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Stem Cells International
Volume 2011, Article ID 274564, 10 pages
http://dx.doi.org/10.4061/2011/274564
Review Article

The Haematopoietic Stem Cell Niche: New Insights into the Mechanisms Regulating Haematopoietic Stem Cell Behaviour

1School of Biosciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK
2School of Life and Health Sciences, Aston University, Aston Triangle, Birmingham, B4 7ET, UK

Received 10 May 2011; Accepted 27 September 2011

Academic Editor: Linheng Li

Copyright © 2011 Andrew J. Lilly 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. C. Lancrin, P. Sroczynska, A. G. Serrano et al., “Blood cell generation from the hemangioblast,” Journal of Molecular Medicine, vol. 88, no. 2, pp. 167–172, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. C. Lancrin, P. Sroczynska, C. Stephenson, T. Allen, V. Kouskoff, and G. Lacaud, “The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage,” Nature, vol. 457, no. 7231, pp. 892–895, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. M. J. Chen, T. Yokomizo, B. M. Zeigler, E. Dzierzak, and N. A. Speck, “Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter,” Nature, vol. 457, no. 7231, pp. 887–891, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. M. Iacovino, D. Chong, I. Szatmari et al., “HoxA3 is an apical regulator of haemogenic endothelium,” Nature Cell Biology, vol. 13, no. 1, pp. 72–78, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. S. J. Morrison, H. D. Hemmati, A. M. Wandycz, and I. L. Weissman, “The purification and characterization of fetal liver hematopoietic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 22, pp. 10302–10306, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Cumano and I. Godin, “Ontogeny of the hematopoietic system,” Annual Review of Immunology, vol. 25, pp. 745–785, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. J. L. Christensen, D. E. Wright, A. J. Wagers, and I. L. Weissman, “Circulation and chemotaxis of fetal hematopoietic stem cells,” PLoS Biology, vol. 2, no. 3, article E75, 2004. View at Publisher · View at Google Scholar · View at PubMed
  8. M. R. Warr, E. M. Pietras, and E. Passegue, “Mechanisms controlling hematopoietic stem cell functions during normal hematopoiesis and hematological malignancies,” Wiley Interdisciplinary Reviews, vol. 3, no. 6, pp. 681–701, 2011. View at Google Scholar
  9. R. Schofield, “The relationship between the spleen colony-forming cell and the haemopoietic stem cell. A hypothesis,” Blood Cells, vol. 4, no. 1-2, pp. 7–25, 1978. View at Google Scholar · View at Scopus
  10. G. B. Bradford, B. Williams, R. Rossi, and I. Bertoncello, “Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment,” Experimental Hematology, vol. 25, no. 5, pp. 445–453, 1997. View at Google Scholar · View at Scopus
  11. S. H. Cheshier, S. J. Morrison, X. Liao, and I. L. Weissman, “In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 6, pp. 3120–3125, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. S. H. Cheshier, S. S. Prohaska, and I. L. Weissman, “The effect of bleeding on hematopoietic stem cell cycling and self-renewal,” Stem Cells and Development, vol. 16, no. 5, pp. 707–717, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. R. S. Taichmana, M. J. Reilly, and S. G. Emerson, “Osteoblasts and the hematopoietic microenvironment,” Hematology, vol. 4, no. 5, pp. 421–426, 2000. View at Google Scholar · View at Scopus
  14. 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 PubMed · View at Scopus
  15. 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 PubMed · View at Scopus
  16. N. S. El-Badri, B. Y. Wang, Cherry, and R. A. Good, “Osteoblasts promote engraftment of allogeneic hematopoietic stem cells,” Experimental Hematology, vol. 26, no. 2, pp. 110–116, 1998. View at Google Scholar · View at Scopus
  17. H. Qian, N. Buza-Vidas, C. D. Hyland et al., “Critical role of thrombopoietin in maintaining adult quiescent qematopoietic stem cells,” Cell Stem Cell, vol. 1, no. 6, pp. 671–684, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  18. M. C. Puri and A. Bernstein, “Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 22, pp. 12753–12758, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. S. Kimura, A. W. Roberts, D. Metcalf, and W. S. Alexander, “Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 3, pp. 1195–1200, 1998. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Yoshihara, F. Arai, K. Hosokawa et al., “Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche,” Cell Stem Cell, vol. 1, no. 6, pp. 685–697, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. F. Arai, H. Yoshihara, K. Hosokawa et al., “Niche regulation of hematopoietic stem cells in the endosteum: the role of thrombopoietinmpl signaling in the maintenance of quiescent hematopoietic stem cells,” Annals of the New York Academy of Sciences, vol. 1176, pp. 36–46, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  22. 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 PubMed · View at Scopus
