Getting blood from bone: An emerging understanding of the role that osteoblasts play in regulating hematopoietic stem cells within their niche

Experimental Hematology

Volumn 40, Issue 9, 2012, Pages 685-694

  Shiozawa, Yusuke ^a   Taichman, Russell S ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; STROMAL CELL DERIVED FACTOR 1; THROMBOPOIETIN; VERY LATE ACTIVATION ANTIGEN 4;

CELL ACTIVITY; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL HOMING; CELL INTERACTION; CELL LINEAGE; CELL PROLIFERATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CIRCADIAN RHYTHM; HEMATOPOIETIC STEM CELL; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; STEM CELL MOBILIZATION; STEM CELL NICHE;

BONE DEVELOPMENT; BONE MARROW; BONE MARROW CELLS; CELL DIFFERENTIATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MODELS, BIOLOGICAL; OSTEOBLASTS; STEM CELL NICHE;

EID: 84864979448     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2012.05.004     Document Type: Review

References (116)

1. Tavian M., Peault B. Embryonic development of the human hematopoietic system. Int J Dev Biol 2005, 49:243-250.
2. Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978, 4:7-25.
3. Patt H.M., Maloney M.A. Bone formation and resorption as a requirement for marrow development. Proc Soc Exp Biol Med 1972, 140:205-207.
4. Lord B.I., Hendry J.H. The distribution of haemopoietic colony-forming units in the mouse femur, and its modification by x rays. Br J Radiol 1972, 45:110-115.
5. Gong J.K. Endosteal marrow: a rich source of hematopoietic stem cells. Science 1978, 199:1443-1445.
6. Taichman R.S., Emerson S.G. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 1994, 179:1677-1682.
7. Calvi L.M., Adams G.B., Weibrecht K.W., et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003, 425:841-846.
8. 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.
9. Zhang J., Niu C., Ye L., et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003, 425:836-841.
10. Zhu J., Garrett R., Jung Y., et al. Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood 2007, 109:3706-3712.
11. Visnjic D., Kalajzic Z., Rowe D.W., Katavic V., Lorenzo J., Aguila H.L. Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 2004, 103:3258-3264.
12. Kiel M.J., Yilmaz O.H., Iwashita T., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
13. Ding L., Saunders T.L., Enikolopov G., Morrison S.J. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 2012, 481:457-462.
14. 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, 25:977-988.
15. Naveiras O., Nardi V., Wenzel P.L., Hauschka P.V., Fahey F., Daley G.Q. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 2009, 460:259-263.
16. Morikawa S., Mabuchi Y., Kubota Y., et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med 2009, 206:2483-2496.
17. Mendez-Ferrer S., Michurina T.V., Ferraro F., et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010, 466:829-834.
18. Watt S.M., Forde S.P. The central role of the chemokine receptor, CXCR4, in haemopoietic stem cell transplantation: will CXCR4 antagonists contribute to the treatment of blood disorders?. Vox Sang 2008, 94:18-32.
19. 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.
20. Taichman R.S. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 2005, 105:2631-2639.
21. Broxmeyer H.E., Orschell C.M., Clapp D.W., et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005, 201:1307-1318.
22. Semerad C.L., Christopher M.J., Liu F., et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 2005, 106:3020-3027.
23. Katayama Y., Battista M., Kao W.M., et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006, 124:407-421.
24. Mendez-Ferrer S., Lucas D., Battista M., Frenette P.S. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008, 452:442-447.
25. Jung Y., Wang J., Schneider A., et al. Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 2006, 38:497-508.
26. Ponomaryov T., Peled A., Petit I., et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 2000, 106:1331-1339.
27. Dar A., Goichberg P., Shinder V., et al. Chemokine receptor CXCR4-dependent internalization and resecretion of functional chemokine SDF-1 by bone marrow endothelial and stromal cells. Nat Immunol 2005, 6:1038-1046.
28. Kollet O., Dar A., Shivtiel S., et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006, 12:657-664.
29. Yin T., Li L. The stem cell niches in bone. J Clin Invest 2006, 116:1195-1201.
30. Ceradini D.J., Kulkarni A.R., Callaghan M.J., et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 2004, 10:858-864.
