Thyroid hormone regulates heparan sulfate proteoglycan expression in the growth plate

Endocrinology

Volumn 147, Issue 1, 2006, Pages 295-305

  Bassett, J H D ^a   Swinhoe, R ^a   Chassande, O ^b   Samarut, J ^c   Williams, G R ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b INSERM   (France)

^c Univ Claude Bernard   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CORE PROTEIN; ISOENZYME; LIOTHYRONINE; MONOCLONAL ANTIBODY; PROTEIN EXT1; PROTEIN GPC6; PROTEIN HS6ST2; PROTEOCHONDROITIN SULFATE; PROTEOHEPARAN SULFATE; THYROID HORMONE; THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL PROLIFERATION; CELL STRAIN; CELLULAR DISTRIBUTION; CONGENITAL MALFORMATION; CONTROLLED STUDY; ENZYME MODIFICATION; EXTRACELLULAR MATRIX; GROWTH PLATE; HORMONAL REGULATION; HORMONE ACTION; HYPOTHYROIDISM; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAINING; THYROID DISEASE; THYROID FUNCTION; TIBIA; TOXICITY;

ANIMALS; ANIMALS, NEWBORN; CELL LINE; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH PLATE; HEPARAN SULFATE PROTEOGLYCANS; MALE; MICE; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THYROID HORMONES; TIBIA;

EID: 29344465140     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0485     Document Type: Article

References (67)

