Bone and the hematopoietic niche: A tale of two stem cells

Blood

Volumn 117, Issue 20, 2011, Pages 5281-5288

  Bianco, Paolo ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; JAGGED1; NERVE CELL ADHESION MOLECULE; PARATHYROID HORMONE; PARATHYROID HORMONE RELATED PROTEIN; STROMAL CELL DERIVED FACTOR 1;

ADIPOCYTE; BONE; CELL PROLIFERATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NONHUMAN; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SKELETAL STEM CELL; STEM CELL; STEM CELL NICHE;

EID: 79956344963     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-315069     Document Type: Review

References (109)

1. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4 (1-2): 7-25. (Pubitemid 8376317)
2. Watt FM, Hogan BL. Out of Eden: stem cells and their niches. Science. 2000;287(5457):1427-1430. (Pubitemid 30127126)
3. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature. 2001;414(6859):98-104. (Pubitemid 33041633)
4. Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell. 2004;116(6):769-778. (Pubitemid 38410723)
5. Li L, Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol. 2005;21:605-631. (Pubitemid 41740648)
6. Lemischka IR, Moore KA. Stem cells: interactive niches. Nature. 2003;425(6960):778-779.
7. Moore KA, Lemischka IR. Stem cells and their niches. Science. 2006;311(5769):1880-1885.
8. Jones DL, Wagers AJ. No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol. 2008;9(1):11-21.
9. Adams GB, Martin RP, Alley IR, et al. Therapeutic targeting of a stem cell niche. Nat Biotechnol. 2007;25(2):238-243. (Pubitemid 46227124)
10. Adams GB, Scadden DT. The hematopoietic stem cell in its place. Nat Immunol. 2006;7(4):333-337.
11. Papayannopoulou T, Scadden DT. Stem-cell ecology and stem cells in motion. Blood. 2008;111(8):3923-3930.
12. Wilson A, Trumpp A. Bone-marrow haematopoietic stem-cell niches. Nat Rev Immunol. 2006;6:93-106.
13. Raaijmakers MH, Scadden DT. Evolving concepts on the microenvironmental niche for hematopoietic stem cells. Curr Opin Hematol. 2008;15(4):301-306.
14. Potten CS, Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development. 1990;110(4):1001-1020. (Pubitemid 120009472)
15. Garrett RW, Emerson SG. Bone and blood vessels: the hard and the soft of hematopoietic stem cell niches. Cell Stem Cell. 2009;4(6):503-506.
16. Kiel MJ, Morrison SJ. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol. 2008;8(4):290-301. (Pubitemid 351432804)
17. Frassoni F, Testa NG, Lord BI. The relative spatial distribution of erythroid progenitor cells (BFUe and CFUe) in the normal mouse femur. Cell Tissue Kinet. 1982;15:447-455. (Pubitemid 12074513)
18. Lord BI, Testa NG, Hendry JH. The relative spatial distributions of CFUS and CFUC in the normal mouse femur. Blood. 1975;46:65-72.
19. Haylock DN, Williams B, Johnston HM, et al. Hemopoietic stem cells with higher hemopoietic potential reside at the bone marrow endosteum. Stem Cells. 2007;25(4):1062-1069. (Pubitemid 46572605)
20. Nilsson SK, Johnston HM, Coverdale JA. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood. 2001;97:2293-2299. (Pubitemid 32291474)
21. Maloney MA, Lamela RA, Dorie MJ, Patt HM. Concentration gradient of blood stem cells in mouse bone marrow: an open question. Blood. 1978;51:521-525. (Pubitemid 8298484)
22. Tavassoli M, Yoffey JM. Bone Marrow: Structure and Function. New York, NY: Alan R Liss; 1983.
23. Tavassoli M. Ultrastructural development of bone marrow adipose cell. Acta Anat (Basel). 1976;94(1):65-77.
24. Adams GB, Chabner KT, Alley IR, et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature. 2006;439(7076):599-603. (Pubitemid 43185384)
25. Jiang Y, Bonig H, Ulyanova T, Chang K, Papayannopoulou T. On the adaptation of endosteal stem cell niche function in response to stress. Blood. 2009;114(18):3773-3782.
26. Xie Y, Yin T, Wiegraebe W, et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature. 2009;457(7225):97-101.
27. Westen H, Bainton DF. Association of alkalinephosphatase-positive reticulum cells in bone marrow with granulocytic precursors. J Exp Med. 1979;150:919-937. (Pubitemid 10227339)
