Osteoblast-adipocyte lineage plasticity in tissue development, maintenance and pathology

Cellular and Molecular Life Sciences

Volumn 71, Issue 3, 2014, Pages 493-497

  Berendsen, Agnes D ^a   Olsen, Bjorn R ^a  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

Adipogenesis; Microenvironment; Osteoblastogenesis; Progenitor; Transcription

Indexed keywords

ADIPOCYTE; ADIPOGENESIS; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL LINEAGE; COMPLEX FORMATION; EPIGENETICS; GENE OVEREXPRESSION; HUMAN; OSTEOBLAST; PATHOGENESIS; PLASTICITY; REVIEW; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION;

ADIPOCYTES; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL LINEAGE; CELLULAR MICROENVIRONMENT; EPIGENESIS, GENETIC; HUMANS; OSTEOBLASTS; REGULATORY ELEMENTS, TRANSCRIPTIONAL;

EID: 84892823844     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1440-z     Document Type: Review

References (59)

1. Rozman C, Feliu E, Berga L, Reverter JC, Climent C, Ferran MJ (1989) Age-related variations of fat tissue fraction in normal human bone marrow depend both on size and number of adipocytes: a stereological study. Exp Hematol 17:34-37 (Pubitemid 19036773)
2. Charbord P, Tavian M, Humeau L, Peault B (1996) Early ontogeny of the human marrow from long bones: an immunohistochemical study of hematopoiesis and its microenvironment. Blood 87:4109-4119 (Pubitemid 26152255)
3. Kirkland JL, Tchkonia T, Pirtskhalava T, Han J, Karagiannides I (2002) Adipogenesis and aging: does aging make fat go MAD? Exp Gerontol 37:757-767 (Pubitemid 34518494)
4. Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147-154
5. Minaire P, Neunier P, Edouard C, Bernard J, Courpron P, Bourret J (1974) Quantitative histological data on disuse osteoporosis: comparison with biological data. Calcif Tissue Res 17:57-73
6. Ahdjoudj S, Lasmoles F, Holy X, Zerath E, Marie PJ (2002) Transforming growth factor beta2 inhibits adipocyte differentiation induced by skeletal unloading in rat bone marrow stroma. J Bone Miner Res 17:668-677 (Pubitemid 34246642)
7. Wronski TJ, Morey-Holton E, Jee WS (1981) Skeletal alterations in rats during space flight. Adv Space Res 1:135-140 (Pubitemid 14481451)
8. Noth U, Osyczka AM, Tuli R, Hickok NJ, Danielson KG, Tuan RS (2002) Multilineage mesenchymal differentiation potential of human trabecular bone-derived cells. J Orthop Res 20:1060-1069
9. Bennett JH, Joyner CJ, Triffitt JT, Owen ME (1991) Adipocytic cells cultured from marrow have osteogenic potential. J Cell Sci 99(Pt 1):131-139
10. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME (1992) Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102(Pt 2):341-351
11. Pignolo RJ, Xu M, Russell E, Richardson A, Kaplan J, Billings PC, Kaplan FS, Shore EM (2011) Heterozygous inactivation of GNAS in adipose-derived mesenchymal progenitor cells enhances osteoblast differentiation and promotes heterotopic ossification. J Bone Miner Res 26:2647-2655
12. Ahdjoudj S, Lasmoles F, Oyajobi BO, Lomri A, Delannoy P, Marie PJ (2001) Reciprocal control of osteoblast/chondroblast and osteoblast/adipocyte differentiation of multipotential clonal human marrow stromal F/STRO-1(+) cells. J Cell Biochem 81:23-38
13. Davis LA, Zur Nieden NI (2008) Mesodermal fate decisions of a stem cell: the Wnt switch. Cell Mol Life Sci 65:2658-2674
14. Gori F, Thomas T, Hicok KC, Spelsberg TC, Riggs BL (1999) Differentiation of human marrow stromal precursor cells: bone morphogenetic protein-2 increases OSF2/CBFA1, enhances osteoblast commitment, and inhibits late adipocyte maturation. J Bone Miner Res 14:1522-1535 (Pubitemid 29416678)
15. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M (1998) Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J Bone Miner Res 13:371-382 (Pubitemid 28146219)
16. Nuttall ME, Gimble JM (2000) Is there a therapeutic opportunity to either prevent or treat osteopenic disorders by inhibiting marrow adipogenesis? Bone 27:177-184 (Pubitemid 30458809)
17. Sabatakos G, Sims NA, Chen J, Aoki K, Kelz MB, Amling M, Bouali Y, Mukhopadhyay K, Ford K, Nestler EJ, Baron R (2000) Overexpression of DeltaFosB transcription factor(s) increases bone formation and inhibits adipogenesis. Nat Med 6:985-990
