Mesenchymal progenitors and the osteoblast lineage in bone marrow hematopoietic niches

Current Osteoporosis Reports

Volumn 12, Issue 1, 2014, Pages 22-32

  Panaroni, Cristina ^a   Tzeng, Yi Shiuan ^a   Saeed, Hamid ^a   Wu, Joy Y ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adipocyte; B Lymphocyte; Erythrocyte; Hematopoiesis; Hematopoietic stem cell niche; Mesenchymal stem cell; Osteoblast; Osteoprogenitor

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; CD146 ANTIGEN; COLLAGEN TYPE 1; ENDOGLIN; ERYTHROPOIETIN; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYPOXIA INDUCIBLE FACTOR; INTERLEUKIN 6; INTERLEUKIN 7; JAGGED1; LEPTIN RECEPTOR; LEUKEMIA INHIBITORY FACTOR; NESTIN; PARATHYROID HORMONE RECEPTOR; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SCLEROSTIN; STEM CELL ANTIGEN 1; STEM CELL FACTOR; STROMAL CELL DERIVED FACTOR 1; THY 1 ANTIGEN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

BONE MARROW; CELL COUNT; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELLULAR DISTRIBUTION; COLONY FORMING UNIT; ERYTHROPOIESIS; FIBROBLAST; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOPOIESIS; MEGAKARYOPOIESIS; MESENCHYMAL STEM CELL; MYELOPOIESIS; NONHUMAN; OSTEOBLAST; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; STEM CELL MOBILIZATION; STEM CELL NICHE;

B-LYMPHOCYTES; BONE MARROW; CELL DIFFERENTIATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS;

EID: 84895918881     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-014-0190-7     Document Type: Review

References (76)

