Sclerostin regulates release of bone mineral by osteocytes by induction of carbonic anhydrase 2

Journal of Bone and Mineral Research

Volumn 28, Issue 12, 2013, Pages 2436-2448

  Kogawa, Masakazu ^a   Wijenayaka, Asiri R ^a   Ormsby, Renee T ^a   Thomas, Gethin P ^b   Anderson, Paul H ^c   Bonewald, Lynda F ^d   Findlay, David M ^a   Atkins, Gerald J ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^d UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

carbonic anhydrase 2; osteocyte; osteocytic osteolysis; Sclerostin; sost

Indexed keywords

ACETAZOLAMIDE; CALCIUM ION; CARBONATE DEHYDRATASE II; MESSENGER RNA; SCLEROSTIN; SMALL INTERFERING RNA;

ARTICLE; BONE MINERAL; CALCIUM TRANSPORT; CELL PH; CONTROLLED STUDY; DRUG EFFECT; ENZYME INDUCTION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN CELL; OSTEOCYTE; OSTEOLYSIS; PROTEIN EXPRESSION; TRABECULAR BONE;

CARBONIC ANHYDRASE 2; OSTEOCYTE; OSTEOCYTIC OSTEOLYSIS; SCLEROSTIN; SOST;

ANIMALS; BONE AND BONES; BONE MORPHOGENETIC PROTEINS; CALCIUM; CARBONIC ANHYDRASES; CELL LINE; CELL SIZE; ENZYME INDUCTION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC MARKERS; GLYCOPROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; MINERALS; OSTEOCYTES; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING;

EID: 84888017770     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2003     Document Type: Article

References (63)

