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The hepatic retinyl ester hydrolase activity is depressed at the onset of diabetes in BB rats

Published online by Cambridge University Press:  09 March 2007

Min Chen
Affiliation:
Department of Agricultural, Food & Nutritional Science, Division of Gastroenterology, University of Alberta, Edmonton, Canada
Alan B. R. Thomson
Affiliation:
Department of Medicine, Division of Gastroenterology, University of Alberta, Edmonton, Canada
Andrew T. C. Tsin
Affiliation:
Division of Life Sciences, University of Texas at San Antonio, San Antonio, Texas, USA
Tapan K. Basu*
Affiliation:
Department of Agricultural, Food & Nutritional Science, Division of Gastroenterology, University of Alberta, Edmonton, Canada
*
*Corresponding author: Dr Tapan K. Basu, fax +1 780 492 9130, email [email protected]
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Abstract

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Dietary vitamin A as retinyl ester is hydrolysed and re-esterified with long-chain fatty acids in the small intestine. The esterified vitamin A is subsequently stored in the liver, where it is hydrolysed to free retinol to be transported by carrier proteins to the target tissue. A decreased availability of retinol carrier proteins has been suggested to be responsible for affecting metabolic availability of vitamin A in type 1 diabetes. Using BB Wistar rats, the present study was undertaken to examine whether the presence of a hyperglycaemic state modifies retinyl ester hydrolase (REH) activity in the intestine and the liver. At the onset of diabetes, hepatic REH enzymatic activity was significantly (P<0·05) decreased. However, REH activity remained unaffected in the small intestine, including both ileum and jejunum. Diabetes also resulted in decreased plasma and liver concentrations of retinol. An in vitro study was conducted to examine the effect of diabetes on the intestinal uptake of retinyl palmitate. Jejunum and ileum from diabetic and non-diabetic BB rats were incubated with labelled retinyl palmitate at different concentrations ranging from 32 to 256 nmol/l. The uptake of retinyl palmitate was increased in both diabetic and non-diabetic rats together with the increase of substrate concentration. However, no significant difference was observed in the uptake of retinyl palmitate between diabetic and non-diabetic rats. These present results suggest that the depressed hepatic REH activities may contribute to the diabetes-associated metabolic derangement of vitamin A.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2003