31. Staller P., Sulitkova J., Lisztwan J., Moch H., Oakeley E.J., Krek W. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL. Nature 2003, 425:307-311.
32. Christopherson K.W., Hangoc G., Mantel C.R., Broxmeyer H.E. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 2004, 305:1000-1003.
33. Schwaiger E., Klaus C., Matheeussen V., et al. Dipeptidyl peptidase IV (DPPIV/CD26) inhibition does not improve engraftment of unfractionated syngeneic or allogeneic bone marrow after nonmyeloablative conditioning. Exp Hematol 2012, 40:97-106.
34. Adams G.B., Chabner K.T., Alley I.R., et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006, 439:599-603.
35. Adams G.B., Alley I.R., Chung U.I., et al. Haematopoietic stem cells depend on Galpha(s)-mediated signalling to engraft bone marrow. Nature 2009, 459:103-107.
36. Abkowitz J.L., Chen J. Studies of c-Mpl function distinguish the replication of hematopoietic stem cells from the expansion of differentiating clones. Blood 2007, 109:5186-5190.
37. Chen J., Larochelle A., Fricker S., Bridger G., Dunbar C.E., Abkowitz J.L. Mobilization as a preparative regimen for hematopoietic stem cell transplantation. Blood 2006, 107:3764-3771.
38. Czechowicz A., Kraft D., Weissman I.L., Bhattacharya D. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science 2007, 318:1296-1299.
39. Li P., Zon L.I. Resolving the controversy about N-cadherin and hematopoietic stem cells. Cell Stem Cell 2010, 6:199-202.
40. Kiel M.J., Radice G.L., Morrison S.J. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 2007, 1:204-217.
41. Haug J.S., He X.C., Grindley J.C., et al. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2008, 2:367-379.
42. Kiel M.J., Acar M., Radice G.L., Morrison S.J. Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell 2009, 4:170-179.
43. Greenbaum A.M., Revollo L.D., Woloszynek J.R., Civitelli R., Link D.C. N-cadherin in osteolineage cells is not required for maintenance of hematopoietic stem cells. Blood 2012 Feb 9, [Epub ahead of print].
44. Jacobsen K., Kravitz J., Kincade P.W., Osmond D.G. Adhesion receptors on bone marrow stromal cells: in vivo expression of vascular cell adhesion molecule-1 by reticular cells and sinusoidal endothelium in normal and gamma-irradiated mice. Blood 1996, 87:73-82.
45. Priestley G.V., Scott L.M., Ulyanova T., Papayannopoulou T. Lack of alpha4 integrin expression in stem cells restricts competitive function and self-renewal activity. Blood 2006, 107:2959-2967.
46. Jung Y., Shiozawa Y., Wang J., et al. Annexin-2 is a regulator of stromal cell-derived factor-1/CXCL12 function in the hematopoietic stem cell endosteal niche. Exp Hematol 2011, 39:151-166.e151.
47. Takahashi S., Reddy S.V., Chirgwin J.M., et al. Cloning and identification of annexin II as an autocrine/paracrine factor that increases osteoclast formation and bone resorption. J Biol Chem 1994, 269:28696-28701.
48. Siever D.A., Erickson H.P. Extracellular annexin II. Int J Biochem Cell Biol 1997, 29:1219-1223.
49. Kwon M., MacLeod T.J., Zhang Y., Waisman D.M. S100A10, annexin A2, and annexin a2 heterotetramer as candidate plasminogen receptors. Front Biosci 2005, 10:300-325.
50. Kang H.M., Choi K.S., Kassam G., Fitzpatrick S.L., Kwon M., Waisman D.M. Role of annexin II tetramer in plasminogen activation. Trends Cardiovasc Med 1999, 9:92-102.
51. Shiozawa Y., Havens A.M., Jung Y., et al. Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem 2008, 105:370-380.
52. Jung Y., Wang J., Song J., et al. Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 2007, 110:82-90.
53. D'Souza S., Kurihara N., Shiozawa Y., et al. Annexin II interactions with the Annexin II receptor enhance multiple myeloma cell adhesion and growth in the bone marrow microenvironment. Blood 2012, 119:1888-1896.
54. Nervi B., Link D.C., DiPersio J.F. Cytokines and hematopoietic stem cell mobilization. J Cell Biochem 2006, 99:690-705.
55. Eash K.J., Greenbaum A.M., Gopalan P.K., Link D.C. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest 2010, 120:2423-2431.
56. Avigdor A., Goichberg P., Shivtiel S., et al. CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 2004, 103:2981-2989.
57. Christopher M.J., Liu F., Hilton M.J., Long F., Link D.C. Suppression of CXCL12 production by bone marrow osteoblasts is a common and critical pathway for cytokine-induced mobilization. Blood 2009, 114:1331-1339.
58. Winkler I.G., Sims N.A., Pettit A.R., et al. Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 2010, 116:4815-4828.
