Hormone regulation of chondrocyte differentiation and endochondral bone formation

Molecular and Cellular Endocrinology

Volumn 151, Issue 1-2, 1999, Pages 195-204

  Stevens, David A ^a   Williams, Graham R ^a  

^a MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

Author keywords

Angiogenesis; Bone morphogenetic proteins; Chondrocyte differentiation; Endochondral ossification; Indian hedgehog; Metalloproteinases; PTHrP

Indexed keywords

BONE MORPHOGENETIC PROTEIN; METALLOPROTEINASE; PARATHYROID HORMONE RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; BONE DEVELOPMENT; BONE TURNOVER; CARTILAGE CELL; CELL DIFFERENTIATION; ENCHONDRAL OSSIFICATION; HEDGEHOG; HORMONAL REGULATION; KNOCKOUT GENE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0033603029     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0303-7207(99)00037-4     Document Type: Article

References (71)

1. Alexander C.M., Werb Z. Targeted disruption of the tissue inhibitor of metalloproteinases gene increases the invasive behavior of primitive mesenchymal cells derived from embryonic stem cells in vitro. J. Cell. Biol. 118:1992;727-739.
2. Alini M., Marriott A., Chen T., Abe S., Poole A.R. A novel angiogenic molecule produced at the time of chondrocyte hypertrophy during endochondral bone formation. Dev. Biol. 176:1996;124-132.
3. Amizuka N., Warshawsky H., Henderson J.E., Goltzman D., Karaplis A.C. Parathyroid hormone-related peptide-depleted mice show abnormal epiphyseal cartilage development and altered endochondral bone formation. J. Cell. Biol. 126:1994;1611-1623.
4. Baker J., Liu J.P., Robertson E.J., Efstratiadis A. Role of insulin-like growth factors in embryonic and postnatal growth. Cell. 75:1993;73-82.
5. Bannister, L.H., Berry, M.M., Collins, P., Dyson, M., Dussik, J.E., Fergusson, J.E., 1995. Skeletal system, Grey's Anatomy, 38th ed. Churchill Livingstone, Edinburgh, pp. 425-736.
6. Bitgood M.J., McMahon A.P. Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172:1995;126-138.
7. Bland R., Sammons R.L., Sheppard M.C., Williams G.R. Thyroid hormone, vitamin D and retinoid receptor expression and signalling in primary cultures of rat osteoblastic and immortalised osteosarcoma cells. J. Endocrinol. 154:1997;63-74.
8. Brown R.A., Weiss J.B. Neovascularisation and its role in the osteoarthritic process. Ann. Rheum. Dis. 47:1988;881-885.
9. Carlevaro M.F., Albini A., Ribatti D., Gentili C., Benelli R., Cermelli S., Cancedda R., Cancedda F.D. Transferrin promotes endothelial cell migration and invasion: implication in cartilage neovascularization. J. Cell. Biol. 136:1997;1375-1384.
10. Cash D.E., Bock C.B., Schughart K., Linney E., Underhill T.M. Retinoic acid receptor alpha function in vertebrate limb skeletogenesis: a modulator of chondrogenesis. J. Cell. Biol. 136:1997;445-457.
11. Colville Nash P.R., Scott D.L. Angiogenesis and rheumatoid arthritis: pathogenic and therapeutic implications. Ann. Rheum. Dis. 51:1992;919-925.
12. Conte F.A., Grumbach M.M., Ito Y., Fisher C.R., Simpson E.R. A syndrome of female pseudohermaphrodism, hypergonadotropic hypogonadism, and multicystic ovaries associated with missense mutations in the gene encoding aromatase (P450arom). J. Clin. Endocrinol. Metab. 78:1994;1287-1292.
13. Dean D.D., Muniz O.E., Woessner J.F. Jr., Howell D.S. Production of collagenase and tissue inhibitor of metalloproteinases (TIMP) by rat growth plates in culture. Matrix. 10:1990;320-330.
14. Denton R.R., Franslon-Vanhulle C., Galien R., Resche-Rigon M., Baron R. Estrogen receptor alpha and beta expression and interaction in bone. Bone. 23:1998;SA192.
15. Forrest D., Hanebuth E., Smeyne R.J., Everds N., Stewart C.L., Wehner J.M., Curran T. Recessive resistance to thyroid hormone in mice lacking thyroid hormone receptor beta: evidence for tissue-specific modulation of receptor function. EMBO J. 15:1996;3006-3015.
