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Intestinal β-carotene 15,15′-dioxygenase activity is markedly enhanced in copper-deficient rats fed on high-iron diets and fructose

Published online by Cambridge University Press:  09 March 2007

Alexandrine During*
Affiliation:
Phytonutrients Laboratory, USDA-ARS, Beltsville Human Nutrition Research Center, Beltsville, Maryland 20705, USA
Meira Fields
Affiliation:
Nutrient Requirements and Functions Laboratory, USDA-ARS, Beltsville Human Nutrition Research Center, Beltsville, Maryland 20705, USA
Charles G. Lewis
Affiliation:
Nutrient Requirements and Functions Laboratory, USDA-ARS, Beltsville Human Nutrition Research Center, Beltsville, Maryland 20705, USA
J. Cecil Smith
Affiliation:
Phytonutrients Laboratory, USDA-ARS, Beltsville Human Nutrition Research Center, Beltsville, Maryland 20705, USA
*
*Corresponding author: Dr Alexandrine During, fax +1 301 504 9098, e-mail [email protected]
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Abstract

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The purpose of the present work was to examine effects of the Cu–Fe interaction on intestinal β-carotene 15,15′-dioxygenase activity when a wide range of dietary Fe (deficiency to excess) was used in relation to Cu status of rats. The effect of dietary carbohydrates was also examined since they play a role in the Cu–Fe interaction in vivo. Weanling male Sprague-Dawley rats (n 72) were divided into twelve dietary groups, which were fed on either low-, normal-, or high-Fe levels (0·9, 9·0, and 90·0 mmol Fe/kg diet respectively) combined with Cu-adequate or -deficient levels (0·94 and 0·09 mmol Cu/kg diet respectively) and with starch or fructose in the diets. The data showed that both Fe concentration and β-carotene 15,15′-dioxygenase activity in small intestinal mucosa were enhanced with increasing dietary Fe and with Cu deficiency v. Cu adequacy. Dietary fructose did not aggravate the Fe-enhancement, related to Cu deficiency, in the small intestine; however, fructose increased the intestinal dioxygenase activity in rats fed on normal- or high-Fe diets when compared with starch controls. Thus, the highest intestinal dioxygenase activity associated with the lowest hepatic retinol (total) concentration was found in rats fed on the Cu-deficient, high-Fe, fructose-based diet. Finally, a positive linear relationship was found between the dioxygenase activity and Fe concentration in intestinal mucosa. In conclusion, the data indicate that β-carotene 15,15′-dioxygenase activity requires Fe as cofactor in vivoand the enzyme is modulated by the three dietary components: Cu, Fe, and fructose.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2000