  23. B. Varnum-Finney, L. Xu, C. Brashem-Stein et al., “Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling,” Nature Medicine, vol. 6, no. 11, pp. 1278–1281, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. J. M. Butler, D. J. Nolan, E. L. Vertes et al., “Endothelial cells are essential for the self-renewal and repopulation of notch-dependent hematopoietic stem cells,” Cell Stem Cell, vol. 6, no. 3, pp. 251–264, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. I. Maillard, U. Koch, A. Dumortier et al., “Canonical notch signaling is dispensable for themaintenance of adult hematopoietic stem cells,” Cell Stem Cell, vol. 2, no. 4, pp. 356–366, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. S. J. C. Mancini, N. Mantei, A. Dumortier, U. Suter, H. R. MacDonald, and F. Radtke, “Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation,” Blood, vol. 105, no. 6, pp. 2340–2342, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. B. Varnum-Finney, L. M. Halasz, M. Sun, T. Gridley, F. Radtke, and I. D. Bernstein, “Notch2 governs the rate of generation of mouse long- and short-term repopulating stem cells,” Journal of Clinical Investigation, vol. 121, no. 3, pp. 1207–1216, 2011. View at Publisher · View at Google Scholar · View at PubMed
  28. M. Takeichi, K. Hatta, A. Nose, and A. Nagafuchi, “Identification of a gene family of cadherin cell adhesion molecules,” Cell Differentiation and Development, vol. 25, supplement, pp. 91–94, 1988. View at Google Scholar · View at Scopus
  29. P. Li and L. I. Zon, “Resolving the controversy about N-cadherin and hematopoietic stem cells,” Cell Stem Cell, vol. 6, no. 3, pp. 199–202, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. K. Hosokawa, F. Arai, H. Yoshihara et al., “Knockdown of N-cadherin suppresses the long-term engraftment of hematopoietic stem cells,” Blood, vol. 116, no. 4, pp. 554–563, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. M. J. Kiel, G. L. Radice, and S. J. Morrison, “Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance,” Cell Stem Cell, vol. 1, no. 2, pp. 204–217, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. K. Hosokawa, F. Arai, H. Yoshihara et al., “Cadherin-based adhesion is a potential target for niche manipulation to protect hematopoietic stem cells in adult bone marrow,” Cell Stem Cell, vol. 6, no. 3, pp. 194–198, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. J. S. Haug, X. C. He, J. C. Grindley et al., “N-Cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells,” Cell Stem Cell, vol. 2, no. 4, pp. 367–379, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. M. J. Kiel, M. Acar, G. L. Radice, and S. J. Morrison, “Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance,” Cell Stem Cell, vol. 4, no. 2, pp. 170–179, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. T. Nagasawa, S. Hirota, K. Tachibana et al., “Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1,” Nature, vol. 382, no. 6592, pp. 635–638, 1996. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. Y. R. Zou, A. H. Kottman, M. Kuroda, I. Taniuchi, and D. R. Littman, “Function of the chemokine receptor CXCR4 in heaematopolesis and in cerebellar development,” Nature, vol. 393, no. 6685, pp. 595–599, 1998. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. I. Petit, M. Szyper-Kravitz, A. Nagler et al., “G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4,” Nature Immunology, vol. 3, no. 7, pp. 687–694, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  38. C. L. Semerad, M. J. Christopher, F. Liu et al., “G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow,” Blood, vol. 106, no. 9, pp. 3020–3027, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. P. Batard, M. N. Monier, N. Fortunel et al., “TGF-β1 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
