Genetic evidence that thyroid hormone is indispensable for prepubertal insulin-like growth factor-I expression and bone acquisition in mice

Journal of Bone and Mineral Research

Volumn 27, Issue 5, 2012, Pages 1067-1079

  Xing, Weirong ^a,b   Govoni, Kristen E ^c   Donahue, Leah Rae ^d   Kesavan, Chandrasekhar ^a,b   Wergedal, Jon ^a,b   Long, Carlin ^e   Bassett, J H Duncan ^f   Gogakos, Apostolos ^f   Wojcicka, Anna ^f   Williams, Graham R ^f   Mohan, Subburaman ^a,b  

^a Jerry L Pettis Memorial VA Medical Center   (United States)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d JACKSON LABORATORY   (United States)

^e UNIVERSITY OF COLORADO   (United States)

^f IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

ACID LABILE SUBUNIT; DUAL OXIDASE 2; GROWTH HORMONE; HYPOTHYROIDISM; IGF BINDING PROTEIN; OSTEOBLASTS; THYROID HORMONE RECEPTOR ALPHA; THYROID HORMONE RECEPTOR BETA

Indexed keywords

LIOTHYRONINE; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C; THYROID HORMONE; THYROXINE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BODY FAT; BONE GROWTH; BONE MINERAL; DUAL ENERGY X RAY ABSORPTIOMETRY; GENETICS; HORMONAL REGULATION; HORMONE BLOOD LEVEL; HORMONE DEFICIENCY; IN VIVO STUDY; METATARSAL BONE; MOUSE; NONHUMAN; OSTEOBLAST; PHENOTYPE; POINT MUTATION; PREPUBERTY; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; TRANSGENIC MOUSE;

ANIMALS; BONE DEVELOPMENT; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OSTEOBLASTS; POLYMERASE CHAIN REACTION; PUBERTY; THYROID HORMONES;

EID: 84859915576     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.1551     Document Type: Article

References (54)

1. Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C., Peak bone mass. Osteoporos Int. 2000; 11 (12): 985-1009.
2. Libanati C, Baylink DJ, Lois-Wenzel E, Srinvasan N, Mohan S., Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab. 1999; 84 (8): 2807-14.
3. Osteoporosis prevention, diagnosis, and therapy. NIH Consens Statement. 2000; 17 (1): 1-45.
4. Hansen MA, Overgaard K, Riis BJ, Christiansen C., Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study. BMJ. 1991; 303 (6808): 961-4.
5. Hui SL, Slemenda CW, Johnston CC Jr., The contribution of bone loss to postmenopausal osteoporosis. Osteoporos Int. 1990; 1 (1): 30-4.
6. Govoni KE, Wergedal JE, Florin L, Angel P, Baylink DJ, Mohan S., Conditional deletion of insulin-like growth factor-I in collagen type 1alpha2-expressing cells results in postnatal lethality and a dramatic reduction in bone accretion. Endocrinology. 2007; 148 (12): 5706-15.
7. Mohan S, Richman C, Guo R, Amaar Y, Donahue LR, Wergedal J, Baylink DJ., Insulin-like growth factor regulates peak bone mineral density in mice by both growth hormone-dependent and -independent mechanisms. Endocrinology. 2003; 144 (3): 929-36.
8. Walenkamp MJ, Karperien M, Pereira AM, Hilhorst-Hofstee Y, van Doorn J, Chen JW, Mohan S, Denley A, Forbes B, van Duyvenvoorde HA, van Thiel SW, Sluimers CA, Bax JJ, de Laat JA, Breuning MB, Romijn JA, Wit JM., Homozygous and heterozygous expression of a novel insulin-like growth factor-I mutation. J Clin Endocrinol Metab. 2005; 90 (5): 2855-64.
9. Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL., Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem. 2002; 277 (46): 44005-12.
10. LeRoith D., Clinical relevance of systemic and local IGF-I: lessons from animal models. Pediatr Endocrinol Rev. 2008; 5 (Suppl 2): 739-43.
11. Ohlsson C, Mohan S, Sjogren K, Tivesten A, Isgaard J, Isaksson O, Jansson JO, Svensson J., The role of liver-derived insulin-like growth factor-I. Endocr Rev. 2009; 30 (5): 494-535.
12. Kasukawa Y, Baylink D, Guo R, Mohan S., Evidence that sensitivity to growth hormone (GH) is growth period and tissue type dependent: studies in GH deficient (lit/lit) mice. Endocrinology. 2003; 144 (9): 3950-7.
13. Savage MO, Burren CP, Rosenfeld RG., The continuum of growth hormone-IGF-I axis defects causing short stature: diagnostic and therapeutic challenges. Clin Endocrinol (Oxf). 2010; 72 (6): 721-8.
14. Walenkamp MJ, Wit JM., Genetic disorders in the GH IGF-I axis in mouse and man. Eur J Endocrinol. 2007; 157 (Suppl 1): S15-26.
15. Edderkaoui B, Baylink DJ, Beamer WG, Wergedal JE, Porte R, Chaudhuri A, Mohan S., Identification of mouse Duffy antigen receptor for chemokines (Darc) as a BMD QTL gene. Genome Res. 2007; 17 (5): 577-85.
16. Ralston SH, Uitterlinden AG., Genetics of osteoporosis. Endocr Rev. 2010; 31 (5): 629-62.
17. Rosen CJ, Beamer WG, Donahue LR., Defining the genetics of osteoporosis: using the mouse to understand man. Osteoporos Int. 2001; 12 (10): 803-10.
18. Richman C, Kutilek S, Miyakoshi N, Srivastava AK, Beamer WG, Donahue LR, Rosen CJ, Wergedal JE, Baylink DJ, Mohan S., Postnatal and pubertal skeletal changes contribute predominantly to the differences in peak bone density between C3H/HeJ and C57BL/6J mice. J Bone Miner Res. 2001; 16 (2): 386-97.
19. Collett-Solberg PF., Update in growth hormone therapy of children. J Clin Endocrinol Metab. 2011; 96 (3): 573-9.
20. Wit JM, Reiter EO, Ross JL, Saenger PH, Savage MO, Rogol AD, Cohen P., Idiopathic short stature: management and growth hormone treatment. Growth Horm IGF Res. 2008; 18 (2): 111-35.
21. Bassett JH, Williams GR., The skeletal phenotypes of TRalpha and TRbeta mutant mice. J Mol Endocrinol. 2009; 42 (4): 269-82.