59. Christopher M.J., Rao M., Liu F., Woloszynek J.R., Link D.C. Expression of the G-CSF receptor in monocytic cells is sufficient to mediate hematopoietic progenitor mobilization by G-CSF in mice. J Exp Med 2011, 208:251-260.
60. Chow A., Lucas D., Hidalgo A., et al. Bone marrow CD169+ macrophages promote the retention of hematopoietic stem and progenitor cells in the mesenchymal stem cell niche. J Exp Med 2011, 208:261-271.
61. Miyamoto K., Yoshida S., Kawasumi M., et al. Osteoclasts are dispensable for hematopoietic stem cell maintenance and mobilization. J Exp Med 2011, 208:2175-2181.
62. Uy G.L., Rettig M.P., Cashen A.F. Plerixafor, a CXCR4 antagonist for the mobilization of hematopoietic stem cells. Expert Opin Biol Ther 2008, 8:1797-1804.
63. Larochelle A., Krouse A., Metzger M., et al. AMD3100 mobilizes hematopoietic stem cells with long-term repopulating capacity in nonhuman primates. Blood 2006, 107:3772-3778.
64. Hess D.A., Bonde J., Craft T.P., et al. Human progenitor cells rapidly mobilized by AMD3100 repopulate NOD/SCID mice with increased frequency in comparison to cells from the same donor mobilized by granulocyte colony stimulating factor. Biol Blood Marrow Transplant 2007, 13:398-411.
65. Winkler I.G., Pettit A.R., Raggatt L.J., et al. Hematopoietic stem cell mobilizing agents G-CSF, cyclophosphamide or AMD3100 have distinct mechanisms of action on bone marrow HSC niches and bone formation. Leukemia 2012 Jan 23, [Epub ahead of print]. 10.1038/leu.2012.17.
66. Ramirez P., Rettig M.P., Uy G.L., et al. BIO5192, a small molecule inhibitor of VLA-4, mobilizes hematopoietic stem and progenitor cells. Blood 2009, 114:1340-1343.
67. Bonig H., Watts K.L., Chang K.H., Kiem H.P., Papayannopoulou T. Concurrent blockade of alpha4-integrin and CXCR4 in hematopoietic stem/progenitor cell mobilization. Stem Cells 2009, 27:836-837.
68. Lucas D., Battista M., Shi P.A., Isola L., Frenette P.S. Mobilized hematopoietic stem cell yield depends on species-specific circadian timing. Cell Stem Cell 2008, 3:364-366.
69. Tsinkalovsky O., Rosenlund B., Laerum O.D., Eiken H.G. Clock gene expression in purified mouse hematopoietic stem cells. Exp Hematol 2005, 33:100-107.
70. Tsinkalovsky O., Filipski E., Rosenlund B., et al. Circadian expression of clock genes in purified hematopoietic stem cells is developmentally regulated in mouse bone marrow. Exp Hematol 2006, 34:1249-1261.
71. Tsinkalovsky O., Smaaland R., Rosenlund B., et al. Circadian variations in clock gene expression of human bone marrow CD34+ cells. J Biol Rhythms 2007, 22:140-150.
72. D'Hondt L., McAuliffe C., Damon J., et al. Circadian variations of bone marrow engraftability. J Cell Physiol 2004, 200:63-70.
73. Fu L., Patel M.S., Bradley A., Wagner E.F., Karsenty G. The molecular clock mediates leptin-regulated bone formation. Cell 2005, 122:803-815.
74. Takeda S., Elefteriou F., Levasseur R., et al. Leptin regulates bone formation via the sympathetic nervous system. Cell 2002, 111:305-317.
75. Sato S., Hanada R., Kimura A., et al. Central control of bone remodeling by neuromedin U. Nat Med 2007, 13:1234-1240.
76. Kondo H., Nifuji A., Takeda S., et al. Unloading induces osteoblastic cell suppression and osteoclastic cell activation to lead to bone loss via sympathetic nervous system. J Biol Chem 2005, 280:30192-30200.
77. Elefteriou F., Ahn J.D., Takeda S., et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 2005, 434:514-520.
78. Wu X., Yu G., Parks H., et al. Circadian mechanisms in murine and human bone marrow mesenchymal stem cells following dexamethasone exposure. Bone 2008, 42:861-870.
79. Nemeth M.J., Topol L., Anderson S.M., Yang Y., Bodine D.M. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci U S A 2007, 104:15436-15441.
80. Fleming H.E., Janzen V., Lo Celso C., et al. Wnt signaling in the niche enforces hematopoietic stem cell quiescence and is necessary to preserve self-renewal in vivo. Cell Stem Cell 2008, 2:274-283.
81. Reya T., Duncan A.W., Ailles L., et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003, 423:409-414.
82. Duncan A.W., Rattis F.M., DiMascio L.N., et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 2005, 6:314-322.
83. Gao J., Graves S., Koch U., et al. Hedgehog signaling is dispensable for adult hematopoietic stem cell function. Cell Stem Cell 2009, 4:548-558.
84. Hofmann I., Stover E.H., Cullen D.E., et al. Hedgehog signaling is dispensable for adult murine hematopoietic stem cell function and hematopoiesis. Cell Stem Cell 2009, 4:559-567.
85. Stier S., Ko Y., Forkert R., et al. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med 2005, 201:1781-1791.