18. Spinella-Jaegle S, Rawadi G, Kawai S, Gallea S, Faucheu C, Mollat P, Courtois B, Bergaud B, Ramez V, Blanchet AM, Adelmant G, Baron R, Roman-Roman S (2001) Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J Cell Sci 114:2085-2094 (Pubitemid 32586633)
19. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR (2010) Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med 16:1400-1406
20. Manier S, Sacco A, Leleu X, Ghobrial IM, Roccaro AM (2012) Bone marrow microenvironment in multiple myeloma progression. J Biomed Biotechnol 2012:157496
21. Nuttall ME, Gimble JM (2004) Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol 4:290-294 (Pubitemid 38585315)
22. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89:747-754 (Pubitemid 27516177)
23. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89:755-764 (Pubitemid 27516178)
24. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ (1997) Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89:765-771 (Pubitemid 27516179)
25. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B (2002) The novel zinc finger-containing transcription factor Osterix is required for osteoblast differentiation and bone formation. Cell 108:17-29 (Pubitemid 34137009)
26. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, Schinke T, Li L, Brancorsini S, Sassone-Corsi P, Townes TM, Hanauer A, Karsenty G (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry syndrome. Cell 117:387-398 (Pubitemid 38534544)
27. Tontonoz P, Hu E, Spiegelman BM (1994) Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79:1147-1156
28. Rosen ED, Spiegelman BM (2001) PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276:37731-37734
29. Khan E, Abu-Amer Y (2003) Activation of peroxisome proliferator-activated receptor-gamma inhibits differentiation of preosteoblasts. J Lab Clin Med 142:29-34 (Pubitemid 36930414)
30. Jeon MJ, Kim JA, Kwon SH, Kim SW, Park KS, Park SW, Kim SY, Shin CS (2003) Activation of peroxisome proliferator-activated receptor-gamma inhibits the Runx2-mediated transcription of osteocalcin in osteoblasts. J Biol Chem 278:23270-23277 (Pubitemid 36830140)
31. Ahdjoudj S, Fromigue O, Marie PJ (2004) Plasticity and regulation of human bone marrow stromal osteoprogenitor cells: potential implication in the treatment of age-related bone loss. Histol Histopathol 19:151-157
32. Muruganandan S, Roman AA, Sinal CJ (2009) Adipocyte differentiation of bone marrow-derived mesenchymal stem cells: cross talk with the osteoblastogenic program. Cell Mol Life Sci 66:236-253
33. Ichida F, Nishimura R, Hata K, Matsubara T, Ikeda F, Hisada K, Yatani H, Cao X, Komori T, Yamaguchi A, Yoneda T (2004) Reciprocal roles of MSX2 in regulation of osteoblast and adipocyte differentiation. J Biol Chem 279:34015-34022 (Pubitemid 39063053)
34. Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R, Mueller E, Benjamin T, Spiegelman BM, Sharp PA, Hopkins N, Yaffe MB (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309:1074-1078 (Pubitemid 41134465)
35. Tokuzawa Y, Yagi K, Yamashita Y, Nakachi Y, Nikaido I, Bono H, Ninomiya Y, Kanesaki-Yatsuka Y, Akita M, Motegi H, Wakana S, Noda T, Sablitzky F, Arai S, Kurokawa R, Fukuda T, Katagiri T, Schonbach C, Suda T, Mizuno Y, Okazaki Y (2010) Id4, a new candidate gene for senile osteoporosis, acts as a molecular switch promoting osteoblast differentiation. PLoS Genet 6:e1001019
36. Backesjo CM, Li Y, Lindgren U, Haldosen LA (2006) Activation of Sirt1 decreases adipocyte formation during osteoblast differentiation of mesenchymal stem cells. J Bone Miner Res 21:993-1002 (Pubitemid 43962828)
37. Hesslein DG, Fretz JA, Xi Y, Nelson T, Zhou S, Lorenzo JA, Schatz DG, Horowitz MC (2009) Ebf1-dependent control of the osteoblast and adipocyte lineages. Bone 44:537-546
38. Calo E, Quintero-Estades JA, Danielian PS, Nedelcu S, Berman SD, Lees JA (2010) Rb regulates fate choice and lineage commitment in vivo. Nature 466:1110-1114
39. Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A, Kodama T, Yamaguchi A, Owen MJ, Takahashi S, Takayanagi H (2010) Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J Clin Invest 120:3455-3465
40. Liu Y, Berendsen AD, Jia S, Lotinun S, Baron R, Ferrara N, Olsen BR (2012) Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation. J Clin Invest 122:3101-3113
41. Rivas D, Li W, Akter R, Henderson JE, Duque G (2009) Accelerated features of age-related bone loss in zmpste24 metalloproteinase-deficient mice. J Gerontol A Biol Sci Med Sci 64:1015-1024
42. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483-495 (Pubitemid 38456178)
43. Chen JR, Lazarenko OP, Shankar K, Blackburn ML, Badger TM, Ronis MJ (2010) A role for ethanol-induced oxidative stress in controlling lineage commitment of mesenchymal stromal cells through inhibition of Wnt/beta-catenin signaling. J Bone Miner Res 25:1117-1127
44. Scheideler M, Elabd C, Zaragosi LE, Chiellini C, Hackl H, Sanchez-Cabo F, Yadav S, Duszka K, Friedl G, Papak C, Prokesch A, Windhager R, Ailhaud G, Dani C, Amri EZ, Trajanoski Z (2008) Comparative transcriptomics of human multipotent stem cells during adipogenesis and osteoblastogenesis. BMC Genomics 9:340
45. Ivey KN, Srivastava D (2010) MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7:36-41
46. Huang S, Wang S, Bian C, Yang Z, Zhou H, Zeng Y, Li H, Han Q, Zhao RC (2012) Upregulation of miR-22 promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells Dev 21:2531-2540
47. Gao J, Yang T, Han J, Yan K, Qiu X, Zhou Y, Fan Q, Ma B (2011) MicroRNA expression during osteogenic differentiation of human multipotent mesenchymal stromal cells from bone marrow. J Cell Biochem 112:1844-1856
48. Zhang JF, Fu WM, He ML, Wang H, Wang WM, Yu SC, Bian XW, Zhou J, Lin MC, Lu G, Poon WS, Kung HF (2011) MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix. Mol Biol Cell 22:3955-3961
49. Liao L, Yang X, Su X, Hu C, Zhu X, Yang N, Chen X, Shi S, Jin Y (2013) Redundant miR-3077-5p and miR-705 mediate the shift of mesenchymal stem cell lineage commitment to adipocyte in osteoporosis bone marrow. Cell Death Dis 4:e600
50. Li H, Li T, Wang S, Wei J, Fan J, Li J, Han Q, Liao L, Shao C, Zhao RC (2013) miR-17-5p and miR-106a are involved in the balance between osteogenic and adipogenic differentiation of adipose-derived mesenchymal stem cells. Stem Cell Res 10:313-324
51. Takada I, Mihara M, Suzawa M, Ohtake F, Kobayashi S, Igarashi M, Youn MY, Takeyama K, Nakamura T, Mezaki Y, Takezawa S, Yogiashi Y, Kitagawa H, Yamada G, Takada S, Minami Y, Shibuya H, Matsumoto K, Kato S (2007) A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 9:1273-1285 (Pubitemid 350042359)
52. Quach JM, Walker EC, Allan E, Solano M, Yokoyama A, Kato S, Sims NA, Gillespie MT, Martin TJ (2011) Zinc finger protein 467 is a novel regulator of osteoblast and adipocyte commitment. J Biol Chem 286:4186-4198
53. Razidlo DF, Whitney TJ, Casper ME, McGee-Lawrence ME, Stensgard BA, Li X, Secreto FJ, Knutson SK, Hiebert SW, Westendorf JJ (2010) Histone deacetylase 3 depletion in osteo/chondroprogenitor cells decreases bone density and increases marrow fat. PLoS One 5:e11492
54. Ye L, Fan Z, Yu B, Chang J, Al Hezaimi K, Zhou X, Park NH, Wang CY (2012) Histone demethylases KDM4B and KDM6B promotes osteogenic differentiation of human MSCs. Cell Stem Cell 11:50-61
55. Deng ZL, Sharff KA, Tang N, Song WX, Luo J, Luo X, Chen J, Bennett E, Reid R, Manning D, Xue A, Montag AG, Luu HH, Haydon RC, He TC (2008) Regulation of osteogenic differentiation during skeletal development. Front Biosci 13:2001-2021 (Pubitemid 351589231)
56. Lowe CE, O'Rahilly S, Rochford JJ (2011) Adipogenesis at a glance. J Cell Sci 124:2681-2686
57. Ralston SH, de Crombrugghe B (2006) Genetic regulation of bone mass and susceptibility to osteoporosis. Genes Dev 20:2492-2506 (Pubitemid 44396835)
58. Prockop DJ (1997) Marrow stromal cells as stem cells for no hematopoietic tissues. Science 276:71-74 (Pubitemid 27161245)
59. Park D, Spencer JA, Koh BI, Kobayashi T, Fujisaki J, Clemens TL, Lin CP, Kronenberg HM, Scadden DT (2012) Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 10:259-272