References

Azais-Braesco, V, Dodeman, I, Delpal, S, Alexandre-Gouabau, MC, Partier, A, Borel, P & Grolier, P (1995) Vitamin A contained in the lipid droplets of rat liver stellate cells is substrate for acid retinyl ester hydrolase. Biochimica et Biophysica Acta 1259, 271276.CrossRefGoogle ScholarPubMed
Bach, JF (1988) Mechanisms of autoimmunity in insulin-dependent diabetes mellitus. Clinical and Experimental Immunology 72, 18.Google ScholarPubMed
Basu, TK, Tze, WJ & Leichter, J (1989) Serum vitamin A and retinol-binding protein in patients with insulin-dependent diabetes mellitus. American Journal of Clinical Nutrition 50, 329331.CrossRefGoogle ScholarPubMed
Baudon, MA, Ferre, P, Penicaud, L, Maulard, P, Ktorza, A, Castano, L & Girard, J (1989) Normal insulin sensitivity during the phase of glucose intolerance but insulin resistance at the onset of diabetes in the spontaneously diabetic BB rat. Diabetologia 32, 839844.CrossRefGoogle ScholarPubMed
Blomhoff, R, Skrede, B & Norum, KR (1990) Uptake of chylomicron remnant retinyl ester via the low-density lipoprotein receptor: implications for the role of vitamin A as a possible preventive for some forms of cancer. Journal of Internal Medicine 228, 207210.CrossRefGoogle ScholarPubMed
Carr, TP, Andresen, CJ & Rudel, LL (1993) Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts. Clinical Biochemistry 26, 3942.CrossRefGoogle ScholarPubMed
Chen, X, Harrison, EH & Fisher, EA (1997) Molecular cloning of the cDNA for rat hepatic bile salt-dependent cholesteryl ester/retinyl ester hydrolase demonstrates identity with pancreatic carboxylester lipase. Proceeding of the Society of Experimental Biology and Medicine 215, 186191.CrossRefGoogle ScholarPubMed
Cooper, DA, Furr, HC & Olson, JA (1987) Factors influencing the level and interanimal variability of retinyl ester hydrolase activity in rat liver. Journal of Nutrition 117, 20662071.CrossRefGoogle ScholarPubMed
Cooper, DA & Olson, JA (1986) Properties of liver retinyl ester hydrolase in young pigs. Biochimica et Biophysica Acta 884, 251258.CrossRefGoogle ScholarPubMed
Gueli, MC, Nicotra, CM, Pintaudi, AM, Paganini, A, Pandolfo, L, De Leo, G & Di Bella, MA (1991) Retinyl ester hydrolases in retinal pigment epithelium. Archives of Biochemistry and Biophysics 288, 572577.CrossRefGoogle ScholarPubMed
Harrison, EH & Gad, MZ (1989) Hydrolysis of retinyl palmitate by enzymes of rat pancreas and liver. Differentiation of bile salt-dependent and bile salt-independent, neutral retinyl ester hydrolases in rat liver. Journal of Biological Chemistry 264, 1714217147.CrossRefGoogle ScholarPubMed
Hollander, D & Muralidhara, KS (1977) Vitamin A1 intestinal absorption in vivo: influence of luminal factors on transport. American Journal of Physiology 232, E471E477.Google ScholarPubMed
Hosszufalusi, N, Chan, E, Teruya, M, Takei, S, Granger, G & Charles, MA (1993) Quantitative phenotypic and functional analyses of islet immune cells before and after diabetes onset in the BB rat. Diabetologia 36, 11461154.CrossRefGoogle ScholarPubMed
Krempf, M, Ranganathan, S, Ritz, P, Morin, M & Charbonnel, B (1991) Plasma vitamin A and E in Type 1 (insulin-dependent) and Type 2 (non-insulin-dependent) adult diabetic patient. International Journal of Vitamin and Nutrition Research 61, 3842.Google Scholar
Logothetopoulos, J, Valiquette, N, Madura, E & Cvet, D (1984) The onset and progression of pancreatic insulitis in the overt, spontaneously diabetic, young adult BB rat studied by pancreatic biopsy. Diabetes 33, 3336.CrossRefGoogle ScholarPubMed
Lu, J, Dixon, WT, Tsin, AT & Basu, TK (2000) The metabolic availability of vitamin A is decreased at the onset of diabetes in BB rats. Journal of Nutrition 130, 19581962.CrossRefGoogle ScholarPubMed
Martinoli, L, Di Felice, M, Seghieri, G, Ciuti, M, De Giorgio, LA, Fazzini, A, Gori, R, Anichini, R & Franconi, F (1993) Plasma retinol and alpha-tocopherol concentrations in insulin-dependent diabetes mellitus: their relationship to microvascular complications. International Journal of Vitamin and Nutrition Research 63, 8792.Google ScholarPubMed
Mentlein, R & Heymann, E (1987) Hydrolysis of retinyl esters by non-specific carboxylesterases from rat liver endoplasmic reticulum. Biochemical Journal 245, 863867.CrossRefGoogle ScholarPubMed
Mercier, M, Forget, A, Grolier, P & Azais-Braesco, V (1994) Hydrolysis of retinyl esters in rat liver. Description of a lysosomal activity. Biochimica et Biophysica Acta 1212, 176182.CrossRefGoogle ScholarPubMed
Mercier, M, Pascal, G & Azais-Braesco, V (1990) Retinyl ester hydrolase and vitamin A status in rats treated with 3,3′,4,4′-tetrachlorobiphenyl. Biochimica et Biophysica Acta 1047, 7076.CrossRefGoogle ScholarPubMed
Omodeo-Salè, F, Marchesini, S, Fishman, PH & Berra, B (1984) A sensitive enzymatic assay for determination of cholesterol in lipid extracts. Analytical Biochemistry 142, 347350.CrossRefGoogle ScholarPubMed
Ong, DE (1993) Retinoid metabolism during intestinal absorption. Journal of Nutrition 123, Suppl. 2, 351355.CrossRefGoogle ScholarPubMed
Parfrey, NA, Prud'homme, GJ, Colle, E, Fuks, A, Seemayer, TA, Guttmann, RD & Ono, SJ (1989) Immunologic and genetic studies of diabetes in the BB rats. Critical Review of Immunology 9, 4565.Google Scholar
Rigtrup, KM & Ong, DE (1992) A retinyl ester hydrolase activity intrinsic to the brush border membrane of rat small intestine. Biochemistry 31, 29202926.CrossRefGoogle Scholar
Ross, AC (1993) Overview of retinoid metabolism. Journal of Nutrition 123, Suppl. 2, 346350.CrossRefGoogle ScholarPubMed
Tsin, AT, Mata, NL, Ray, JA & Villazana, ET (2000) Substrate specificities of retinyl ester hydrolases in retinal pigment epithelium. Methods of Enzymology 316, 384400.CrossRefGoogle ScholarPubMed
Tuitoek, PJ, Ritter, SJ, Smith, JE & Basu, TK (1996 a) Streptozotocin-induced diabetes lowers retinol-binding protein and transthyretin concentrations in rats. British Journal of Nutrition 76, 891897.CrossRefGoogle ScholarPubMed
Tuitoek, PJ, Thomson, ABR, Rajotte, RV & Basu, TK (1994) Intestinal absorption of vitamin A in streptozotocin-induced diabetic rats. Diabetes Research 25, 151158.Google ScholarPubMed
Tuitoek, PJ, Ziari, S, Tsin, AT, Rajotte, RV, Suh, M & Basu, TK (1996 b) Streptozotocin-induced diabetes in rats is associated with impaired metabolic availability of vitamin A. British Journal of Nutrition 75, 615622.CrossRefGoogle ScholarPubMed
Uehara, F, Yasumura, D & LaVail, MM (1989) New isolation method of retina and interphotoreceptor matrix. Experimental Eye Research 49, 305309.CrossRefGoogle ScholarPubMed
van Bennekum, AM, Li, L, Piantedosi, R, Shamir, R, Vogel, S, Fisher, EA, Blaner, WS & Harrison, EH (1999) Carboxyl ester lipase overexpression in rat hepatoma cells and CEL deficiency in mice have no impact on hepatic uptake or metabolism of chylomicron-retinyl ester. Biochemistry 38, 41504156.CrossRefGoogle ScholarPubMed
Wang, XD, Liu, C, Chung, J, Stickel, F, Seitz, HK & Russell, RM (1998) Chronic alcohol intake reduces retinoic acid concentration and enhances AP-1 (c-Jun and c-Fos) expression in rat liver. Hepatology 28, 744750.CrossRefGoogle ScholarPubMed
Weng, W, Li, L, ven Bennekum, AM, Potter, SH, Harrison, EH, Blaner, WS, Breslow, JL & Fisher, EA (1999) Intestinal absorption of dietary cholesteryl ester is decreased but retinyl ester absorption is normal in carboxyl ester lipase knockout mice. Biochemistry 38, 41434149.CrossRefGoogle ScholarPubMed