16. Fraichard A., Chassande O., Plateroti M., Roux J.P., Trouillas J., Dehay C., Legrand C., Gauthier K., Kedinger M., Malaval L., Rousset B., Samarut J. The T3R alpha gene encoding a thyroid hormone receptor is essential for post-natal development and thyroid hormone production. EMBO J. 16:1997;4412-4420.
17. Fu G.K., Lin D., Zhang M.Y., Bikle D.D., Shackleton C.H., Miller W.L., Portale A.A. Cloning of human 25-hydroxyvitamin D-1 alpha-hydroxylase and mutations causing vitamin D-dependent rickets type 1. Mol. Endocrinol. 11:1997;1961-1970.
18. Hewison M., O'Riordan J.L. Hormone-nuclear receptor interactions in health and disease. Vitamin D resistance. Baillieres Clin. Endocrinol. Metab. 8:1994;305-315.
19. Hiraki Y., Inoue H., Iyama K., Kamizono A., Ochiai M., Shukunami C., Iijima S., Suzuki F., Kondo J. Identification of chondromodulin I as a novel endothelial cell growth inhibitor. Purification and its localization in the avascular zone of epiphyseal cartilage. J. Biol. Chem. 272:1997;32419-32426.
20. Hogan B.L. Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10:1996;1580-1594.
21. Hughes M.R., Malloy P.J., O'Malley B.W., Pike J.W., Feldman D. Genetic defects of the 1,25-dihydroxyvitamin D3 receptor. J. Recept. Res. 11:1991;699-716.
22. Iwasaki M., Le A.X., Helms J.A. Expression of indian hedgehog, bone morphogenetic protein 6 and gli during skeletal morphogenesis. Mech. Dev. 69:1997;197-202.
23. Jobert A.S., Zhang P., Couvineau A., Bonaventure J., Roume J., Le Merrer M., Silve C. Absence of functional receptors for parathyroid hormone and parathyroid hormone-related peptide in Blomstrand chondrodysplasia. J. Clin. Invest. 102:1998;34-40.
24. Johansson N., Saarialho Kere U., Airola K., Herva R., Nissinen L., Westermarck J., Vuorio E., Heino J., Kahari V.M. Collagenase-3 (MMP-13) is expressed by hypertrophic chondrocytes, periosteal cells, and osteoblasts during human fetal bone development. Dev. Dyn. 208:1997;387-397.
25. Karaplis A.C., Kronenberg H.M. Physiological roles for parathyroid hormone-related protein: lessons from gene knockout mice. Vitam. Horm. 52:1996;177-193.
26. Karaplis A.C., Luz A., Glowacki J., Bronson R.T., Tybulewicz V.L., Kronenberg H.M., Mulligan R.C. Lethal skeletal dysplasia from targeted disruption of the parathyroid hormone-related peptide gene. Genes Dev. 8:1994;277-289.
27. Kato Y., Shimazu A., Iwamoto M., Nakashima K., Koike T., Suzuki F., Nishii Y., Sato K. Role of 1,25-dihydroxycholecalciferol in growth-plate cartilage: inhibition of terminal differentiation of chondrocytes in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 87:1990;6522-6526.
28. Kawashima Ohya Y., Satakeda H., Kuruta Y., Kawamoto T., Yan W., Akagawa Y., Hayakawa T., Noshiro M., Okada Y., Nakamura S., Kato Y. Effects of parathyroid hormone (PTH) and PTH-related peptide on expressions of matrix metalloproteinase-2, -3, and -9 in growth plate chondrocyte cultures. Endocrinology. 139:1998;2120-2127.
29. Kitanaka S., Takeyama K., Murayama A., Sato T., Okumura K., Nogami M., Hasegawa Y., Niimi H., Yanagisawa J., Tanaka T., Kato S. Inactivating mutations in the 25-hydroxyvitamin D3 lalpha-hydroxylase gene in patients with pseudovitamin D-deficiency rickets. N. Engl. J. Med. 338:1998;653-661.
30. Korach K.S., Couse J.F., Curtis S.W., Washburn T.F., Lindzey J., Kimbro K.S., Eddy E.M., Migliaccio S., Snedeker S.M., Lubahn D.B., Schomberg D.W., Smith E.P. Estrogen receptor gene disruption: molecular characterization and experimental and clinical phenotypes. Recent Prog. Horm. Res. 51:1996;159-186.
31. Lanske B., Karaplis A.C., Lee K., Luz A., Vortkamp A., Pirro A., Karperien M., Defize L.H.K., Ho C., Mulligan R.C., Abou Samra A.B., Juppner H., Segre G.V., Kronenberg H.M. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science. 273:1996;663-666.
