Cellular complexity of the bone marrow hematopoietic stem cell niche

Calcified Tissue International

Volumn 94, Issue 1, 2014, Pages 112-124

  Calvi, Laura M ^a   Link, Daniel C ^b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipocyte; Bone marrow cell; Mesenchymal stem cell; Osteoblast; Osteoclast

Indexed keywords

ADIPOCYTE; ADULT STEM CELL; APOPTOSIS; CELL DIFFERENTIATION; CELL HOMING; CELL LINEAGE; CELL MIGRATION; CELL RENEWAL; CELLULAR DISTRIBUTION; ENDOTHELIUM CELL; FLOW CYTOMETRY; GENETIC MODEL; GLIA CELL; HEMATOPOIETIC STEM CELL; HUMAN; MACROPHAGE; MESENCHYMAL STEM CELL; NEUTROPHIL; NONHUMAN; OSTEOCLAST; PERIVASCULAR EPITHELIOID CELL TUMOR; PRIORITY JOURNAL; REVIEW; STEM CELL NICHE;

ANIMALS; BONE AND BONES; BONE MARROW; CELL DIFFERENTIATION; CELL LINEAGE; HEMATOPOIETIC STEM CELLS; HUMANS; STEM CELL NICHE;

EID: 84893692635     PISSN: 0171967X     EISSN: 14320827     Source Type: Journal    
DOI: 10.1007/s00223-013-9805-8     Document Type: Review

References (150)

