Portal de Periódicos da CAPES

Expression and release of insulin-like growth factor binding proteins in isolated epiphyseal growth plate chondrocytes from the ovine fetus

2000; Wiley; Volume: 183; Issue: 2 Linguagem: Inglês

10.1002/(sici)1097-4652(200005)183

1097-4652

Paolo De Los Rios, David J. Hill,

Neonatal Respiratory Health Research

Journal of Cellular PhysiologyVolume 183, Issue 2 p. 172-181 Original Article Expression and release of insulin-like growth factor binding proteins in isolated epiphyseal growth plate chondrocytes from the ovine fetus P. De Los Rios, P. De Los Rios Lawson Research Institute, St. Joseph's Health Centre, London, Ontario, Canada Department of Physiology, University of Western Ontario, London, Ontario, CanadaSearch for more papers by this authorD.J. Hill, Corresponding Author D.J. Hill [email protected] Lawson Research Institute, St. Joseph's Health Centre, London, Ontario, Canada Department of Physiology, University of Western Ontario, London, Ontario, Canada Department of Medicine, University of Western Ontario, London, Ontario, Canada Department of Paediatrics, University of Western Ontario, London, Ontario, CanadaLawson Research Institute, St. Joseph's Health Centre, 268 Grosvenor Street, London, Ontario, Canada, N6A 4V2. tel: (519) 646-6100 × 4716, fax: (519) 646-6110,Search for more papers by this author P. De Los Rios, P. De Los Rios Lawson Research Institute, St. Joseph's Health Centre, London, Ontario, Canada Department of Physiology, University of Western Ontario, London, Ontario, CanadaSearch for more papers by this authorD.J. Hill, Corresponding Author D.J. Hill [email protected] Lawson Research Institute, St. Joseph's Health Centre, London, Ontario, Canada Department of Physiology, University of Western Ontario, London, Ontario, Canada Department of Medicine, University of Western Ontario, London, Ontario, Canada Department of Paediatrics, University of Western Ontario, London, Ontario, CanadaLawson Research Institute, St. Joseph's Health Centre, 268 Grosvenor Street, London, Ontario, Canada, N6A 4V2. tel: (519) 646-6100 × 4716, fax: (519) 646-6110,Search for more papers by this author First published: 24 March 2000 https://doi.org/10.1002/(SICI)1097-4652(200005)183:2 3.0.CO;2-SCitations: 16AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Insulin-like growth factor-II (IGF-II) is an autocrine modulator of epiphyseal chondrogenesis in the fetus. The cellular availability of IGFs are influenced by the IGF-binding proteins (IGFBPs). In this study, we investigated the control of expression and release of IGFBPs from isolated epiphyseal growth plate chondrocytes from the ovine fetus by hormones and growth factors implicated in the chondrogenic process. Chondrocytes were isolated from the proliferative zone of the fetal ovine proximal tibial growth plate and maintained in monolayer culture at early passage number. Culture media conditioned by chondrocytes under basal conditions released IGFBPs of 24, 34, and 29 kDa, and a less abundant species of 39–43 kDa that were identified immunologically as IGFBP-4, IGFBP-2, IGFBP-5, and IGFBP-3, respectively. Messenger RNAs encoding each species were identified by Northern blot analysis within chondrocytes, as was mRNA encoding IGFBP-6. Exposure to IGF-I or IGF-II (13 or 26 nM) caused an increase in expression and release of IGFBP-3. The release of IGFBP-2 and IGFBP-5 were also potentiated without changes to steady state mRNA, and for IGFBP-5 this was due in part to a release from the cell