Invest 112: 42–49.PubMedGoogle Scholar
  46. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, et al. 2001. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103: 634–637.PubMedGoogle Scholar
  47. Kollet O, Shivtiel S, Chen YQ, Suriawinata J, Thung SN, Dabeva MD, et al. 2003. HGF, SDF-1, and MMP-9 are involved in stress-induced human CD34+ stem cell recruitment to the liver. J Clin Invest 112: 160–169.PubMedGoogle Scholar
  48. Kucia M, Dawn B, Hunt G, Guo Y, Wysoczynski M, Majka M, et al. 2004. Cells expressing early cardiac markers reside in the bone marrow and are mobilized into the peripheral blood after myocardial infarction. Circ Res 95: 1191–1199.PubMedCrossRefGoogle Scholar
  49. Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, et al. 2007. Morphological and molecular characterization of novel population of CXCR4(+) SSEA-4(+) Oct-4(+) very small embryonic-like cells purified from human cord blood — preliminary report. Leukemia 21: 297–303.PubMedCrossRefGoogle Scholar
  50. Kucia M, Ratajczak J, Ratajczak MZ, 2005a. Are bone marrow stem cells plastic or heterogeneous — that is the question. Exp Hematol 33: 613–623.PubMedCrossRefGoogle Scholar
  51. Kucia M, Ratajczak J, Ratajczak MZ, 2005b. Bone marrow as a source of circulating CXCR4+ tissue-committed stem cells. Biol Cell 97: 133–146.PubMedCrossRefGoogle Scholar
  52. Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, et al. 2006a. A population of very small embryonic-like (VSEL) CXCR4(+) SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 20: 857–869.PubMedCrossRefGoogle Scholar
  53. Kucia M, Reca R, Jala VR, Dawn B, Ratajczak J, Ratajczak MZ, 2005c. Bone marrow as a home of heterogeneous populations of nonhematopoietic stem cells. Leukemia 19: 1118–1127.PubMedCrossRefGoogle Scholar
  54. Kucia M, Wojakowski W, Reca R, Machalinski B, Gozdzik J, Majka M, et al. 2006b. The migration of bone marrow-derived non-hematopoietic tissue-committed stem cells is regulated in an SDF-1-, HGF-, and LIF-dependent manner. Arch Immunol Ther Exp (Warsz) 54: 121–135.CrossRefGoogle Scholar
  55. Kucia M, Zhang YP, Reca R et al. 2006c. Cells enriched in markers of neural tissue-committed stem cells reside in the bone marrow and are mobilized into the peripheral blood following stroke. Leukemia 20: 18–28.PubMedCrossRefGoogle Scholar
  56. Kucia M, Zhang YP, Reca R, Wysoczynski M, Machalinski B, Majka M, et al. 2006d. Cells enriched in markers of neural tissue-committed stem cells reside in the bone marrow and are mobilized into the peripheral blood following stroke. Leukemia 20: 18–28.PubMedCrossRefGoogle Scholar
  57. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG, 2001. Circulating skeletal stem cells. J Cell Biol 153: 1133–1140.PubMedCrossRefGoogle Scholar
  58. LaBarge MA, Blau HM, 2002. Biological progression from adult bone marrow to mononucleate muscle stem cell to multinucleate muscle fiber in response to injury. Cell 111: 589–601.PubMedCrossRefGoogle Scholar
  59. Lagasse E, Connors H, Al-Dhalimy M, Reitsma M, Dohse M, Osborne L, et al. 2000. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 6: 1229–1234.PubMedCrossRefGoogle Scholar
  60. Lazarini F, Tham TN, Casanova P, Arenzana-Seisdedos F, Dubois-Dalcq M, 2003. Role of the al-pha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42: 139–148.PubMedCrossRefGoogle Scholar