1. Hartenstein V (2006) Blood cells and blood cell development in the animal kingdom. Annu Rev Cell Dev Biol 22:677-712
2. Bianco P, Robey PG et al (2010) "Mesenchymal" stem cells in human bone marrow (skeletal stem cells): a critical discussion of their nature, identity, and significance in incurable skeletal disease. Hum Gene Ther 21(9):1057-1066
3. Chang MK, Raggatt LJ et al (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181(2):1232-1244
4. Fazeli PK, Horowitz MC et al (2013) Marrow fat and bone - new perspectives. J Clin Endocrinol Metab 98(3):935-945
5. Wilson A, Murphy MJ et al (2004) c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 18(22):2747-2763
6. Xie Y, Yin T et al (2009) Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 457(7225):97-101
7. Zhang J, Niu C et al (2003) Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425(6960):836-841
8. Kiel MJ, Yilmaz OH et al (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121(7):1109-1121
9. Sugiyama T, Kohara H et al (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977-988
10. Mendez-Ferrer S, Michurina TV et al (2010) Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308):829-834
11. Nombela-Arrieta C, Pivarnik G et al (2013) Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol 15(5):533-543
12. Cantor AB, Orkin SH (2001) Hematopoietic development: a balancing act. Curr Opin Genet Dev 11(5):513-519
13. Enver T, Pera M et al (2009) Stem cell states, fates, and the rules of attraction. Cell Stem Cell 4(5):387-397
14. Graf T, Enver T (2009) Forcing cells to change lineages. Nature 462(7273):587-594
15. Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4(1-2):7-25
16. Gong JK (1978) Endosteal marrow: a rich source of hematopoietic stem cells. Science 199(4336):1443-1445
17. Lord BI, Testa NG et al (1975) The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 46(1):65-72
18. Lo Celso C, Fleming HE et al (2009) Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 457(7225):92-96
19. Nilsson SK, Dooner MS et al (1997) Potential and distribution of transplanted hematopoietic stem cells in a nonablated mouse model. Blood 89(11):4013-4020
20. Nilsson SK, Johnston HM et al (2001) Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 97(8):2293-2299
21. Kai T, Spradling A (2003) An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc Natl Acad Sci USA 100(8):4633-4638
22. Fuchs E, Tumbar T et al (2004) Socializing with the neighbors: stem cells and their niche. Cell 116(6):769-778
23. Losick VP, Morris LX et al (2011) Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell 21(1):159-171
24. Dzierzak E, Speck NA (2008) Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 9(2):129-136
25. Medvinsky A, Dzierzak E (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86(6):897-906
26. Dzierzak E (1999) Embryonic beginnings of definitive hematopoietic stem cells. Ann NY Acad Sci 872:256-262
27. Fliedner MC (2002) Research within the field of blood and marrow transplantation nursing: how can it contribute to higher quality of care? Int J Hematol 76(Suppl 2):289-291
28. Osawa M, Hanada K et al (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273(5272):242-245
29. Suzuki N, Ohneda O et al (2006) Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci USA 103(7):2202-2207
30. Storb R, Graham TC et al (1977) Demonstration of hemopoietic stem cells in the peripheral blood of baboons by cross circulation. Blood 50(3):537-542
31. Wagers AJ, Sherwood RI et al (2002) Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297(5590):2256-2259
32. Wright DE, Wagers AJ et al (2001) Physiological migration of hematopoietic stem and progenitor cells. Science 294(5548):1933-1936
33. Lapid K, Itkin T et al (2013) GSK3beta regulates physiological migration of stem/progenitor cells via cytoskeletal rearrangement. J Clin Invest 123(4):1705-1717
34. Katayama Y, Battista M et al (2006) Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 124(2):407-421
35. Mendez-Ferrer S, Lucas D et al (2008) Haematopoietic stem cell release is regulated by circadian oscillations. Nature 452(7186):442-447
36. Haylock DN, Williams B et al (2007) Hemopoietic stem cells with higher hemopoietic potential reside at the bone marrow endosteum. Stem Cells 25(4):1062-1069
37. Taichman RS, Emerson SG (1994) Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 179(5):1677-1682
38. Taichman RS, Reilly MJ et al (1996) Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood 87(2):518-524
39. Visnjic D, Kalajzic I et al (2001) Conditional ablation of the osteoblast lineage in Col2.3deltatk transgenic mice. J Bone Miner Res 16(12):2222-2231
40. Visnjic D, Kalajzic Z et al (2004) Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 103(9):3258-3264
41. Calvi LM, Adams GB et al (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425(6960):841-846
42. Marusic A, Kalinowski JF et al (1993) Production of leukemia inhibitory factor mRNA and protein by malignant and immortalized bone cells. J Bone Miner Res 8(5):617-624
43. Arai F, Hirao A et al (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118(2):149-161