1. Stevens DA, Williams GR 1999 Hormone regulation of chondrocyte differentiation and endochondral bone formation. Mol Cell Endocrinol 151:195-204
2. Robson H, Siebler T, Shalet SM, Williams GR 2002 Interactions between GH, IGF-I, glucocorticoids, and thyroid hormones during skeletal growth. Pediatr Res 52:137-147
3. Bassett JH, Williams GR 2003 The molecular actions of thyroid hormone in bone. Trends Endocrinol Metab 14:356-364
4. Boersma B, Otten BJ, Stoelinga GB, Wit JM 1996 Catch-up growth after prolonged hypothyroidism. Eur J Pediatr 155:362-367
5. Weiss RE, Refetoff S 1996 Effect of thyroid hormone on growth. Lessons from the syndrome of resistance to thyroid hormone. Endocrinol Metab Clin North Am 25:719-730
6. Stevens DA, Hasserjian RP, Robson H, Siebler T, Shalet SM, Williams GR 2000 Thyroid hormones regulate hypertrophic chondrocyte differentiation and expression of parathyroid hormone-related peptide and its receptor during endochondral bone formation. J Bone Miner Res 15:2431-2442
7. Lewinson D, Harel Z, Shenzer P, Silbermann M, Hochberg Z 1989 Effect of thyroid hormone and growth hormone on recovery from hypothyroidism of epiphyseal growth plate cartilage and its adjacent bone. Endocrinology 124:937-945
8. Freitas FR, Capelo LP, O'Shea PJ, Jorgetti V, Moriscot AS, Scanlan TS, Williams GR, Zorn TM, Gouveia CH 2005 The thyroid hormone receptor β-specific agonist GC-1 selectively affects the bone development of hypothyroid rats. J Bone Miner Res 20:294-304
9. 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
10. 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
11. Ord W 1878 On myxoedema, term proposed to be applied to an essential condition in the "cretinoid" affection occasionally observed in middle-aged women. Med Chir Trans Lond 61:57-78
12. Safer JD, Fraser LM, Ray S, Holick MF 2001 Topical triiodothyronine stimulates epidermal proliferation, dermal thickening, and hair growth in mice and rats. Thyroid 11:717-724
13. Parving HH, Helin G, Garbarsch C, Johansen AA, Jensen BA, Helin P, Lund P, Lyngsoe J 1982 Acid glycosaminoglycans in myxoedema. Clin Endocrinol (Oxf) 16:207-210
14. Shishiba Y, Yanagishita M, Hascall VC 1988 Effect of thyroid hormone deficiency on proteoglycan synthesis by human skin fibroblast cultures. Connect Tissue Res 17:119-135
15. Calloni GW, Alvarez-Silva M, Vituri C, Trentin AG 2001 Thyroid hormone deficiency alters extracellular matrix protein expression in rat brain. Brain Res Dev Brain Res 126:121-124
16. Kim SW, Ho SC, Hong SJ, Kim KM, So EC, Christoffolete M, Harney JW 2005 A novel mechanism of thyroid hormone-dependent negative regulation by thyroid hormone receptor, nuclear receptor corepressor (NCoR), and GAGA-binding factor on the rat CD44 promoter. J Biol Chem 280:14545-14555
17. Kerr JM, Gordon DF, Woodmansee WW, Sarapura VD, Ridgway EC, Wood WM 2005 Growth arrest of thyrotropic tumors by thyroid hormone is correlated with novel changes in Wnt-10A. Mol Cell Endocrinol 238:57-67
18. Greenfield B, Wang WC, Marquardt H, Piepkorn M, Wolff EA, Aruffo A, Bennett KL 1999 Characterization of the heparan sulfate and chondroitin sulfate assembly sites in CD44. J Biol Chem 274:2511-2517
19. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ, Mohammadi M 2000 Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6:743-750
20. Jeong J, McMahon AP 2002 Cholesterol modification of Hedgehog family proteins. J Clin Invest 110:591-596
21. Forsberg E, Kjellen L 2001 Heparan sulfate: lessons from knockout mice. J Clin Invest 108:175-180
22. Duncan G, McCormick C, Tufaro F 2001 The link between heparan sulfate and hereditary bone disease: finding a function for the EXT family of putative tumor suppressor proteins. J Clin Invest 108:511-516
23. Li JP, Gong F, Hagner-McWhirter A, Forsberg E, Abrink M, Kisilevsky R, Zhang X, Lindahl U 2003 Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem 278:28363-28366
24. Govindraj P, West L, Koob TJ, Neame P, Doege K, Hassell JR 2002 Isolation and identification of the major heparan sulfate proteoglycans in the developing bovine rib growth plate. J Biol Chem 277:19461-19469
25. Gallagher JT 2001 Heparan sulfate: growth control with a restricted sequence menu. J Clin Invest 108:357-361
26. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M 1999 Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777
27. Fang KC, Wolters PJ, Steinhoff M, Bidgol A, Blount JL, Caughey GH 1999 Mast cell expression of gelatinases A and B is regulated by kit ligand and TGF-β. J Immunol 162:5528-5535
28. Siebler T, Robson H, Bromley M, Stevens DA, Shalet SM, Williams GR 2002 Thyroid status affects number and localization of thyroid hormone receptor expressing mast cells in bone marrow. Bone 30:259-266
29. David G, Bai XM, Van der Schueren B, Cassiman JJ, Van den Berghe H 1992 Developmental changes in heparan sulfate expression: in situ detection with mAbs. J Cell Biol 119:961-975
30. Shukunami C, Shigeno C, Atsumi T, Ishizeki K, Suzuki F, Hiraki Y 1996 Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J Cell Biol 133:457-468
31. Shukunami C, Ishizeki K, Atsumi T, Ohta Y, Suzuki F, Hiraki Y 1997 Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J Bone Miner Res 12:1174-1188
32. 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 2001 Genetic analysis reveals different functions for the products of the thyroid hormone receptor α locus. Mol Cell Biol 21:4748-4760
33. Mansouri A, Chowdhury K, Gruss P 1998 Follicular cells of the thyroid gland require Pax8 gene function. Nat Genet 19:87-90
34. 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