1. Weissman IL, Shizuru JA. The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood. 2008;112(9):3543-53.
2. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132(4):631-44. (Pubitemid 351260057)
3. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997;89(5):747-54. (Pubitemid 27516177)
4. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, et al. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89(5):755-64. (Pubitemid 27516178)
5. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002;108(1):17-29. (Pubitemid 34137009)
6. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, et al. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89(5):765-71. (Pubitemid 27516179)
7. Aubin JE. Regulation of osteoblast formation and function. Rev Endocr Metab Disord. 2001;2(1):81-94. (Pubitemid 33643895)
8. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21(2):115-37. (Pubitemid 32275592)
9. Matsuo K, Irie N. Osteoclast-osteoblast communication. Arch Biochem Biophys. 2008;473(2):201-9.
10. Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med. 1994;179(5):1677-82. (Pubitemid 24129586)
11. 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(4):509-17. (Pubitemid 26127501)
12. Taichman RS, Reilly MJ, Verma RS, Emerson SG. Augmented production of interleukin-6 by normal human osteoblasts in response to CD34+ hematopoietic bone marrow cells in vitro. Blood. 1997;89(4):1165-72. (Pubitemid 27079979)
13. Malaval L, Aubin JE. Biphasic effects of leukemia inhibitory factor on osteoblastic differentiation. J Cell Biochem Suppl. 2001;Suppl 36:63-70.
14. Nelissen JM, Torensma R, Pluyter M, Adema GJ, Raymakers RA, van Kooyk Y, et al. Molecular analysis of the hematopoiesis supporting osteoblastic cell line U2-OS. Exp Hematol. 2000;28(4):422-32. (Pubitemid 30214154)
15. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003;425(6960):841-6. (Pubitemid 37351468)
16. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature. 2003;425(6960):836-41. (Pubitemid 37351467)
17. Visnjic D, Kalajzic I, Gronowicz G, Aguila HL, Clark SH, Lichtler AC, et al. Conditional ablation of the osteoblast lineage in Col2.3deltatk transgenic mice. J Bone Miner Res. 2001;16(12):2222-31. (Pubitemid 33104712)
18. 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):3258-64. (Pubitemid 38525648)
19. Corral DA, Amling M, Priemel M, Loyer E, Fuchs S, Ducy P, et al. Dissociation between bone resorption and bone formation in osteopenic transgenic mice. Proc Natl Acad Sci U S A. 1998;95(23):13835-40. (Pubitemid 28523059)
20. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res. 2003;18(4):696-704. (Pubitemid 36899319)
21. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell. 2007;131(2):324-36. (Pubitemid 47592917)
22. Tormin A, Li O, Brune JC, Walsh S, Schutz B, Ehinger M, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood. 2011;117(19):5067-77.
23. Morikawa S, Mabuchi Y, Kubota Y, Nagai Y, Niibe K, Hiratsu E, et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J Exp Med. 2009;206(11):2483-96.
24. Arai F, Yoshihara H, Hosokawa K, Nakamura Y, Gomei Y, Iwasaki H, et al. Niche regulation of hematopoietic stem cells in the endosteum. Ann N Y Acad Sci. 2009;1176:36-46.
25. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301-13.
26. Corselli M, Chin CJ, Parekh C, Sahaghian A, Wang W, Ge S, et al. Perivascular support of human hematopoietic stem/progenitor cells. Blood. 2013;121(15):2891-901.
27. Stopp S, Bornhauser M, Ugarte F, Wobus M, Kuhn M, Brenner S, et al. Expression of the melanoma cell adhesion molecule in human mesenchymal stromal cells regulates proliferation, differentiation, and maintenance of hematopoietic stem and progenitor cells. Haematologica. 2013;98(4):505-13.
28. Isern J, Martin-Antonio B, Ghazanfari R, Martin AM, Lopez JA, del Toro R, et al. Self-renewing human bone marrow mesenspheres promote hematopoietic stem cell expansion. Cell Rep. 2013;3(5):1714-24.
29. .•• Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010;466(7308):829-34. This paper demonstrated that perivascular mesenchymal stem cells support HSCs in vivo.
30. .•• Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature. 2013;495(7440):231-5. This article (along with Greenbaum, 2013) demonstrated that CXCL12 produced by mesenchymal stem/progenitor cells is required for HSC maintenance and retention, while CXCL12 produced by osteoprogenitors and osteoblasts supports B lymphopoiesis.