44. Jung Y, Wang J et al (2007) Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 110(1):82-90
45. Qian H, Buza-Vidas N et al (2007) Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 1(6):671-684
46. Weber JM, Forsythe SR et al (2006) Parathyroid hormone stimulates expression of the Notch ligand Jagged1 in osteoblastic cells. Bone 39(3):485-493
47. Yoshihara H, Arai F et al (2007) Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 1(6):685-697
48. Adams GB, Martin RP et al (2007) Therapeutic targeting of a stem cell niche (vol 25, pg 238, 2007). Nat Biotechnol 25(8):944-945
49. Bromberg O, Frisch BJ et al (2012) Osteoblastic N-cadherin is not required for microenvironmental support and regulation of hematopoietic stem and progenitor cells. Blood 120(2):303-313
50. Calvi LM, Sims NA et al (2001) Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J Clin Invest 107(3):277-286
51. Goltzman D (2008) Studies on the mechanisms of the skeletal anabolic action of endogenous and exogenous parathyroid hormone. Arch Biochem Biophys 473(2):218-224
52. Ballen KK, Shpall EJ et al (2007) Phase I trial of parathyroid hormone to facilitate stem cell mobilization. Biol Blood Marrow Transplant 13(7):838-843
53. Brunner S, Theiss HD et al (2007) Primary hyperparathyroidism is associated with increased circulating bone marrow-derived progenitor cells. Am J Physiol Endocrinol Metab 293(6):E1670-E1675
54. Lymperi S, Horwood N et al (2008) Strontium can increase some osteoblasts without increasing hematopoietic stem cells. Blood 111(3):1173-1181
55. Schepers K, Hsiao EC et al (2012) Activated Gs signaling in osteoblastic cells alters the hematopoietic stem cell niche in mice. Blood 120(17):3425-3435
56. Ma YD, Park C et al (2009) Defects in osteoblast function but no changes in long-term repopulating potential of hematopoietic stem cells in a mouse chronic inflammatory arthritis model. Blood 114(20):4402-4410
57. Nakamura Y, Arai F et al (2010) Isolation and characterization of endosteal niche cell populations that regulate hematopoietic stem cells. Blood 116(9):1422-1432
58. Cheng YH, Chitteti BR et al (2011) Impact of maturational status on the ability of osteoblasts to enhance the hematopoietic function of stem and progenitor cells. J Bone Miner Res 26(5):1111-1121
59. Chitteti BR, Cheng YH et al (2010) Impact of interactions of cellular components of the bone marrow microenvironment on hematopoietic stem and progenitor cell function. Blood 115(16):3239-3248
60. Chitteti BR, Cheng YH et al (2010) Osteoblast lineage cells expressing high levels of Runx2 enhance hematopoietic progenitor cell proliferation and function. J Cell Biochem 111(2):284-294
61. Calvi LM, Bromberg O et al (2012) Osteoblastic expansion induced by parathyroid hormone receptor signaling in murine osteocytes is not sufficient to increase hematopoietic stem cells. Blood 119(11):2489-2499
62. Xiao L, Liu P et al (2009) Exported 18-kDa isoform of fibroblast growth factor-2 is a critical determinant of bone mass in mice. J Biol Chem 284(5):3170-3182
63. Yoon KA, Cho HS et al (2012) Differential regulation of CXCL5 by FGF2 in osteoblastic and endothelial niche cells supports hematopoietic stem cell migration. Stem Cells Dev 21:3391-3402
64. Song X, Zhu CH et al (2002) Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296(5574):1855-1857
65. Hosokawa K, Arai F et al (2010) Cadherin-based adhesion is a potential target for niche manipulation to protect hematopoietic stem cells in adult bone marrow. Cell Stem Cell 6(3):194-198
66. Hosokawa K, Arai F et al (2010) Knockdown of N-cadherin suppresses the long-term engraftment of hematopoietic stem cells. Blood 116(4):554-563
67. Levesque JP (2012) N(o)-cadherin role for HSCs. Blood 120(2):237-238
68. Dominici M, Rasini V et al (2009) Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood 114(11):2333-2343
69. Greenbaum AM, Revollo LD et al (2012) N-cadherin in osteolineage cells is not required for maintenance of hematopoietic stem cells. Blood 120(2):295-302
70. 2 treatment alters the bone marrow microenvironment and preferentially expands short-term hematopoietic stem cells. Blood 114(19):4054-4063
71. 2 enhances human cord blood stem cell xenotransplants and shows long-term safety in preclinical nonhuman primate transplant models. Cell Stem Cell 8(4):445-458
72. 2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447(7147):1007-1011
73. 2 increases hematopoietic stem cell survival and accelerates hematopoietic recovery after radiation injury. Stem Cells 31(2):372-383
74. Sugimura R, He XC et al (2012) Noncanonical wnt signaling maintains hematopoietic stem cells in the niche. Cell 150(2):351-365
75. Bedi B, Li JY et al (2012) Silencing of parathyroid hormone (PTH) receptor 1 in T cells blunts the bone anabolic activity of PTH. Proc Natl Acad Sci USA 109(12):E725-E733
76. Tawfeek H, Bedi B et al (2010) Disruption of PTH receptor 1 in T cells protects against PTH-induced bone loss. PLoS One 5(8):e12290