28. Ashton BA, Eaglesom CC, Bab I, Owen ME. Distribution of fibroblastic colony-forming cells in rabbit bone marrow and assay of their osteogenic potential by an in vivo diffusion chamber method. Calcif Tissue Int. 1984;36(1):83-86. (Pubitemid 14026372)
29. Short BJ, Brouard N, Simmons PJ. Prospective isolation of mesenchymal stem cells from mouse compact bone. Methods Mol Biol. 2009;482:259-268.
30. Charlton DE, Utteridge TD, Beddoe AH. Microdosimetry of haemopoietic stem cells irradiated by alpha particles from the short-lived products of 222Rn decays in fat cells and haemopoietic tissue. Int J Radiat Biol. 1996;69(5):585-592.
31. Bourke VA, Watchman CJ, Reith JD, Jorgensen ML, Dieudonne A, Bolch WE. Spatial gradients of blood vessels and hematopoietic stem and progenitor cells within the marrow cavities of the human skeleton. Blood. 2009;114(19):4077-4080.
32. Calvi LM, Adams GB, Weibrecht KW, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425(6960):841-846. (Pubitemid 37351468)
33. Zhang J, Niu C, Ye L, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425(6960):836-841. (Pubitemid 37351467)
34. Koelliker A. Mikroskopische Anatomie der Gewebelehre des Menschen. Leipzig: Verlag von Wilhelm Engelmann; 1850.
35. Gehron Robey P, Bianco P. The cellular biology and molecular biochemistry of bone. In: Coe FL, Favus MJ, eds. Disorders of Bone and Mineral Metabolism. Philadelphia, PA: Lippincott Williams and Wilkins; 2002:199-226.
36. Wu JY, Scadden DT, Kronenberg HM. Role of the osteoblast lineage in the bone marrow hematopoietic niches. J Bone Miner Res. 2009;24(5):759-764.
37. Weinstein RS. Clinical use of bone biopsy. In: Coe FL, Favus MJ, eds. Disorders of Bone and Mineral Metabolism. Philadelphia, PA: Lippincott Williams & Wilkins; 2002:469-485.
38. Calvi LM, Sims NA, Hunzelman JL, et al. Activated parathyroid hormone/parathyroid hormonerelated protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J Clin Invest. 2001;107(3):277-286. (Pubitemid 32157960)
39. Visnjic D, Kalajzic Z, Rowe DW, Katavic V, Lorenzo J, Aguila HL. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood. 2004;103(9):3258-3264. (Pubitemid 38525648)
40. Visnjic D, Kalajzic I, Gronowicz G, et al. Conditional ablation of the osteoblast lineage in Col2. 3deltatk transgenic mice. J Bone Miner Res. 2001;16(12):2222-2231. (Pubitemid 33104712)
41. Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood. 2005;105(7):2631-2639. (Pubitemid 40446251)
42. Zhu J, Garrett R, Jung Y, et al. Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood. 2007;109(9):3706-3712. (Pubitemid 46641719)
43. Wu JY, Purton LE, Rodda SJ, et al. Osteoblastic regulation of B lymphopoiesis is mediated by Gs{alpha}-dependent signaling pathways. Proc Natl Acad Sci U S A. 2008;105(44):16976-16981.
44. Sacchetti B, Funari A, Michienzi S, et al. Selfrenewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131:324-336. (Pubitemid 47592917)
45. Satomura K, Krebsbach P, Bianco P, Gehron Robey P. Osteogenic imprinting upstream of marrow stromal cell differentiation. J Cell Biochem. 2000;78(3):391-403. (Pubitemid 30491068)
46. Bianco P, Kuznetsov SA, Riminucci M, Robey PG. Post-natal skeletal stem cells. Methods Enzymol. 2006;419:117-149.
47. Bianco P, Gehron Robey P. Marrow stromal stem cells. J Clin Invest. 2000;105(12):1663-1668. (Pubitemid 30421745)
48. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121. (Pubitemid 40884400)
49. Bianco P, Riminucci M, Bonucci E, Termine JD, Robey PG. Bone sialoprotein (BSP) secretion and osteoblast differentiation: relationship to bromodeoxyuridine incorporation, alkaline phosphatase, and matrix deposition. J Histochem Cytochem. 1993;41(2):183-191. (Pubitemid 23039097)
50. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature. 2003;423(6937):337-342. (Pubitemid 40852708)
51. Tavassoli M, Crosby WH. Transplantation of marrow to extramedullary sites. Science. 1968;161(836):54-56.
52. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation. 1974;17(4):331-340.
