Cellular localization and expression of insulin-like growth factors (IGFS) and IGF binding proteins within the epiphyseal growth plate of the ovine fetus: Possible functional implications

Canadian Journal of Physiology and Pharmacology

Volumn 77, Issue 4, 1999, Pages 235-249

  De Los Rios, P ^a,b   Hill, D J ^b  

^a LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Cartilage; Chondrocyte; Epiphyseal growth plate; Insulin like growth factor; Insulin like growth factor binding protein

Indexed keywords

DNA; MESSENGER RNA; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN BINDING PROTEIN 6;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CARTILAGE CELL; CELLULAR DISTRIBUTION; CHONDROGENESIS; CONTROLLED STUDY; DNA SYNTHESIS; EPIPHYSIS PLATE; FEMALE; GROWTH PLATE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHEEP;

EID: 0032859669     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/y99-015     Document Type: Article

References (63)

1. Baker, J., Liu, J.-P., Robertson, E.J., and Efstratiadis, A. 1993. Role of insulin-like growth factors in embryonic and postnatal growth. Cell, 75: 73-82.
2. Bautista, C.M., Baylink, D.J., and Mohan, S. 1991. Isolation of a novel insulin-like growth factor (IGF) binding protein from human bone: a potential candidate for fixing IGF-11 in human bone. Biochem. Biophys. Res. Commun. 176: 756-763.
3. Bhaumick, B. 1993. Insulin-like growth factor (IGF I) binding proteins and insulinlike growth factor secretion by cultured chondrocyte cells: identification, characterization and ontogeny during cell differentiation. Regul. Pept. 48: 113-122.
4. Blum, W.F., Jenne, E.W., Reppin, J.F., Kietzmann, K., Ranke, M.B., and Bierich, J.R. 1989. Insulin-like growth factor I (IGF-I)-binding protein complex is a better mitogen than free IGF-I. Endocrinology, 125: 766-772.
5. Bohme, K., Conscience-Egli, M., Tschan, T., Winterhalter, K.H., and Bruckner, P. 1992. Induction of proliferation or hypertrophy of chondrocytes in serum-free culture: the role of insulin-like growth factor-1, insulin, or thyroxine. J. Cell Biol. 116: 1035-1042.
6. Bourner, M.J., Busby, W.H., Jr., Siegel, N.R., Krivi, G.G., McCusker, R.H., and Clemmons, D.R. 1992. Cloning and sequence determination of bovine insulin-like growth factor binding protein-2 (IGFBP-2): comparison of its structural and functional properties. J. Cell. Biochem. 48: 215-226.
7. Brinkman, A., Groffen, C., Kortleve, D.J., van Kessel, A.G., and Drop, L.S. 1988. Isolation and characterization of a cDNA encoding the low molecular weight insulin-like growth factor binding protein (IBP-1). EMBO J. 7: 2417-2423.
8. Burch, W.M., Correa, J., Shively, J.E., and Powell, D.R. 1990. The 25-kilodalton insulin-like growth factor (IGF)-binding protein inhibits both basal and IGF-1 mediated growth of chick embryo pelvic cartilage in vitro. J. Clin. Endocrinol. Metab. 70: 173-180.
9. Camacho-Hubner, C., Busby, W.H., McCusker, R.H., Wright, G., and Clemmons, D.R. 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.
10. Carr, J.M., Owens, J.A., Grant, P.A., Walton, P.E., Owens, P.C., and Wallace, J.C. 1995. Circulating insulin-like growth factors (IGFs), IGF-binding proteins (IGFBPs) and tissue mRNA levels of IGFBP-2 and IGFBP-4 in the ovine fetus. J. Endocrinol. 145: 545-557.
11. Chomczynski, P., and Sacchi, N. 1987. Single step method of RNA isolation by acid guanidium thiocyanate - phenol - chloroform extraction. Anal. Biochem. 162: 156-159.
12. Clemmons, D.R. 1991. Insulin-like growth factor binding proteins. In Insulin-like growth factors: molecular and cellular aspects. Vol. 1. Edited by D. LeRoith. CRC Press, Boca Raton, Fla. pp. 151-179.
