Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-13T05:18:04.277Z Has data issue: false hasContentIssue false
  • English
  • Français

Vitamin C and copper interactions in guinea-pigs and a study of collagen cross-links

Published online by Cambridge University Press:  09 March 2007

H Tsuchiya  and
C. J Bates†
H Tsuchiya
Affiliation:
MRC Dunn Nutrition Unit, Downhams Lane, Milton Road, Cambridge CB4 IXJ
C. J Bates†
Affiliation:
MRC Dunn Nutrition Unit, Downhams Lane, Milton Road, Cambridge CB4 IXJ
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The purpose of this study was, first to explore metabolic interactions between Cu and ascorbic acid in guinea-pigs, particularly with respect to any possible disadvantages of high ascorbatein the presence of low Cu intakes, and second, to test the hypothesis that variations in ascorbate and/or Cu status might inhence collagen cross-linking, either by inducing a change in thecross-links: hydroxyproline ratio, or by inducing a change in the pyridinoline: deoxypyridinoline cross-linls ratio. Four matched groups, each of eight male weanliig Dunkin-Hartley guinea-pigs, were maintained on purified diets containing either no added Cu, or 150 mg Cu/kg diet, and either 0·1 g or 30 g ascorbic acid/kg diet. They were then killed 8 weeks later, and the following indices were measured body and organ weights; blood haemoglobin; adrenal ascorbate concentrations; Cu concentrations in plasma, liver and femur; superoxide dismutase (EC 1.15.1.1) activity in whole blood and liver; hydroxyproline, pyridinoline and deoxypyridinoline in femur and in urine. The principal observations were: Cu intake significantly affected blood and tissue Cu concentrations and superoxide dismutase activity; and ascorbic acid intake significantlyaffected adrenal ascorbate levels and the deoxypyridinoline: pyridinoline cross-links ratio, especially in bone (femur). There was evidence of a significant interaction between ascorbateand Cu with respect to adrenal and plasma Cu concentrations, blood superoxide dismutase activityand body weights. We conclude that interactions between ascorbate and Cu at the functional level were present but modest, and that a new and potentially powerful functional index of ascorbate status may exist within the deoxypyridinoline: pyridinoliie collagen cross-link ratio.

Keywords

AscorbateCopperGuinea-pigCollagen
Type
General Nutrition
Information
British Journal of Nutrition , Volume 77 , Issue 2 , February 1997 , pp. 315 - 325
Copyright
Copyright © The Nutrition Society 1997

