Blood and bone: Two tissues whose fates are intertwined to create the hematopoietic stem-cell niche

Blood

Volumn 105, Issue 7, 2005, Pages 2631-2639

  Taichman, Russell S ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CALCITRIOL; COLLAGEN TYPE 1; COLONY STIMULATING FACTOR 1; FIBROBLAST GROWTH FACTOR; FIBROMODULIN; FIBRONECTIN; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON; INTERLEUKIN 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 7; LEUKEMIA INHIBITORY FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; ONCOSTATIN M; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEONECTIN; OSTEOPONTIN; OSTEOPROTEGERIN; PARATHYROID HORMONE; PROTEOHEPARAN SULFATE; SCATTER FACTOR; SOMATOMEDIN; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN;

BLOOD; BONE TISSUE; CELL ADHESION; CELL INTERACTION; CELL MATURATION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; REVIEW;

EID: 15944377835     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2004-06-2480     Document Type: Review

References (101)

1. Dexter TM, Spooncer E. Growth and differentiation in the hemopoietic system. Ann Rev Cell Biol. 1987;3:432-441.
2. Moore KA, Pytowski B, Witte L, Hicklin D, Lemischka IR. Hematopoietic activity of a stromal cell transmembrane protein containing epidermal growth factor-like repeat motifs. Proc Natl Acad Sci U S A. 1997;94:4011-4016.
3. Lemischka IR. Microenvironmental regulation of hematopoietic stem cells. Stem Cells. 1997;15(suppl 1):63-68.
4. Trentin JJ. Hematopoietic microenvironments: historical perspectives, status, projections. In: Tavassoli M, ed. Handbook of the Hemopoietic Microenvironment. Clifton, NJ: Humana Press; 1989.
5. Bloom W, Bloom M, McLean F. Calcification and ossification: medullary bone changes in the reproductive cycle of female pigeons. Am J Anat. 1941;81:443-445.
6. Patt HM, Maloney MA. Bone formation and resorption as a requirement for marrow development. Proc Soc Exp Biol Med. 1972;140:205-207.
7. Maloney M, Patt H. Regulation of stem cells after local bone marrow injury: the role of an osseous environment. In: Cairnie A, ed. Stem Cells of Renewing Populations. New York, NY: Academic Press; 1976:239-253.
8. Lord BI, Hendry JH. The distribution of haemopoietic colony-forming units in the mouse femur, and its modification by x rays. Br J Radiol. 1972;45:110-115.
9. Lord BI, Testa NG, Hendry JH. The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood. 1975;46:65-72.
10. Lord BI. The architecture of bone marrow cell populations. Int J Cell Cloning. 1990;8:317-331.
11. Curry JL, Trentin JJ. Hemopoietic spleen colony studies, I: growth and differentiation. Dev Biol. 1967;15:395-413.
12. McCuskey RS, McClugag SG, Younker WJ. Microscopy of living bone marrow in situ. Blood. 1971;38:87-95.
13. Rodan GA, Martin TJ. Role of osteoblasts in hormonal control of bone resorption: a hypothesis [abstract]. Calcif Tissue Int. 1981;33:349-351.
14. Roodman GD. Mechanisms of disease: mechanisms of bone metastasis. N Engl J Med. 2004;350:1655-1664.
15. Taichman RS, Emerson SG. The role of osteoblasts in the hematopoietic microenvironment. Stem Cells. 1998;16:7-15.
16. Greenfield E, Horowitz M, Lavish S. Stimulation by parathyroid hormone of interleukin-6 and leukemia inhibitory factor expression in osteoblasts is an immediate-early gene response induced by cAMP signal transduction. J Biol Chem. 1996;271:10984-10989.
17. Ponomaryov T, Peled A, Peled I, et al. Increased production of SDF-1 following treatment with DNA damaging agents: relevance for human stem cell homing and repopulation of NOD/SCID mice. J Clin Invest. 2000;106:1331-1339.