22. Gogakos AI, Duncan Bassett JH, Williams GR., Thyroid and bone. Arch Biochem Biophys. 2010; 503 (1): 129-36.
23. Gothe S, Wang Z, Ng L, Kindblom JM, Barros AC, Ohlsson C, Vennstrom B, Forrest D., Mice devoid of all known thyroid hormone receptors are viable but exhibit disorders of the pituitary-thyroid axis, growth, and bone maturation. Genes Dev. 1999; 13 (10): 1329-41.
24. Kindblom JM, Gothe S, Forrest D, Tornell J, Vennstrom B, Ohlsson C., GH substitution reverses the growth phenotype but not the defective ossification in thyroid hormone receptor alpha 1-/-beta-/- mice. J Endocrinol. 2001; 171 (1): 15-22.
25. Bassett JH, Nordstrom K, Boyde A, Howell PG, Kelly S, Vennstrom B, Williams GR., Thyroid status during skeletal development determines adult bone structure and mineralization. Mol Endocrinol. 2007; 21: 1893-904.
26. Kawai M, Devlin MJ, Rosen CJ., Fat targets for skeletal health. Nat Rev Rheumatol. 2009; 5 (7): 365-72.
27. Castillo M, Hall JA, Correa-Medina M, Ueta C, Kang HW, Cohen DE, Bianco AC., Disruption of thyroid hormone activation in type 2 deiodinase knockout mice causes obesity with glucose intolerance and liver steatosis only at thermoneutrality. Diabetes. 2011; 60 (4): 1082-9.
28. Qin X, Strong DD, Baylink DJ, Mohan S., Structure-function analysis of the human insulin-like growth factor binding protein-4. J Biol Chem. 1998; 273 (36): 23509-16.
29. Kinugawa K, Jeong MY, Bristow MR, Long CS., Thyroid hormone induces cardiac myocyte hypertrophy in a thyroid hormone receptor alpha1-specific manner that requires TAK1 and p38 mitogen-activated protein kinase. Mol Endocrinol. 2005; 19 (6): 1618-28.
30. Johnson KR, Marden CC, Ward-Bailey P, Gagnon LH, Bronson RT, Donahue LR., Congenital hypothyroidism, dwarfism and hearing impairment caused by a missense mutation in the mouse dual oxidase 2 gene, Duox2. Mol Endocrinol. 2007; 21 (7): 1593-602.
31. Gauthier K, Plateroti M, Harvey CB, Williams GR, Weiss RE, Refetoff S, Willott JF, Sundin V, Roux JP, Malaval L, Hara M, Samarut J, Chassande O., Genetic analysis reveals different functions for the products of the thyroid hormone receptor alpha locus. Mol Cell Biol. 2001; 21 (14): 4748-60.
32. Gauthier K, Chassande O, Plateroti M, Roux JP, Legrand C, Pain B, Rousset B, Weiss R, Trouillas J, Samarut J., Different functions for the thyroid hormone receptors TRalpha and TRbeta in the control of thyroid hormone production and post-natal development. EMBO J. 1999; 18 (3): 623-31.
33. Ortiga-Carvalho TM, Shibusawa N, Nikrodhanond A, Oliveira KJ, Machado DS, Liao XH, Cohen RN, Refetoff S, Wondisford FE., Negative regulation by thyroid hormone receptor requires an intact coactivator-binding surface. J Clin Invest. 2005; 115 (9): 2517-23.
34. Mohan S, Baylink DJ., Development of a simple valid method for the complete removal of insulin-like growth factor (IGF)-binding proteins from IGFs in human serum and other biological fluids: comparison with acid-ethanol treatment and C18 Sep-Pak separation. J Clin Endocrinol Metab. 1995; 80 (2): 637-47.
35. Kim J, Xing W, Wergedal J, Chan JY, Mohan S., Targeted disruption of nuclear factor erythroid-derived 2-like 1 in osteoblasts reduces bone size and bone formation in mice. Physiol Genomics. 2010; 40 (2): 100-10.
36. Xing W, Singgih A, Kapoor A, Alarcon CM, Baylink DJ, Mohan S., Nuclear factor-E2-related factor-1 mediates ascorbic acid induction of osterix expression via interaction with antioxidant-responsive element in bone cells. J Biol Chem. 2007; 282 (30): 22052-61.
37. Mohan S, Kapoor A, Singgih A, Zhang Z, Taylor T, Yu H, Chadwick RB, Chung YS, Donahue LR, Rosen C, Crawford GC, Wergedal J, Baylink DJ., Spontaneous fractures in the mouse mutant sfx are caused by deletion of the gulonolactone oxidase gene, causing vitamin C deficiency. J Bone Miner Res. 2005; 20 (9): 1597-610.