References

REFERENCES

Bates, C. J. (1979). Vitamin C deficiency in guinea pigs: variable sensitivity of collagen at different sites. International Journal of Vitamin and Nutrition Research 49, 77–86.Google ScholarPubMed
Bates, C. J., Prynne, C. J. & Levene, C. I. (1972). Ascorbate-dependent differences in the hydroxylation of proline and lysine in collagen synthesized by 3T6 fibroblasts in culture. Biochimica et Biophysica Acta 278, 610–616.CrossRefGoogle ScholarPubMed
Bates, C. J., Tsuchiya, H. & Evans, P. H. (1992). A study of whole-body isotope dilution of [14C]ascorbic acid in guinea-pigs with graded ascorbate intakes. British Journal of Nutrition 68, 717–728.CrossRefGoogle ScholarPubMed
Carlton, W. W. & Henderson, W. (1965). Studies in chickens fed a copper-deficient diet supplemented with ascorbic acid, reserpine and diethylstilbestrol. Journal of Nutrition 85, 67–72.CrossRefGoogle ScholarPubMed
Clarke, H. E., Coates, M. E., Eva, J. K., Ford, D. J., Milner, C. K., O'Donaghue, P. N., Scott, P. P. & Ward, R. J. (1977). Dietary standards for laboratory animals: report of the Laboratory Animals Centre Diets Advisory Committee. Laboratory Animals 11, 1–28.CrossRefGoogle ScholarPubMed
DiSilvestro, R. A. (1986). Effects of ascorbic acid and inflammation on ceruloplasmin activity levels in guinea pigs. Nutrition Research 6, 1009–1012.Google Scholar
DiSilvestro, R. A. & Harris, E. D. (1981). A postabsorption effect of L-ascorbic acid on copper metabolism in chicks. Journal of Nutrition 11, 1964–1968.CrossRefGoogle Scholar
Farquharson, C., Duncan, A. & Robins, S. P. (1989). The effects of copper deficiency on the pyridinium crosslinks of mature collagen in the rat skeleton and cardiovascular system. Proceedings of the Society for Experimental Biology and Medicine 192, 166–171.CrossRefGoogle ScholarPubMed
Finley, E. B. & Cerklewski, F. L. (1983). Influence of ascorbic acid supplementation on copper status in young adult men. American Journal of Clinical Nutrition 37, 553–556.CrossRefGoogle ScholarPubMed
Ginter, E., Bobek, P. & Ovecka, M. (1968). Model of chronic hypovitaminosis C in guinea pigs. International Journal of Vitamin and Nutrition Research 38, 104–113.Google ScholarPubMed
Greenfield, H., Briggs, G. M., Watson, R. H. J. & Yudkin, J. (1969). An improved diet for carbohydrate preference studies with rats some criticisms of experimental diets. Proceedings of the Nutrition Society 28, 43A.Google Scholar
Harris, F. D. & Percival, S. S. (1991). A role for ascorbic acid in copper transport. American Journal of Clinical Nutrition 54, 1193S–1197S.CrossRefGoogle ScholarPubMed
Hill, C. H. & Starcher, B. (1965). Effect of reducing agents on copper deficiency in the chick. Journal of Nutrition 185, 271–274.Google Scholar
Hitier, Y. (1976). Repercussions de la carence en acide ascorbique sur la ceruloplasmine et le cuiver tissulaire (Ceruloplasmin and copper levels in plasma, liver and kidneys of the scorbutic guinea-pig). International Journal of Vitamin and Nutrition Research 46, 48–57.Google Scholar
Ho, K. -C. & Pang, C. P. (1989). Automated analysis of urinary hydroxyproline. Clinica Chimica Acta 185, 191–196.Google Scholar
Hunt, C. E. & Carlton, W. W. (1965). Cardiovascular lesions associated with experimental copper deficiency in the rabbit. Journal of Nutrition 87, 385–393.CrossRefGoogle ScholarPubMed
Jacob, R. A., Skala, J. H., Omaye, S. T. & Turnlund, J. R. (1987). Effect of varying ascorbic acid intakes on copper absorption and ceruloplasmin levels of young men. Journal of Nutrition 117, 2109–2115.CrossRefGoogle ScholarPubMed
Johnson, M. A. & Murphy, C. L. (1988). Adverse effects of high dietary iron and ascorbic acid on copper status in copper-deficient and copper-adequate rats. American Journal of Clinical Nutrition 47, 96–101.CrossRefGoogle ScholarPubMed
Kassouny, M. E., Coen, C. H. & Bebok, S. T. (1985). Influence of vitamin C and magnesium on calcium, magnesium and copper contents of guinea pig tissues. International Journal of Vitamin and Nutrition Research 55, 295–300.Google ScholarPubMed