18. Hofbauer LC, Khosla S, Dunstan CR, et al. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res. 2000;15:2-12.
19. Dexter TM, Coutinhot LH, Spooncer E, et al. Stromal cells in haemopoiesis. In: Molecular Control of Haemopoiesis. Ciba Foundation Symp. 1990;148:76-86; discussion 86-95.
20. Tavassoli M, Hardy CL. The molecular mechanism for recognition of intravenously transplanted progenitor cells. In: Long MW, Wicha MS, eds. The Hematopoietic Microenvironment: The Functional Basis of Blood Cell Development. Baltimore, MD: John Hopkins University Press; 1993:217-231.
21. Quesenberry PJ. Stromal cells in long-term bone marrow cultures. In: Tavassoli M, ed. Handbook of the Hematopoietic Microenvironment. Clifton, NJ: Humana Press; 1989:253-285.
22. Moore KA, Ema H, Lemischka IR. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood. 1997;89:4337-4347.
23. Kuznetsov S, Kerbsbach P, Satomura K, et al. Single-colony derived strains of marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res. 1997;12:1335-1347.
24. Benayahu D, Horowitz M, Zipori D, Weintroub S. Hematopoietic functions of marrow-derived osteogenic cells. Calcif Tissue Int. 1992;51:195-201.
25. Friedenstein AJ, Chailakhjan RK. The development of fibroblast colonies in monolayer cultures of guinea pig bone marrow and spleen cells. Cell Tissue Kinet. 1970;3:393-403.
26. Grigoriadis AE, Heersche NJ, Aubin JE. Differentiation of muscle, fat, cartilage and bone from progenitor cells present in a bone derived clonal cell population: effect of dexamethasone. J Cell Physiol. 1988;106:2139-2151.
27. Kuznetsov SA, Krebsbach PH, Satomura K, et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res. 1997;12:1335-1347.
28. Benayahu D, Gurevitch O, Zipori D, Wientroub S. Bone formation by marrow osteogenic cells (MBA-15) is not accompanied by osteoclastogenesis and generation of hematopoietic supportive microenvironment. J Bone Miner Res. 1994;9:1107-1114.
29. Taichman RS, Reilly MJ, Emerson SG. Human osteosarcomas inhibit hematopoietic colony formation: partial reversal by antibody to transforming growth factor-β1. Bone. 1997;21:353-361.
30. Rochet N, Leroy P, Far DF, et al. CAL72: a human osteosarcoma cell line with unique effects on hematopoietic cells. Eur J Haematol. 2003;70:43-52.
31. Nelissen JM, Torensma R, Pluyter M, et al. Molecular analysis of the hematopoiesis supporting osteoblastic cell line U2-OS. Exp Hematol. 2000;28:422-432.
32. Taichman RS, Emerson SG. Human osteosarcoma cell lines MG-63 and SaOS-2 produce G-CSF and GM-CSF: identification and partial characterization of cell-associated isoforms. Exp Hematol. 1996;24:509-517.
33. + hematopoietic bone marrow cells in vitro. Blood. 1997;89:1165-1172.
34. Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994;179:1677-1682.
35. Taichman RS, Reilly MJ, Emerson SG. Human osteoblasts support human hematopoietic progenitor cells In vitro bone marrow cultures. Blood. 1996;87:518-524.
36. Taichman RS, Reilly MJ, Verma RS, Ehrenman K, Emerson SG. Hepatocyte growth factor is secreted by osteoblasts and cooperatively permits the survival of haematopoietic progenitors. Br J Haematol. 2001;112:438-448.
37. Taichman RS, Reilly MJ, Matthews LS. Human osteoblast-like cells and osteosarcoma cell lines synthesize MIP-1α in response to IL-1β and TNF-α stimulation in vitro. Br J Haematol. 2000;108:275-283.
38. Lee B, Thirunavukkarasu K, Zhou L, et al. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia. Nat Genet. 1997;16:307-310.
39. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997;89:747-754.
