A lack of thyroid hormones rather than excess thyrotropin causes abnormal skeletal development in hypothyroidism

Molecular Endocrinology

Volumn 22, Issue 2, 2008, Pages 501-512

  Bassett, J H Duncan ^a   Williams, Allan J ^a   Murphy, Elaine ^a   Boyde, Alan ^b   Howell, Peter G T ^b,c   Swinhoe, Rowan ^a   Archanco, Marta ^a   Flamant, Frédéric ^d   Samarut, Jacques ^d   Costagliola, Sabine ^e   Vassart, Gilbert ^e   Weiss, Roy E ^f   Refetoff, Samuel ^f   Williams, Graham R ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITÉ DE LYON   (France)

^e UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^f UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; THYROID HORMONE; THYROTROPIN;

ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; BONE REMODELING; CARTILAGE CELL; CELL DIFFERENTIATION; CELL FUNCTION; CONGENITAL HYPOTHYROIDISM; CONTROLLED STUDY; CORTICAL BONE; GENE EXPRESSION; HORMONE ACTION; HYPOTHYROIDISM; MOUSE; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SKELETON MALFORMATION; TRABECULAR BONE;

MUS;

EID: 38749088288     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2007-0221     Document Type: Article

References (49)

1. Kanis JA, Johnell O 2005 Requirements for DXA for the management of osteoporosis in Europe. Osteoporos Int 16:229-238
2. Ray NF, Chan JK, Thamer M, Melton 3rd LJ 1997 Medical expenditures for the treatment of osteoporotic fractures in the United States in 1995: report from the National Osteoporosis Foundation. J Bone Miner Res 12:24-35
3. Mosekilde L, Eriksen EF, Charles P 1990 Effects of thyroid hormones on bone and mineral metabolism. Endocrinol Metab Clin North Am 19:35-63
4. Vestergaard P, Mosekilde L 2002 Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid 12:411-419
5. Bauer DC, Ettinger B, Nevitt MC, Stone LS 2001 Risk for fracture in women with low serum levels of thyroid-stimulating hormone. Ann Intern Med 134:561-568
6. Murphy E, Williams GR 2004 The thyroid and the skeleton. Clin Endocrinol (Oxf) 61:285-298
7. Abe E, Marians RC, Yu W, Wu XB, Ando T, Li Y, Iqbal J, Eldeiry L, Rajendren G, Blair HC, Davies TF, Zaidi M 2003 TSH is a negative regulator of skeletal remodeling. Cell 115:151-162
8. Vassart G, Dumont JE 1992 The thyrotropin receptor and the regulation of thyrocyte function and growth. Endocr Rev 13:596-611
9. Marians RC, Ng L, Blair HC, Unger P, Graves PN, Davies TF 2002 Defining thyrotropin-dependent and -independent steps of thyroid hormone synthesis by using thyrotropin receptor-null mice. Proc Natl Acad Sci USA 99:15776-15781
10. Boersma B, Otten BJ, Stoelinga GB, Wit JM 1996 Catch-up growth after prolonged hypothyroidism. Eur J Pediatr 155:362-367
11. Rivkees SA, Bode HH, Crawford JD 1988 Long-term growth in juvenile acquired hypothyroidism: the failure to achieve normal adult stature. N Engl J Med 318:599-602
12. -/- mouse model of congenital hypothyroidism. Endocrinology 144:777-784
13. Weiss RE, Chassande O, Koo EK, Macchia PE, Cua K, Samarut J, Refetoff S, Refetoff S 2002 Thyroid function and effect of aging in combined hetero/homozygous mice deficient in thyroid hormone receptors α and β genes. J Endocrinol 172:177-185
14. Gu WX, Du GG, Kopp P, Rentoumis A, Albanese C, Kohn LD, Madison LD, Jameson JL 1995 The thyrotropin (TSH) receptor transmembrane domain mutation (Pro556-Leu) in the hypothyroid hyt/hyt mouse results in plasma membrane targeting but defective TSH binding. Endocrinology 136:3146-3153
15. O'Shea PJ, Bassett JH, Sriskantharajah S, Ying H, Cheng SY, Williams GR 2005 Contrasting skeletal phenotypes in mice with an identical mutation targeted to thyroid hormone receptor α1 or β. Mol Endocrinol 19:3045-3059