  40. M. Bhatia, D. Bonnet, D. Wu et al., “Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells,” Journal of Experimental Medicine, vol. 189, no. 7, pp. 1139–1147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  41. I. A. Silver, R. J. Murrills, and D. J. Etherington, “Microelectrode studies on the acid microenvironment beneath adherent macrophages and osteoclasts,” Experimental Cell Research, vol. 175, no. 2, pp. 266–276, 1988. View at Google Scholar · View at Scopus
  42. G. B. Adams, K. T. Chabner, I. R. Alley et al., “Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor,” Nature, vol. 439, no. 7076, pp. 599–603, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. S. Lymperi, A. Ersek, F. Ferraro, F. Dazzi, and N. J. Horwood, “Inhibition of osteoclast function reduces hematopoietic stem cell numbers in vivo,” Blood, vol. 117, no. 5, pp. 1540–1549, 2011. View at Publisher · View at Google Scholar · View at PubMed
  44. J. W. Pollard, “Trophic macrophages in development and disease,” Nature Reviews Immunology, vol. 9, no. 4, pp. 259–270, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. M. K. Chang, L. J. Raggatt, K. A. Alexander et al., “Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo,” Journal of Immunology, vol. 181, no. 2, pp. 1232–1244, 2008. View at Google Scholar · View at Scopus
  46. I. G. Winkler, N. A. Sims, A. R. Pettit et al., “Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs,” Blood, vol. 116, no. 23, pp. 4815–4828, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. S. Takeda, F. Elefteriou, R. Levasseur et al., “Leptin regulates bone formation via the sympathetic nervous system,” Cell, vol. 111, no. 3, pp. 305–317, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Bliziotes, S. McLoughlin, M. Gunness, F. Fumagalli, S. R. Jones, and M. G. Caron, “Bone histomorphometric and biomechanical abnormalities in mice homozygous for deletion of the dopamine transporter gene,” Bone, vol. 26, no. 1, pp. 15–19, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. P. S. Frenette and L. Weiss, “Sulfated glycans induce rapid hematopoietic progenitor cell mobilization: evidence for selectin-dependent and independent mechanisms,” Blood, vol. 96, no. 7, pp. 2460–2468, 2000. View at Google Scholar · View at Scopus
  50. Y. Katayama and P. S. Frenette, “Galactocerebrosides are required postnatally for stromal-dependent bone marrow lymphopoiesis,” Immunity, vol. 18, no. 6, pp. 789–800, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Katayama, M. Battista, W. M. Kao et al., “Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow,” Cell, vol. 124, no. 2, pp. 407–421, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. H. Taniguchi, T. Toyoshima, K. Fukao, and H. Nakauchi, “Presence of hematopoietic stem cells in the adult liver,” Nature Medicine, vol. 2, no. 2, pp. 198–203, 1996. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Morita, A. Iseki, S. Okamura, S. Suzuki, H. Nakauchi, and H. Ema, “Functional characterization of hematopoietic stem cells in the spleen,” Experimental Hematology, vol. 39, no. 3, pp. 351.e3–359.e3, 2011. View at Publisher · View at Google Scholar · View at PubMed
  54. M. J. Kiel and S. J. Morrison, “Uncertainty in the niches that maintain haematopoietic stem cells,” Nature Reviews Immunology, vol. 8, no. 4, pp. 290–301, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. J. E. Cardier and E. Barberá-Guillem, “Extramedullary hematopoiesis in the adult mouse liver is associated with specific hepatic sinusoidal endothelial cells,” Hepatology, vol. 26, no. 1, pp. 165–175, 1997. View at Google Scholar · View at Scopus
  56. W. Li, S. A. Johnson, W. C. Shelley, and M. C. Yoder, “Hematopoietic stem cell repopulating ability can be maintained in vitro by some primary endothelial cells,” Experimental Hematology, vol. 32, no. 12, pp. 1226–1237, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. J. P. Chute, G. Muramoto, J. Fung, and C. Oxford, “Quantitative analysis demonstrates expansion of SCID-repopulating cells and increased engraftment capacity in human cord blood following ex vivo culture with human brain endothelial cells,” Stem Cells, vol. 22, no. 2, pp. 202–215, 2004. View at Google Scholar · View at Scopus