  61. Lemoli RM, Catani L, Talarico S, Loggi E, Gramenzi A, Baccarani U, et al. 2006. Mobilization of bone marrow-derived hematopoietic and endothelial stem cells after orthotopic liver transplantation and liver resection. Stem Cells 24: 2817–2825.PubMedCrossRefGoogle Scholar
  62. Li HC, Stoicov C, Rogers AB, Houghton J, 2006. Stem cells and cancer: evidence for bone marrow stem cells in epithelial cancers. World J Gastroenterol 12: 363–371.PubMedGoogle Scholar
  63. Liu C, Chen Z, Chen Z, Zhang T, Lu Y, 2006. Multiple tumor types may originate from bone marrow-derived cells. Neoplasia 8: 716–724.PubMedCrossRefGoogle Scholar
  64. Long MA, Corbel SY, Rossi FM, 2005. Circulating myogenic progenitors and muscle repair. Semin Cell Dev Biol 16: 632–640.PubMedCrossRefGoogle Scholar
  65. Makino S, Fukuda K, Miyoshi S, Konishi F, Kodama H, Pan J, et al. 1999. Cardiomyocytes can be generated from marrow stromal cells in vitro. J Clin Invest 103: 697–705.PubMedCrossRefGoogle Scholar
  66. Martin GR, 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 78: 7634–7638.PubMedCrossRefGoogle Scholar
  67. Matsui Y, Zsebo K, Hogan BL, 1992. Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70: 841–847.PubMedCrossRefGoogle Scholar
  68. McKinney-Freeman SL, Jackson KA, Camargo FD, Ferrari G, Mavilio F, Goodell MA, 2002. Muscle-derived hematopoietic stem cells are hematopoietic in origin. Proc Natl Acad Sci USA 99: 1341–1346.PubMedCrossRefGoogle Scholar
  69. McLaren A, 1992. Development of primordial germ cells in the mouse. Andrologia 24: 243–247.PubMedCrossRefGoogle Scholar
  70. McLaren A, 2003. Primordial germ cells in the mouse. Dev Biol 262: 1–15.PubMedCrossRefGoogle Scholar
  71. McLaren A, Lawson KA, 2005. How is the mouse germ-cell lineage established? Differentiation 73: 435–437.PubMedCrossRefGoogle Scholar
  72. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR, 2000. Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290: 1779–1782.PubMedCrossRefGoogle Scholar
  73. Mieno S, Ramlawi B, Boodhwani M, Clements RT, Minamimura K, Maki T, et al. 2006. Role of stromal-derived factor-1 alpha in the induction of circulating CD34+CXCR4+ progenitor cells after cardiac surgery. Circulation 114: I186–192.PubMedCrossRefGoogle Scholar
  74. Murry CE, Soonpaa MH, Reinecke H, Nakajima H, Nakajima HO, Rubart M, et al. 2004. Haematopoietic stem cells do not transdifferentiate into cardiac myocytes in myocardial infarcts. Nature 428: 664–668.PubMedCrossRefGoogle Scholar
  75. Nayernia K, Lee JH, Drusenheimer N, Nolte J, Wulf G, Dressel R, et al. 2006. Derivation of male germ cells from bone marrow stem cells. Lab Invest 86: 654–663.PubMedCrossRefGoogle Scholar
  76. O’Farrell PH, Stumpff J, Su TT, 2004. Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol 14: R35–45.PubMedGoogle Scholar
  77. Orkin SH, Zon LI, 2002. Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat Immunol 3: 323–328.PubMedCrossRefGoogle Scholar
  78. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, et al. 2001. Bone marrow cells regenerate infarcted myocardium. Nature 410: 701–705.PubMedCrossRefGoogle Scholar
  79. Palermo AT, Labarge MA, Doyonnas R, Pomerantz J, Blau HM, 2005. Bone marrow contribution to skeletal muscle: a physiological response to stress. Dev Biol 279: 336–344.PubMedCrossRefGoogle Scholar
  80. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ, 2004. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103: 1662–1668.PubMedCrossRefGoogle Scholar