13. Conover, C.A., and Kiefer, M.C. 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.
14. Conover, C.A., Ronk, M., Lombana, F., and Powell, D.R. 1990. Structural and biological characterization of bovine insulin-like growth factor binding protein-3. Endocrinology, 127: 2795-2803.
15. DeChiara, T.M., Efstratiadis, A., and Robertson, E.J. 1990. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature (London), 345: 78-80.
16. DeChiara, T.M., Efstratiadis, A., and Robertson, E.J. 1991. Paternal imprinting of the mouse insulin-like growth factor II gene. Cell, 64: 849-859.
17. DeMellow, J.S.M., and Baxter, R.C. 1988. Growth hormone-dependent insulin-like growth factor (IGF) binding protein both inhibits and potentiates IGF-I-stimulated DNA synthesis in human skin fibroblasts. Biochem. Biophys. Res. Commun. 156: 199-204.
18. Delhanty, P.J.D., and Han, V.K.M. 1992. The characterization and expression of ovine insulin-like growth factor binding protein-2 (IGFBP-2). J. Mol. Endocrinol. 9: 31-38.
19. Delhanty, P.J., and Han, V.K.M. 1993. The expression of insulin-like growth factor (IGF)-binding protein-2 and IGF-II genes in the tissues of the developing ovine fetus. Endocrinology, 132: 41-52.
20. Duan, C., and Clemmons, D.R. 1998. Differential expression and biological effects of insulin-like growth factor-binding protein-4 and -5 in vascular smooth muscle cells. J. Biol. Chem. 273: 16836-16842.
21. Francis, G.L., Ross, M., Ballard, F.J., Milner, S.J., Senn, C., McNeil, K.A., Wallace, J.C., King, R., and Wells, J.R.E. 1992. Novel recombinant fusion protein analogues of insulin-like growth factor (IGF)-1 indicate the relative importance of IGF-binding protein and receptor binding for enhanced biological activity. J. Mol. Endocrinol. 8: 213-223.
22. Froger-Gaillard, B., Hossenlopp, P., Adolphe, M., and Binoux, M. 1989. Production of insulin-like growth factors and their binding proteins by rabbit articular chondrocytes: relationships with cell multiplication. Endocrinology, 124: 2365-2372.
23. Hahnel, A., and Schultz, G.A. 1994. Insulin-like growth factor binding proteins are transcribed by preimplantation mouse embryos. Endocrinology, 134: 1956-1959.
24. Han, V.K.M., D'Ercole, A.J., and Lund, P.K. 1987. Cellular localization of somatomedin (insulin-like growth factor) messenger RNA in the human fetus. Science (Washington, D.C.), 236: 193-197.
25. Han, V.K.M., Lund, P.K., Lee, D.C., and D'Ercole, A.J. 1988. Expression of somatomedin/insulin-like growth factor messenger ribonucleic acids in the human fetus: identification, characterization, and tissue distribution. J. Clin. Endocrinol. Metab. 66: 422-429.
26. Han, V.K.M., Lu, F., Bassett, N., Yang, K.P., Delhanty, P.J., and Challis, J.R.G. 1992. Insulin-like growth factor-II (IGF-II) messenger ribonucleic acid is expressed in steroidogenic cells of the developing ovine adrenal gland: evidence of an autocrine/paracrine role for IGF-II. Endocrinology, 131: 3100-3109.
27. Harvey, M.B., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A., and Watson, A.J. 1995. Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryos coculture. Biol. Reprod. 53: 530-538.
28. Hill, D.J. 1990. Relative abundance and molecular size of immunoreactive insulin-like growth factors I and II in human fetal tissues. Early Hum. Dev. 21: 49-58.
29. Hill, D.J., and De Sousa, D. 1990. Insulin is a mitogen for isolated epiphyseal growth plate chondrocytes from the fetal lamb. Endocrinology, 126: 2661-2670.
30. Hill, D.J., and Logan, A. 1992. Interactions of peptide growth factors during DNA synthesis in isolated ovine fetal growth plate chondrocytes. Growth Regul. 2: 122-132.
