Resorption controls bone anabolism driven by parathyroid hormone (PTH) receptor signaling in osteocytes

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29809-29820

  Rhee, Yumie ^a,c   Lee, Eun Young ^a,c   Lezcano, Virginia ^a,d   Ronda, Ana C ^a,d   Condon, Keith W ^a   Allen, Matthew R ^a   Plotkin, Lilian I ^a   Bellido, Teresita ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RICHARD L ROUDEBUSH VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Yonsei University College of Medicine   (South Korea)

^d UNIVERSIDAD NACIONAL DEL SUR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BISPHOSPHONATES; BONE FORMATION; CANCELLOUS BONE; OSTEOCLAST ACTIVITY; PARATHYROID HORMONES; RECEPTOR SIGNALING; THERAPEUTIC POTENTIALS; TRANSGENIC MICE;

METABOLISM; SIGNALING;

BONE;

ALENDRONIC ACID; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR; PLACEBO; SCLEROSTIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE METABOLISM; BONE REMODELING; BONE STRUCTURE; BONE TISSUE; CALVARIA; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCORTICAL BONE; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE OVEREXPRESSION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOCYTE; OSTEOLYSIS; PERIOSTEUM; PHARMACOLOGICAL BLOCKING; POROSITY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOST GENE; SURFACE PROPERTY; TRABECULAR BONE; TRANSGENIC MOUSE;

BONE; BONE MODELING/REMODELING; OSTEOCLAST; OSTEOCYTE; PARATHYROID HORMONE; PTH RECEPTOR; RESORPTION; SOST/SCLEROSTIN; WNT SIGNALING;

ABSORPTIOMETRY, PHOTON; ALENDRONATE; ANIMALS; BONE AND BONES; BONE DENSITY; BONE DENSITY CONSERVATION AGENTS; BONE REMODELING; BONE RESORPTION; GENE EXPRESSION; GLYCOPROTEINS; IMMUNOHISTOCHEMISTRY; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OSTEOCYTES; OSTEOGENESIS; RECEPTOR, PARATHYROID HORMONE, TYPE 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY;

EID: 84885654460     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.485938     Document Type: Article

References (34)