membrane in the presence of IGF-II. Insulin (16.7 or 167 nM) selectively increased mRNA and the release of IGFBP-3, while cortisol (1 or 5 μM) inhibited both mRNA and release of IGFBP-2 and IGFBP-5. Transforming growth factor-β1 (TGF-β1) (0.1 or 0.2 nM) increased the expression and release of IGFBP-3, and caused an increase in mRNAs encoding IGFBP-2 and IGFBP-5. Neither growth hormone (GH), fibroblast growth factor-2, nor thyroxine (T4) had any effect on IGFBP expression or release. The results suggest that IGFBP expression and release within the developing growth plate can be modulated by IGF-II and other trophic factors, thus controlling IGF availability and action. J. Cell. Physiol. 183:172–181, 2000. © 2000 Wiley-Liss, Inc. LITERATURE CITED Bach LA, Thotakura NR, Rechler MM. 1992. Human insulin-like growth factor binding protein-6 is O-glycosylated. Biochem Biophys Res Commun 186: 301–307. Bale LK, Conover CA. 1992. Regulation of insulin-like growth factor binding protein-3 messenger ribonucleic acid expression by insulin-like growth factor I. Endocrinology 131: 608–614. Camacho-Hubner C, Busby WH, McCusker RH, Wright G, Clemmons DR. 1992. Identification of the forms of insulin-like growth factor-binding proteins produced by human fibroblasts and the mechanisms that regulate their secretion. J Biol Chem 267: 11949–11956. Chen TL, Chang LY, Bates RL, Perlman AJ. 1991. Dexamethasone and 1,25-dihydroxyvitamin D3 modulation of insulin-like growth factor-binding proteins in rat osteoblast-like cell cultures. Endocrinology 128: 73–80. Coffin JD, Florkiewicz RZ, Neumann J, Mort Hopkins T, Dorn GW II, Lightfoot P, German R, Howles PN, Kier A, OToole BA. 1995. Abnormal bone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol Biol Cell 6: 1861–1873. Conover CA. 1992. Potentiation of insulin-like growth factor (IGF) action by IGF-binding protein-3: studies of underlying mechanism. Endocrinology 130: 3191–3199. Conover CA, Kiefer MC. 1993. Regulation and biological effect of endogenous insulin-like growth factor binding protein-5 in human osteoblastic cells. J Clin Endocrinol Metab 76: 1153–1159. Conover CA, Liu F, Powell D, Rosenfeld RG, Hintz RL. 1989. Insulin-like growth factor binding proteins from cultured human fibroblasts: characterization and hormonal regulation. J Clin Invest 83: 852–859. De Chiara TM, Efstratiadis A, Robertson EJ. 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345: 78–80. De los Rios P, Hill DJ. 1999. Cellular localization and expression of insulin-like growth factors (IGFs) and IGF binding proteins within epiphyseal growth plate of the ovine fetus: possible functional implications. Can J Physiol Pharmacol 77: 235–249. Delhanty PJD, Han VKM. 1992. The characterization and expression of ovine insulin-like growth factor binding protein-2 (IGFBP-2). J Mol Endocrinol 9: 31–38. Erondu NE, Toland B, Boes M, Dake B, Moser DR, Bar RS. 1997. Bovine insulin-like growth factor binding protein-3: organization of the chromosomal gene and functional analysis of its promoter. Endocrinology 138: 2856–2862. Farquharson C, Law AS, Seawright E, Burt DW, Whitehead CC. 1996. The expression of transforming growth factor-beta by cultured chick growth plate chondrocytes: differential regulation by 1,25-dihydroxyvitamin D3. J Endocrinol 149: 277–285. Fowlkes J, Freemark M. 1992. Evidence for a novel insulin-like growth factor (IGF)-dependent protease regulating IGF-binding protein-4 in dermal fibroblasts. Endocrinology 131: 2071–2076. Gabbitas B, Pash JM, Delany AM, Canalis E. 