31. Hill, D.J., Logan, A., McGarry, M., and De Sousa, 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-β. J. Endocrinol. 133: 363-373.
32. Hogg, J., Han, V.K.M., Clemmons, D.R., and Hill, D.J. 1993. Interactions of glucose, insulin-like growth factors (IGFs) and IGF binding proteins in the regulation of DNA synthesis by isolated fetal rat islets of Langerhans. J. Endocrinol. 138: 401-412.
33. Hunziker, E.B., Wagner, J., and Zapf, J. 1994. Differential effects of insulin-like growth factor I and growth hormone on developmental stages of rat growth plate chondrocytes in vivo. J. Clin. Invest. 93: 1078-1086.
34. Hsu, S., Raine, L., and Fanger, H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures. J. Histochem. Cytochem. 29: 577-580.
35. Ito, J., Natale, D., Wallen, L., Hayatsu, J., Nygard, K., and Han, V.K.M. 1995. Cloning and development of ovine IGFBP-6. Program of the 77th Annual Meeting of the Endocrine Society, Washington, D.C. The Endocrine Society Press, Bethesda, Md. Abstr. 231, p. 170.
36. Ito, J., Yam, H., Wallen, L., Nygard, K., and Han, V.K.M. 1996. Cloning and developmental expression of ovine IGFBP-5. Program of the 78th Annual Meeting of the Endocrine Society, San Francisco, Calif. The Endocrine Society, Bethesda, Md. Abstr. 71, p. 772.
37. Jones, A. Gockerman, A., Busby, W.H.J., Camacho Hubner, C., and Clemmons, D.R. 1993. Extracellular matrix contains insulin-like growth factor binding protein-5: potentiation of the effects of IGF-I. J. Cell Biol. 121: 679-687.
38. Jones, J.I., and Clemmons, D.R. 1995. Insulin-like growth factor and their binding proteins: biological actions. Endocrine Rev. 16: 3-34.
39. Kiefer, M.C., Schmid, C., Waldvogel, M., Schlapfer, L., Futo, E., Masiarz, F.K., Green, K., Barr, P.J., and 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.
40. Lui, J.-P., Baker, J., Perkins, A.S., Robertson, E.J., and Efstratiadis, A. 1993. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type I IGF receptor (Igf-1r). Cell, 75: 59-72.
41. Lund, P.K., Moats-Staats, B.M., Hynes, M.A., Simmons, J.G., Jansen, M., D'Ercole, A.J., and Wyk, J.J. 1986. Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. J. Biol. Chem. 261: 14539-14544.
42. Mohan, S., Nakao, Y., Honda, Y., Landale, E., Leser, V., Dony, C., Lang, K., and Baylink, D.J. 1995. Studies on the mechanisms by which insulin-like growth factor (IGF) binding protein-4 (IGFBP-4) and IGFBP-5 modulate IGF actions in bone cells. J. Biol. Chem. 270: 20424-20431.
43. Morales, T.I. 1997. The role and content of endogenous insulin-like growth factor-binding proteins in bovine articular cartilage. Arch. Biochem. Biophys. 343: 164-172.
44. Moser, D.R., Lowe, W.L., Jr., Dake, B.L., Booth, B.A., Boes, M., Clemmons, D.R., and Bar, R.S. 1992. Endothelial cells express insulin-like growth factor-binding proteins 2 to 6. Mol. Endocrinol. 6: 1805-1814.
45. Nickersoa, T., Huynh, H., and Pollak, M. 1997. Insulin-like growth factor binding protein-3 induces apoptosis in MCF7 breast cancer cells. Biochem. Biophys. Res. Commun. 237: 690-693.
46. Ohlsson, C., Nilsson, A., Isaksson, O.G.P., and Lindahl, A. 1992. Effect of growth hormone and insulin-like growth factor-I on DNA synthesis and matrix production in rat epiphyseal chondrocytes in monolayer culture. J. Endocrinol. 133: 291-300.
47. Olney, R.C., Smith, R.L., Kee, Y., and Wilson, D.M. 1993. Production and hormonal regulation of insulin-like growth factor binding proteins in bovine chondrocytes. Endocrinology, 133: 563-570.