1. Jilka, R. L. (2007) Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone 40, 1434-1446
2. Kim, S. W., Pajevic, P. D., Selig, M., Barry, K. J., Yang, J. Y., Shin, C. S., Baek, W. Y., Kim, J. E., and Kronenberg, H. M. (2012) Intermittent parathyroid hormone administration converts quiescent lining cells to active osteoblasts. J. Bone Miner. Res. 27, 2075-2084
3. Hodsman, A. B., Bauer, D. C., Dempster, D. W., Dian, L., Hanley, D. A., Harris, S. T., Kendler, D. L., McClung, M. R., Miller, P. D., Olszynski, W. P., Orwoll, E., and Yuen, C. K. (2005) Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr. Rev. 26, 688-703
4. Bellido, T., Saini, V., and Pajevic, P. D. (2013) Effects of PTH on osteocyte function. Bone 54, 250-257
5. Bellido, T., Ali, A. A., Gubrij, I., Plotkin, L. I., Fu, Q., O'Brien, C. A., Manolagas, S. C., and Jilka, R. L. (2005) Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 146, 4577-4583
6. Keller, H., and Kneissel, M. (2005) SOST is a target gene for PTH in bone. Bone 37, 148-158
7. Yang, M., Trettel, L. B., Adams, D. J., Harrison, J. R., Canalis, E., and Kream, B. E. (2010) Col3.6-HSD2 transgenic mice: a glucocorticoid lossof- function model spanning early and late osteoblast differentiation. Bone 47, 573-582
8. Lavi-Moshayoff, V., Wasserman, G., Meir, T., Silver, J., and Naveh-Many, T. (2010) PTH increases FGF23 gene expression and mediates the high- FGF23 levels of experimental kidney failure: a bone parathyroid feedback loop. Am. J. Physiol. Renal Physiol. 299, F882-F889
9. O'Brien, C. A., Plotkin, L. I., Galli, C., Goellner, J., Gortazar, A. R., Allen, M. R., Robling, A. G., Bouxsein, M., Schipani, E., Turner, C. H., Jilka, R. L., Weinstein, R. S., Manolagas, S. C., and Bellido, T. (2008) Control of bone mass and remodeling by PTH receptor signaling in osteocytes. PLoS ONE 3, e2942
10. Rhee, Y., Allen, M. R., Condon, K., Lezcano, V., Ronda, A. C., Galli, C., Olivos, N., Passeri, G., O'Brien, C. A., Bivi, N., Plotkin, L. I., and Bellido, T. (2011) PTH receptor signaling in osteocytes governs periosteal bone formation and intracortical remodeling. J. Bone Miner. Res. 26, 1035-1046
11. Rhee, Y., Bivi, N., Farrow, E. G., Lezcano, V., Plotkin, L. I., White, K. E., and Bellido, T. (2011) Parathyroid hormone receptor signaling in osteocytes increases the expression of fibroblast growth factor-23 in vitro and in vivo. Bone 49, 636-643
12. Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., and Parfitt, A. M. (2013) Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 28, 2-17
13. Bivi, N., Pacheco-Costa, R., Brun, L. R., Murphy, T. R., Farlow, N. R., Robling, A. G., Bellido, T., and Plotkin, L. I. (2013) Absence of Cx43 selectively from osteocytes enhances responsiveness to mechanical force in mice. J. Orthop. Res. 31, 1075-1081
14. Li, C., Xing, Q., Yu, B., Xie, H., Wang, W., Shi, C., Crane, J. L., Cao, X., and Wan, M. (2013) Disruption of LRP6 in osteoblasts blunts the bone anabolic activity of PTH. J. Bone Miner. Res. 10.1002/jbmr.1962
15. Signorelli, S., Jennings, P., Leonard, M. O., and Pfaller, W. (2010) Differential effects of hypoxic stress in alveolar epithelial cells and microvascular endothelial cells. Cell Physiol. Biochem. 25, 135-144
16. Plotkin, L. I., Bivi, N., and Bellido, T. (2011) A bisphosphonate that does not affect osteoclasts prevents osteoblast and osteocyte apoptosis and the loss of bone strength induced by glucocorticoids in mice. Bone 49, 122-127
17. Cheung, M. S., Glorieux, F. H., and Rauch, F. (2009) Large osteoclasts in pediatric osteogenesis imperfecta patients receiving intravenous pamidronate. J. Bone Miner. Res. 24, 669-674
18. Weinstein, R. S., Roberson, P. K., and Manolagas, S. C. (2009) Giant osteoclast formation and long-term oral bisphosphonate therapy. N. Engl. J. Med. 360, 53-62
19. Martin, R. B., Burr, D. B., and Sharkey, N. A. (1998) Skeletal Tissue Mechanics, 1st Ed., Springer-Verlag, New York