40. Deguchi K, Yagi H, Inada M, et al. Excessive extramedullary hematopoiesis in Cbfa1-deficient mice with a congenital lack of bone marrow*1, *2. Biochem Biophys Res Comm. 1999;255:352-359.
41. Sasaki K, Yagi H, Bronson RT, et al. Absence of fetal liver hematopoiesis in mice deficient in transcriptional coactivator core binding factor beta. Proc Natl Acad Sci U S A. 1996;93:12359-12363.
42. Wang Q, Stacy T, Binder M, et al. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996;93:3444-3449.
43. Wang Q, Stacy T, Miller JD, et al. The CBFβ sub-unit is essential for CBFα2 (AML1) function in vivo. Cell. 1996;87:697-708.
44. Yoshida CA, Furuichi T, Fujita T, et al. Core-binding factor beta interacts with Runx-2 and is required for skeletal development. Nat Genet. 2002;32:633-638.
45. Nilsson SK, Bertoncello I. Age-related changes in extramedullary hematopoiesis in the spleen of normal and perturbed osteopetrotic (op/op) mice [erratum appears in Exp Hematol. 1994;22:527-528]. Exp Hematol. 1994;22:377-383.
46. Nilsson SK, Bertoncello I. Age-related changes in extramedullary hematopoiesis in the spleen of normal and perturbed osteopetrotic (op/op) mice [erratum appears in Exp Hematol. 1994;22:527-528]. Exp Hematol. 1994;22:377-383.
47. Begg SK, Radley JM, Pollard JW, et al. Delayed hematopoietic development in osteopetrotic (op/op) mice. J Exp Med. 1993;177:237-242.
48. Wang ZQ, Ovitt C, Grigoriadis AE, et al. Bone and haematopoietic defects in mice lacking c-fos. Nature. 1992;360:741-745.
49. Lowe C, Yoneda T, Boyce BF, et al. Osteopetrosis in Src-deficient mice is due to an autonomous defect of osteoclasts. Proc Natl Acad Sci U S A. 1993;90:4485-4489.
50. Lowell CA, Niwa M, Soriano P, Varmus HE. Deficiency of the Hck and Src tyrosine kinases results in extreme levels of extramedullary hematopoiesis. Blood. 1996;87:1780-1792.
51. Gress CJ, Jacenko O. Growth plate compressions and altered hematopoiesis in collagen X null mice. J Cell Biol. 2000;149:983-993.
52. Jacenko O, Roberts DW, Campbell MR, et al. Linking hematopoiesis to endochondral skeletogenesis through analysis of mice transgenic for collagen X. Am J Pathol. 2002;160:2019-2034.
53. Gerber HP, Vu TH, Ryan AM, et al. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5:623-628.
54. Nakayama N, Lee J, Chiu L. Vascular endothelial growth factor synergistically enhances bone morphogenetic protein-4-dependent lymphohematopoietic cell generation from embryonic stem cells in vitro. Blood. 2000;95:2275-2283.
55. Wang LC, Swat W, Fujiwara Y, et al. The TEL/ETV6 gene is required specifically for hematopoiesis in the bone marrow. Genes Dev. 1998;12:2392-2402.
56. Wang LC, Kuo F, Fujiwara Y, et al. Yolk sac angiogenic defect and intra-embryonic apoptosis in mice lacking the Ets-related factor TEL. EMBO J. 1997;16:4374-4383.
57. Kim CH, Broxmeyer HE. SLC/exodus2/6Ckine/TCA4 induces chemotaxis of hematopoietic progenitor cells: differential activity of ligands of CCR7, CXCR3, or CXCR4 in chemotaxis vs. suppression of progenitor proliferation. J Leukoc Biol. 1999;66:455-461.
58. Aiuti A, Tavian M, Cipponi A, et al. Expression of CXCR4, the receptor for stromal cell-derived factor-1 on fetal and adult human lymphohematopoietic progenitors. Eur J Immunol. 1999;29:1823-1831.