  81. Pesce M, Orlandi A, Iachininoto MG, Straino S, Torella AR, Rizzuti V, et al. 2003. Myoendothelial differentiation of human umbilical cord blood-derived stem cells in ischemic limb tissues. Circ Res 93: e51–62.PubMedCrossRefGoogle Scholar
  82. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, et al. 1999. Bone marrow as a potential source of hepatic oval cells. Science 284: 1168–1170.PubMedCrossRefGoogle Scholar
  83. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, et al. 2002. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3: 687–694.PubMedCrossRefGoogle Scholar
  84. Phillips RJ, Burdick MD, Hong K, Lutz MA, Murray LA, Xue YY, et al. 2004. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J Clin Invest 114: 438–446.PubMedGoogle Scholar
  85. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143–147.PubMedCrossRefGoogle Scholar
  86. Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, et al. 2000. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 106: 1331–1339.PubMedCrossRefGoogle Scholar
  87. Prockop DJ, 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71–74.PubMedCrossRefGoogle Scholar
  88. Ratajczak MZ, Kucia M, Reca R, Majka M, Janowska-Wieczorek A, Ratajczak J, 2004. Stem cell plasticity revisited: CXCR4-positive cells expressing mRNA for early muscle, liver and neural cells ‘hide out’ in the bone marrow. Leukemia 18: 29–40.PubMedCrossRefGoogle Scholar
  89. Ratajczak MZ, Majka M, Kucia M, Drukala J, Pietrzkowski Z, Peiper S, et al. 2003. Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells 21: 363–371.PubMedCrossRefGoogle Scholar
  90. Resnick JL, Bixler LS, Cheng L, Donovan PJ, 1992. Long-term proliferation of mouse primordial germ cells in culture. Nature 359: 550–551.PubMedCrossRefGoogle Scholar
  91. Resnick JL, Ortiz M, Keller JR, Donovan PJ, 1998. Role of fibroblast growth factors and their receptors in mouse primordial germ cell growth. Biol Reprod 59: 1224–1229.PubMedCrossRefGoogle Scholar
  92. Reya T, Morrison SJ, Clarke MF, Weissman IL, 2001. Stem cells, cancer, and cancer stem cells. Nature 414: 105–111.PubMedCrossRefGoogle Scholar
  93. Rideout WMr, Eggan K, Jaenisch R, 2001. Nuclear cloning and epigenetic reprogramming of the genome. Science 293: 1093–1098.PubMedCrossRefGoogle Scholar
  94. Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, et al. 2003. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med 198: 1391–1402.PubMedCrossRefGoogle Scholar
  95. Sell S, 2004. Stem cell origin of cancer and differentiation therapy. Crit Rev Oncol Hematol 51: 1–28.PubMedCrossRefGoogle Scholar
  96. Shamblott MJ, Axelman J, Wang S, Bugg EM, Littlefield JW, Donovan PJ, et al. 1998. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 95: 13726–13731.PubMedCrossRefGoogle Scholar
  97. Shi Q, Rafii S, Wu MH, Wijelath ES, Yu C, Ishida A, et al. 1998. Evidence for circulating bone marrow-derived endothelial cells. Blood 92: 362–367.PubMedGoogle Scholar
  98. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, et al. 2001. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103: 2776–2779.PubMedCrossRefGoogle Scholar
  99. Shyu WC, Lin SZ, Yang HI, Tzeng YS, Pang CY, Yen PS, et al. 2004. Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 110: 1847–1854.PubMedCrossRefGoogle Scholar
  100. Song YS, Ryu YH, Choi SR, Kim JC, 2005. The involvement of adult stem cells originated from bone marrow in the pathogenesis of pterygia. Yonsei Med J 46: 687–692.PubMedCrossRefGoogle Scholar
