Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/β-catenin signaling

Journal of Bone and Mineral Research

Volumn 24, Issue 10, 2009, Pages 1651-1661

  Lin, Chuwen ^a,b,c   Jiang, Xuan ^b   Dai, Zhongquan ^d   Guo, Xizhi ^a   Weng, Tujun ^e   Wang, Jun ^f   Li, Yinghui ^d   Feng, Guoyin ^a   Gao, Xiang ^a,b   He, Lin ^a,c,g  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

^c Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^d China Astronaut Research and Training Center   (China)

^e BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^f FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^g FUDAN UNIVERSITY   (China)

Author keywords

Bone; Mechanical unloading; Mechanotransduction; Sclerostin; Wnt catenin signaling

Indexed keywords

BETA CATENIN; SCLEROSTIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE ATROPHY; BONE DENSITOMETRY; BONE MASS; CONTROLLED STUDY; CROSS REACTION; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE TARGETING; MALE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MORPHOMETRICS; MOUSE; NICK END LABELING; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCYTE; OSTEOLYSIS; OSTEOPOROSIS; PROTEIN TARGETING; RADIOGRAPHY; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BETA CATENIN; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; BONE RESORPTION; GENE DELETION; GENE TARGETING; GENETIC MARKERS; MICE; MODELS, BIOLOGICAL; ORGAN SIZE; OSTEOBLASTS; OSTEOCYTES; OSTEOGENESIS; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; UP-REGULATION; WNT PROTEINS;

EID: 70349934212     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.090411     Document Type: Article

References (43)