59. Nagasawa T, Hirota S, Tachibana K, et al. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 1996;382:635-638.
60. Peled A, Petit I, Kollet O, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science. 1999;283:845-848.
61. McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol. 1999;213:442-456.
62. Hamada T, Mohle R, Hesselgesser J, et al. Trans-endothelial migration of megakaryocytes in response to stromal cell-derived factor 1 (SDF-1) enhances platelet formation. J Exp Med. 1998;188:539-548.
63. Wang JF, Liu ZY, Groopman JE. The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion. Blood. 1998;92:756-764.
64. Yu XF, Huang YF, Collin-Osdoby P, Osdoby P. Stromal cell-derived factor-1 (SDF-1) recruits osteoclast precursors by inducing chemotaxis, matrix metalloproteinase-9 (MMP-9) activity, and collagen transmigration. J Bone Mineral Res. 2003;18:1404-1418.
65. Tada N, Ikeda T, Sato M, et al. Genetic ablation of osteoblasts causes osteopenia without affecting osteoclastogenesis in transgenic mice. Transgenics. 1995;1:649-662.
66. Corral D, Amling M, Priemel M, et al. Dissociation between bone resorption and bone formation in osteopenic transgenic mice. Proc Natl Acad Sci U S A. 1998;95:13835-13840.
67. Visnjic D, Kalajzic I, Gronowicz G, et al. Conditional ablation of the osteoblast lineage in Col2.3deltatk transgenic mice. J Bone Mineral Res. 2001;16:2222-2231.
68. Visnjic D, Kalajzic Z, Rowe DW, et al. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood. 2004;103:3258-3264.
69. Klein RF. Osteoblasts make for good neighbors [abstract]. Blood. 2004;103:3247.
70. Zhang JW, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425:836-841.
71. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425:841-846.
72. Arai F, Hirao A, Ohmura M, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 2004;118:149-161.
73. Lemischka IR, Moore KA. Stem cells: interactive niches [comment]. Nature. 2003;425:778-779.
74. Puri MC, Bernstein A. Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis. Proc Natl Acad Sci U S A. 2003;100:12753-12758.
75. Eipers PG, Kale S, Taichman RS, et al. Bone marrow accessory cells regulate human bone precursor cell development. Exp Hematol. 2000;28:815-825.
76. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4:7-25.
77. Crean SM, Meneski JP, Hullinger TG, et al. N-linked sialyated sugar receptors support haematopoietic cell-osteoblast adhesions. Br J Haematol. 2004;124:534-546.
78. Simmons PJ, Zannettino A, Gronthos S, Leavesly D. Potential adhesion mechanisms for localization of hematopoietic progenitors to bone marrow stroma. Leuk Lymphoma. 1994;12:353-363.
79. Coombe DR, Watt SM, Rarish CR. Mac-1(CD11b/CD18) and CD45 mediate the adhesion of hematopoietic progenitor cells to stromal cell elements via recognition of stromal heparan sulfate. Blood. 1994;84:739-752.
80. Teixido J, Hemler ME, Greenberger J, Anklesaria P. Role of beta1 and beta2 integrins in the adhesion of human CD34 hi stem cells to bone marrow stroma. J Clin Invest. 1992;90:358-367.
81. Bhatia R, McGlave P, Verfaille C. Treatment of marrow stroma with interferon-alpha restores normal beta 1 integrin-dependent adhesion of chronic myelogenous leukemia hematopoietic progenitors: role of MIP-1 alpha. J Clin Invest. 1995;96:931-939.
82. Rose DM, Cardarelli PM, Cobb RR, Ginsberg MH. Soluble VCAM-1 binding to alpha4 integrins is cell-type specific and activation dependent and is disrupted during apoptosis in T cells. Blood. 2000;95:602-609.
83. Verfaillie CM. Adhesion receptors as regulators of the hematopoietic process. Blood. 1998;92:2609-2612.
84. Toksoz D, Zsebo KM, Smith KA, et al. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci U S A. 1992;89:7350-7354.