20. Zanchetta, J. R., Bogado, C. E., Ferretti, J. L., Wang, O., Wilson, M. G., Sato, M., Gaich, G. A., Dalsky, G. P., and Myers, S. L. (2003) Effects of teriparatide [recombinant human parathyroid hormone (1-34)] on cortical bone in postmenopausal women with osteoporosis. J. Bone Miner. Res. 18, 539-543
21. Jilka, R. L., O'Brien, C. A., Ali, A. A., Roberson, P. K., Weinstein, R. S., and Manolagas, S. C. (2009) Intermittent PTH stimulates periosteal bone formation by actions on post-mitotic preosteoblasts. Bone 44, 275-286
22. Calvi, L. M., Sims, N. A., Hunzelman, J. L., Knight, M. C., Giovannetti, A., Saxton, J. M., Kronenberg, H. M., Baron, R., and Schipani, E. (2001) Activated parathyroid hormone/parathyroid hormone-related protein receptor in osteoblastic cells differentially affects cortical and trabecular bone. J. Clin. Invest. 107, 277-286
23. Calvi, L. M., Shin, H. I., Knight, M. C., Weber, J. M., Young, M. F., Giovannetti, A., and Schipani, E. (2004) Constitutively active PTH/PTHrP receptor in odontoblasts alters odontoblast and ameloblast function and maturation. Mech. Dev. 121, 397-408
24. Parfitt, A. M. (2002) Parathyroid hormone and periosteal bone expansion. J. Bone Miner. Res. 17, 1741-1743
25. Powell, W. F., Jr., Barry, K. J., Tulum, I., Kobayashi, T., Harris, S. E., Bringhurst, F., and Pajevic, P. (2011) Targeted ablation of the PTH/PTHrP receptor in osteocytes impairs bone structure and homeostatic calcemic responses. J. Endocrinol. 209, 21-32
26. Nakanishi, R., Shimizu, M., Mori, M., Akiyama, H., Okudaira, S., Otsuki, B., Hashimoto, M., Higuchi, K., Hosokawa, M., Tsuboyama, T., and Nakamura, T. (2006) Secreted frizzled-related protein 4 is a negative regulator of peak BMD in SAMP6 mice. J. Bone Miner. Res. 21, 1713-1721
27. Li, X., Ominsky, M. S., Niu, Q. T., 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, P. J., Lacey, D. L., Simonet, W. S., Ke, H. Z., and 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
28. Li, J., Sarosi, I., Cattley, R. C., Pretorius, J., Asuncion, F., Grisanti, M., Morony, S., Adamu, S., Geng, Z., Qiu, W., Kostenuik, P., Lacey, D. L., Simonet, W. S., Bolon, B., Qian, X., Shalhoub, V., Ominsky, M. S., Zhu, K. H., Li, X., and Richards, W. G. (2006) Dkk1-mediated inhibition of Wnt signaling in bone results in osteopenia. Bone 39, 754-766
29. Winkler, D. G., Sutherland, M. K., Geoghegan, J. C., Yu, C., Hayes, T., Skonier, J. E., Shpektor, D., Jonas, M., Kovacevich, B. R., Staehling-Hampton, K., Appleby, M., Brunkow, M. E., and Latham, J. A. (2003) Osteocyte control of bone formation via sclerostin, a novelBMPantagonist.EMBOJ. 22, 6267-6276
30. Loots, G. G., Kneissel, M., Keller, H., Baptist, M., Chang, J., Collette, N. M., Ovcharenko, D., Plajzer-Frick, I., and Rubin, E. M. (2005) Genomic deletion of a long-range bone enhancer misregulates sclerostin in Van Buchem disease. Genome Res. 15, 928-935
31. Tu, X., Rhee, Y., Condon, K. W., Bivi, N., Allen, M. R., Dwyer, D., Stolina, M., Turner, C. H., Robling, A. G., Plotkin, L. I., and Bellido, T. (2012) Sost downregulation and local Wnt signaling are required for the osteogenic response to mechanical loading. Bone 50, 209-217
32. Kramer, I., Halleux, C., Keller, H., Pegurri, M., Gooi, J. H., Weber, P. B., Feng, J. Q., Bonewald, L. F., and Kneissel, M. (2010) Osteocyte Wnt/betacatenin signaling is required for normal bone homeostasis. Mol. Cell Biol. 30, 3071-3085
33. Glass, D. A., 2nd, Bialek, P., Ahn, J. D., Starbuck, M., Patel, M. S., Clevers, H., Taketo, M. M., Long, F., McMahon, A. P., Lang, R. A., and Karsenty, G. (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev. Cell 8, 751-764
34. Holmen, S. L., Zylstra, C. R., Mukherjee, A., Sigler, R. E., Faugere, M. C., Bouxsein, M. L., Deng, L., Clemens, T. L., and Williams, B. O. (2005) Essential role of beta-catenin in postnatal bone acquisition. J. Biol. Chem. 280, 21162-21168