  101. Tacchini L, Matteucci E, De Ponti C, Desiderio MA, 2003. Hepatocyte growth factor signaling regulates transactivation of genes belonging to the plasminogen activation system via hypoxia inducible factor-1. Exp Cell Res 290: 391–401.PubMedCrossRefGoogle Scholar
  102. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, et al. 1998. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393: 591–594.PubMedCrossRefGoogle Scholar
  103. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, et al. 1999. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 5: 434–438.PubMedCrossRefGoogle Scholar
  104. Tarkowski AK, 1959. Experiments on the development of isolated blastomeres of mouse eggs. Nature 184: 1286–1287.PubMedCrossRefGoogle Scholar
  105. Tögel F, Isaac J, Hu Z, Weiss K, Westenfelder C, 2005. Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int 67: 1772–1784.PubMedCrossRefGoogle Scholar
  106. Tolar J, Nauta AJ, Osborn MJ, Panoskaltsis Mortari A, McElmurry RT, Bell S, et al. 2007. Sarcoma derived from cultured mesenchymal stem cells. Stem Cells 25: 371–379.PubMedCrossRefGoogle Scholar
  107. Turnpenny L, Brickwood S, Spalluto CM, Piper K, Cameron IT, Wilson DI, et al. 2003. Derivation of human embryonic germ cells: an alternative source of pluripotent stem cells. Stem Cells 21: 598–609.PubMedCrossRefGoogle Scholar
  108. Urbich C, Dimmeler S, 2004. Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95: 343–353.PubMedCrossRefGoogle Scholar
  109. Vasyutina E, Stebler J, Brand-Saberi B, Schulz S, Raz E, Birchmeier C, 2005. CXCR4 and Gab1 cooperate to control the development of migrating muscle progenitor cells. Genes Dev 19: 2187–2198.PubMedCrossRefGoogle Scholar
  110. Virchow R, 1855. Editorial Archive fuer pathologische Anatomie und Physiologie fuer klinische Medizin. 8: 23–54.Google Scholar
  111. Wagers A J, Sherwood RI, Christensen JL, Weissman IL, 2002. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297: 2256–2259.PubMedCrossRefGoogle Scholar
  112. Wojakowski W, Tendera M, Michalowska A, Majka M, Kucia M, Maslankiewicz K, et al. 2004. Mobilization of CD34/CXCR4+, CD34/CD117+, c-met+ stem cells, and mononuclear cells expressing early cardiac, muscle, and endothelial markers into peripheral blood in patients with acute myocardial infarction. Circulation 110: 3213–3220.PubMedCrossRefGoogle Scholar
  113. Wu G, Mannam AP, Wu J, Kirbis S, Shie JL, Chen C, et al. 2003. Hypoxia induces myocyte-dependent COX-2 regulation in endothelial cells: role of VEGF. Am J Physiol Heart Circ Physiol 285: H2420–2429.PubMedGoogle Scholar
  114. Wylie C, 1999. Germ cells. Cell 96: 165–174PubMedCrossRefGoogle Scholar
  115. Zhang H, Vutskits L, Pepper MS, Kiss JZ, 2003. VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163: 1375–1384.PubMedCrossRefGoogle Scholar
  116. Zwaka TP, Thomson JA, 2005. A germ cell origin of embryonic stem cells? Development 132: 227–233PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Plant Genetics, Polish Academy of Sciences, Poznan 2007

Authors and Affiliations

  • Mariusz Z. Ratajczak
    • 1
    • 2
  • Ewa K. Zuba-Surma
    • 1
  • Bogusław Machalinski
    • 1
    • 2
  • Magdalena Kucia
    • 1
  1. 1.Hoenig Endowed Chair in Cancer Biology, Stem Cell InstituteUniversity of LouisvilleLouisville, KYUSA
  2. 2.Department of PhysiopathologyPomeranian Medical UniversitySzczecinPoland

Personalised recommendations