1. Poole KE, van Bezooijen RL, Loveridge N, Hamersma H, Papapoulos SE, Lowik CW, Reeve J., Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. Faseb J. 2005; 19: 1842-4.
2. 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., Osteocyte control of bone formation via sclerostin, a novel BMP antagonist. Embo J. 2003; 22: 6267-76.
3. 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., Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Human Mol Genet. 2001; 10: 537-43.
4. 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., Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet. 2001; 68: 577-89.
5. 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., Identification of a 52 kb deletion downstream of the SOST gene in patients with van Buchem disease. J Med Genet. 2002; 39: 91-7.
6. 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., 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. 2002; 110: 144-52.
7. 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., Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res. 2008; 23: 860-9.
8. Semenov M, Tamai K, He X., SOST is a ligand for LRP5/LRP6 and a Wnt signaling inhibitor. J Biol Chem. 2005; 280: 26770-5.
9. Williams BO, Insogna KL., Where Wnts went: the exploding field of Lrp5 and Lrp6 signaling in bone. J Bone Miner Res. 2009; 24: 171-8.
10. Choi HY, Dieckmann M, Herz J, Niemeier A., Lrp4, a novel receptor for Dickkopf 1 and sclerostin, is expressed by osteoblasts and regulates bone growth and turnover in vivo. PLoS ONE. 2009; 4: e7930.
11. Leupin O, Piters E, Halleux C, Hu S, Kramer I, Morvan F, Bouwmeester T, Schirle M, Bueno-Lozano M, Ramos Fuentes FJ, Itin PH, Boudin E, De Freitas F, Jennes K, Brannetti B, Charara N, Ebersbach H, Geisse S, Lu CX, Bauer A, Van Hul W, Kneissel M., Bone overgrowth-associated mutations in LRP4 impair sclerostin-facilitator function. J Biol Chem. 2011; 286: 19489-500.
12. Atkins GJ, Rowe PS, Lim HP, Welldon KJ, Ormsby R, Wijenayaka AR, Zelenchuk L, Evdokiou A, Findlay DM., Sclerostin is a locally acting regulator of late-osteoblast/preosteocyte differentiation and regulates mineralization through a MEPE-ASARM-dependent mechanism. J Bone Miner Res. 2011; 26: 1425-36.
13. Wijenayaka AR, Kogawa M, Lim HP, Bonewald LF, Findlay DM, Atkins GJ., Sclerostin stimulates osteocyte support of osteoclast activity by a RANKL-dependent pathway. PLoS One. 2011; 6: e25900.
14. Nakashima T, Hayashi M, Fukunaga T, Kurata K, Oh-Hora M, Feng JQ, Bonewald LF, Kodama T, Wutz A, Wagner EF, Penninger JM, Takayanagi H., Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat Med. 2011; 17: 1231-4.
15. Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O'Brien CA., Matrix-embedded cells control osteoclast formation. Nat Med. 2011; 17: 1235-41.
16. Atkins GJ, Findlay DM., Osteocyte regulation of bone mineral: a little give and take. Osteoporos Int. 2012; 23: 2067-79.
17. Baud CA, Boivin G., Effects of hormones on osteocyte function and perilacunar wall structure. Clin Orthop Relat Res. 1978; 136: 270-81.
18. Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, Kato S, Wysolmerski J, Bonewald LF., Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res. 2012; 27: 1018-29.
19. Tang SY, Herber RP, Ho SP, Alliston T., Matrix metalloproteinase-13 is required for osteocytic perilacunar remodeling and maintains bone fracture resistance. J Bone Miner Res. 2012; 27: 1936-50.
20. Teti A, Zallone A., Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone. 2009; 44: 11-6.
21. Belanger LF., Osteocytic osteolysis. Calcif Tissue Res. 1969; 4: 1-12.
22. Krempien B, Friedrich E, Ritz E., Effect of PTH on osteocyte ultrastructure. Adv Exp Med Biol. 1978; 103: 437-50.
23. Tazawa K, Hoshi K, Kawamoto S, Tanaka M, Ejiri S, Ozawa H., Osteocytic osteolysis observed in rats to which parathyroid hormone was continuously administered. J Bone Miner Metab. 2004; 22: 524-9.
24. Bivi N, Bereszczak JZ, Romanello M, Zeef LA, Delneri D, Quadrifoglio F, Moro L, Brancia FL, Tell G., Transcriptome and proteome analysis of osteocytes treated with nitrogen-containing bisphosphonates. J Proteome Res. 2009; 8: 1131-42.
25. Kato Y, Windle JJ, Koop BA, Mundy GR, Bonewald LF., Establishment of an osteocyte-like cell line, MLO-Y4. J Bone Miner Res. 1997; 12: 2014-23.