85. Gordon MY, Ford AM, Greaves MF. Interactions of hematopoietic progenitor cells with extracellular matrix. In: Long MW, Wicha MS, eds. The Hematopoietic Microenvironment: Functional Basis of Blood Cell Development. Baltimore, MD: John Hopkins University Press; 1993:152-174.
86. Hardy C, Minguell J. Modulation of the adhesion of hemopoietic progenitor cells to the RGD site of fibronectin by interleukin 3. J Cell Physiol. 1995;164:315-323.
87. Slanicka KM, Nissen C, Manz CY, et al. The membrane-bound isoform of stem cell factor synergizes with soluble flt3 ligand in supporting early hematopoietic cells in long-term cultures of normal and aplastic anemia bone marrow. Exp Hematol. 1998;26:365-373.
88. Horton MA, Dorey EL, Nesbitt SA, et al. Modulation of vitronectin receptor-mediated osteoclast adhesion by Arg-Gly-Asp peptide analogs: a structure-function analysis. J Bone Miner Res. 1993;8:239-247.
89. Duong L, Tanaka H, Rodan G. VCAM-1 involvement in osteoblast-osteoclast interactions during osteoclast differentiation [abstract]. J Bone Miner Res. 1995;9(suppl):S131.
90. Tanaka Y, Mine S, Hanagiri T, et al. Constitutive up-regulation of integrin-mediated adhesion of tumor-infiltrating lymphocytes to osteoblasts and bone marrow-derived stromal cells. Cancer Res. 1998;58:4138-4145.
91. Nilsson SK, Dooner MS, Tiarks CY, et al. Potential and distribution of transplanted hematopoietic stem cells in a nonablated mouse model. Blood. 1997;89:4013-4020.
92. Nilsson SK, Dooner MS, Weier HU, et al. Cells capable of bone production engraft from whole bone marrow transplants in nonablated mice. J Exp Med. 1999;189:729-734.
93. El-Badri NS, Wang BY, Cherry, Good RA. Osteoblasts promote engraftment of allogeneic hematopoietic stem cells. Exp Hematol. 1998;26:110-116.
94. Kushida T, Inaba M, Hisha H, et al. Intra-bone marrow injection of allogeneic bone marrow cells: a powerful new strategy for treatment of intractable autoimmune diseases in MRL/lpr mice. Blood. 2001;97:3292-3299.
95. Li Y, Hisha H, Inaba M, et al. Evidence for migration of donor bone marrow stromal cells into recipient thymus after bone marrow transplantation plus bone grafts: a role of stromal cells in positive selection. Exp Hematol. 2000;28:950-960.
96. Ishida T, Inaba M, Hisha H, et al. Requirement of donor-derived stromal cells in the bone marrow for successful allogeneic bone marrow transplantation: complete prevention of recurrence of auto-immune diseases in MRL/MP-lpr/lpr mice by transplantation of bone marrow plus bones (stromal cells) from the same donor. J Immunol. 1994;152:3119-3127.
97. Cahill RA, Jones C, Mueller TO, El Badri NS, Good RA. Replacement of recipient stromal/mesenchymal cells after bone marrow transplant using bone fragments and cultured osteoblast-like cells [abstract]. Blood. 2002;100:63.
98. Cahill RA, Klemperer MR, Steele A, El Badri NS, Good RA. Successful transplantation to correct a metabolic bone disease (infantile hypophosphatasia) using bone fragments plus cultured osteoblasts with T-cell depleted mismatched bone marrow lymphohematopoietic engraftment [abstract]. Blood. 2001;98:796-797.
99. Skjodt H, Moller T, Freiesleben SF. Human osteoblast-like cells expressing MHC class II determinants stimulate allogeneic and autologous peripheral-blood mononuclear cells and function as antigen-presenting cells. Immunology. 1989;68:416-420.
100. Reyes-Botella CMM. Antigenic phenotype of cultured human osteoblast-like cells. Cell Physiol Biochem. 2002;12:359-364.
101. Almeida-Porada G, Zanjani ED. A large animal noninjury model for study of human stem cell plasticity. Blood Cells Mol Dis. 2004;32:77-81.