Loss of wnt/β-catenin signaling causes cell fate shift of preosteoblasts from osteoblasts to adipocytes

Journal of Bone and Mineral Research

Volumn 27, Issue 11, 2012, Pages 2344-2358

  Song, Lige ^a   Liu, Minlin ^a   Ono, Noriaki ^a   Bringhurst, F Richard ^a   Kronenberg, Henry M ^a   Guo, Jun ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

CATENIN; ADIPOGENESIS; CANONICAL WNT SIGNALING; OSTEOGENESIS

Indexed keywords

BETA CATENIN; TRANSCRIPTION FACTOR OSTERIX; WNT PROTEIN;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW; BONE MARROW CELL; BONE MASS; CELL CULTURE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL TRANSFORMATION; CONTROLLED STUDY; GENE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYOBLAST; NONHUMAN; OBESITY; OSTEOBLAST; PERINATAL PERIOD; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADIPOCYTES; ADIPOGENESIS; ADIPOSITY; ANIMALS; BETA CATENIN; BONE MARROW CELLS; CELL LINEAGE; CELL SEPARATION; CELLS, CULTURED; GENE DELETION; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; INTEGRASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOBLASTS; OSTEOGENESIS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; WNT SIGNALING PATHWAY;

EID: 84867505259     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1694     Document Type: Article

References (41)

