Calcitonin impairs the anabolic effect of PTH in young rats and stimulates expression of sclerostin by osteocytes

Bone

Volumn 46, Issue 6, 2010, Pages 1486-1497

  Gooi, J H ^a   Pompolo, S ^a   Karsdal, M A ^b   Kulkarni, N H ^c   Kalajzic, I ^d   McAhren, S H M ^c   Han, B ^c   Onyia, J E ^c   Ho, P W M ^a   Gillespie, M T ^a   Walsh, N C ^a   Chia, L Y ^a   Quinn, J M W ^a   Martin, T J ^a   Sims, N A ^a  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b Nordic Bioscience Inc   (Denmark)

^c ELI LILLY AND COMPANY   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Calcitonin; Coupling; Osteoclast; Osteocyte; PTH; Sclerostin

Indexed keywords

CALCITONIN; CALCITONIN RECEPTOR; EPHRIN; EPHRIN B2; EPHRIN B6; INTERLEUKIN 6; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; PARATHYROID HORMONE[1-34]; SCLEROSTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE DENSITY; BONE MASS; CALVARIA; CELL DIFFERENTIATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; FEMALE; FEMUR; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; METAPHYSIS; MICROARRAY ANALYSIS; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOCLAST; OSTEOCYTE; OSTEOLYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; THYROID HORMONE SYNTHESIS; TIBIA; UPREGULATION;

EID: 77952961232     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.02.018     Document Type: Article

References (75)