1996. Cortisol inhibits the synthesis of insulin-like growth factor-binding protein-5 in bone cell cultures by transcriptional mechanisms. J Biol Chem 271: 9033–9038. Han VKM, Lauder JM, D'Ercole AJ. 1988. Rat astroglial somatomedin/insulin-like growth factor binding proteins: characterization and evidence of biologic function. J Neurosci 8: 3135–3143. Han VKM, Matsell DG, Delhanty PJD, Hill DJ, Shimasaki S, Nygard K. 1996. IGF binding protein mRNAs in the human fetus: tissue and cellular distribution of developmental expression. Horm Res 45: 160–166. Hill DJ. 1981. Effects of cortisol on cell proliferation and proteoglycan synthesis and degradation in cartilage zones of the calf costochondral growth plate in vitro with and without rat plasma somatomedin activity. J Endocrinol 88: 425–435. Hill DJ, De Sousa D. 1990. Insulin is a mitogen for isolated epiphyseal growth plate chondrocytes from the fetal lamb. Endocrinology 126: 2661–2670. Hill DJ, Logan A. 1992a. Peptide growth factors and their interactions during chondrogenesis. Rec Prog Growth Factor Res 4: 45–68. Hill DJ, Logan A. 1992b. Interactions of peptide growth factors during DNA synthesis in isolated ovine fetal growth plate chondrocytes. Growth Regul 2: 122–132. Hill DJ, Logan A, McGarry M, DeSousa D. 1992. Control of protein and matrix-molecule synthesis in isolated ovine fetal growth-plate chondrocytes by the interactions of basic fibroblast growth factor, insulin-like growth factors-I and -II, insulin and transforming growth factor-β1. J Endocrinol 133: 363–373. Hogg J, Hill DJ, Han VKM. 1994. The ontogeny of insulin-like growth factor (IGF) and IGF binding protein gene expression in the rat pancreas. J Mol Endocrinol 13: 49–58. Horner A, Kemp P, Summers C, Bord S, Bishop NJ, Kelsall AW, Coleman N, Compston JE. 1998. Expression and distribution of transforming growth factor-beta isoforms and their signaling receptors in growing human bone. Bone 23: 95–102. Horton WE. 1997. Fibroblast growth factor receptor 3 and the human chondroplasias. Curr Opin Pediatr 9: 437–442. Horton WE, Higginbotham JD, Chandrasekhar S. 1989. Transforming growth factor-beta and fibroblast growth factor act synergistically to inhibit collagen II synthesis through a mechanism involving regulatory DNA sequences. J Cell Physiol 141: 8–15. Hossenlopp P, Seurin D, Segovia-Quinson B, Hardouin S, Binoux M. 1986. Analysis of serum insulin-like growth factor binding proteins using Western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal Biochem 154: 138–143. Inoue H, Kato Y, Iwamoto M, Hiraki Y, Sakuda M, Suzuki F. 1989. Stimulation of cartilage-matrix proteoglycan synthesis by morphologically transformed chondrocytes grown in the presence of fibroblast growth factor and transforming growth factor β. J Cell Physiol 138: 329–337. Itagane Y, Inada H, Fujita K, Isshiki G. 1991. Interactions between steroid hormones and insulin-like growth factor-I in rabbit chondrocytes. Endocrinology 128: 1419–1424. Ito J, Natale D, Wallen L, Hayatsu J, Nygard K, Han VKM. 1995. Cloning and development of ovine IGFBP-6. Prog 77th Ann Meeting Endocrine Soc, Washington DC. Abstract 231: 170. Ito J, Yam H, Wallen L, Nygard K, Han VKM. 1996. Cloning and developmental expression of ovine IGFBP-5. Prog 78th Ann Meeting Endocr Soc, San Francisco, CA. Abstract 71: 772. Jones JI, Clemmons DR. 1995. Insulin-like growth factor and their binding proteins: biological actions. Endocr Rev 16: 3–34. Kiefer MC, Schmid C, Waldvogel M, Schlapfer I, Futo E, Masiarz FK, Green K, Barr PJ, Zapf