1. Harada S, Rodan GA 2003 Control of osteoblast function and regulation of bone mass. Nature 423:349-355. (Pubitemid 40852710)
2. Robling AG, Castillo AB, Turner CH 2006 Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 8:455-498. (Pubitemid 44314825)
3. Bikle DD, Halloran BP 1999 The response of bone to unloading. J Bone Miner Metab 17:233-244.
4. Tatsumi S, Ishii K, Amizuka N, Li M, Kobayashi T, Kohno K, Ito M, Takeshita S, Ikeda K 2007 Targeted ablation of osteocytes induces osteoporosis with defective mechanotransduction. Cell Metab 5:464-475. (Pubitemid 46825494)
5. Bonewald LF 2006 Mechanosensation and Transduction in Osteocytes. Bonekey Osteovision 3:7-15.
6. Noble BS 2008 The osteocyte lineage. Arch Biochem Biophys 473:106-111.
7. Glass DA II, Karsenty G 2006 Molecular bases of the regulation of bone remodeling by the canonical Wnt signaling pathway. Curr Top Dev Biol 73:43-84. (Pubitemid 43878129)
8. Day TF, Guo X, Garrett-Beal L, Yang Y 2005 Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev Cell 8:739-750. (Pubitemid 40585296)
9. Hill TP, Spater D, Taketo MM, Birchmeier W, Hartmann C 2005 Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev Cell 8:727-738. (Pubitemid 40585295)
10. Robinson JA, Chatterjee-Kishore M, Yaworsky PJ, Cullen DM, Zhao W, Li C, Kharode Y, Sauter L, Babij P, Brown EL, Hill AA, Akhter MP, Johnson ML, Recker RR, Komm BS, Bex FJ 2006 Wnt/beta-catenin signaling is a normal physiological response to mechanical loading in bone. J Biol Chem 281:31720-31728. (Pubitemid 46043263)
11. Brunkow ME, Gardner JC, Van Ness J, Paeper BW, Kovacevich BR, Proll S, Skonier JE, Zhao L, Sabo PJ, Fu Y, Alisch RS, Gillett L, Colbert T, Tacconi P, Galas D, Hamersma H, Beighton P, Mulligan J 2001 Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet 68:577-589. (Pubitemid 32202753)
12. Balemans W, Ebeling M, Patel N, Van Hul E, Olson P, Dioszegi M, Lacza C, Wuyts W, Van Den Ende J, Willems P, Paes-Alves AF, Hill S, Bueno M, Ramos FJ, Tacconi P, Dikkers FG, Stratakis C, Lindpaintner K, Vickery B, Foernzler D, Van Hul W 2001 Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 10:537-543. (Pubitemid 32184286)
13. Balemans W, Patel N, Ebeling M, Van Hul E, Wuyts W, Lacza C, Dioszegi M, Dikkers FG, Hildering P, Willems PJ, Verheij JB, Lindpaintner K, Vickery B, Foernzler D, Van Hul W 2002 Identification of a 52 kb deletion downstream of the SOST gene in patients with van Buchem disease. J Med Genet 39:91-97. (Pubitemid 34146376)
14. Li X, Ominsky MS, Niu QT, Sun N, Daugherty B, D'Agostin D, Kurahara C, Gao Y, Cao J, Gong J, Asuncion F, Barrero M, Warmington K, Dwyer D, Stolina M, Morony S, Sarosi I, Kostenuik PJ, Lacey DL, Simonet WS, Ke HZ, Paszty C 2008 Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res 23:860-869. (Pubitemid 351768804)
15. Staehling-Hampton K, Proll S, Paeper BW, Zhao L, Charmley P, Brown A, Gardner JC, Galas D, Schatzman RC, Beighton P, Papapoulos S, Hamersma H, Brunkow ME 2002 A 52-kb deletion in the SOST-MEOX1 intergenic region on 17q12-q21 is associated with van Buchem disease in the Dutch population. Am J Med Genet 110:144-152.
16. Winkler DG, Sutherland MK, Geoghegan JC, Yu C, Hayes T, Skonier JE, Shpektor D, Jonas M, Kovacevich BR, Staehling-Hampton K, Appleby M, Brunkow ME, Latham JA 2003 Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. EMBO J 22:6267-6276. (Pubitemid 37522584)
17. Winkler DG, Sutherland MS, Ojala E, Turcott E, Geoghegan JC, Shpektor D, Skonier JE, Yu C, Latham JA 2005 sclerostin inhibition of Wnt-3a-induced C3H10T1/2 cell differentiation is indirect and mediated by bone morphogenetic proteins. J Biol Chem 280:2498-2502. (Pubitemid 40189350)
18. van Bezooijen RL, Roelen BA, Visser A, van der Wee-Pals L, de Wilt E, Karperien M, Hamersma H, Papapoulos SE, ten Dijke P, Lowik CW 2004 sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J Exp Med 199:805-814.
19. Li X, Zhang Y, Kang H, Liu W, Liu P, Zhang J, Harris SE, Wu D 2005 sclerostin binds to Lrp5/6 and antagonizes canonical Wnt signaling. J Biol Chem 280:19883-19887. (Pubitemid 41379516)
20. Semenov M, Tamai K, He X 2005 SOST is a ligand for Lrp5/Lrp6 and a Wnt signaling inhibitor. J Biol Chem 280:26770-26775. (Pubitemid 41040710)
21. Poole KE, van Bezooijen RL, Loveridge N, Hamersma H, Papapoulos SE, Lowik CW, Reeve J 2005 sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J 19:1842-1844. (Pubitemid 41598769)
22. Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH 2008 Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866-5875.
23. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR 1987 Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595-610.
24. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A 1999 The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 96:5522-5527. (Pubitemid 29234650)
25. Kusu N, Laurikkala J, Imanishi M, Usui H, Konishi M, Miyake A, Thesleff I, Itoh N 2003 sclerostin is a novel secreted osteoclast-derived bone morphogenetic protein antagonist with unique ligand specificity. J Biol Chem 278:24113-24117. (Pubitemid 36830246)
26. van der Heyden MA, Rook MB, Hermans MM, Rijksen G, Boonstra J, Defize LH, Destree OH 1998 Identification of connexin43 as a functional target for Wnt signalling. J Cell Sci 111:1741-1749. (Pubitemid 28330560)
27. Valdimarsdottir G, Goumans MJ, Rosendahl A, Brugman M, Itoh S, Lebrin F, Sideras P, ten Dijke P 2002 Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 106:2263-2270. (Pubitemid 35222223)
28. Strom TM, Francis F, Lorenz B, Boddrich A, Econs MJ, Lehrach H, Meitinger T 1997 Pex gene deletions in Gy and Hyp mice provide mouse models for X-linked hypophosphatemia. Hum Mol Genet 6:165-171. (Pubitemid 27078072)
29. Toyosawa S, Shintani S, Fujiwara T, Ooshima T, Sato A, Ijuhin N, Komori T 2001 Dentin matrix protein 1 is predominantly expressed in chicken and rat osteocytes but not in osteoblasts. J Bone Miner Res 16:2017-2026. (Pubitemid 32995392)
30. Sutherland MK, Geoghegan JC, Yu C, Turcott E, Skonier JE, Winkler DG, Latham JA 2004 sclerostin promotes the apoptosis of human osteoblastic cells: A novel regulation of bone formation. Bone 35:828-835. (Pubitemid 39349213)
31. Baron R, Rawadi G 2007 Targeting the Wnt/beta-catenin pathway to regulate bone formation in the adult skeleton. Endocrinology 148:2635-2643. (Pubitemid 46984775)
32. Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schutz G, Glorieux FH, Chiang CY, Zajac JD, Insogna KL, Mann JJ, Hen R, Ducy P, Karsenty G 2008 Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135:825-837.
33. Pinson KI, Brennan J, Monkley S, Avery BJ, Skarnes WC 2000 An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535-538. (Pubitemid 30746710)
34. Tamai K, Semenov M, Kato Y, Spokony R, Liu C, Katsuyama Y, Hess F, Saint-Jeannet JP, He X 2000 LDL-receptor-related proteins in Wnt signal transduction. Nature 407:530-535. (Pubitemid 30746709)
35. Bafico A, Liu G, Yaniv A, Gazit A, Aaronson SA 2001 Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with Lrp6/Arrow. Nat Cell Biol 3:683-686. (Pubitemid 32624426)
36. Semenov MV, Tamai K, Brott BK, Kuhl M, Sokol S, He X 2001 Head inducer Dickkopf-1 is a ligand for Wnt coreceptor Lrp6. Curr Biol 11:951-961. (Pubitemid 32589186)
37. van Bezooijen RL, ten Dijke P, Papapoulos SE, Lowik CW 2005 SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev 16:319-327.
38. Krishnan V, Bryant HU, Macdougald OA 2006 Regulation of bone mass by Wnt signaling. J Clin Invest 116:1202-1209.
39. Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, Warden SJ, Li J, Maye P, Rowe DW, Duncan RL, Warman ML, Turner CH 2006 The Wnt co-receptor Lrp5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem 281:23698-23711. (Pubitemid 44274145)
40. Ahmed Y, Hayashi S, Levine A, Wieschaus E 1998 Regulation of armadillo by a Drosophila APC inhibits neuronal apoptosis during retinal development. Cell 93:1171-1182. (Pubitemid 28307422)
41. Almeida M, Han L, Bellido T, Manolagas SC, Kousteni S 2005 Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J Biol Chem 280:41342-41351. (Pubitemid 41832191)
42. Bodine PV, Billiard J, Moran RA, Ponce-de-Leon H, McLarney S, Mangine A, Scrimo MJ, Bhat RA, Stauffer B, Green J, Stein GS, Lian JB, Komm BS 2005 The Wnt antagonist secreted frizzled-related protein-1 controls osteoblast and osteocyte apoptosis. J Cell Biochem 96:1212-1230. (Pubitemid 41681864)
43. Bodine PV, Zhao W, Kharode YP, Bex FJ, Lambert AJ, Goad MB, Gaur T, Stein GS, Lian JB, Komm BS 2004 The Wnt antagonist secreted frizzled-related protein-1 is a negative regulator of trabecular bone formation in adult mice. Mol Endocrinol 18:1222-1237. (Pubitemid 38591287)