26. Atkins GJ, Kostakis P, Pan B, Farrugia A, Gronthos S, Evdokiou A, Harrison K, Findlay DM, Zannettino AC., RANKL expression is related to the differentiation state of human osteoblasts. J Bone Miner Res. 2003; 18: 1088-98.
27. Atkins GJ, Welldon KJ, Halbout P, Findlay DM., Strontium ranelate treatment of human primary osteoblasts promotes an osteocyte-like phenotype while eliciting an osteoprotegerin response. Osteoporos Int. 2009; 20: 653-64.
28. Atkins GJ, Welldon KJ, Holding CA, Haynes DR, Howie DW, Findlay DM., The induction of a catabolic phenotype in human primary osteoblasts and osteocytes by polyethylene particles. Biomaterials. 2009; 30: 3672-81.
29. Atkins GJ, Welldon KJ, Wijenayaka AR, Bonewald LF, Findlay DM., Vitamin K promotes mineralization, osteoblast-to-osteocyte transition, and an anticatabolic phenotype by γ-carboxylation-dependent and -independent mechanisms. Am J Physiol Cell Physiol. 2009; 297: C1358-67.
30. Atkins GJ, Anderson PH, Findlay DM, Welldon KJ, Vincent C, Zannettino AC, O'Loughlin PD, Morris HA., Metabolism of vitamin D(3) in human osteoblasts: evidence for autocrine and paracrine activities of 1alpha,25-dihydroxyvitamin D(3). Bone. 2007; 40: 1517-28.
31. Kogawa M, Findlay DM, Anderson PH, Ormsby R, Vincent C, Morris HA, Atkins GJ., Osteoclastic metabolism of 25(OH)-vitamin D3: a potential mechanism for optimization of bone resorption. Endocrinology. 2010; 151: 4613-25.
32. Matsumoto M, Kogawa M, Wada S, Takayanagi H, Tsujimoto M, Katayama S, Hisatake K, Nogi Y., Essential role of p38 mitogen-activated protein kinase in cathepsin K gene expression during osteoclastogenesis through association of NFATc1 and PU.1. J Biol Chem. 2004; 279: 45969-79.
33. Thomas JA, Johnson DL., Fluorescein conjugates of cytochrome c as internal pH probes in submitochondrial particles. Biochem Biophys Res Comm. 1975; 65: 931-9.
34. Gunawardana SC, Sharp GW., Intracellular pH plays a critical role in glucose-induced time-dependent potentiation of insulin release in rat islets. Diabetes. 2002; 51: 105-13.
35. Thomas JA, Buchsbaum RN, Zimniak A, Racker E., Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry. 1979; 18: 2210-8.
36. Findlay DM, Welldon K, Atkins GJ, Howie DW, Zannettino AC, Bobyn D., The proliferation and phenotypic expression of human osteoblasts on tantalum metal. Biomaterials. 2004; 25: 2215-27.
37. Loots GG, Kneissel M, Keller H, Baptist M, Chang J, Collette NM, Ovcharenko D, Plajzer-Frick I, Rubin EM., Genomic deletion of a long-range bone enhancer misregulates sclerostin in Van Buchem disease. Genome Res. 2005; 15: 928-35.
38. Scherr M, Morgan MA, Eder M., Gene silencing mediated by small interfering RNAs in mammalian cells. Curr Med Chem. 2003; 10: 245-56.
39. Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I, Mantila SM, Gluhak-Heinrich J, Bellido TM, Harris SE, Turner CH., Mechanical stimulation of bone in vivo reduces osteocyte expression of sost/sclerostin. J Biol Chem. 2008; 283: 5866-75.
40. Moustafa A, Sugiyama T, Saxon LK, Zaman G, Sunters A, Armstrong VJ, Javaheri B, Lanyon LE, Price JS., The mouse fibula as a suitable bone for the study of functional adaptation to mechanical loading. Bone. 2009; 44: 930-5.
41. Moustafa A, Sugiyama T, Prasad J, Zaman G, Gross TS, Lanyon LE, Price JS., Mechanical loading-related changes in osteocyte sclerostin expression in mice are more closely associated with the subsequent osteogenic response than the peak strains engendered. Osteoporos Int. 2012; 23: 1225-34.
42. Imtaiyaz Hassan M, Shajee B, Waheed A, Ahmad F, Sly WS., Structure, function and applications of carbonic anhydrase isozymes. Bioorg Med Chem. 2013; 21: 1570-82.
43. Kamiya N, Ye L, Kobayashi T, Mochida Y, Yamauchi M, Kronenberg HM, Feng JQ, Mishina Y., BMP signaling negatively regulates bone mass through sclerostin by inhibiting the canonical Wnt pathway. Development. 2008; 135: 3801-11.
44. Li X, Ominsky MS, Warmington KS, Morony S, Gong J, Cao J, Gao Y, Shalhoub V, Tipton B, Haldankar R, Chen Q, Winters A, Boone T, Geng Z, Niu QT, Ke HZ, Kostenuik PJ, Simonet WS, Lacey DL, Paszty C., Sclerostin antibody treatment increases bone formation, bone mass, and bone strength in a rat model of postmenopausal osteoporosis. J Bone Miner Res. 2009; 24: 578-88.
45. Padhi D, Jang G, Stouch B, Fang L, Posvar E., Single-dose, placebo-controlled, randomized study of AMG 785, a sclerostin monoclonal antibody. J Bone Miner Res. 2011; 26: 19-26.