86. Nilsson S.K., Johnston H.M., Whitty G.A., et al. Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 2005, 106:1232-1239.
87. Yilmaz O.H., Valdez R., Theisen B.K., et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 2006, 441:475-482.
88. Huang J., Zhang Y., Bersenev A., et al. Pivotal role for glycogen synthase kinase-3 in hematopoietic stem cell homeostasis in mice. J Clin Invest 2009, 119:3519-3529.
89. Campbell T.B., Basu S., Hangoc G., Tao W., Broxmeyer H.E. Overexpression of Rheb2 enhances mouse hematopoietic progenitor cell growth while impairing stem cell repopulation. Blood 2009, 114:3392-3401.
90. Yoshihara H., Arai F., Hosokawa K., et al. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007, 1:685-697.
91. Qian H., Buza-Vidas N., Hyland C.D., et al. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 2007, 1:671-684.
92. Tong W., Lodish H.F. Lnk inhibits Tpo-mpl signaling and Tpo-mediated megakaryocytopoiesis. J Exp Med 2004, 200:569-580.
93. Bersenev A., Wu C., Balcerek J., Tong W. Lnk controls mouse hematopoietic stem cell self-renewal and quiescence through direct interactions with JAK2. J Clin Invest 2008, 118:2832-2844.
94. Nostro M.C., Cheng X., Keller G.M., Gadue P. Wnt, activin, and BMP signaling regulate distinct stages in the developmental pathway from embryonic stem cells to blood. Cell Stem Cell 2008, 2:60-71.
95. Lengerke C., Schmitt S., Bowman T.V., et al. BMP and Wnt specify hematopoietic fate by activation of the Cdx-Hox pathway. Cell Stem Cell 2008, 2:72-82.
96. Goldman D.C., Bailey A.S., Pfaffle D.L., Al Masri A., Christian J.L., Fleming W.H. BMP4 regulates the hematopoietic stem cell niche. Blood 2009, 114:4393-4401.
97. Jung Y., Song J., Shiozawa Y., et al. Hematopoietic stem cells regulate mesenchymal stromal cell induction into osteoblasts thereby participating in the formation of the stem cell niche. Stem Cells 2008, 26:2042-2051.
98. Shiozawa Y., Jung Y., Ziegler A.M., et al. Erythropoietin couples hematopoiesis with bone formation. PLoS One 2010, 5:e10853.
99. Parmar K., Mauch P., Vergilio J.A., Sackstein R., Down J.D. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007, 104:5431-5436.
100. Ito K., Hirao A., Arai F., et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006, 12:446-451.
101. Ito K., Hirao A., Arai F., et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004, 431:997-1002.
102. Wilson A., Laurenti E., Oser G., et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008, 135:1118-1129.
103. Chan C.K., Chen C.C., Luppen C.A., et al. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature 2009, 457:490-494.
104. Raaijmakers M.H., Mukherjee S., Guo S., et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 2010, 464:852-857.
105. Lo Celso C., Fleming H.E., Wu J.W., et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009, 457:92-96.
106. Xie Y., Yin T., Wiegraebe W., et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 2009, 457:97-101.
107. Fujisaki J., Wu J., Carlson A.L., et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 2011, 474:216-219.
108. Chitteti B.R., Cheng Y.H., Poteat B., et al. Impact of interactions of cellular components of the bone marrow microenvironment on hematopoietic stem and progenitor cell function. Blood 2010, 115:3239-3248.
109. Myers K.C., Davies S.M. Hematopoietic stem cell transplantation for bone marrow failure syndromes in children. Biol Blood Marrow Transplant 2009, 15:279-292.
110. Hofmeister C.C., Zhang J., Knight K.L., Le P., Stiff P.J. Ex vivo expansion of umbilical cord blood stem cells for transplantation: growing knowledge from the hematopoietic niche. Bone Marrow Transplant 2007, 39:11-23.
111. Adams G.B., Scadden D.T. A niche opportunity for stem cell therapeutics. Gene Ther 2008, 15:96-99.
112. Lane S.W., Scadden D.T., Gilliland D.G. The leukemic stem cell niche: current concepts and therapeutic opportunities. Blood 2009, 114:1150-1157.
113. Shiozawa Y., Havens A.M., Pienta K.J., Taichman R.S. The bone marrow niche: habitat to hematopoietic and mesenchymal stem cells, and unwitting host to molecular parasites. Leukemia 2008, 22:941-950.
114. Shiozawa Y., Pedersen E.A., Havens A.M., et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 2011, 121:1298-1312.
115. Walkley C.R., Olsen G.H., Dworkin S., et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 2007, 129:1097-1110.
116. Walkley C.R., Shea J.M., Sims N.A., Purton L.E., Orkin S.H. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 2007, 129:1081-1095.