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Effect of protein restriction on the messenger RNA contents of bone-matrix proteins, insulin-like growth factors and insulin-like growth factor binding proteins in femur of ovariectomized rats

Published online by Cambridge University Press:  09 March 2007

Yusuke Higashi
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biological Chemistry, Division of Agriculture and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
Asako Takenaka
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biological Chemistry, Division of Agriculture and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
Shin-Ichiro Takahashi
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biological Chemistry, Division of Agriculture and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
Tadashi Noguchi
Affiliation:
Laboratory of Nutritional Biochemistry, Department of Applied Biological Chemistry, Division of Agriculture and Life Sciences, University of Tokyo, Bunkyo-ku, Tokyo 113, Japan
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Abstract

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It has been reported that loss of ovarian oestrogen after menopause or by ovariectomy causes osteoporosis. In order to elucidate the effect of dietary protein restriction on bone metabolism after ovariectomy, we fed ovariectomized young female rats on a casein-based diet (50g/kg diet (protein restriction) or 200g/kg diet (control)) for 3 weeks and measured mRNA contents of bone-matrix proteins such as osteocalcin, osteopontin and α1 type I collagen, insulin-like growth factors (IGF) and IGF-binding proteins (IGFBP) in femur. Ovariectomy decreased the weight of fat-free dry bone and increased urinary excretion of pyridinium cross-links significantly, although dietary protein restriction did not affect them. Neither ovariectomy nor protein restriction affected the content of mRNA of osteopontin and osteocalcin; however, ovariectomy increased and protein restriction extensively decreased the α1 type I collagen mRNA content in bone tissues. Ovariectomy increased IGF-I mRNA only in the rats fed on the control diet. Conversely, protein rest riction increased and ovariectomy decreased the IGF-II mRNA content in femur. Furthermore, the contents of IGFBP-2, IGFBP-4 and IGFBP-5 mRNA increased, but the content of IGFBP-3 mRNA decreased in femur of the rats fed on the protein-restricted diet. In particular, ovariectomy decreased the IGFBP-2 mRNA content in the protein-restricted rats and the IGFBP-6 mRNA content in the rats fed on the control diet. These results clearly show that the mRNA for some of the proteins which have been shown to be involved in bone formation are regulated by both quantity of dietary proteins and ovarian hormones.

Type
Effect of protein restriction on rat bone
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

American Institute of Nutrition (1977). Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. Journal of Nuirition 107, 13401348.Google Scholar
Andreas, D. L. & Birnbaum, R. S. (1992). Human osteoblast-derived insulin-like growth factor (IGF) binding protein-5 stimulates osteoblast mitogenesis and potentiates IGF action. Journal of Biological Chemistry 267, 2246722472.CrossRefGoogle Scholar
Baylink, D. J., Finkelman, R. D. & Mohan, S. (1993). Growth factors to stimulate bone formation. Journal of Bone and Mineral Research 8, S565S572.CrossRefGoogle ScholarPubMed