77. Terauchi M, Li JY et al (2009) T lymphocytes amplify the anabolic activity of parathyroid hormone through Wnt10b signaling. Cell Metab 10(3):229-240
78. Li JY, Adams J et al (2012) PTH expands short-term murine hemopoietic stem cells through T cells. Blood 120(22):4352-4362
79. Fulciniti M, Tassone P et al (2009) Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma. Blood 114(2):371-379
80. Qiang YW, Chen Y et al (2008) Myeloma-derived Dickkopf-1 disrupts Wnt-regulated osteoprotegerin and RANKL production by osteoblasts: a potential mechanism underlying osteolytic bone lesions in multiple myeloma. Blood 112(1):196-207
81. Vallet S, Pozzi S et al (2011) A novel role for CCL3 (MIP-1alpha) in myeloma-induced bone disease via osteocalcin downregulation and inhibition of osteoblast function. Leukemia 25(7):1174-1181
82. Colmone A, Amorim M et al (2008) Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 322(5909):1861-1865
83. Frisch BJ, Ashton JM et al (2012) Functional inhibition of osteoblastic cells in an in vivo mouse model of myeloid leukemia. Blood 119(2):540-550
84. Shiozawa Y, Pedersen EA et al (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 121(4):1298-1312
85. Simmons PJ, Torok-Storb B (1991) CD34 expression by stromal precursors in normal human adult bone marrow. Blood 78(11):2848-2853
86. Simmons PJ, Torok-Storb B (1991) Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78(1):55-62
87. Park D, Spencer JA et al (2012) Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 10(3):259-272
88. Masuda S, Ageyama N et al (2009) Cotransplantation with MSCs improves engraftment of HSCs after autologous intra-bone marrow transplantation in nonhuman primates. Exp Hematol 37(10):1250-1257
89. Ahn JY, Park G et al (2010) Intramarrow injection of beta-catenin- activated, but not naive mesenchymal stromal cells stimulates self-renewal of hematopoietic stem cells in bone marrow. Exp Mol Med 42(2):122-131
90. Sacchetti B, Funari A et al (2007) Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131(2):324-336
91. McNiece I, Harrington J et al (2004) Ex vivo expansion of cord blood mononuclear cells on mesenchymal stem cells. Cytotherapy 6(4):311-317
92. Robinson SN, Ng J et al (2006) Superior ex vivo cord blood expansion following co-culture with bone marrow-derived mesenchymal stem cells. Bone Marrow Transplant 37(4):359-366
93. de Lima M, McNiece I et al (2012) Cord-blood engraftment with ex vivo mesenchymal-cell coculture. N Engl J Med 367(24):2305-2315
94. + sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med 210:1351-1367
95. Nie Y, Han YC et al (2008) CXCR4 is required for the quiescence of primitive hematopoietic cells. J Exp Med 205(4):777-783
96. Tzeng YS, Li H et al (2011) Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood 117(2):429-439
97. Ara T, Itoi M et al (2003) A role of CXC chemokine ligand 12/stromal cell-derived factor-1/pre-B cell growth stimulating factor and its receptor CXCR4 in fetal and adult T cell development in vivo. J Immunol 170(9):4649-4655
98. Bonig H, Priestley GV et al (2004) PTX-sensitive signals in bone marrow homing of fetal and adult hematopoietic progenitor cells. Blood 104(8):2299-2306
99. Kawabata K, Ujikawa M et al (1999) A cell-autonomous requirement for CXCR4 in long-term lymphoid and myeloid reconstitution. Proc Natl Acad Sci USA 96(10):5663-5667
100. Peled A, Petit I et al (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283(5403):845-848
101. Ding L, Morrison SJ (2013) Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 495(7440):231-235
102. Greenbaum A, Hsu YM et al (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495(7440):227-230
103. Ding L, Saunders TL et al (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481(7382):457-462
104. Chen MJ, Yokomizo T et al (2009) Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457(7231):887-891
105. - cells are transiently reconstituting multipotent progenitors with little or no stem cell activity. Blood 111(8):4413-4414 author reply 4414-4415
106. Butler JM, Nolan DJ et al (2010) Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6(3):251-264
107. Chute JP, Muramoto GG et al (2006) Molecular profile and partial functional analysis of novel endothelial cell-derived growth factors that regulate hematopoiesis. Stem Cells 24(5):1315-1327
108. Kobayashi H, Butler JM et al (2010) Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol 12(11):1046-1056
109. Hooper AT, Butler JM et al (2009) Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 4(3):263-274
110. Winkler IG, Barbier V et al (2012) Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med 18(11):1651-1657
111. Barker JE (1994) Sl/Sld hematopoietic progenitors are deficient in situ. Exp Hematol 22(2):174-177
112. Barker JE (1997) Early transplantation to a normal microenvironment prevents the development of Steel hematopoietic stem cell defects. Exp Hematol 25(6):542-547
113. Yamazaki S, Iwama A et al (2009) TGF-beta as a candidate bone marrow niche signal to induce hematopoietic stem cell hibernation. Blood 113(6):1250-1256