32. Laron Z., Kowadlo Silbergeld A., Eshet R., Pertzelan A. Growth hormone resistance. Ann. Clin. Res. 12:1980;269-277.
33. Lee K., Lanske B., Karaplis A.C., Deeds J.D., Kohno H., Nissenson R.A., Kronenberg H.M., Segre G.V. Parathyroid hormone-related peptide delays terminal differentiation of chondrocytes during endochondral bone development. Endocrinology. 137:1996;5109-5118.
34. Lee Y.H., Sauer B., Gonzalez F.J. Laron dwarfism and non-insulin-dependent diabetes mellitus in the Hnf-lalpha knockout mouse. Mol. Cell. Biol. 18:1998;3059-3068.
35. Lohnes D., Kastner P., Dierich A., Mark M., LeMeur M., Chambon P. Function of retinoic acid receptor gamma in the mouse. Cell. 73:1993;643-658.
36. Luo J., Pasceri P., Conlon R.A., Rossant J., Giguere V. Mice lacking all isoforms of retinoic acid receptor beta develop normally and are susceptible to the teratogenic effects of retinoic acid. Mech. Dev. 53:1995;61-71.
37. Macias D., Ganan Y., Sampath T.K., Piedra M.E., Ros M.A., Hurle J.M. Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development. 124:1997;1109-1117.
38. Mendelsohn C., Ruberte E., LeMeur M., Morriss Kay G., Chambon P. Developmental analysis of the retinoic acid-inducible RAR-beta 2 promoter in transgenic animals. Development. 113:1991;723-734.
39. Morishima A., Grumbach M.M., Simpson E.R., Fisher C., Qin K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J. Clin. Endocrinol. Metab. 80:1995;3689-3698.
40. Nilsson A., Ohlsson C., Isaksson O.G., Lindahl A., Isgaard J. Hormonal regulation of longitudinal bone growth. Eur. J. Clin. Nutr. 48:1994;S150-S160.
41. Nilsson O., Grigelioniene G., Arai N., Ohlsson C., Boman A., Engstrom M., Ritzen M., Wroblewski J. Expression of estrogen receptors in mouse and human growth plates. Bone. 23:1998;SA191.
42. Ohlsson C., Ispaard J., Tornell J., Nilsson A., Isaksson O.G., Lindahl A. Endocrine regulation of longitudinal bone growth. Acta Paediatr. 391:1993;33-40.
43. Pepper M.S., Montesano R., Vassalli J.D., Orci L. Chondrocytes inhibit endothelial sprout formation in vitro: evidence for involvement of a transforming growth factor-beta. J. Cell. Physiol. 146:1991;170-179.
44. Refetoff S., Weiss R.E., Usala S.J. The syndromes of resistance to thyroid hormone. Endocr. Rev. 14:1993;348-399.
45. Rhodin J.A.G. Histology. A Text and Atlas. 1974;Oxford University Press, Oxford.
46. Ruberte E., Dolle P., Krust A., Zelent A., Morriss Kay G., Chambon P. Specific spatial and temporal distribution of retinoic acid receptor gamma transcripts during mouse embryogenesis. Development. 108:1990;213-222.
47. Schipani E., Kruse K., Juppner H. A constitutively active mutant PTH-PTHrP receptor in Jansen-type metaphyseal chondrodysplasia. Science. 268:1995;98-100.
48. Schipani E., Lanske B., Hunzelman J., Luz A., Kovacs C.S., Lee K., Pirro A., Kronenberg H.M., Juppner H. Targeted expression of constitutively active receptors for parathyroid hormone and parathyroid hormone-related peptide delays endochondral bone formation and rescues mice that lack parathyroid hormone-related peptide. Proc. Natl. Acad. Sci. USA. 94:1997;13689-13694.
49. Schmitz J.P., Dean D.D., Schwartz Z., Cochran D.L., Grant G.M., Klebe R.J., Nakaya H., Boyan B.D. Chondrocyte cultures express matrix metalloproteinase mRNA and immunoreactive protein; stromelysin-1 and 72 kDa gelatinase are localized in extracellular matrix vesicles. J. Cell. Biochem. 61:1996a;375-391.
50. Schmitz J.P., Schwartz Z., Sylvia V.L., Dean D.D., Calderon F., Boyan B.D. Vitamin D3 regulation of stromelysin-1 (MMP-3) in chondrocyte cultures is mediated by protein kinase C. J. Cell. Physiol. 168:1996b;570-579.
51. Smith E.P., Boyd J., Frank G.R., Takahashi H., Cohen R.M., Specker B., Williams T.C., Lubahn D.B., Korach K.S. Estrogen resistance caused by a mutation in the estrogenreceptor gene in a man. N. Engl. J. Med. 331:1994;1056-1061.