  58. X. Cheng, T. Macvittie, B. Meisenberg et al., “Human brain endothelial cells (HUBEC) promote SCID repopulating cell expansion through direct contact,” Growth Factors, vol. 25, no. 3, pp. 141–150, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. K. Yoshida, T. Taga, M. Saito et al., “Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 1, pp. 407–411, 1996. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Yao, T. Yokota, L. Xia, P. W. Kincade, and R. P. McEver, “Bone marrow dysfunction in mice lacking the cytokine receptor gp130 in endothelial cells,” Blood, vol. 106, no. 13, pp. 4093–4101, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. L. Laterveer, I. J. D. Lindley, M. S. Hamilton, R. Willemze, and W. E. Fibbe, “Interleukin-8 induces rapid mobilization of hematopoietic stem cells with radioprotective capacity and long-term myelolymphoid repopulating ability,” Blood, vol. 85, no. 8, pp. 2269–2275, 1995. View at Google Scholar · View at Scopus
  62. B. Heissig, K. Hattori, S. Dias et al., “Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of Kit-ligand,” Cell, vol. 109, no. 5, pp. 625–637, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. M. J. Kiel, Ö. H. Yilmaz, T. Iwashita, 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 PubMed · View at Scopus
  64. T. Sugiyama, H. Kohara, M. Noda, and T. Nagasawa, “Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches,” Immunity, vol. 25, no. 6, pp. 977–988, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. Y. Omatsu, T. Sugiyama, H. Kohara et al., “The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche,” Immunity, vol. 33, no. 3, pp. 387–399, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  66. A. I. Caplan, “Mesenchymal stem cells,” Journal of Orthopaedic Research, vol. 9, no. 5, pp. 641–650, 1991. View at Google Scholar · View at Scopus
  67. 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
  68. P. Bianco, P. G. Robey, and P. J. Simmons, “Mesenchymal stem cells: revisiting history, concepts, and assays,” Cell Stem Cell, vol. 2, no. 4, pp. 313–319, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. B. Sacchetti, A. Funari, S. Michienzi et al., “Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment,” Cell, vol. 131, no. 2, pp. 324–336, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  70. 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 PubMed · View at Scopus
  71. W. Wagner, R. Saffrich, and A. D. Ho, “The stromal activity of mesenchymal stromal cells,” Transfusion Medicine and Hemotherapy, vol. 35, no. 3, pp. 185–193, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. A. M. Vannucchi, L. Bianchi, C. Cellai et al., “Development of myelofibrosis in mice genetically impaired for GATA-1 expression (GATA-1low mice),” Blood, vol. 100, no. 4, pp. 1123–1132, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. R. A. Shivdasani and S. H. Orkin, “Erythropoiesis and globin gene expression in mice lacking the transcription factor NF-E2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 19, pp. 8690–8694, 1995. View at Publisher · View at Google Scholar · View at Scopus
  74. 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 PubMed · View at Scopus
  75. M. Tavassoli and M. Aoki, “Localization of megakaryocytes in the bone marrow,” Blood Cells, vol. 15, no. 1, pp. 3–14, 1989. View at Google Scholar · View at Scopus
  76. M. A. Kacena, R. A. Shivdasani, K. Wilson et al., “Megakaryocyte-osteoblast interaction revealed in mice deficient in transcription factors GATA-1 and NF-E2,” Journal of Bone and Mineral Research, vol. 19, no. 4, pp. 652–660, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  77. W. A. Ciovacco, C. G. Goldberg, A. F. Taylor et al., “The role of gap junctions in megakaryocyte-mediated osteoblast proliferation and differentiation,” Bone, vol. 44, no. 1, pp. 80–86, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  78. J. M. Lemieux, M. C. Horowitz, and M. A. Kacena, “Involvement of integrins α3β1 and α5β1 and glycoprotein IIb in megakaryocyte-induced osteoblast proliferation,” Journal of Cellular Biochemistry, vol. 109, no. 5, pp. 927–932, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  79. R. A. Shivdasani, M. F. Rosenblatt, D. Zucker-Franklin et al., “Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/ MGDF in megakaryocyte development,” Cell, vol. 81, no. 5, pp. 695–704, 1995. View at Google Scholar · View at Scopus
  80. M. A. Kacena, C. M. Gundberg, T. Nelson, and M. C. Horowitz, “Loss of the transcription factor p45 NF-E2 results in a developmental arrest of megakaryocyte differentiation and the onset of a high bone mass phenotype,” Bone, vol. 36, no. 2, pp. 215–223, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  81. N. Banu and N. Williams, “Immunochemical characterisation of megakaryocyte potentiator activity from mouse bone marrow,” Journal of Cellular Physiology, vol. 163, no. 3, pp. 486–492, 1995. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  82. W. S. Alexander, A. W. Roberts, N. A. Nicola, R. Li, and D. Metcalf, “Deficiencies in progenitor cells of multiple hematopoietic lineages and defective megakaryocytopoiesis in mice lacking the thrombopoietin receptor c-Mpl,” Blood, vol. 87, no. 6, pp. 2162–2170, 1996. View at Google Scholar · View at Scopus