1. Neer R.M., Arnaud C.D., Zanchetta J.R., Prince R., Gaich G.A., Reginster J.Y., et al. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 2001, 344:1434-1441.
2. Jiang Y., Zhao J.J., Mitlak B.H., Wang O., Genant H.K., Eriksen E.F. Recombinant human parathyroid hormone (1-34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res 2003, 18:1932-1941.
3. Dobnig H., Turner R.T. Evidence that intermittent treatment with parathyroid hormone increases bone formation in adult rats by activation of bone lining cells. Endocrinology 1995, 136:3632-3638.
4. Jilka R.L., Weinstein R.S., Bellido T., Roberson P., Parfitt A.M., Manolagas S.C. Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest 1999, 104:439-446.
5. Bellido T., Ali A.A., Gubrij I., Plotkin L.I., Fu Q., O'Brien C.A., et al. Chronic elevation of parathyroid hormone in mice reduces expression of sclerostin by osteocytes: a novel mechanism for hormonal control of osteoblastogenesis. Endocrinology 2005, 146:4577-4583.
6. Keller H., Kneissel M. SOST is a target gene for PTH in bone. Bone 2005, 37:148-158.
7. Frost Dynamics of bone remodeling. Bone Biodynamics 1964, 315-333.
8. Parfitt A.M. The cellular basis of bone remodeling: the quantum concept reexamined in light of recent advances in the cell biology of bone. Calcif Tissue Int 1984, 36(Suppl 1):S37-S45.
9. Martin T.J., Gooi J.H., Sims N.A. Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr 2009, 19:73-88.
10. Martin T.J., Sims N.A. Osteoclast-derived activity in the coupling of bone formation to resorption. Trends Mol Med 2005, 11:76-81.
11. Holtrop M.E., King G.J., Cox K.A., Reit B. Time-related changes in the ultrastructure of osteoclasts after injection of parathyroid hormone in young rats. Calcif Tissue Int 1979, 27:129-135.
12. Delmas P.D., Vergnaud P., Arlot M.E., Pastoureau P., Meunier P.J., Nilssen M.H. The anabolic effect of human PTH (1-34) on bone formation is blunted when bone resorption is inhibited by the bisphosphonate tiludronate-is activated resorption a prerequisite for the in vivo effect of PTH on formation in a remodeling system?. Bone 1995, 16:603-610.
13. Demiralp B., Chen H.L., Koh A.J., Keller E.T., McCauley L.K. Anabolic actions of parathyroid hormone during bone growth are dependent on c-fos. Endocrinology 2002, 143:4038-4047.
14. Koh A.J., Demiralp B., Neiva K.G., Hooten J., Nohutcu R.M., Shim H., et al. Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology 2005, 146:4584-4596.
15. Karsdal M.A., Martin T.J., Bollerslev J., Christiansen C., Henriksen K. Are nonresorbing osteoclasts sources of bone anabolic activity?. J Bone Miner Res 2007, 22:487-494.
16. Chambers T.J., Athanasou N.A., Fuller K. Effect of parathyroid hormone and calcitonin on the cytoplasmic spreading of isolated osteoclasts. J Endocrinol 1984, 102:281-286.
17. Martin T.J., Findlay D.M., Moseley J.M., Sexton P.M. Calcitonin. Metabolic bone disease and clinically related disorders 1998, 95-121. Academic Press. 3rd Edition. L.V. Avioli, S.M. Krane (Eds.).
18. Kumar M.A., Slack E., Edwards A., Soliman H.A., Baghdiantz A., Foster G.V., et al. A biological assay for calcitonin. J Endocrinol 1965, 33:469-475.
19. McManus J.F., Davey R.A., Maclean H.E., Doust E.A., Chiu W.S., Sims N.A., et al. Intermittent Fugu parathyroid hormone 1 (1-34) is an anabolic bone agent in young male rats and osteopenic ovariectomized rats. Bone 2008, 42:1164-1174.
20. Onyia J.E., Bidwell J., Herring J., Hulman J., Hock J.M. In vivo, human parathyroid hormone fragment (hPTH 1-34) transiently stimulates immediate early response gene expression, but not proliferation, in trabecular bone cells of young rats. Bone 1995, 17:479-484.
21. Sims N.A., White C.P., Sunn K.L., Thomas G.P., Drummond M.L., Morrison N.A., et al. Human and murine osteocalcin gene expression: conserved tissue restricted expression and divergent responses to 1, 25-dihydroxyvitamin D3 in vivo. Mol Endocrinol 1997, 11:1695-1708.
22. Walker E.C., Mcgregor N.E., Pompolo S., Poulton I.J., Quinn J.M.W., Zhang J.G., et al. Oncostatin M promotes bone formation independently of resorption when signaling through leukemia inhibitory factor receptor in mice. J Clin Invest 2010, 582-592.
23. Han B., Copeland M., Geiser A.G., Hale L.V., Harvey A., Ma Y.L., et al. Development of a highly sensitive, high-throughput, mass spectrometry-based assay for rat procollagen type-I N-terminal propeptide (PINP) to measure bone formation activity. J Proteome Res 2007, 6:4218-4229.
24. Sims N.A., Brennan K., Spaliviero J., Handelsman D.J., Seibel M.J. Perinatal testosterone surge is required for normal adult bone size but not for normal bone remodeling. Am J Physiol Endocrinol Metab 2006, 290:E456-E462.
25. Sims N.A., Jenkins B.J., Quinn J.M., Nakamura A., Glatt M., Gillespie M.T., et al. Glycoprotein 130 regulates bone turnover and bone size by distinct downstream signaling pathways. J Clin Invest 2004, 113:379-389.
26. Ma Y.L., Cain R.L., Halladay D.L., Yang X., Zeng Q., Miles R.R., et al. Catabolic effects of continuous human PTH (1-38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology 2001, 142:4047-4054.