Birnbaum, R. S. & Wiren, K. M. (1994). Changes in insulin-like growth factor-binding protein expression and secretion during the proliferation, differentiation, and mineralization of primary cultures of rat osteoblasts. Endocrinology 135, 223230.CrossRefGoogle ScholarPubMed
Brown, A. L., Chiarotti, L. & Orlowski, C. C. (1989). Nucleotide sequence and expression of a cDNA clone encoding a fetal rat binding protein for insulin-like growth factors. Journal of Biological Chemistry 264, 51485154.CrossRefGoogle ScholarPubMed
Campbell, P. G. & Novak, J. F. (1991). Insulin-like growth factor binding protein (IGFBP) inhibits IGF action on human osteosarcoma cells. Journal of Cellular Physiology 149, 293300.CrossRefGoogle ScholarPubMed
Canalis, E. (1980). Effect of insulin-like growth factor I on DNA and protein synthesis in cultured rat calvaria. Journal of Clinical Investigation 66, 709719.CrossRefGoogle Scholar
Canalis, E., McCarthy, T. & Centrella, M. (1988). Isolation and characterization of insulin-like growth factor I (somatomedin-C) from cultures of fetal rat calvariae. Endocrinology 122, 2227.CrossRefGoogle ScholarPubMed
Canalis, E., Pash, J. & Varghese, S. (1993). Skeletal growth factors. Critical Reviews in Eukaryotic Gene Expression 3, 155166.Google ScholarPubMed
Celeste, A. J., Rosen, V., Buecker, J. L., Wang, E. A. & Wozney, J. M. (1986). Isolation of the human gene for bone gla protein utilizing mouse and rat cDNA clones. EMBO Journal 5, 18851890.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidium thiocyanate–phenol–chloroform extraction. Analytical Biochemistry 162, 156159.CrossRefGoogle Scholar
Christiansen, C., Christiansen, M. S., Larsen, N. E. & Transbol, I. B. (1982). Pathophysiological mechanisms of estrogen effect on bone metabolism. Dose-response relationships in early postmenopausal women. Journal of Clinical Endocrinology and Metabolism 55, 11241130.CrossRefGoogle Scholar
Donovan, S. M., Atilano, L. C., Hintz, R. L., Wilson, D. M. & Rosenfeld, R. G. (1991). Differential regulation of the insulin-like growth factors (IGF-I and -11) and IGF binding proteins during malnutrition in the neonatal rat. Endocrinology 129, 149157.CrossRefGoogle Scholar
Ernst, M., Heath, J. K. & Rodan, G. (1989). Estradiol effects on proliferation, messenger ribonucleic acid for collagen and insulin-like growth factor-I, and parathyroid hormone-stimulated adenylate cyclase activity in osteoblastic cells from calvariae and long bones. Endocrinology 125, 825833.CrossRefGoogle ScholarPubMed
Feyen, J. H. M., Evans, D. B., Binkert, C., Heinlich, G. F., Geisse, S. & Kocher, H. P. (1991). Recombinant human [Cys281] insulin-like growth factor-binding protein 2 inhibits both basal and insulin-like growth factor I-stimulated proliferation and collagen synthesis in fetal rat calvariae. Journal of Biological Chemistry 266, 1946919474.CrossRefGoogle ScholarPubMed
Gallagher, J. C. (1990). The pathogenesis of osteoporosis. Bone and Mineral 9, 215227.CrossRefGoogle ScholarPubMed
Genovese, C., Rowe, D. & Kream, B. (1984). Construction of DNA sequences complementary to rat α1 and α2 collagen mRNA and their use in studying the regulation of type I collagen synthesis by 1,25-dihydroxyvitamin D. Biochemistry 23, 62016216.CrossRefGoogle Scholar
Gray, T. K., Mohan, S., Linkhart, T. A. & Baylink, D. J. (1989). Estradiol stimulates in vitro the secretion of insulin-like growth factors by the clonal osteoblastic cell line, UMR-106. Biochemical and Biophysical Research Communications 158, 407412.CrossRefGoogle Scholar