53. Hooper AT, Butler JM, Nolan DJ, et al. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell. 2009;4(3):263-274.
54. Ren G, Zhang L, Zhao X, et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell. 2008;2(2):141-150. (Pubitemid 351181031)
55. North TE, Goessling W, Peeters M, et al. Hematopoietic stem cell development is dependent on blood flow. Cell. 2009;137(4):736-748.
56. Aicher A, Heeschen C, Mildner-Rihm C, et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med. 2003;9(11):1370-1376. (Pubitemid 37466185)
57. Quesenberry PJ, Becker PS. Stem cell homing: rolling, crawling, and nesting. Proc Natl Acad Sci U S A. 1998;95(26):15155-15157. (Pubitemid 29018665)
58. Mazo IB, Gutierrez-Ramos J-C, Frenette PS, Hynes RO, Wagner DD, von Andrian UH. Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med. 1998:465-474. (Pubitemid 28369136)
59. Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD. Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci U S A. 1998;95(24):14423-14428. (Pubitemid 28549383)
60. Sipkins DA, Wei X, Wu JW, et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature. 2005;435(7044):969-973. (Pubitemid 40896324)
61. Zovein AC, Hofmann JJ, Lynch M, et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell. 2008;3(6):625-636.
62. Lo Celso C, Fleming HE, Wu JW, et al. Liveanimal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature. 2009;457(7225):92-96.
63. Weiss L. The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat Rec. 1976;186(2):161-184.
64. Bianco P, Boyde A. Confocal images of marrow stromal (Westen-Bainton) cells. Histochemistry. 1993;100(2):93-99. (Pubitemid 23272957)
65. Bianco P, Costantini M, Dearden LC, Bonucci E. Alkaline phosphatase positive precursors of adipocytes in the human bone marrow. Br J Haematol. 1988;68(4):401-403.
66. Friedenstein AJ. Osteogenic stem cells in bone marrow. In: Heersche JNM, Kanis JA, eds. Bone and Mineral Research. New York: Elsevier; 1990.
67. Bianco P, Robey PG, Simmons PJ. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell. 2008;2(4):313-319. (Pubitemid 351467394)
68. Song J, Kiel MJ, Wang Z, et al. An in vivo model to study and manipulate the hematopoietic stem cell niche. Blood. 2010;115(13):2592-2600.
69. Chan CK, Chen CC, Luppen CA, et al. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature. 2009;457(7228):490-494.
70. Kuznetsov SA, Riminucci M, Ziran N, et al. The interplay of osteogenesis and hematopoiesis: expression of a constitutively active PTH/PTHrP receptor in osteogenic cells perturbs the establishment of hematopoiesis in bone and of skeletal stem cells in the bone marrow. J Cell Biol. 2004;167(6):1113-1122. (Pubitemid 40066626)
71. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25(6):977-988. (Pubitemid 44894948)
72. Omatsu Y, Sugiyama T, Kohara H, et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity. 2010;33:387-399.
73. Méndez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466(7308):829-834.
74. Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97(6):512-523. (Pubitemid 41361741)
75. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9(6):685-693. (Pubitemid 36749217)
76. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277(5323):242- 245. (Pubitemid 27446080)
77. Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA. An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci U SA. 1989;86(12):4544-4548. (Pubitemid 19164588)
78. Hirschi KK, D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res. 1996;32(4):687-698. (Pubitemid 26332308)
79. Olsen BR, Reginato AM, Wang W. Bone development. Annu Rev Cell Dev Biol. 2000;16:191-220. (Pubitemid 32037505)
80. Arai F, Ohneda O, Miyamoto T, Zhang XQ, Suda T. Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med. 2002;195(12):1549-1563. (Pubitemid 34666069)
81. Suri C, Jones PF, Patan S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell. 1996;87(7):1171-1180. (Pubitemid 27010101)
82. 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(2):149-161. (Pubitemid 38962572)