31. .• Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481(7382):457-62. This paper reported that deletion of SCF from mesenchymal progenitors but not maturing osteoblasts leads to loss of bone marrow HSPCs.
32. Chan CK, Chen CC, Luppen CA, Kim JB, DeBoer AT, Wei K, et al. Endochondral ossification is required for haematopoietic stem-cell niche formation. Nature. 2009;457(7228):490-4.
33. Chan CK, Lindau P, Jiang W, Chen JY, Zhang LF, Chen CC, et al. Clonal precursor of bone, cartilage, and hematopoietic niche stromal cells. Proc Natl Acad Sci U S A. 2013;110(31):12643-8.
34. Broudy VC. Stem cell factor and hematopoiesis. Blood. 1997;90(4):1345-64. (Pubitemid 27355406)
35. Tzeng YS, Li H, Kang YL, Chen WC, Cheng WC, Lai DM. 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. 2011;117(2):429-39.
36. •• Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495(7440):227-30. This article (along with Ding, 2013) demonstrated that CXCL12 produced by mesenchymal stem/progenitor cells is required for HSC maintenance and retention, while CXCL12 produced by osteoprogenitors and osteoblasts supports B lymphopoiesis.
37. .• Omatsu Y, Sugiyama T, Kohara H, Kondoh G, Fujii N, Kohno K, et al. The essential functions of adipo-osteogenic progenitors as the hematopoietic stem and progenitor cell niche. Immunity. 2010;33(3):387-99. This paper revealed that CXCL12-expressing reticular cells have osteogenic and adipogenic potential, and are required for maintenance of HSCs, lymphoid and erythroid progenitors.
38. 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):977-88. (Pubitemid 44894948)
39. Walkley CR, Shea JM, Sims NA, Purton LE, Orkin SH. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell. 2007;129(6):1081-95. (Pubitemid 46908695)
40. Park D, Spencer JA, Koh BI, Kobayashi T, Fujisaki J, Clemens TL, et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell. 2012;10(3):259-72.
41. .• Maes C, Kobayashi T, Selig MK, Torrekens S, Roth SI, Mackem S, et al. Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell. 2010;19(2):329-44. This article reported that osteoprogenitors are found adjacent to blood vessels in developing bone and have the capacity to migrate and differentiate into trabecular osteoblasts.
42. Song L, Liu M, Ono N, Bringhurst FR, Kronenberg HM, Guo J. Loss of wnt/beta-catenin signaling causes cell fate shift of preosteoblasts from osteoblasts to adipocytes. J Bone Miner Res. 2012;27(11):2344-58.
43. Liu Y, Strecker S, Wang L, Kronenberg MS, Wang W, Rowe DW, et al. Osterix-cre labeled progenitor cells contribute to the formation and maintenance of the bone marrow stroma. PLoS One. 2013;8(8):e71318.
44. Grcevic D, Pejda S, Matthews BG, Repic D, Wang L, Li H, et al. In vivo fate mapping identifies mesenchymal progenitor cells. Stem Cells. 2012;30(2):187-96.
45. Kalajzic Z, Li H, Wang LP, Jiang X, Lamothe K, Adams DJ, et al. Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population. Bone. 2008;43(3):501-10.
46. Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell. 2008;135(2):240-9.
47. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, et al. White fat progenitor cells reside in the adipose vasculature. Science. 2008;322(5901):583-6.
48. Gupta RK, Arany Z, Seale P, Mepani RJ, Ye L, Conroe HM, et al. Transcriptional control of preadipocyte determination by Zfp423. Nature. 2010;464(7288):619-23.
49. Tran KV, Gealekman O, Frontini A, Zingaretti MC, Morroni M, Giordano A, et al. The vascular endothelium of the adipose tissue gives rise to both white and brown fat cells. Cell Metab. 2012;15(2):222-9.
50. .• Calvi LM, Bromberg O, Rhee Y, Weber JM, Smith JN, Basil MJ, et al. Osteoblastic expansion induced by parathyroid hormone receptor signaling in murine osteocytes is not sufficient to increase hematopoietic stem cells. Blood. 2012;119(11):2489-99. This article found that targeting of the constitutively active PPR to osteocytes, unlike targeting to maturing osteoblasts, fails to increase bone marow HSC frequency despite an increase in osteoblast numbers.
51. Calvi LM, Sims NA, Hunzelman JL, Knight MC, Giovannetti A, Saxton JM, et al. Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J Clin Invest. 2001;107(3):277-86. (Pubitemid 32157960)
52. Wu J, Purton LE, Rodda SJ, Chen M, Weinstein LS, McMahon AP, et al. Osteoblastic regulation of B lymphopoiesis is mediated by Gsalpha-dependent signaling pathways. Proc Natl Acad Sci U S A. 2008;105(44):16976-81.