Horowitz, M. C. (1993). Cytokines and estrogen in bone: anti-osteoporotic effects. Science 260, 626627.CrossRefGoogle ScholarPubMed
Ismail, F., Epstein, S., Fallon, M. D., Thomas, S. B. & Reinhardt, T. A. (1988). Serum bone gla protein and the vitamin D endocrine system in the oophorectomized rat. Endocrinology 122, 624630.CrossRefGoogle ScholarPubMed
Kalu, D. N., Liu, C. C., Hardin, R. R. & Hollis, B. W. (1989). The aged rat model of ovarian hormone deficiency bone loss. Endocrinology 124, 716.CrossRefGoogle ScholarPubMed
Kalu, D. N., Liu, C. C., Salerno, E., Hollis, B., Echon, R. & Ray, M. (1991). Skeletal response of ovariectomized rats to low and high doses of 17β-estradiol. Bone and Mineral 14, 175187.CrossRefGoogle Scholar
Kato, H., Takenaka, A., Miura, Y., Nishiyama, M. & Noguchi, T. (1990). Evidence of introduction by molecular cloning of artificial inverted sequence at the 5' terminus of the sense strand of rat insulin-like growth factor-I cDNA. Agricultural and Biological Chemistry 54, 22252230.Google ScholarPubMed
Lemozy, S., Pucilowska, J. B. & Underwood, L. E. (1994). Reduction of insulin-like growth factor-I (IGF-I) in protein restricted rats is associated with differential regulation of IGF-binding protein messenger ribonucleic acids in liver and kidney, and peptides in liver and serum. Endocrinology 135, 617623.CrossRefGoogle ScholarPubMed
LeRoith, D. & Pimstone, B. L. (1973). Bone metabolism and comparison in the protein-deprived rat. Clinical Science 44, 305319.CrossRefGoogle Scholar
McCarthy, T. L., Centrella, M. & Canalis, E. (1989). Regulatory effects of insulin-like growth factors I and II on bone collagen synthesis in rat calvarial cultures. Endocrinology 124, 301309.CrossRefGoogle Scholar
Manolagas, S. C. & Jilka, R. L. (1992). Cytokines, hematopoiesis, osteoclastogenesis, and estrogens. Calcified Tissue International 50, 199202.CrossRefGoogle ScholarPubMed
Miura, Y., Kato, H. & Noguchi, T. (1992). Effects of dietary proteins on insulin-like growth factor-l (IGF-1) messenger ribonucleic acid content in rat liver. British Journal of Nutrition 67, 257265.CrossRefGoogle Scholar
Mohan, S., Bautista, C. M., Wergedal, J. & Baylink, D. J. (1989). Isolation of an inhibitory insulin-like growth factor (IGF) binding protein from bone cell-conditioned medium: a potential local regulator of IGF action. Proceedings of the National Acadamy of Sciences USA 86, 83388342.CrossRefGoogle ScholarPubMed
Nemeth, G. G., Heydemann, A. & Bolander, M. E. (1989). Isolation and analysis of ribonucleic acids from skeletal tissues. Analytical Biochemistry 183, 301304.CrossRefGoogle ScholarPubMed
Nilsson, A., Ohlsson, C., Isaksson, O. G. P., Lindahl, A. & Isgaard, J.(1994). Hormonal regulation of longitudinal bone growth. European Journal of Clinical Nutrition 48, S150S160.Google ScholarPubMed
Oldberg, A., Franzen, A. & Heinegard, D. (1986). Cloning and sequence analysis of rat bone sialoprotein (osteopontin) cDNA reveals an Arg-Gly-Asp cell-binding sequence. Proceedings of the National Academy of Sciences USA 83, 88198823.CrossRefGoogle ScholarPubMed
Prewitt, T. E., D'Ercole, A. J., Switzer, B. R. & Van Wyk, J. J. (1982). Relationship of serum immunoreactive somatomedin-C to dietary protein and energy in growing rats. Journal of Nutrition 112, 144150.CrossRefGoogle ScholarPubMed
Puissant, C. & Houdebine, L. M. (1990). An improvement of the single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. BioTechniques 8, 148149.Google ScholarPubMed