Kim, M., Otsuka, M. & Arakawa, N. (1994). Age-related changes in the pyridinoline content of guinea pig cartilage and Achilles tendon collagen. Journal of Nutrition Science and Vitaminology 40, 95–103.CrossRefGoogle ScholarPubMed
Kivirikko, K. I. & Myllyla, R. (1982). Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. In Methods in Enzymology, vol. 82, pp. 245–304 [Colowick, S. P. and Kaplan, N. O., editors]. New York: Academic Press.Google Scholar
Milne, D. B. & Omaye, S. T. (1980). Effect of vitamin C on copper and iron metabolism in the guinea pig. International Journal of Vitamin and Nutrition Research 50, 301–308.Google Scholar
Milne, D. B., Klevay, L. H. & Hunt, J. R. (1988). Effects of ascorbic acid supplements and a diet marginal in copper on indices of copper nutriture in women. Nutrition Research 8, 865–873.Google Scholar
Milne, D. B., Omaye, S. T. & Amos, W. H. (1981). Effects of ascorbic acid on copper and cholesterol in adult cynomolgus monkeys fed a diet marginal in copper. American Journal of Clinical Nutrition 34, 2389–2393.Google Scholar
Pekiner, B. & Nebioglu, S. (1994). Effect of vitamin C on copper and iron status in men and guinea pigs. Journal of Nutritional Science and Vitaminulogy 40, 401–410.CrossRefGoogle ScholarPubMed
Powers, H. J., Loban, A., Silvers, K. & Gibson, A. T. (1995). Vitamin C at concentrations observed in premature babies inhibits the ferroxidase activity of caeruloplasmin. Free Radical Research 22, 57–65.CrossRefGoogle ScholarPubMed
Robins, S. P. (1994). Biochemical markers for assessing skeletal growth. European Journal of Clinical Nutrition 48, S199–S209.Google Scholar
Robins, S. P., Milne, G. & Stewart, P. (1985). The effects of copper deficiency on the lysine-derived pyridinium crosslinks of rat bone collagen. In Trace Elements in Man and Animals-TEMA 5, pp. 42–45 [Mills, C. F., Bremner, L. and Chesters, J. K., editors]. Aberdeen: Commonwealth Agricultural Bureaux.Google Scholar
Rucker, R. B., Romero-Chapman, N., Wong, T., Lee, J., Steinberg, F. M., McGee, C., Clegg, M. S., Reiser, K.Kosonen, T., Urui-Hare, J. Y., Murphy, J. & Keen, C. L. (1996). Modulation of lysyl oxidase by dietary copper in rats. Journal of Nutrition 126, 51–60.Google Scholar
Silvers, K. M., Gibson, A. T. & Powers, H. J. (1994). High plasma vitamin C concentrations at birth associated with low antioxidant status and poor outcome in premature infants. Archives of Disease in Childhood 71, F40–F44.CrossRefGoogle ScholarPubMed
Smith, C. H. & Bidlack, W. R. (1980). Inter-relationship of dietary ascorbic acid and iron on the tissue distribution of ascorbic acid, iron and copper in female guinea pigs. Journal of Nutrition 110, 1398–1408.CrossRefGoogle Scholar
Starcher, B., Hill, C. H. & Matrone, G. (1964). Importance of dietary copper in the formation of aortic elastin. Journal of Nutrition 82, 318–322.Google Scholar
Tsuchiya, H. & Bates, C. J. (1994). Ascorbic acid deficiency in guinea pigs: contrasting effects of tissue ascorbic acid depletion and of associated inanition on status indices related to collagen and vitamin D. British Journal of Nutrition 72, 745–752.CrossRefGoogle ScholarPubMed
Van Campen, D. & Gross, E. (1968). Influence of ascorbic acid on the absorption of copper by rats. Journal of Nutrition 95, 617–622.CrossRefGoogle ScholarPubMed
Van den Berg, G. J., Yu, S., Lemmens, A. G. & Beynen, A. C. (1994). Dietary ascorbic acid lowers the concentration of soluble copper in the small intestinal lumen of rats. British Journal of Nutrition 71, 701–707.CrossRefGoogle ScholarPubMed
Vuilleumier, J. P. & Keck, E. (1989). Fluorometric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. Journal of Micronutrient Analysis 5, 25–34.Google Scholar
Yeowell, H. N., Walker, L. C., Marshall, M. K., Murad, S. & Pinnell, S. R. (1995). The mRNA and the activity of lysyl hydroxylase are up-regulated by the administration of ascorbate and hydralazine to human skin fibroblasts from a patient with Ehlers-Danlos Syndrome Type VI. Archives of Biochemistry and Biophysics 321, 510–516.CrossRefGoogle ScholarPubMed