46. Semenov MV, He X., LRP5 mutations linked to high bone mass diseases cause reduced LRP5 binding and inhibition by SOST. J Biol Chem. 2006; 281: 38276-84.
47. Tian X, Setterberg RB, Li X, Paszty C, Ke HZ, Jee WS., Treatment with a sclerostin antibody increases cancellous bone formation and bone mass regardless of marrow composition in adult female rats. Bone. 2010; 47: 529-33.
48. Sly WS, Sato S, Zhu XL., Evaluation of carbonic anhydrase isozymes in disorders involving osteopetrosis and/or renal tubular acidosis. Clin Biochem. 1991; 24: 311-8.
49. Margolis DS, Szivek JA, Lai LW, Lien YH., Phenotypic characteristics of bone in carbonic anhydrase II-deficient mice. Calcif Tissue Int. 2008; 82: 66-76.
50. Sawakami K, Robling AG, Ai M, Pitner ND, Liu D, Warden SJ, Li J, Maye P, Rowe DW, Duncan RL, Warman ML, Turner CH., The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatment. J Biol Chem. 2006; 281: 23698-711.
51. Bourhis E, Wang W, Tam C, Hwang J, Zhang Y, Spittler D, Huang OW, Gong Y, Estevez A, Zilberleyb I, Rouge L, Chiu C, Wu Y, Costa M, Hannoush RN, Franke Y, Cochran AG., Wnt antagonists bind through a short peptide to the first beta-propeller domain of LRP5/6. Structure. 2011; 19: 1433-42.
52. Holdsworth G, Slocombe P, Doyle C, Sweeney B, Veverka V, Le Riche K, Franklin RJ, Compson J, Brookings D, Turner J, Kennedy J, Garlish R, Shi J, Newnham L, McMillan D, Muzylak M, Carr MD, Henry AJ, Ceska T, Robinson MK., Characterization of the interaction of sclerostin with the low density lipoprotein receptor-related protein (LRP) family of Wnt co-receptors. J Biol Chem. 2012; 287: 26464-77.
53. Li X, Zhang Y, Kang H, Liu W, Liu P, Zhang J, Harris SE, Wu D., Sclerostin binds to LRP5/6 and antagonizes canonical Wnt signaling. J Biol Chem. 2005; 280: 19883-7.
54. Balemans W, Piters E, Cleiren E, Ai M, Van Wesenbeeck L, Warman ML, Van Hul W., The binding between sclerostin and LRP5 is sltered by DKK1 and by high-bone mass LRP5 mutations. Calcif Tissue Int. 2008; 82: 445-53.
55. Holmen SL, Giambernardi TA, Zylstra CR, Buckner-Berghuis BD, Resau JH, Hess JF, Glatt V, Bouxsein ML, Ai M, Warman ML, Williams BO., Decreased BMD and limb deformities in mice carrying mutations in both Lrp5 and Lrp6. J Bone Miner Res. 2004; 19: 2033-40.
56. Ettenberg SA, Charlat O, Daley MP, Liu S, Vincent KJ, Stuart DD, Schuller AG, Yuan J, Ospina B, Green J, Yu Q, Walsh R, Li S, Schmitz R, Heine H, Bilic S, Ostrom L, Mosher R, Hartlepp KF, Zhu Z, Fawell S, Yao YM, Stover D, Finan PM, Porter JA, Sellers WR, Klagge IM, Cong F., Inhibition of tumorigenesis driven by different Wnt proteins requires blockade of distinct ligand-binding regions by LRP6 antibodies. Proc Natl Acad Sci USA. 2010; 107: 15473-8.
57. Findlay DM, Atkins GJ., TWEAK and TNF regulation of sclerostin: a novel pathway for the regulation of bone remodelling. Adv Exp Med Biol. 2011; 691: 337-48.
58. Vincent C, Findlay DM, Welldon KJ, Wijenayaka AR, Zheng TS, Haynes DR, Fazzalari NL, Evdokiou A, Atkins GJ., Pro-inflammatory cytokines TNF-related weak inducer of apoptosis (TWEAK) and TNFalpha induce the mitogen-activated protein kinase (MAPK)-dependent expression of sclerostin in human osteoblasts. J Bone Miner Res. 2009; 24: 1434-49.
59. Yao W, Cheng Z, Busse C, Pham A, Nakamura MC, Lane NE., Glucocorticoid excess in mice results in early activation of osteoclastogenesis and adipogenesis and prolonged suppression of osteogenesis: a longitudinal study of gene expression in bone tissue from glucocorticoid-treated mice. Arthritis Rheum. 2008; 58: 1674-86.
60. Sevetson B, Taylor S, Pan Y., Cbfa1/RUNX2 directs specific expression of the sclerosteosis gene (SOST). J Biol Chem. 2004; 279: 13849-858.
61. Sutherland MK, Geoghegan JC, Yu C, Winkler DG, Latham JA., Unique regulation of SOST, the sclerosteosis gene, by BMPs and steroid hormones in human osteoblasts. Bone. 2004; 35: 448-54.
62. Leupin O, Halleux C, Morvan F, Hu S, Lu C, Bauer A, Kneissel M., LRP4 is a novel osteoblast and osteocyte expressed specific facilitator of SOST-mediated inhibition of in vitro bone formation. J Bone Miner Res. 2009; 24 (Suppl 1). Available at http://www.asbmr.org/Meetings/AnnualMeeting/AbstractDetail.aspx? aid=c8cba0d3-a82c-4036-b4d8-29979e61e7a2
63. 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: 1451-61.