Robins, S. P. (1982). An enzyme-linked immunoassay for the collagen cross-link pyridinoline. Biochemical Journal 207, 617620.CrossRefGoogle ScholarPubMed
Rosen, C. J., Donahue, L. R. & Hunter, S. J. (1994). Insulin-like growth factors and bone: the osteoporosis connection. Proceedings of the Society for Experimental Biology and Medicine 206, 83102.CrossRefGoogle ScholarPubMed
Rosen, K. M., Lamperti, E. D. & Villa-Komaroff, L. (1990). Optimizing the Northern blot procedure. BioTechniques 8, 398403.Google ScholarPubMed
Sandberg, M., Autio-Harmainen, H. & Vuorio, E. (1988). Localization of the expression of types I, III, and IV collagen, TGF-jβ1 and c-fos genes in developing human calvarial bones. Developmental Biology 130, 324334.CrossRefGoogle ScholarPubMed
Sandberg, M., Tamminen, M., Hirvonen, H., Vuorio, E. & Pihlajaniemi, T. (1989). Expression of mRNAs coding for the α1 chain of type XIII collagen in human fetal tissues: comparison with expression of mRNAs for collagen types I, II, and III. Journal of Cell Biology 109, 13711379.CrossRefGoogle Scholar
Sandberg, M. & Vuorio, E. (1987). Localization of types I, II, and III collagen mRNAs in developing human skeletal tissues by in situ hybridization. Journal of Cell Biology 104, 10771084.CrossRefGoogle ScholarPubMed
Schmid, C., Schlapfer, I., Futo, E., Waldvogel, M., Schwander, J., Zapf, J. & Froesch, E. R. (1992). Triiodothyronine (T3) stimulates insulin-like growth factor (IGF)-l and IGF binding protein (1GFBP)-2 production by rat osteoblasts in vitro. Acta Endocrinologica 126, 467473.Google Scholar
Shimasaki, S., Gao, L., Shimonaka, M. & Ling, N. (1991 a). Isolation and molecular cloning of insulin-like growth factor-binding protein-6. Molecular Endocrinology 5, 938948.CrossRefGoogle ScholarPubMed
Shimasaki, S., Shimonaka, M., Zhang, H.-P. & Ling, N. (1991 b). Identification of five different insulin-like growth factor binding-proteins (IGFBPs) from adult rat serum and molecular cloning of a novel IGFBP-5 in rat plasma. Journal of Biological chemistry 266, 1064610653.CrossRefGoogle Scholar
Shimasaki, S., Uchiyama, F., Shimonaka, M. & Ling, N. (1990). Molecular cloning of the cDNAs encoding a novel insulin-like growth factor binding protein from rat and human. Molecular Endocrinology 4, 14511458.CrossRefGoogle ScholarPubMed
Snedecor, G. W. & Cochran, W. G. (1967). One-way classifications. Analysis of variance. Inspection of all differences between pairs of means. In Statistical Methoris, 6th ed., pp. 271273. Ames, Iowa: Iowa State University Press.Google Scholar
Stracke, H., Schulz, A., Moeller, D., Rossol, S. & Schatz, H. (1984). Effect of growth hormone on osteoblasts and demonstration of somatomedin-C/IGF-I in bone organ culture. Acta Endocrinologica 107, 1624.Google ScholarPubMed
Straus, D. S. & Takemoto, C. D. (1990). Effect of dietary protein deprivation on insulin-like growth factor (1GF)-I and -II, IGF binding protein-2, and serum albumin gene expression in rat. Endocrinology 127, 18491860.CrossRefGoogle Scholar
Takahashi, S., Kajikawa, M., Umezawa, T., Takahashi, S.-I., Kato, H., Miura, Y., Nam, T. J., Noguchi, T. & Naito, H. (1990). Effect of dietary proteins on the plasma immunoreactive insulin-like growth factor-l/somatomedin C concentration in the rat. British Journal of Nutrition 63, 521534.CrossRefGoogle Scholar
Takenaka, A., Hirosawa, M., Mori, M., Yamada, S., Miura, Y., Kato, H., Takahashi, S. I. & Noguchi, T. (1993). Effect of protein nutrition on the mRNA content of insulin-like growth factor-binding protein-1 in liver and kidney of rats. British Journal of Nutrition 69, 7382.CrossRefGoogle ScholarPubMed