114. Yamazaki S, Ema H et al (2011) Nonmyelinating Schwann cells maintain hematopoietic stem cell hibernation in the bone marrow niche. Cell 147(5):1146-1158
115. Kirkland JL, Tchkonia T et al (2002) Adipogenesis and aging: does aging make fat go MAD? Exp Gerontol 37(6):757-767
116. Rosen CJ, Ackert-Bicknell C et al (2009) Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr 19(2):109-124
117. Berkahn L, Keating A (2004) Hematopoiesis in the elderly. Hematology 9(3):159-163
118. Van Zant G, Liang Y (2012) Concise review: hematopoietic stem cell aging, life span, and transplantation. Stem Cells Transl Med 1(9):651-657
119. DiMascio L, Voermans C et al (2007) Identification of adiponectin as a novel hemopoietic stem cell growth factor. J Immunol 178(6):3511-3520
120. Berner HS, Lyngstadaas SP et al (2004) Adiponectin and its receptors are expressed in bone-forming cells. Bone 35(4):842-849
121. Naveiras O, Nardi V et al (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460(7252):259-263
122. Lymperi S, Ersek A et al (2011) Inhibition of osteoclast function reduces hematopoietic stem cell numbers in vivo. Blood 117(5):1540-1549
123. Mansour A, Abou-Ezzi G et al (2012) Osteoclasts promote the formation of hematopoietic stem cell niches in the bone marrow. J Exp Med 209(3):537-549
124. Adams GB, Chabner KT et al (2006) Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 439(7076):599-603
125. Christopher MJ, Liu F et al (2009) Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood 114(7):1331-1339
126. Levesque JP, Hendy J et al (2003) Disruption of the CXCR4/CXCL12 chemotactic interaction during hematopoietic stem cell mobilization induced by GCSF or cyclophosphamide. J Clin Invest 111(2):187-196
127. Petit I, Szyper-Kravitz M et al (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. [Erratum appears in Nat Immunol 2002;3(8):787]. Nat Immunol 3(7):687-694
128. Semerad CL, Christopher MJ et al (2005) G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 106(9):3020-3027
129. Kollet O, Dar A et al (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12(6):657-664
130. Miyamoto K, Yoshida S et al (2011) Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization. J Exp Med 208(11):2175-2181
131. Winkler IG, Barbier V et al (2010) 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 116(3):375-385
132. Winkler IG, Sims NA et al (2010) Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116(23):4815-4828
133. Yona S, Kim KW et al (2013) Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38(1):79-91
134. Alexander KA, Chang MK et al (2011) Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res 26(7):1517-1532
135. + macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med 208(2):261-271
136. Ludin A, Itkin T et al (2012) Monocytes-macrophages that express alpha-smooth muscle actin preserve primitive hematopoietic cells in the bone marrow. Nat Immunol 13(11):1072-1082
137. + macrophages provide a niche promoting erythropoiesis under homeostasis and stress. Nat Med 19(4):429-436
138. Westerterp M, Gourion-Arsiquaud S et al (2012) Regulation of hematopoietic stem and progenitor cell mobilization by cholesterol efflux pathways. Cell Stem Cell 11(2):195-206
139. Liu F, Poursine-Laurent J et al (2000) Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood 95(10):3025-3031
140. Christopher MJ, Rao M et al (2011) Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 208(2):251-260
141. Heissig B, Hattori K et al (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109(5):625-637
142. Levesque JP, Takamatsu Y et al (2001) Vascular cell adhesion molecule-1 (CD106) is cleaved by neutrophil proteases in the bone marrow following hematopoietic progenitor cell mobilization by granulocyte colony-stimulating factor. Blood 98(5):1289-1297
143. Levesque JP, Liu F et al (2004) Characterization of hematopoietic progenitor mobilization in protease-deficient mice. Blood 104(1):65-72
144. Singh P, Hu P et al (2012) Expansion of bone marrow neutrophils following G-CSF administration in mice results in osteolineage cell apoptosis and mobilization of hematopoietic stem and progenitor cells. Leukemia 26(11):2375-2383
145. Boneberg EM, Hareng L et al (2000) Human monocytes express functional receptors for granulocyte colony-stimulating factor that mediate suppression of monokines and interferon-gamma. Blood 95(1):270-276
146. Wang Y, Wan C et al (2007) The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 117(6):1616-1626
147. Rankin EB, Wu C et al (2012) The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell 149(1):63-74
148. Forristal CE, Winkler IG et al (2013) Pharmacologic stabilization of HIF-1alpha increases hematopoietic stem cell quiescence in vivo and accelerates blood recovery after severe irradiation. Blood 121(5):759-769
149. Takubo K, Goda N et al (2010) Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7(3):391-402
150. Levesque JP, Winkler IG et al (2007) Hematopoietic progenitor cell mobilization results in hypoxia with increased hypoxia-inducible transcription factor-1 alpha and vascular endothelial growth factor A in bone marrow. Stem Cells 25(8):1954-1965