  83. R. V. B. Emmons, D. M. Reid, R. L. Cohen et al., “Human thrombopoietin levels are high when thrombocytopenia is due to megakaryocyte deficiency and low when due to increased platelet destruction,” Blood, vol. 87, no. 10, pp. 4068–4071, 1996. View at Google Scholar · View at Scopus
  84. C. S. Zent, J. Ratajczak, M. Z. Ratajczak, J. Anastasi, P. C. Hoffman, and A. M. Gewirtz, “Relationship between megakaryocyte mass and serum thrombopoietin levels as revealed by a case of cyclic amegakaryocytic thrombocytopenic purpura,” British Journal of Haematology, vol. 105, no. 2, pp. 452–458, 1999. View at Google Scholar · View at Scopus
  85. C. A. De Graaf, M. Kauppi, T. Baldwin et al., “Regulation of hematopoietic stem cells by their mature progeny,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 50, pp. 21689–21694, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  86. E. Pelosi, M. Valtieri, S. Coppola et al., “Identification of the hemangioblast in postnatal life,” Blood, vol. 100, no. 9, pp. 3203–3208, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  87. C. R. Cogle, D. A. Wainman, M. L. Jorgensen, S. M. Guthrie, R. N. Mames, and E. W. Scott, “Adult human hematopoietic cells provide functional hemangioblast activity,” Blood, vol. 103, no. 1, pp. 133–135, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  88. E. Gunsilius, “Evidence from a leukemia model for maintenance of vascular endothelium by bone-marrow-derived endothelial cells,” Advances in Experimental Medicine and Biology, vol. 522, pp. 17–24, 2003. View at Google Scholar · View at Scopus
  89. S. B. Miller, “Prostaglandins in health and disease: an overview,” Seminars in Arthritis and Rheumatism, vol. 36, no. 1, pp. 37–49, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  90. Y. Sugimoto and S. Narumiya, “Prostaglandin E receptors,” Journal of Biological Chemistry, vol. 282, no. 16, pp. 11613–11617, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  91. J. Hoggatt, P. Singh, J. Sampath, and L. M. Pelus, “Prostaglandin E2 enhances hematopoietic stem cell homing, survival, and proliferation,” Blood, vol. 113, no. 22, pp. 5444–5455, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  92. C. Miyaura, M. Inada, C. Matsumoto et al., “An essential role of cytosolic phospholipase A2α in prostaglandin E2-mediated bone resorption associated with inflammation,” Journal of Experimental Medicine, vol. 197, no. 10, pp. 1303–1310, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  93. C. N. Pagel, S. J. Song, L. H. Loh et al., “Thrombin-stimulated growth factor and cytokine expression in osteoblasts is mediated by protease-activated receptor-1 and prostanoids,” Bone, vol. 44, no. 5, pp. 813–821, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  94. C. Schmidt, G. Steinbach, R. Decking, L. E. Claes, and A. A. Ignatius, “IL-6 and PGE2 release by human osteoblasts on implant materials,” Biomaterials, vol. 24, no. 23, pp. 4191–4196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  95. L. M. Pelus, H. E. Broxmeyer, and M. A. S. Moore, “Regulation of human myelopoiesis by prostaglandin E and lactoferrin,” Cell and Tissue Kinetics, vol. 14, no. 5, pp. 515–526, 1981. View at Google Scholar · View at Scopus
  96. M. S. Kennedy, J. D. Stobo, and M. E. Goldyne, “In vitro synthesis of prostaglandins and related lipids by populations of human peripheral blood mononuclear cells,” Prostaglandins, vol. 20, no. 1, pp. 135–145, 1980. View at Publisher · View at Google Scholar · View at Scopus
  97. N. Hashimoto, T. Watanabe, Y. Shiratori et al., “Prostanoid secretion by rat hepatic sinusoidal endothelial cells and its regulation by exogenous adenosine triphosphate,” Hepatology, vol. 21, no. 6, pp. 1713–1718, 1995. View at Google Scholar · View at Scopus
  98. H. Rieder, G. Ramadori, K. H. Allmann, and K. H. Meyer Zum Buschenfelde, “Prostanoid release of cultured liver sinusoidal endothelial cells in response to endotoxin and tumor necrosis factor. Comparison with umbilical vein endothelial cells,” Journal of Hepatology, vol. 11, no. 3, pp. 359–366, 1990. View at Publisher · View at Google Scholar · View at Scopus