Takenaka, A., Miura, Y., Mori, M., Hirosawa, M., Kato, H. & Noguchi, T. (1991). Distribution of messenger RNAs of insulin-like growth factor (IGF)-binding proteins-1 and -3 between parenchymal and nonparenchymal cells in rat liver. Agricultural and Biological Chemistry 55, 11911193.Google Scholar
Tanaka, H., Hirayama, N., Tachikawa, H., Fujimoto, D., Nokokuma, S. & Hasegawa, M. (1993). Measurement of pyridinium cross-links by enzyme-linked immunoassay. Seikagaku 65, 798.Google Scholar
Thiebaud, D., Whang, K., Findlay, D. M., Harker, M. & Martin, T. J. (1990). Insulin-like growth factor I regulates mRNA levels of osteonectin and pro-α1(I)-collagen in clonal preosteoblastic calvarial cells. Journal of Bone and Mineral Research 5, 761767.CrossRefGoogle Scholar
Thissen, J.-P., Underwood, L. E., Maiter, D., Maes, M., Clemmons, D. R. & Ketelslegers, J.-M. (1991). Failure of insulin-like growth factor-l (IGF-I) infusion to promote growth in protein-restricted rats despite normalization of serum IGF-I concentrations. Endocrinology 128, 885890.CrossRefGoogle Scholar
Turner, R. T., Colvard, D. S. & Spelsberg, T. C. (1990). Estrogen inhibition of periosteal bone formation in rat long bones: down-regulation of gene expression for bone matrix proteins. Endocrinology 127, 13461351.CrossRefGoogle ScholarPubMed
Umezawa, T., Ohsawa, Y., Miura, Y., Kato, H. & Noguchi, T. (1991). Effect of protein deprivation on insulin-like growth factor-binding proteins in rats. British Journal of Nutrition 66, 105116.CrossRefGoogle ScholarPubMed
Westerlind, K. C., Wakley, G. K., Evans, G. L. & Turner, R. T. (1993). Estrogen does not increase bone formation in growing rats. Endocrinology 133, 29242934.CrossRefGoogle Scholar
Westerlind, K. C., Wronski, T. J., Evans, G. L. & Turner, R. T. (1994). The effect of long-term ovarian hormone deficiency on transforming growth factor-β and bone matrix protein mRNA expression in rat femora. Biochemical and Biophysical Research Communications 200, 283289.CrossRefGoogle ScholarPubMed
Whitfield, H. J., Bruni, C. B., Frunzio, R., Terrell, J. E., Nissley, S. P. & Rechler, M. M. (1984). Isolation of a cDNA clone encoding rat insulin-like growth factor-II precursor. Nature 312, 277280.CrossRefGoogle ScholarPubMed
Wong, G. L. & Cohn, D. W. (1974). Separation of parathyroid hormone and calcitonin-sensitive cells from non-responsive bone cells. Nafure 252, 713715.Google ScholarPubMed
Wronski, T. J., Cintron, M. & Dann, L. M. (1988 a). Temporal relationship between bone loss and increased bone turnover in ovariectomized rats. Calcified Tissue International 43, 179183.CrossRefGoogle ScholarPubMed
Wronski, T. J., Cintron, M., Doherty, A. L. & Dann, L. M. (1988 b). Estrogen treatment prevents osteopenia and depresses bone turnover in ovariectomized rats. Endocrinology 123, 681686.CrossRefGoogle ScholarPubMed
Wronski, T. J., Lowry, P. L., Walsh, C. C. & Ignaszewski, L. A. (1985). Skeletal alterations in ovariectomized rats. CalciJied Tissue International 37, 324328.CrossRefGoogle ScholarPubMed
Wronski, T. J., Walsh, C. C. & Ignaszewski, L. A. (1986). Histologic evidence for osteopenia and increased bone turnover in ovariectomized rats. Bone 7, 119123.CrossRefGoogle ScholarPubMed
Zhu, X., Ling, N. & Shimasaki, S. (1993). Structural characterization of the rat insulin-like growth factor binding protein-6 gene. Biochemical and Biophysical Research Communications 191, 12371243.CrossRefGoogle ScholarPubMed