References

Bradford, MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248254.CrossRefGoogle Scholar
Conrad, ME (1993) Regulation of iron absorption. Progress in Clinical and Biological Research 380, 203219.Google ScholarPubMed
Dmitrovskii, AA and Ershov, YuV (1993) Possible participation of free radicals in enzymatic conversion of β-carotene to retinal. Prikladnaya Biokhimiya i Mikrobiologiya 29, 125130.Google Scholar
Dulin, A, Bieri, JG and Smith, JC (1992) Copper deficiency fails to affect vitamin A status. Nutrition Research 12, 13651372.CrossRefGoogle Scholar
Dulin, A, Bieri, JG and Smith, JC (1995) Copper deficiency does not affect conversion of β-carotene to vitamin A in rats. Nutrition Research 15, 589594.CrossRefGoogle Scholar
During, A, Fields, M, Lewis, CH and Smith, JC (1999) β-Carotene 15,15′-dioxygenase activity is responsive to copper and iron concentrations in rat small intestine. Journal of the American College of Nutrition 18, 309315.CrossRefGoogle ScholarPubMed
During, A, Nagao, A, Hoshino, C and Terao, J (1996) Assay of β-carotene 15,15′-dioxygenase activity by reverse phase high-pressure liquid chromatography. Analytical Biochemistry 241, 199205.CrossRefGoogle ScholarPubMed
During, A, Nagao, A and Terao, J (1998) β-Carotene 15,15′-dioxygenase activity and cellular retinol-binding protein type II level are enhanced by dietary unsaturated triacylglycerols in rat intestine. Journal of Nutrition 128, 16141619.CrossRefGoogle Scholar
Fidge, NH, Smith, FR and Goodman, DS (1969) The enzymatic conversion of β-carotene into retinal in hog intestinal mucosa. Biochemical Journal 114, 689694.CrossRefGoogle Scholar
Fields, M, Ferretti, RJ, Reiser, S and Smith, JC (1984) The severity of copper deficiency in rats is determined by the type of dietary carbohydrate. Proceedings of the Society for Experimental Biology and Medicine 175, 530537.CrossRefGoogle ScholarPubMed
Fields, M, Lewis, CG, Lure, MD, Burns, WA and Antholine, WE (1991) The severity of copper deficiency can be ameliorated by deferoxamine. Metabolism 40, 105109.CrossRefGoogle ScholarPubMed
Furr, HC, Clifford, AJ, Smith, LM and Olson, JA (1989) The effect of dietary fatty acid composition on liver retinyl ester (vitamin A ester) composition in the rat. Journal of Nutrition 119, 581585.CrossRefGoogle ScholarPubMed
Goodman, DS and Huang, HS (1965) Biosynthesis of vitamin A with rat intestinal enzymes. Science 149, 879880.CrossRefGoogle ScholarPubMed
Goodman, DS, Huang, HS, Kanai, M and Shiratori, T (1967) The enzymatic conversion of all-trans β-carotene into retinal. Journal of Biological Chemistry 242, 35433554.CrossRefGoogle Scholar
Gronowska-Senger, A and Rupniewska, A (1979) Intake of essential unsaturated fatty acids and vitamin E, and the demand for vitamin A. Bromatologia i Chemia Toksykologiczna 12, 1319.Google Scholar
Hill, AD, Patterson, KY, Veillon, C and Morris, ER (1986) Digestion of biological materials for mineral analyses using a combination of wet and dry ashing. Analytical Chemistry 58, 23402342.CrossRefGoogle Scholar
Livrea, MA, Tesoriere, L, Bongiorno, A, Pintaudi, AM, Ciaccio, M and Riccio, A (1995) Contribution of vitamin A to the oxidation resistance of human low density lipoproteins. Free Radical Biology and Medicine 18, 401409.CrossRefGoogle Scholar
Mordi, RC (1993) Mechanism of β-carotene degradation. Biochemical Journal 292, 310312.CrossRefGoogle ScholarPubMed
Moore, T (1969) Vitamin A and copper. American Journal of Clinical Nutrition 22, 10171018.CrossRefGoogle ScholarPubMed
Nagao, A, During, A, Hoshino, C, Terao, J and Olson, JA (1996) Stoichiometric conversion of all-trans-β-carotene to retinal by pig intestinal extract. Archives of Biochemistry and Biophysics 328, 5763.CrossRefGoogle ScholarPubMed
National Research Council (1985) Guide for the Care and Use of Laboratory Animals, publication 85–23 (rev.). Washington, DC: National Institute of Health.Google Scholar
Olivieri, NF and Brittenham, GM (1997) Iron-chelating therapy and the treatment of thalassemia. Blood 89, 739761.CrossRefGoogle ScholarPubMed
Olson, JA and Hayaishi, O (1965) The enzymatic cleavage of beta-carotene into vitamin A by soluble enzymes of rat liver and intestine. Proceedings of the National Academy of Sciences USA 54, 13641370.CrossRefGoogle ScholarPubMed
Owen, CA (1978) Effects of iron on copper metabolism and copper on iron metabolism in rats. American Journal of Physiology 224, 514518.CrossRefGoogle Scholar
Rachman, F, Conjat, F, Carreau, JP, Bleiberg-Daniel, F and Amedee-Manesme, O (1987) Modification of vitamin A metabolism in rats fed a copper-deficient diet. International Journal for Vitamin and Nutrition Research 57, 247252.Google ScholarPubMed
Ross, AC (1986) Separation and quantification of retinyl esters and retinol by high-performance liquid chromatography. Methods in Enzymology 123, 6874.CrossRefGoogle Scholar
Seaborn, CD, Kiangura, RK, Brusewitz, GH and Stoecker, BJ (1991) Effects of copper and selenium on beta-carotene conversion and bone strength in rats. FASEB Journal 5, A1313.Google Scholar
Singh, H and Cama, HR (1974) Enzymatic cleavage of carotenoids. Biochimica et Biophysica Acta 370, 4961.CrossRefGoogle ScholarPubMed
Sommer, A (1998) Xerophthalmia and vitamin A status. Progress in Retinal and Eye Research 1, 931.CrossRefGoogle Scholar
Swanson, JE and Parker, RS (1993) Effect of iron on liver vitamin A and β-carotene stores in rats fed β-carotene as sole source of vitamin A. FASEB Journal 7, A276.Google Scholar
Swartz, KB, Cox, JM, Sharma, S, Clement, L, Humphrey, J, Gleason, C, Abbey, H, Sehnert, SS and Risby, TH (1997) Possible antioxidant effect of vitamin A supplementation in premature infants. Journal of Pediatric Gastroenterology and Nutrition 25, 408414.Google Scholar
Villard, L and Bates, CJ (1986) Carotene dioxygenase (EC 1.13.11.21) activity in rat intestine: effect of vitamin A deficiency and of pregnancy. British Journal of Nutrition 56, 115122.CrossRefGoogle ScholarPubMed
Vliet van, T, van Vlissingen, MF, van Schaik, F and van den Berg, H (1996) β-Carotene absorption and cleavage in rats is affected by vitamin A concentration in the diet. Journal of Nutrition 126, 499508.CrossRefGoogle Scholar
Vulpe, CD, Kuo, YM, Murphy, TL, Cowley, L, Askwith, C, Libina, N, Gatschier, J and Anderson, GJ (1999) Hephaest, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the SLA mouse. Nature Genetics 21, 195199.CrossRefGoogle ScholarPubMed
Williams, DM, Kennedy, FS and Green, BG (1983) Hepatic iron accumulation in copper deficient rats. British Journal of Nutrition 50, 653660.CrossRefGoogle ScholarPubMed
Yu, J and Wessling-Resnick, M (1998) Influence of copper depletion on iron uptake mediated by SFT, a stimulator of Fe transport. Journal of Biological Chemistry 273, 69096915.CrossRefGoogle ScholarPubMed