27. Walker E., McGregor N., Poulton I., Pompolo S., Allan E., Quinn J., et al. Cardiotrophin-1 is an osteoclast-derived stimulus of bone formation required for normal bone remodeling. J Bone Miner Res 2008, 23:2025-2032.
28. Benjamini Y., Hochberg Y. Controlling the false discovery rate; a practical and powerful approach to multiple testing. J R Stat Soc 1995, 57:289-300.
29. Quinn J.M., Whitty G.A., Byrne R.J., Gillespie M.T., Hamilton J.A. The generation of highly enriched osteoclast-lineage cell populations. Bone 2002, 30:164-170.
30. Kalajzic I., Staal A., Yang W.P., Wu Y., Johnson S.E., Feyen J.H., et al. Expression profile of osteoblast lineage at defined stages of differentiation. J Biol Chem 2005, 280:24618-24626.
31. Paic F., Igwe J.C., Nori R., Kronenberg M.S., Franceschetti T., Harrington P., et al. Identification of differentially expressed genes between osteoblasts and osteocytes. Bone 2009, 45:682-692.
32. Nicholson G.C., Moseley J.M., Sexton P.M., Mendelsohn F.A., Martin T.J. Abundant calcitonin receptors in isolated rat osteoclasts. Biochemical and autoradiographic characterization. J Clin Invest 1986, 78:355-360.
33. Quinn J.M., Morfis M., Lam M.H., Elliott J., Kartsogiannis V., Williams E.D., et al. Calcitonin receptor antibodies in the identification of osteoclasts. Bone 1999, 25:1-8.
34. Takahashi N., Akatsu T., Sasaki T., Nicholson G.C., Moseley J.M., Martin T.J., et al. Induction of calcitonin receptors by 1 alpha, 25-dihydroxyvitamin D3 in osteoclast-like multinucleated cells formed from mouse bone marrow cells. Endocrinology 1988, 123:1504-1510.
35. Forrest S.M., Ng K.W., Findlay D.M., Michelangeli V.P., Livesey S.A., Partridge N.C., et al. Characterization of an osteoblast-like clonal cell line which responds to both parathyroid hormone and calcitonin. Calcif Tissue Int 1985, 37:51-56.
36. Wada S., Udagawa N., Akatsu T., Nagata N., Martin T.J., Findlay D.M. Regulation by calcitonin and glucocorticoids of calcitonin receptor gene expression in mouse osteoclasts. Endocrinology 1997, 138:521-529.
37. Pederson L., Ruan M., Westendorf J.J., Khosla S., Oursler M.J. Regulation of bone formation by osteoclasts involves Wnt/BMP signaling and the chemokine sphingosine-1-phosphate. Proc Natl Acad Sci U S A 2008, 105:20764-20769.
38. Ryu J., Kim H.J., Chang E.J., Huang H., Banno Y., Kim H.H. Sphingosine 1-phosphate as a regulator of osteoclast differentiation and osteoclast-osteoblast coupling. EMBO J 2006, 25:5840-5851.
39. Robling A.G., Bellido T., Turner C.H. Mechanical stimulation in vivo reduces osteocyte expression of sclerostin. J Musculoskelet Neuronal Interact 2006, 6:354.
40. Ikegame M., Rakopoulos M., Zhou H., Houssami S., Martin T.J., Moseley J.M., et al. Calcitonin receptor isoforms in mouse and rat osteoclasts. J Bone Miner Res 1995, 10:59-65.
41. Houssami S., Findlay D.M., Brady C.L., Myers D.E., Martin T.J., Sexton P.M. Isoforms of the rat calcitonin receptor: consequences for ligand binding and signal transduction. Endocrinology 1994, 135:183-190.
42. Inoue D., Shih C., Galson D.L., Goldring S.R., Horne W.C., Baron R. Calcitonin-dependent down-regulation of the mouse C1a calcitonin receptor in cells of the osteoclast lineage involves a transcriptional mechanism. Endocrinology 1999, 140:1060-1068.
43. Tikellis C., Xuereb L., Casley D., Brasier G., Cooper M.E., Wookey P.J. Calcitonin receptor isoforms expressed in the developing rat kidney. Kidney Int 2003, 63:416-426.
44. Kramer I., Loots G.G., Studer A., Keller H., Kneissel M. Parathyroid Hormone (PTH) Induced Bone Gain is Blunted in SOST Overexpressing and Deficient Mice. J Bone Miner Res 2010, 25:178-189.
45. Sims N.A. Building bone with a SOST-PTH partnership. J Bone Miner Res 2010, 25:175-177.
46. van Bezooijen R.L., Svensson J.P., Eefting D., Visser A., van der Horst G., Karperien M., et al. Wnt but not BMP signaling is involved in the inhibitory action of sclerostin on BMP-stimulated bone formation. J Bone Miner Res 2007, 22:19-28.
47. Poole K.E., van Bezooijen R.L., Loveridge N., Hamersma H., Papapoulos S.E., Lowik C.W., et al. Sclerostin is a delayed secreted product of osteocytes that inhibits bone formation. FASEB J 2005, 19:1842-1844.
48. van Bezooijen R.L., Roelen B.A., Visser A., van der Wee-Pals L., de Wilt E., Karperien M., et al. Sclerostin is an osteocyte-expressed negative regulator of bone formation, but not a classical BMP antagonist. J Exp Med 2004, 199:805-814.
49. van Bezooijen R.L., ten Dijke P., Papapoulos S.E., Lowik C.W. SOST/sclerostin, an osteocyte-derived negative regulator of bone formation. Cytokine Growth Factor Rev 2005, 16:319-327.
50. Kusu N., Laurikkala J., Imanishi M., Usui H., Konishi M., Miyake A., et al. Sclerostin is a novel secreted osteoclast-derived bone morphogenetic protein antagonist with unique ligand specificity. J Biol Chem 2003, 278:24113-24117.