48. Petrik, J., Arany, E., McDonald, T.J., and Hill, D.J. 1998. Apoptosis in the pancreatic islet cells of the neonatal rat is associated with a reduced expression of insulin-like growth factor-II which may act as a survival factor. Endocrinology, 139: 2994-3004.
49. Phillips, I.D., Delhanty, P.J.D., Hill, D.J., and Han, V.K.M. 1991. Ontogeny of insulin-like growth factor binding protein-1 (IGFBP-1) mRNA expression in sheep. J. Endocrinol. 129(Suppl.): 209.
50. Phillips, I.D., Becks, G.P., Wang, J.F., Han, V.K.M., and Hill, D.J. 1994. Hormonal regulation and biological actions of insulin-like growth factor binding proteins in isolated ovine thyroid follicles. Endocrinology, 134: 1238-1246.
51. Rajah, R., Valentinis, B., and Cohen, P. 1997. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-beta-1 on programmed cell death through a p53-and IGF-independent mechanism. J. Biol. Chem. 272: 12181-12188.
52. Schiltz, P.M., Mohan, S., and Baylink, D.J. 1993. Insulin-like growth factor-4 inhibits both basal and IGF-mediated chick pelvic cartilage growth in vitro. J. Bone Miner. Res. 8: 391-402.
53. Shimasaki, S., and Ling, N. 1991. Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1, -2, -3, -4, -5 and -6). Prog. Growth Factor Res. 3: 243-266.
54. Shimasaki, S., Shimonaka, M., Zhang, H.P., and Ling, N. 1991. Identification of five different insulin-like growth factor binding proteins (IGFBPs) from adult rat serum and molecular cloning of novel IGFBP-5 in rat and human. J. Biol. Chem. 266: 10646-10653.
55. Shinar, D.M., Endo, N., Halperin, D., Rodan, G.A., and Weinreb, D. 1993. Differential expression of insulin-like growth factor-I (IGF-I) and IGF-II messenger ribonucleic acid in growing rat bone. Endocrinology, 132: 1158-1167.
56. Spratt, S.K., Tatsuno, G.P., and Sommer, A. 1991. Cloning and characterization of bovine insulin-like growth factor binding protein-3 (bIGFBP-3). Biochem. Biophys. Res. Commun. 177: 1025-1032.
57. Sunic, D., Belford, D.A., McNeil, J.D., and Wiebkin, O.W. 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.
58. Takigawa, M., Okawa, T., Pan, H., Aoki, C., Takahashi, K., Zue, J., Suzuki, F., and Kinoshita, A. 1997. Insulin-like growth factors I and II are autocrine factors in stimulating proteoglycan synthesis, a marker of differentiated chondrocytes, acting through their respective receptors on a clonal human chondrosarcoma-derived chondrocyte line, HCS-2/8. Endocrinology, 138: 4390-4400.
59. Valentinis, B., Bhala, A., DeAngelis, T., Baserga, R., and Cohen, P. 1995. The human insulin-like growth factor (IGF) binding protein-3 inhibits the growth of fibroblasts with a targeted disruption of the IGF-I receptor gene. Mol. Endocrinol. 9: 361-367.
60. Vetter, U., Zapf, J., Heit, W., Helbing, G., Heinze, E., Froesch, E.R., and Teller, W.M. 1986. Human fetal and adult chondrocytes. Effect of insulin like growth factors I and II, insulin, and growth hormone on clonal growth. J. Clin. Invest. 77: 1903-1908.
61. Wang, E., Wang, J., Chin, E., Zhou, J., and Bondy, C.A. 1995. Cellular patterns of insulin-like growth factor system gene expression in murine chondrogenesis and osteogenesis. Endocrinology, 136: 2741-2751.
62. Watson, A.J., Watson, P.H., Arcellana-Panlilio, M., Warnes, D., Walker, S.K., Schultz, G.A., Armstrong, D.T., and Seamark, R.F. 1994. A growth factor phenotype map for ovine preimplantation development. Biol. Reprod. 50: 725-733.
63. Wood, W.I., Cachianes, G., Henzel, W.J., Winslow, G.A., Spencer, S.A., Hellmiss, R., Martin, J.L., and Baxter, R.C. 1988. Cloning and expression of the growth hormone dependent insulin-like growth factor-binding protein. Mol. Endocrinol. 2: 1176-1185.