83. Au P, Daheron LM, Duda DG, et al. Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood. 2008;111(3):1302-1305. (Pubitemid 351213415)
84. Gillette JM, Larochelle A, Dunbar CE, Lippincott-Schwartz J. Intercellular transfer to signalling endosomes regulates an ex vivo bone marrow niche. Nat Cell Biol. 2009;11(3):303-311.
85. Elefteriou F, Ahn JD, Takeda S, et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature. 2005;434(7032):514-520. (Pubitemid 40477060)
86. Katayama Y, Battista M, Kao WM, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell. 2006;124(2):407-421. (Pubitemid 43121987)
87. Méndez-Ferrer S, Lucas D, Battista M, Frenette PS. Haematopoietic stem cell release is regulated by circadian oscillations. Nature. 2008;452(7186):442-447. (Pubitemid 351450836)
88. Lucas D, Battista M, Shi PA, Isola L, Frenette PS. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell. 2008;3(4):364-366.
89. Vogler JB, Murphy WA. Bone marrow imaging. Radiology. 1988;168:679-693.
90. Neumann E. Das Gesetz Verbreitung des gelben und roten Markes in den Extremitatenknochen. Centr Med Wiss. 1882;20:321-323.
91. Ascenzi A. Physiological relationship and pathological interferences between bone tissue and marrow. In: Bourne GH, ed. The Biochemistry and Physiology of Bone. Vol IV. 2nd ed. New York: Academic Press; 1976:403-445.
92. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009;460:259-263.
93. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development. 1998;125(9):1591-1598. (Pubitemid 28256727)
94. Bachman ES, Dhillon H, Zhang CY, et al. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science. 2002;297(5582):843- 845. (Pubitemid 34839635)
95. Lane SW, Scadden DT, Gilliland DG. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood. 2009;114(6):1150-1157.
96. Scadden DT. The stem-cell niche as an entity of action. Nature. 2006;441(7097):1075-1079. (Pubitemid 43990719)
97. Scadden DT. The stem cell niche in health and leukemic disease. Best Pract Res Clin Haematol. 2007;20(1):19-27.
98. Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science. 2008;322:1861-1864.
99. Tripodo C, Di Bernardo A, Ternullo MP, et al. CD146 (+) bone marrow osteoprogenitors increase in the advanced stages of primary myelofibrosis. Haematologica. 2009;94(1):127-130.
100. Bianco P, Kuznetsov SA, Riminucci M, Fisher LW, Spiegel AM, Robey PG. Reproduction of human fibrous dysplasia of bone in immunocompromised mice by transplanted mosaics of normal and Gsalpha-mutated skeletal progenitor cells. J Clin Invest. 1998;101(8):1737-1744. (Pubitemid 28198504)
101. Bianco P, Bonucci E. Endosteal surfaces in hyperparathyroidism: an enzyme cytochemical study on low-temperature-processed, glycolmethacrylate-embedded bone biopsies. Virchows Arch A Pathol Anat Histopathol. 1991;419(5):425-431.
102. Walkley CR, Olsen GH, Dworkin S, et al. Amicroenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell. 2007;129(6):1097-1110. (Pubitemid 46908696)
103. Raaijmakers MH, Mukherjee S, Guo S, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature. 2010;464(7290):852-859.
104. Xie T, Spradling AC. decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell. 1998;94(2):251-260. (Pubitemid 28348012)
105. Kiger AA, White-Cooper H, Fuller MT. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature. 2000;407(6805):750-754.
106. Crittenden SL, Bernstein DS, Bachorik JL, et al. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature. 2002;417(6889):660-663. (Pubitemid 34614826)
107. Deguchi K, Yagi H, Inada M, Yoshizaki K, Kishimoto T, Komori T. Excessive extramedullar hematopoiesis in Cbfa1-deficient mice with a congenital lack of bone marrow. Biochem Biophys Res Commun. 1999;255(2):352-359. (Pubitemid 29292263)
108. Scharrer E. The histology of the meningeal myeloid tissue in the ganoids amia and lepisosteus. Z Zellforsch. 1944;88:291-310.
109. Morrison SJ, Shah NM, Anderson DJ. Regulatory mechanisms in stem cell biology. Cell. 1997;88(3):287-298. (Pubitemid 27131370)