51. Sutherland M.K., Geoghegan J.C., Yu C., Winkler D.G., Latham J.A. Unique regulation of SOST, the sclerosteosis gene, by BMPs and steroid hormones in human osteoblasts. Bone 2004, 35:448-454.
52. Vincent C., Findlay D.M., Welldon K.J., Wijenayaka A.R., Zheng T.S., Haynes D.R., et al. 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, 24:1434-1449.
53. Harris S.E., Gluhak-Heinrich J., Harris M.A., Yang W., Bonewald L.F., Riha D., et al. DMP1 and MEPE expression are elevated in osteocytes after mechanical loading in vivo: theoretical role in controlling mineral quality in the perilacunar matrix. J Musculoskelet Neuronal Interact 2007, 7:313-315.
54. Farley J., Dimai H.P., Stilt-Coffing B., Farley P., Pham T., Mohan S. Calcitonin increases the concentration of insulin-like growth factors in serum-free cultures of human osteoblast-line cells. Calcif Tissue Int 2000, 67:247-254.
55. Farley J.R., Tarbaux N.M., Hall S.L., Linkhart T.A., Baylink D.J. The anti-bone-resorptive agent calcitonin also acts in vitro to directly increase bone formation and bone cell proliferation. Endocrinology 1988, 123:159-167.
56. Plotkin L.I., Weinstein R.S., Parfitt A.M., Roberson P.K., Manolagas S.C., Bellido T. Prevention of osteocyte and osteoblast apoptosis by bisphosphonates and calcitonin. J Clin Invest 1999, 104:1363-1374.
57. Naot D., Cornish J. The role of peptides and receptors of the calcitonin family in the regulation of bone metabolism. Bone 2008, 43:813-818.
58. Rao L.G., Heersche J.N., Marchuk L.L., Sturtridge W. Immunohistochemical demonstration of calcitonin binding to specific cell types in fixed rat bone tissue. Endocrinology 1981, 108:1972-1978.
59. Warshawsky H., Goltzman D., Rouleau M.F., Bergeron J.J. Direct in vivo demonstration by radioautography of specific binding sites for calcitonin in skeletal and renal tissues of the rat. J Cell Biol 1980, 85:682-694.
60. Leupin O., Kramer I., Collette N.M., Loots G.G., Natt F., Kneissel M., et al. Control of the SOST bone enhancer by PTH using MEF2 transcription factors. J Bone Miner Res 2007, 22:1957-1967.
61. Horne W.C., Shyu J.F., Chakraborty M., Baron R. Signal transduction by calcitonin multiple ligands, receptors, and signaling pathways. Trends Endocrinol Metab 1994, 5:395-401.
62. Findlay D.M., Houssami S., Sexton P.M., Brady C.L., Martin T.J., Myers D.E. Calcium inflow in cells transfected with cloned rat and porcine calcitonin receptors. Biochim Biophys Acta 1995, 1265:213-219.
63. Alam A.S., Bax C.M., Shankar V.S., Bax B.E., Bevis P.J., Huang C.L., et al. Further studies on the mode of action of calcitonin on isolated rat osteoclasts: pharmacological evidence for a second site mediating intracellular Ca2+ mobilization and cell retraction. J Endocrinol 1993, 136:7-15.
64. McHugh K.P., Shen Z., Fleming J.D., Crotti T.N., Harada Y., Bierbaum B.E., et al. Bone substrate-specific induction of the CTR gene in peri-implant osteolysis. Orthopedic Res Soc Transactions 2005, Paper 0147.
65. Dean A.K., Harris S.E., Kalajzic I., Ruan J. A systems biology approach to the identification and analysis of transcriptional regulatory networks in osteocytes. BMC Bioinformatics 2009, 10(Suppl 9):S5.
66. Hirsch P.F., Baruch H. Is calcitonin an important physiological substance?. Endocrine 2003, 21:201-208.
67. Hoff A.O., Catala-Lehnen P., Thomas P.M., Priemel M., Rueger J.M., Nasonkin I., et al. Increased bone mass is an unexpected phenotype associated with deletion of the calcitonin gene. J Clin Invest 2002, 110:1849-1857.
68. Woodrow J.P., Sharpe C.J., Fudge N.J., Hoff A.O., Gagel R.F., Kovacs C.S. Calcitonin plays a critical role in regulating skeletal mineral metabolism during lactation. Endocrinology 2006, 147:4010-4021.
69. Schinke T., Liese S., Priemel M., Haberland M., Schilling A.F., Catala-Lehnen P., et al. Decreased bone formation and osteopenia in mice lacking alpha-calcitonin gene-related peptide. J Bone Miner Res 2004, 19:2049-2056.
70. Dacquin R., Davey R.A., Laplace C., Levasseur R., Morris H.A., Goldring S.R., et al. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol 2004, 164:509-514.
71. Davey R.A., Turner A., McManus J.F., Chiu W.S., Tjahyono F., Moore A.J., et al. The calcitonin receptor plays a physiological role to protect against hypercalcemia in mice. J Bone Miner Res 2008, 23:1182-1193.
72. Keller J.H., Huebner A.K., Catala-Lehnen P., Schinke T., Amling M. High bone mass due to increased bone formation in mice lacking the calcitonin receptor. J Bone Miner Res 2008, 23S:S171.
73. Huebner A.K., Keller J., Catala-Lehnen P., Perkovic S., Streichert T., Emeson R.B., et al. The role of calcitonin and alpha-calcitonin gene-related peptide in bone formation. Arch Biochem Biophys 2008, 473:210-217.
74. Huebner A.K., Schinke T., Priemel M., Schilling S., Schilling A.F., Emeson R.B., et al. Calcitonin deficiency in mice progressively results in high bone turnover. J Bone Miner Res 2006, 21:1924-1934.
75. Zhao C., Irie N., Takada Y., Shimoda K., Miyamoto T., Nishiwaki T., et al. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab 2006, 4:111-121.