J. 1992. Characterization of recombinant human insulin-like growth factor binding proteins 4, 5, and 6 produced in yeast. J Biol Chem 267: 12692–12699. Kronenberg HM, Lanske B, Kovacs CS, Chung UI, Lee K, Segre GV, Schipani E, Juppner H. 1998. Rec Prog Horm Res 53: 283–301. Li J, Saunders JC, Fowden AL, Dauncey MJ, Gilmour RS. 1998. Transcriptional regulation of insulin-like growth factor-II gene expression by cortisol in fetal sheep during late gestation. J Biol Chem 273: 10586–10593. Lowry OH, Rosebrough NJ, Farr AC, Randall RJ. 1951. Protein measurement with the folin phenol reagent. J Biol Chem 193: 265–275. Lui J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75: 59–72. Martin JL, Ballesteros M, Baxter RC. 1992. Insulin-like growth factor-I (IGF-I) and transforming growth factor-β1 release IGF-binding protein-3 from human fibroblasts by different mechanisms. Endocrinology 131: 1703–1710. Matsunaga S, Yamamoto T, Fukumura K. 1999. Temporal and spatial expressions of transforming growth factor-betas and their receptors in epiphyseal growth plate. Int J Oncol 14: 1063–1067. Oh Y, Muller HL, Pham H, Lamson G, Rosenfeld RG. 1992. Non-receptor mediated, post-transcriptional regulation of insulin-like growth factor binding protein (IGFBP)-3 in Hs578T human breast cancer cells. Endocrinology 131: 3123–3125. O'Keefe RJ, Puzas JE, Brand JS, Rosier RN. 1988. Effects of transforming growth factor-β on DNA synthesis by growth plate chondrocytes: modulation by factors present in serum. Calcif Tissue Int 43: 353–358. Pedrozo HA, Schwartz Z, Gomez R, Ornoy A, Sheng X, Dallas SL, Bonewald LF, Dean DD, Boyan BD. 1998. Growth plate chondrocytes store latent transforming growth factor (TGF)-beta 1 in their matrix through latent TGF-beta 1 binding protein-1. J Cell Physiol 177: 343–354. Pedrozo HA, Boyan BD, Mazock J, Dean DD, Gomez R, Schwartz Z. 1999. TGFbeta1 regulates 25-hydroxyvitamin D3 1 alpha- and 24-hydroxylase activity in cultured growth plate chondrocytes in a maturation-dependent manner. Calcif Tissue Int 64: 50–56. Peterson GL. 1983. Determination of total protein. Methods Enzymol 91: 95–119. Phillips ID, Delhanty PJD, Hill DJ, Han VKM. 1991. Ontogeny of insulin-like growth factor binding protein-1 (IGFBP-1) mRNA expression in sheep. J Endocrinol 129[Suppl]: 209. Phillips ID, Becks GP, Wang JF, Han VKM, Hill DJ. 1994. Hormonal regulation and biological actions of insulin-like growth factor binding proteins in isolated ovine thyroid follicles. Endocrinology 134: 1238–1246. Sunic D, Belford DA, McNeil JD, Wiebkin OW. 1995. Insulin-like growth factor binding proteins (IGF-BPs) in bovine articular and ovine growth-plate chondrocyte cultures: their regulation by IGFs and modulation of proteoglycan synthesis. Biochem Biophys Acta 1245: 43–48. Villafuerte BC, Zhao W, Herington AC, Saffery R, Phillips LS. 1997. Identification of an insulin-response element in the rat insulin-like growth factor-binding protein-3 -gene. J Biol Chem 272: 5024–5030. Walter HJ, Berry M, Hill DJ, Cwyfan-Hughes S, Holly J, Logan A. 1999. Distinct sites of insulin-like growth factor (IGF)-II expression and localisation in lesioned rat brain: Possible roles of IGF binding proteins in mediating IGF-II action. Endocrinology 140: 5209–532. Wang E, Wang J, Chin E, Zhou J, Bondy CA. 1995. Cellular patterns of insulin-like growth factor system gene expression in murine chondrogenesis and osteogenesis. Endocrinology 136: 2741–2751. Citing Literature Volume183, Issue2May 2000Pages 172-181 ReferencesRelatedInformation