16. O'Shea PJ, Guigon CJ, Williams GR, Cheng SY 2007 Regulation of fibroblast growth factor receptor-1 by thyroid hormone: identification of a thyroid hormone response element in the murine Fgfr1 promoter. Endocrinology 148:5966-5976
17. Stevens DA, Harvey CB, Scott AJ, O'Shea PJ, Barnard JC, Williams AJ, Brady G, Samarut J, Chassande O, Williams GR 2003 Thyroid hormone activates fibroblast growth factor receptor-1 in bone. Mol Endocrinol 17:1751-1766
18. Costagliola S, Bonomi M, Morgenthaler NG, Van Durme J, Panneels V, Refetoff S, Vassart G 2004 Delineation of the discontinuous-conformational epitope of a monoclonal antibody displaying full in vitro and in vivo thyrotropin activity. Mol Endocrinol 18:3020-3034
19. Costagliola S, Khoo D, Vassart G 1998 Production of bioactive amino-terminal domain of the thyrotropin receptor via insertion in the plasma membrane by a glycosylphosphatidylinositol anchor. FEBS Lett 436:427-433
20. Sanders J, Evans M, Premawardhana LD, Depraetere H, Jeffreys J, Richards T, Furmaniak J, Rees Smith B 2003 Human monoclonal thyroid stimulating autoantibody. Lancet 362:126-128
21. Bassett JH, O'Shea PJ, Sriskantharajah S, Rabier B, Boyde A, Howell PG, Weiss RE, Roux JP, Malaval L, Clement-Lacroix P, Samarut J, Chassande O, Williams GR 2007 Thyroid hormone excess rather than thyrotropin deficiency induces osteoporosis in hyperthyroidism. Mol Endocrinol 21:1095-1107
22. Ballock RT, Zhou X, Mink LM, Chen DH, Mita BC, Stewart MC 2000 Expression of cyclin-dependent kinase inhibitors in epiphyseal chondrocytes induced to terminally differentiate with thyroid hormone. Endocrinology 141:4552-4557
23. Britto JM, Fenton AJ, Holloway WR, Nicholson GC 1994 Osteoblasts mediate thyroid hormone stimulation of osteoclastic bone resorption. Endocrinology 134:169-176
24. 3) and dexamethasone interact to modulate osteoprogenitor cell differentiation in fetal rat calvaria cell cultures. Bone 16:545-549
25. Milne M, Kang MI, Quail JM, Baran DT 1998 Thyroid hormone excess increases insulin-like growth factor I transcripts in bone marrow cell cultures: divergent effects on vertebral and femoral cell cultures. Endocrinology 139:2527-2534
26. Mundy GR, Shapiro JL, Bandelin JG, Canalis EM, Raisz LG 1976 Direct stimulation of bone resorption by thyroid hormones. J Clin Invest 58:529-534
27. Ohishi K, Ishida H, Nagata T, Yamauchi N, Tsurumi C, Nishikawa S, Wakano Y 1994 Thyroid hormone suppresses the differentiation of osteoprogenitor cells to osteoblasts, but enhances functional activities of mature osteoblasts in cultured rat calvaria cells. J Cell Physiol 161:544-552
28. Robson H, Siebler T, Stevens DA, Shalet SM, Williams GR 2000 Thyroid hormone acts directly on growth plate chondrocytes to promote hypertrophic differentiation and inhibit clonal expansion and cell proliferation. Endocrinology 141:3887-3897
29. Bell A, Gagnon A, Dods P, Papineau D, Tiberi M, Sorisky A 2002 TSH signaling and cell survival in 3T3-L1 preadipocytes. Am J Physiol Cell Physiol 283:C1056-C1064
30. Rivas M, Santisteban P 2003 TSH-activated signaling pathways in thyroid tumorigenesis. Mol Cell Endocrinol 213:31-45
31. Laugwitz KL, Allgeier A, Offermanns S, Spicher K, Van Sande J, Dumont JE, Schultz G 1996 The human thyrotropin receptor: a heptahelical receptor capable of stimulating members of all four G protein families. Proc Natl Acad Sci USA 93:116-120
32. Hoffmann S, Hofbauer LC, Scharrenbach V, Wunderlich A, Hassan I, Lingelbach S, Zielke A 2004 Thyrotropin (TSH)-induced production of vascular endothelial growth factor in thyroid cancer cells in vitro: evaluation of TSH signal transduction and of angiogenesis-stimulating growth factors. J Clin Endocrinol Metab 89:6139-6145