  99. T. E. North, W. Goessling, C. R. Walkley et al., “Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis,” Nature, vol. 447, no. 7147, pp. 1007–1011, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  100. W. Goessling, T. E. North, S. Loewer et al., “Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration,” Cell, vol. 136, no. 6, pp. 1136–1147, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  101. J. Hoggatt and L. M. Pelus, “Eicosanoid regulation of hematopoiesis and hematopoietic stem and progenitor trafficking,” Leukemia, vol. 24, no. 12, pp. 1993–2002, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  102. A. Kojima, M. Shiraki, and R. Takahashi, “Prostaglandin D2 is the major prostaglandin of arachidonic acid metabolism in rat bone marrow homogenate,” Prostaglandins, vol. 20, no. 1, pp. 171–176, 1980. View at Publisher · View at Google Scholar
  103. J. A. Lindgren, L. Stenke, M. Mansour et al., “Formation and effects of leukotrienes and lipoxins in human bone marrow,” Journal of Lipid Mediators, vol. 6, no. 1–3, pp. 313–320, 1993. View at Google Scholar · View at Scopus
  104. L. Stenke, M. Mansour, P. Reizenstein, and J. A. Lindgren, “Stimulation of human myelopoiesis by leukotrienes B4 and C4: interactions with granulocyte-macrophage colony-stimulating factor,” Blood, vol. 81, no. 2, pp. 352–356, 1993. View at Google Scholar · View at Scopus
  105. M. G. Cipolleschi, P. D. Sbarba, and M. Olivotto, “The role of hypoxia in the maintenance of hematopoietic stem cells,” Blood, vol. 82, no. 7, pp. 2031–2037, 1993. View at Google Scholar · View at Scopus
  106. Z. Ivanovic, P. D. Sbarba, F. Trimoreau, J. L. Faucher, and V. Praloran, “Primitive human HPCs are better maintained and expanded in vitro at 1 perent oxygen than at 20 percent,” Transfusion, vol. 40, no. 12, pp. 1482–1488, 2000. View at Publisher · View at Google Scholar · View at Scopus
  107. D. C. Chow, L. A. Wenning, W. M. Miller, and E. T. Papoutsakis, “Modeling pO2 distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models,” Biophysical Journal, vol. 81, no. 2, pp. 685–696, 2001. View at Google Scholar · View at Scopus
  108. K. Parmar, P. Mauch, J. A. Vergilio, R. Sackstein, and J. D. Down, “Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 13, pp. 5431–5436, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  109. I. G. Winkler, V. Barbier, R. Wadley, A. C. W. Zannettino, S. Williams, and J. P. Lévesque, “Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches,” Blood, vol. 116, no. 3, pp. 375–385, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  110. A. Foudi, K. Hochedlinger, D. Van Buren et al., “Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells,” Nature Biotechnology, vol. 27, no. 1, pp. 84–90, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  111. S. E. Schriner, N. J. Linford, G. M. Martin et al., “Medecine: extension of murine life span by overexpression of catalase targeted to mitochondria,” Science, vol. 308, no. 5730, pp. 1909–1911, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  112. K. Ito, A. Hirao, F. Arai et al., “Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells,” Nature, vol. 431, no. 7011, pp. 997–1002, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  113. Y. Y. Jang and S. J. Sharkis, “A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche,” Blood, vol. 110, no. 8, pp. 3056–3063, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  114. K. Hosokawa, F. Arai, H. Yoshihara et al., “Function of oxidative stress in the regulation of hematopoietic stem cell-niche interaction,” Biochemical and Biophysical Research Communications, vol. 363, no. 3, pp. 578–583, 2007. View at Publisher · View at Google Scholar · View at PubMed
  115. K. Ito, A. Hirao, F. Arai et al., “Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells,” Nature Medicine, vol. 12, no. 4, pp. 446–451, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  116. T. Takaku, D. Malide, J. Chen, R. T. Calado, S. Kajigaya, and N. S. Young, “Hematopoiesis in 3 dimensions: human and murine bone marrow architecture visualized by confocal microscopy,” Blood, vol. 116, no. 15, pp. e41–e55, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  117. C. Lo Celso, C. P. Lin, and D. T. Scadden, “In vivo imaging of transplanted hematopoietic stem and progenitor cells in mouse calvarium bone marrow,” Nature Protocols, vol. 6, no. 1, pp. 1–14, 2011. View at Publisher · View at Google Scholar · View at PubMed