35. van den Born J, Salmivirta K, Henttinen T, Ostman N, Ishimaru T, Miyaura S, Yoshida K, Salmivirta M 2005 Novel heparan sulfate structures revealed by monoclonal antibodies. J Biol Chem 280:20516-20523
36. Nackaerts K, Verbeken E, Deneffe G, Vanderschueren B, Demedts M, David G 1997 Heparan sulfate proteoglycan expression in human lung-cancer cells. Int J Cancer 74:335-345
37. Bayliss MT, Osborne D, Woodhouse S, Davidson C 1999 Sulfation of chondroitin sulfate in human articular cartilage. The effect of age, topographical position, and zone of cartilage on tissue composition. J Biol Chem 274:15892-15900
38. SundarRaj N, Fite D, Ledbetter S, Chakravarti S, Hassell JR 1995 Perlecan is a component of cartilage matrix and promotes chondrocyte attachment. J Cell Sci 108:2663-2672
39. Krause DS, Ito T, Fackler MJ, Smith OM, Collector MI, Sharkis SJ, May WS 1994 Characterization of murine CD34, a marker for hematopoietic progenitor and stem cells. Blood 84:691-701
40. Samuels HH, Stanley F, Casanova J 1979 Depletion of l-3,5,3′- triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology 105:80-85
41. WilliamsGR2000 Cloning and characterization of two novel thyroid hormone receptor β isoforms. Mol Cell Biol 20:8329-8342
42. Veugelers M, De Cat B, Ceulemans H, Bruystens AM, Coomans C, Durr J, Vermeesch J, Marynen P, David G 1999 Glypican-6, a new member of the glypican family of cell surface heparan sulfate proteoglycans. J Biol Chem 274:26968-27743
43. Han C, Belenkaya TY, Wang B, Lin X 2004 Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process. Development 131:601-611
44. Filmus J, Selleck SB 2001 Glypicans: proteoglycans with a surprise. J Clin Invest 108:497-501
45. Hilton MJ, Gutierrez L, Martinez DA, Wells DE 2005 EXT1 regulates chondrocyte proliferation and differentiation during endochondral bone development. Bone 36:379-386
46. Murphy E, Williams GR 2004 The thyroid and the skeleton. Clin Endocrinol (Oxf) 61:285-298
47. Habuchi H, Tanaka M, Habuchi O, Yoshida K, Suzuki H, Ban K, Kimata K 2000 The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J Biol Chem 275:2859-2868
48. Habuchi H, Miyake G, Nogami K, Kuroiwa A, Matsuda Y, Kusche-Gullberg M, Habuchi O, Tanaka M, Kimata K 2003 Biosynthesis of heparan sulphate with diverse structures and functions: two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties. Biochem J 371:131-142
49. Thiele H, Sakano M, Kitagawa H, Sugahara K, Rajab A, Hohne W, Ritter H, Leschik G, Nurnberg P, Mundlos S 2004 Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc Natl Acad Sci USA 101:10155-10160
50. Chassande O 2003 Do unliganded thyroid hormone receptors have physiological functions? J Mol Endocrinol 31:9-20
51. Feng X, Jiang Y, Meltzer P, Yen PM 2000 Thyroid hormone regulation of hepatic genes in vivo detected by complementary DNA microarray. Mol Endocrinol 14:947-955
52. Lazar MA 2003 Thyroid hormone action: a binding contract. J Clin Invest 112:497-499
53. Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, Mansouri A, Samarut J 2002 Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TRα gene. Mol Endocrinol 16:24-32
54. Mittag J, Friedrichsen S, Heuer H, Polsfuss S, Visser TJ, Bauer K 2005 Athyroid Pax8-/- mice cannot be rescued by the inactivation of thyroid hormone receptor α1. Endocrinology 146:3179-3184
55. Ornitz DM, Marie PJ 2002 FGF signaling pathways in endochondral and intramembranous bone development and human genetic disease. Genes Dev 16:1446-1465
56. Chung UI, Schipani E, McMahon AP, Kronenberg HM 2001 Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J Clin Invest 107:295-304
57. Ornitz DM, Itoh N 2001 Fibroblast growth factors. Genome Biol 2:REVIEWS3005
58. Liu Z, Xu J, Colvin JS, Ornitz DM 2002 Coordination of chondrogenesis and osteogenesis by fibroblast growth factor 18. Genes Dev 16:859-869
59. Karp SJ, Schipani E, St-Jacques B, Hunzelman J, Kronenberg H, McMahon AP 2000 Indian hedgehog coordinates endochondral bone growth and morphogenesis via parathyroid hormone related-protein-dependent and -independent pathways. Development 127:543-548
60. Naski MC, Colvin JS, Coffin JD, Ornitz DM 1998 Repression of hedgehog signaling and BMP4 expression in growth plate cartilage by fibroblast growth factor receptor 3. Development 125:4977-4988
61. Humphries DE, Nicodemus CF, Schiller V, Stevens RL 1992 The human serglycin gene. Nucleotide sequence and methylation pattern in human promyelocytic leukemia HL-60 cells and T-lymphoblast Molt-4 cells. J Biol Chem 267:13558-13563
62. Gong F, Jemth P, Escobar Galvis ML, Vlodavsky I, Horner A, Lindahl U, Li JP 2003 Processing of macromolecular heparin by heparanase. J Biol Chem 278:35152-35158
63. Razin E, Stevens RL, Akiyama F, Schmid K, Austen KF 1982 Culture from mouse bone marrow of a subclass of mast cells possessing a distinct chondroitin sulfate proteoglycan with glycosaminoglycans rich in N-acetylgalactosamine-4,6- disulfate. J Biol Chem 257:7229-7236
64. Walgenbach KJ, Gorospe JR, Gratas C, Brunagel G, Hoffman EP, Shestak KC 2002 A potential role for mast cells in the of bFGF from normal myocytes during angiogenesis in vivo. J Invest Surg 15:153-162
65. Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, Bernfield M 1998 Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat Med 4:691-697
66. Fine JD, Couchman JR 1988 Chondroitin-6-sulfate-containing proteoglycan: a new component of human skin dermoepidermal junction. J Invest Dermatol 90:283-288
67. O'Shea PJ, Bassett JH, Sriskantharajah S, Ying H, Cheng SY, Williams GR 28 July 2005 Contrasting skeletal phenotypes in mice with an identical mutation targeted to thyroid hormone receptor α1 or β. Mol Endocrinol 10.1210/me.2005-0224