33. Park ES, Kim H, Suh JM, Park SJ, You SH, Chung HK, Lee KW, Kwon OY, Cho BY, Kim YK, Ro HK, Chung J, Shong M 2000 Involvement of JAK/STAT (Janus kinase/ signal transducer and activator of transcription) in the thyrotropin signaling pathway. Mol Endocrinol 14:662-670
34. Park YJ, Park ES, Kim MS, Kim TY, Lee HS, Lee S, Jang IS, Shong M, Park DJ, Cho BY 2002 Involvement of the protein kinase C pathway in thyrotropin-induced STAT3 activation in FRTL-5 thyroid cells. Mol Cell Endocrinol 194:77-84
35. Suh JM, Song JH, Kim DW, Kim H, Chung HK, Hwang JH, Kim JM, Hwang ES, Chung J, Han JH, Cho BY, Ro HK, Shong M 2003 Regulation of the phosphatidylinositol 3-kinase, Akt/protein kinase B, FRAP/mammalian target of rapamycin, and ribosomal S6 kinase 1 signaling pathways by thyroid-stimulating hormone (TSH) and stimulating type TSH receptor antibodies in the thyroid gland. J Biol Chem 278:21960-21971
36. -/- mutant mice can be rescued by inactivating the TRα gene. Mol Endocrinol 16:24-32
37. Dumitrescu AM, Liao XH, Weiss RE, Millen K, Refetoff S 2006 Tissue-specific thyroid hormone deprivation and excess in monocarboxylate transporter (mct) 8-deficient mice. Endocrinology 147:4036-4043
38. Pohlenz J, Maqueem A, Cua K, Weiss RE, Van Sande J, Refetoff S 1999 Improved radioimmunoassay for measurement of mouse thyrotropin in serum: strain differences in thyrotropin concentration and thyrotroph sensitivity to thyroid hormone. Thyroid 9:1265-1271
39. O'Shea PJ, Harvey CB, Suzuki H, Kaneshige M, Kaneshige K, Cheng SY, Williams GR 2003 A thyrotoxic skeletal phenotype of advanced bone formation in mice with resistance to thyroid hormone. Mol Endocrinol 17:1410-1424
40. Barnard JC, Williams AJ, Rabier B, Chassande O, Samarut J, Cheng SY, Bassett JH, Williams GR 2005 Thyroid hormones regulate fibroblast growth factor receptor signaling during chondrogenesis. Endocrinology 146:5568-5580
41. Bassett JH, Nordstrom K, Boyde A, Howell PG, Kelly S, Vennstrom B, Williams GR 2007 Thyroid status during skeletal development determines adult bone structure and mineralization. Mol Endocrinol 21:1893-1904
42. Lloyd G 1987 Atomic number and crystallographic contrast images with the SEM: a review of backscattered electron techniques. Mineralogical Magazine 51:3-19
43. Boyde A, Firth EC 2005 Musculoskeletal responses of 2-year-old Thoroughbred horses to early training. 8. Quantitative back-scattered electron scanning electron microscopy and confocal fluorescence microscopy of the epiphysis of the third metacarpal bone. NZ Vet J 53:123-132
44. Boyde A, Travers R, Glorieux FH, Jones SJ 1999 The mineralization density of iliac crest bone from children with osteogenesis imperfecta. Calcif Tissue Int 64:185-190
45. Siebler T, Robson H, Shalet SM, Williams GR 2002 Dexamethasone inhibits and thyroid hormone promotes differentiation of mouse chondrogenic ATDC5 cells. Bone 31:457-464
46. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ 1998 Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165-176
47. Saftig P, Hunziker E, Everts V, Jones S, Boyde A, Wehmeyer O, Suter A, von Figura K 2000 Functions of cathepsin K in bone resorption. Lessons from cathepsin K deficient mice. Adv Exp Med Biol 477:293-303
48. Sanders J, Jeffreys J, Depraetere H, Evans M, Richards T, Kiddie A, Brereton K, Premawardhana LD, Chirgadze DY, Nunez Miguel R, Blundell TL, Furmaniak J, Rees Smith B 2004 Characteristics of a human monoclonal autoantibody to the thyrotropin receptor: sequence structure and function. Thyroid 14:560-570
49. Smits G, Campillo M, Govaerts C, Janssens V, Richter C, Vassart G, Pardo L, Costagliola S 2003 Glycoprotein hormone receptors: determinants in leucine-rich repeats responsible for ligand specificity. EMBO J 22:2692-2703