52. St Arnaud R., Messerlian S., Moir J.M., Omdahl J.L., Glorieux F.H. The 25hydroxyvitamin D 1-alpha-hydroxylase gene maps to the pseudovitamin D-deficiency rickets (PDDR) disease locus. J. Bone Miner. Res. 12:1997;1552-1559.
53. Standeven A.M., Davies P.J., Chandraratna R.A., Mader D.R., Johnson A.T., Thomazy V.A. Retinoid-induced epiphyseal plate closure in guinea pigs. Fundam. Appl. Toxicol. 34:1996;91-98.
54. Su S., Dehnade F., Zafarullah M. Regulation of tissue inhibitor of metalloproteinases-3 gene expression by transforming growth factor-beta and dexamethasone in bovine and human articular chondrocytes. DNA Cell Biol. 15:1996;1039-1048.
55. Sucov H.M., Izpisua Belmonte J.C., Ganan Y., Evans R.M. Mouse embryos lacking RXR alpha are resistant to retinoic-acid-induced limb defects. Development. 121:1995;3997-4003.
56. Takeyama K., Kitanaka S., Sato T., Kobori M., Yanagisawa J., Kato S. 25-Hydroxyvitamin D3 lalpha-hydroxylase and vitamin D synthesis. Science. 277:1997;1827-1830.
57. Underwood, L.E., Van Wyk, J.J., 1992. Normal and aberrant growth. In: Wilson, J.D., Foster, D.W. (Eds.), Williams Textbook of Endocrinology. Saunders, Philadelphia, pp. 1079-1138.
58. Vortkamp A., Lee K., Lanske B., Segre G.V., Kronenberg H.M., Tabin C.J. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 273:1996;613-622.
59. Vortkamp A., Pathi S., Peretti G.M., Caruso E.M., Zaleske D.J., Tabin C.J. Recapitulation of signals regulating embryonic bone formation during postnatal growth and in fracture repair. Mech. Dev. 71:1998;65-76.
60. Vu T.H., Shipley J.M., Bergers G., Berger J.E., Helms J.A., Hanahan D., Shapiro S.D., Senior R.M., Werb Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 93:1998;411-422.
61. Weir E.C., Philbrick W.M., Amling M., Neff L.A., Baron R., Broadus A.E. Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc. Natl. Acad. Sci. USA. 93:1996;10240-10245.
62. Weiss R.E., Refetoff S. Effect of thyroid hormone on growth: lessons from the syndrome of resistance to thyroid hormone. Endocrinol. Metab. Clin. N. Am. 25:1996;719-730.
63. Williams G.R., Bland R., Sheppard M.C. Retinoids modify regulation of endogenous gene expression by vitamin D3 and thyroid hormone in three osteosarcoma cell lines. Endocrinology. 136:1995;4304-4314.
64. Williams G.R., Robson H., Shalet S.M. Thyroid hormone actions on cartilage and bone; interactions with other hormones at the epiphyseal plate and effects on linear growth. J. Endocrinol. 157:1998;391-403.
65. Witty J.P., Foster S.A., Stricklin G.P., Matrisian L.M., Stern P.H. Parathyroid hormone-induced resorption in fetal rat limb bones is associated with production of the metalloproteinases collagenase and gelatinase B. J. Bone Miner. Res. 11:1996;72-78.
66. Woessner J.F. Jr. Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J. 5:1991;2145-2154.
67. Yoshizawa T., Handa Y., Uematsu Y., Takeda S., Sekine K., Yoshihara Y., Kawakami T., Arioka K., Sato H., Uchiyama Y., Masushige S., Fukamizu A., Matsumoto T., Kato S. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nature Gen. 16:1997;391-396.
68. Zafarullah M., Su S., Martel Pelletier J., DiBattista J.A., Costello B.G., Stetler Stevenson W.G., Pelletier J.P. Tissue inhibitor of metalloproteinase-2 (TIMP-2) mRNA is constitutively expressed in bovine, human normal, and osteoarthritic articular chondrocytes. J. Cell. Biochem. 60:1996;211-217.
69. Zhou X., Mita B.C., Ballock R.T. Both vitamin D and retinoic acid inhibit thyroid hormone induced terminal differentiation of growth plate chondrocytes. J. Bone Miner. Res. 12:1997a;F270.
70. Zhou Y., Xu B.C., Maheshwari H.G., He L., Reed M., Lozykowski M., Okada S., Cataldo L., Coschigamo K., Wagner T.E., Baumann G., Kopchick J.J. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc. Natl. Acad. Sci. USA. 94:1997b;13215-13220.
71. Zou H., Wieser R., Massague J., Niswander L. Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11:1997;2191-2203.