53. Aguila HL, Mun SH, Kalinowski J, Adams DJ, Lorenzo JA, Lee SK. Osteoblast-specific overexpression of human interleukin-7 rescues the bone mass phenotype of interleukin-7-deficient female mice. J Bone Miner Res. 2012;27(5):1030-42.
54. .• Fulzele K, Krause DS, Panaroni C, Saini V, Barry KJ, Liu X, et al. Myelopoiesis is regulated by osteocytes through Gsalpha-dependent signaling. Blood. 2013;121(6):930-9. This article revealed a role for osteocytes in the regulation of the myeloid lineage.
55. Schepers K, Hsiao EC, Garg T, Scott MJ, Passegue E. Activated Gs signaling in osteoblastic cells alters the hematopoietic stem cell niche in mice. Blood. 2012;120(17):3425-35.
56. Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science. 1999;283(5403):845-8.
57. Semerad CL, Christopher MJ, Liu F, Short B, Simmons PJ, Winkler I, et al. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood. 2005;106(9):3020-7. (Pubitemid 41565894)
58. Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity. 2004;20(6):707-18. (Pubitemid 38757441)
59. Blin-Wakkach C, Wakkach A, Sexton PM, Rochet N, Carle GF. Hematological defects in the oc/oc mouse, a model of infantile malignant osteopetrosis. Leukemia. 2004;18(9):1505-11. (Pubitemid 39264073)
60. Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, Brown KD, et al. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev. 1997;11(24):3482-96. (Pubitemid 28023969)
61. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, Capparelli C, et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature. 1999;397(6717):315-23.
62. Tagaya H, Kunisada T, Yamazaki H, Yamane T, Tokuhisa T, Wagner EF, et al. Intramedullary and extramedullary B lymphopoiesis in osteopetrotic mice. Blood. 2000;95(11):3363-70. (Pubitemid 30428465)
63. Blin-Wakkach C, Wakkach A, Rochet N, Carle GF. Characterization of a novel bipotent hematopoietic progenitor population in normal and osteopetrotic mice. J Bone Miner Res. 2004;19(7):1137-43. (Pubitemid 41110566)
64. Scimeca JC, Franchi A, Trojani C, Parrinello H, Grosgeorge J, Robert C, et al. The gene encoding the mouse homologue of the human osteoclast-specific 116-kDa V-ATPase subunit bears a deletion in osteosclerotic (oc/oc) mutants. Bone. 2000;26(3):207-13. (Pubitemid 30101642)
65. Mansour A, Anginot A, Mancini SJ, Schiff C, Carle GF, Wakkach A, et al. Osteoclast activity modulates B-cell development in the bone marrow. Cell Res. 2011;21(7):1102-15.
66. Semenov M, Tamai K, He X. SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem. 2005;280(29):26770-5. (Pubitemid 41040710)
67. Cain CJ, Rueda R, McLelland B, Collette NM, Loots GG, Manilay JO. Absence of sclerostin adversely affects B-cell survival. J Bone Miner Res. 2012;27(7):1451-61.
68. Tamura M, Sato MM, Nashimoto M. Regulation of CXCL12 expression by canonical Wnt signaling in bone marrow stromal cells. Int J Biochem Cell Biol. 2011;43(5):760-7.
69. Ahmed N, Khokher MA, Hassan HT. Cytokine-induced expansion of human CD34+ stem/progenitor and CD34+CD41+ early megakaryocytic marrow cells cultured on normal osteoblasts. Stem Cells. 1999;17(2):92-9. (Pubitemid 29149398)
70. Cheng L, Qasba P, Vanguri P, Thiede MA. Human mesenchymal stem cells support megakaryocyte and pro-platelet formation from CD34(+) hematopoietic progenitor cells. J Cell Physiol. 2000;184(1):58-69. (Pubitemid 30349628)
71. Avraham H, Scadden DT, Chi S, Broudy VC, Zsebo KM, Groopman JE. Interaction of human bone marrow fibroblasts with megakaryocytes: role of the c-kit ligand. Blood. 1992;80(7):1679-84.
72. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, et al. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med. 2004;10(1):64-71. (Pubitemid 38524700)
73. Kacena MA, Gundberg CM, Horowitz MC. A reciprocal regulatory interaction between megakaryocytes, bone cells, and hematopoietic stem cells. Bone. 2006;39(5):978-84. (Pubitemid 44528390)
74. Olson TS, Caselli A, Otsuru S, Hofmann TJ, Williams R, Paolucci P, et al. Megakaryocytes promote murine osteoblastic HSC niche expansion and stem cell engraftment after radioablative conditioning. Blood. 2013;121(26):5238-49.
75. .• Rankin EB, Wu C, Khatri R, Wilson TL, Andersen R, Araldi E, et al. The HIF signaling pathway in osteoblasts directly modulates erythropoiesis through the production of EPO. Cell. 2012;149(1):63-74. This article demonstrated that the osteoblast lineage can be a source of erythropoietin and regulate erythropoiesis.
76. Wang Y, Wan C, Deng L, Liu X, Cao X, Gilbert SR, et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest. 2007;117(6):1616-26. (Pubitemid 46871346)