38. Amaar YG, Baylink DJ, Mohan S., Ras-association domain family 1 protein, RASSF1C, is an IGFBP-5 binding partner and a potential regulator of osteoblast cell proliferation. J Bone Miner Res. 2005; 20 (8): 1430-9.
39. Xing W, Kim J, Wergedal J, Chen ST, Mohan S., Ephrin B1 regulates bone marrow stromal cell differentiation and bone formation by influencing TAZ transactivation via complex formation with NHERF1. Mol Cell Biol. 2010; 30 (3): 711-21.
40. Mukherjee A, Rotwein P., Akt promotes BMP2-mediated osteoblast differentiation and bone development. J Cell Sci. 2009; 122 (Pt 5): 716-26.
41. Gu WX, Du GG, Kopp P, Rentoumis A, Albanese C, Kohn LD, Madison LD, Jameson JL., 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. 1995; 136 (7): 3146-53.
42. Bassett JH, Williams AJ, Murphy E, Boyde A, Howell PG, Swinhoe R, Archanco M, Flamant F, Samarut J, Costagliola S, Vassart G, Weiss RE, Refetoff S, Williams GR., A lack of thyroid hormones rather than excess thyrotropin causes abnormal skeletal development in hypothyroidism. Mol Endocrinol. 2008; 22 (2): 501-12.
43. Sprenkle PM, McGee J, Bertoni JM, Walsh EJ., Development of auditory brainstem responses (ABRs) in Tshr mutant mice derived from euthyroid and hypothyroid dams. J Assoc Res Otolaryngol. 2001; 2 (4): 330-47.
44. Xiong S, Chirala SS, Hsu MH, Wakil SJ., Identification of thyroid hormone response elements in the human fatty acid synthase promoter. Proc Natl Acad Sci U S A. 1998; 95 (21): 12260-5.
45. Waxman DJ, O'Connor C., Growth hormone regulation of sex-dependent liver gene expression. Mol Endocrinol. 2006; 20: 2613-29.
46. Klotz DM, Hewitt SC, Ciana P, Raviscioni M, Lindzey JK, Foley J, Maggi A, DiAugustine RP, Korach KS., Requirement of estrogen receptor-alpha in insulin-like growth factor-1 (IGF-1)-induced uterine responses and in vivo evidence for IGF-1/estrogen receptor cross-talk. J Biol Chem. 2002; 277 (10): 8531-7.
47. O'Shea PJ, Bassett JH, Sriskantharajah S, Ying H, Cheng SY, Williams GR., Contrasting skeletal phenotypes in mice with an identical mutation targeted to thyroid hormone receptor alpha1 or beta. Mol Endocrinol. 2005; 19 (12): 3045-59.
48. Cacciari E, Cicognani A, Pirazzoli P, Bernardi F, Zappulla F, Salardi S, Mazzanti L, Biasini A, Valenti E., Effect of long-term GH administration on pituitary-thyroid function in idiopathic hypopituitarism. Acta Paediatr Scand. 1979; 68 (3): 405-9.
49. Leone TC, Cresci S, Carter ME, Zhang Z, Lala DS, Strauss AW, Kelly DP., The human medium chain acyl-CoA dehydrogenase gene promoter consists of a complex arrangement of nuclear receptor response elements and Sp1 binding sites. J Biol Chem. 1995; 270 (41): 24622.
50. Lopez G, Schaufele F, Webb P, Holloway JM, Baxter JD, Kushner PJ., Positive and negative modulation of Jun action by thyroid hormone receptor at a unique AP1 site. Mol Cell Biol. 1993; 13 (5): 3042-9.
51. Forrest D, Hanebuth E, Smeyne RJ, Everds N, Stewart CL, Wehner JM, Curran T., Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue-specific modulation of receptor function. EMBO J. 1996; 15 (12): 3006-15.
52. Mackie EJ, Tatarczuch L, Mirams M., The growth plate chondrocyte and endochondral ossification. J Endocrinol. 2011; 211 (2): 109-21.
53. Stevens DA, Harvey CB, Scott AJ, O'Shea PJ, Barnard JC, Williams AJ, Brady G, Samarut J, Chassande O, Williams GR., Thyroid hormone activates fibroblast growth factor receptor-1 in bone. Mol Endocrinol. 2003; 17 (9): 1751-66.
54. Wang L, Shao YY, Ballock RT., Thyroid hormone-mediated growth and differentiation of growth plate chondrocytes involves IGF-1 modulation of beta-catenin signaling. J Bone Miner Res. 2010; 25 (5): 1138-46.