1. Nuttall ME, Gimble JM., Is there a therapeutic opportunity to either prevent or treat osteopenic disorders by inhibiting marrow adipogenesis?. Bone. 2000; 27 (2): 177-84. (Pubitemid 30458809)
2. Minaire P, Neunier P, Edouard C, Bernard J, Courpron P, Bourret J., Quantitative histological data on disuse osteoporosis: comparison with biological data. Calcif Tissue Res. 1974; 17 (1): 57-73.
3. Ahdjoudj S, Lasmoles F, Holy X, Zerath E, Marie PJ., Transforming growth factor beta2 inhibits adipocyte differentiation induced by skeletal unloading in rat bone marrow stroma. J Bone Miner Res. 2002; 17 (4): 668-77. (Pubitemid 34246642)
4. Wronski TJ, Morey-Holton E, Jee WS., Skeletal alterations in rats during space flight. Adv Space Res. 1981; 1 (14): 135-40. (Pubitemid 14481451)
5. Meunier P, Aaron J, Edouard C, Vignon G., 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. 1971; 80: 147-54.
6. Kajkenova O, Lecka-Czernik B, Gubrij I, Hauser SP, Takahashi K, Parfitt AM, Jilka RL, Manolagas SC, Lipschitz DA., Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res. 1997; 12 (11): 1772-9. (Pubitemid 27500188)
7. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M., Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology. 2001; 2 (3): 165-71. (Pubitemid 32851325)
8. Rosen ED, Spiegelman BM., Molecular regulation of adipogenesis. Annu Rev Cell Dev Biol. 2000; 16: 145-71. (Pubitemid 32037503)
9. Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM., Transcriptional regulation of adipogenesis. Genes Dev. 2000; 14 (11): 1293-307. (Pubitemid 30397073)
10. Darlington GJ, Ross SE, MacDougald OA., The role of C/EBP genes in adipocyte differentiation. J Biol Chem. 1998; 273 (46): 30057-60. (Pubitemid 28545461)
11. Krishnan V, Bryant HU, Macdougald OA., Regulation of bone mass by Wnt signaling. J Clin Invest. 2006; 116 (5): 1202-9.
12. Gambardella A, Nagaraju CK, O'Shea PJ, Mohanty ST, Kottam L, Pilling J, Sullivan M, Djerbi M, Koopmann W, Croucher PI, Bellantuono I., Glycogen synthase kinase-3alpha/beta inhibition promotes in vivo amplification of endogenous mesenchymal progenitors with osteogenic and adipogenic potential and their differentiation to the osteogenic lineage. J Bone Miner Res. 2011; 26 (4): 811-21.
13. Guo W, Flanagan J, Jasuja R, Kirkland J, Jiang L, Bhasin S., The effects of myostatin on adipogenic differentiation of human bone marrow-derived mesenchymal stem cells are mediated through cross-communication between Smad3 and Wnt/beta-catenin signaling pathways. J Biol Chem. 2008; 283 (14): 9136-45.
14. Kang S, Bennett CN, Gerin I, Rapp LA, Hankenson KD, Macdougald OA., Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem. 2007; 282 (19): 14515-24. (Pubitemid 47100486)
15. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA., Inhibition of adipogenesis by Wnt signaling. Science. 2000; 289 (5481): 950-3. (Pubitemid 30659947)
16. Chen JR, Lazarenko OP, Wu X, Tong Y, Blackburn ML, Shankar K, Badger TM, Ronis MJ., Obesity reduces bone density associated with activation of PPARgamma and suppression of Wnt/beta-catenin in rapidly growing male rats. PLoS One. 2010; 5 (10): e13704.
17. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C., Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell. 2005; 8 (5): 727-38. (Pubitemid 40585295)
18. Day TF, Guo X, Garrett-Beal L, Yang Y., Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell. 2005; 8 (5): 739-50. (Pubitemid 40585296)
19. Hu H, Hilton MJ, Tu X, Yu K, Ornitz DM, Long F., Sequential roles of Hedgehog and Wnt signaling in osteoblast development. Development. 2005; 132 (1): 49-60. (Pubitemid 40207966)
20. Rodda SJ, McMahon AP., Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development. 2006; 133 (16): 3231-44. (Pubitemid 44404346)
21. Glass DA 2nd, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, Karsenty G., Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell. 2005; 8 (5): 751-64. (Pubitemid 40585297)
22. Holmen SL, Zylstra CR, Mukherjee A, Sigler RE, Faugere MC, Bouxsein ML, Deng L, Clemens TL, Williams BO., Essential role of beta-catenin in postnatal bone acquisition. J Biol Chem. 2005; 280 (22): 21162-8. (Pubitemid 40805677)
23. Kramer I, Halleux C, Keller H, Pegurri M, Gooi JH, Weber PB, Feng JQ, Bonewald LF, Kneissel M., Osteocyte Wnt/beta-catenin signaling is required for normal bone homeostasis. Mol Cell Biol. 2010; 30 (12): 3071-85.
24. Bennett CN, Ouyang H, Ma YL, Zeng Q, Gerin I, Sousa KM, Lane TF, Krishnan V, Hankenson KD, MacDougald OA., Wnt10b increases postnatal bone formation by enhancing osteoblast differentiation. J Bone Miner Res. 2007; 22 (12): 1924-32. (Pubitemid 351229309)
25. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD, MacDougald OA., Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A. 2005; 102 (9): 3324-9. (Pubitemid 40328044)
26. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, Sommer L, Boussadia O, Kemler R., Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development. 2001; 128 (8): 1253-64. (Pubitemid 32409648)
27. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L., A global double-fluorescent Cre reporter mouse. Genesis. 2007; 45 (9): 593-605. (Pubitemid 350013057)
28. Yang D, Guo J, Divieti P, Bringhurst FR., Parathyroid hormone activates PKC-delta and regulates osteoblastic differentiation via a PLC-independent pathway. Bone. 2006; 38 (4): 485-96.
29. Yang D, Singh R, Divieti P, Guo J, Bouxsein ML, Bringhurst FR., Contributions of parathyroid hormone (PTH)/PTH-related peptide receptor signaling pathways to the anabolic effect of PTH on bone. Bone. 2007; 40 (6): 1453-61. (Pubitemid 46779002)
30. Quach JM, Walker EC, Allan E, Solano M, Yokoyama A, Kato S, Sims NA, Gillespie MT, Martin TJ., Zinc finger protein 467 is a novel regulator of osteoblast and adipocyte commitment. J Biol Chem. 2011; 286 (6): 4186-98.
31. Calo E, Quintero-Estades JA, Danielian PS, Nedelcu S, Berman SD, Lees JA., Rb regulates fate choice and lineage commitment in vivo. Nature. 2010; 466 (7310): 1110-4.
32. Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A, Kodama T, Yamaguchi A, Owen MJ, Takahashi S, Takayanagi H., Maf promotes osteoblast differentiation in mice by mediating the age-related switch in mesenchymal cell differentiation. J Clin Invest. 2010; 120 (10): 3455-65.
33. Mendez-Ferrer S, Michurina TV, Ferraro F, Mazloom AR, Macarthur BD, Lira SA, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS., Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2010; 466 (7308): 829-34.
34. Nakashima K, Zhou X, Kunkel G, Zhang Z, Deng JM, Behringer RR, de Crombrugghe B., The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell. 2002; 108 (1): 17-29. (Pubitemid 34137009)
35. Tang QQ, Gronborg M, Huang H, Kim JW, Otto TC, Pandey A, Lane MD., Sequential phosphorylation of CCAAT enhancer-binding protein beta by MAPK and glycogen synthase kinase 3beta is required for adipogenesis. Proc Natl Acad Sci U S A. 2005; 102 (28): 9766-71. (Pubitemid 40993643)
36. Liu J, Farmer SR., Regulating the balance between peroxisome proliferator-activated receptor gamma and beta-catenin signaling during adipogenesis. A glycogen synthase kinase 3beta phosphorylation-defective mutant of beta-catenin inhibits expression of a subset of adipogenic genes. J Biol Chem. 2004; 279 (43): 45020-7. (Pubitemid 39430916)
37. Liu J, Wang H, Zuo Y, Farmer SR., Functional interaction between peroxisome proliferator-activated receptor gamma and beta-catenin. Mol Cell Biol. 2006; 26 (15): 5827-37. (Pubitemid 44134337)
38. Khan E, Abu-Amer Y., Activation of peroxisome proliferator-activated receptor-gamma inhibits differentiation of preosteoblasts. J Lab Clin Med. 2003; 142 (1): 29-34. (Pubitemid 36930414)
39. Jeon MJ, Kim JA, Kwon SH, Kim SW, Park KS, Park SW, Kim SY, Shin CS., Activation of peroxisome proliferator-activated receptor-gamma inhibits the Runx2-mediated transcription of osteocalcin in osteoblasts. J Biol Chem. 2003; 278 (26): 23270-7. (Pubitemid 36830140)
40. Thomas DM, Carty SA, Piscopo DM, Lee JS, Wang WF, Forrester WC, Hinds PW., The retinoblastoma protein acts as a transcriptional coactivator required for osteogenic differentiation. Mol Cell. 2001; 8 (2): 303-16. (Pubitemid 32831548)
41. Fajas L, Landsberg RL, Huss-Garcia Y, Sardet C, Lees JA, Auwerx J., E2Fs regulate adipocyte differentiation. Dev Cell. 2002; 3 (1): 39-49. (Pubitemid 34778394)