Abstract
The current studies explore the effect of hypertension on D-glucose transport into jejunal brush-border membrane vesicles (BBMV). Spontaneously hypertensive rats (SHR) and normotensive Wistar-Kyoto (WKY) rats, as a control group, were used. The purity of the BBMV from both groups of animals was validated by the finding that the specific activity of brush-border enzyme marker, sucrase, was severalfold greater in membrane vesicles compared with corresponding values in mucosal homogenate. D-glucose uptake was Na+ dependent in both groups of animals, with a transient increase in the intravesicular concentration of D-glucose. However, the initial rate and the magnitude of the accumulation of Na+-dependent D-glucose was significantly higher in SHR compared with WKY rats. In order to investigate the mechanism(s) for the increase in Na+-dependent D-glucose transport in SHR, several experiments were performed: (1) an experiment that indicated 22Na uptake, as an indicator for Na+ permeability, was similar between SHR and WKY rats, (2) kinetic studies that indicated that Vmax values of SHR were significantly greater that those of WKY rats. In contrast, similar Km values for glucose were found between SHR and WKY rats, (3) Na+-dependent phlorizin binding measurements that were not altered by hypertension and (4) a study of the brush-border membrane lipid composition that showed a significant increase in the free cholesterol/phospholipid ratio in SHR. We conclude that altered membrane cholesterol content and consequently altered lipid fluidity could be, at least in part, responsible for the observed increase in Na+-dependent D-glucose transport in SHR.
Similar content being viewed by others
References
Abdulkarim MS, Beatle DC (1990) Kinetic properties of the Na+/H+ antiporter of lymphocytes from the spontaneously hypertensive rat: role of intracellular pH. J Clin Invest 85:1734–1739
Bin Talib HK, Zicha J (1993) Red cell ouabain-resistant Na+-K+ transport in Wistar, Brown Norway and Spontaneously Hypertensive Rats. Physiol Res 42:181–188
Blaustein MP (1984) Sodium transport and hypertension, where are we going? Hypertension 6:445–453
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein-dye binding. Anal Biochem 72:248–254
Bretaudiere JP, Spilman T (1984) In: Methods of enzymatic analysis, pp 75–82
Carriere B, Le Grimellec C (1986) Effects of benzyl alcohol on enzyme activities and D-glucose transport in kidney brush-border membranes. Biochim Biophys Acta 857:131–138
Dahlquist A (1964) Method for assay of intestinal disacchari-dases. Anal Biochem 7:18–25
Dall’Aglio E, Tosini P, Ferrari P, Zavaroni I, Passeri M, Reaven GM (1991) Abnormalities of insulin and metabolism in Milan hypertensive rats. J Am Med Assoc 4:773–775
De Schrijver R, Vermeulen D (1991) Separation and quantification of phospholipids in animal tissues by latroscan TLC/ FID. Lipids 26:74–76
Devaskar S, Mueckler MM (1992) The mammalian glucose transporters. Pediatr Res 31:1–13
Dinda PK, Beck IT (1981) Ethanol-induced inhibition of glucose transport across the isolated brush-border membrane of hamster jejunum. Dig Dis Sci 26:23–32
Duhm J (1989) Possible role of plasma lipids in alterations of cell membrane sodium transport in essential hypertension. In: Meyer P, Marche P (eds) Blood cells and arteries in hypertension and atherosclerosis. Raven, New York, pp 247 270
Fernandez YJ, Boigegrain AM, Gambon-Gros CD, Mitjavilla SE (1984) Sensitivity of Na+-coupled D-glucose uptake, Mg2+-ATPase and sucrase to perturbations of the fluidity of brush-border membrane vesicles induced by n-aliphatic alcohols. Biochim Biophys Acta 770:171–177
Ferrari P, Torielli L, Salardi S, Rizzo A, Bianchi G (1992) Na+/K+/CL- cotransport in resealed ghosts from erythrocytes of the Milan hypertensive rats. Biochim Biophys Acta 1111:111–119
Folch J, Less M, Sloan-Stanley GH (1957) A sample method for the isolation and purification of total lipids from the animal tissues. J Biol Chem 33:497–509
Hediger MA, Coady MJ, Ikeda TS, Wright WM (1987) Expression cloning and cDNA sequencing of the Na+/glucose cotransporter. Nature 330:379–381
Hennessen U, Drueke T, Comte L, Steuf MC, McCarron A, Lacour B (1990) Calcium uptake kinetics into brush-border membrane vesicles: higher Vmax in the spontaneously hypertensive rat than in normotensive control. Biochem Biophys Res Commun 170:742–747
Hilton PJ (1986) Cellular sodium transport in essential hypertension. N Engl J Med 314:222–229
Hirayama BA, Wright EM (1992) Glycosylation of the rabbit intestinal brush border Na+/glucose cotransporter. Biochim Biophys Acta 1103:37–44
Hirayama BA, Wong HC, Smith CD, Hagenbuch BA, Hediger MA, Wright EM (1991) Intestinal and renal Na+/glucose cotransporters share common structures. Am J Physiol 261:C296-C304
Kinne R, Schmitz JE, Kinne-Saffran E (1971) The localization of the Na+-K+-ATPase in the cells of rat kidney cortex. A study on isolates plasma membranes. Pflügers Arch 329:191–209
Meddings JB, DeSouza D, Goel M, Thiessen S (1990) Glucose transport and microvillus membrane physical properties along the crypt-villus axis of the rabbit. J Clin Invest 85:1099–1107
Monteith GR, Chen S, Roufogalis BD (1993) Measurement of Ca2+ pump-mediated efflux in hypertension. J Pharmacol Toxicol Methods 31:117–124
Morduchowicz GA, Sheikh-Hamad D, Jo Ok D, Nord EP, Lee DBN, Yanagawa N (1989) Increased Na+/H+ antiport activity in the renal brush-border membrane of SHR. Kidney Int 36:576–581
Peerce BE, Clarke RD (1990) Isolation and reconstitution of the intestinal Na+/glucose cotransporter. J Biol Chem 265:1731–1736
Ragone E, Strazzullo P, Siani A, Pagano E, Sacchi A, Cipriano P, Vaccaro O, Mancinim M (1993) Essential hypertension, impaired glucose tolerance and hyperlipidaemia: multiple relationships with sodium-lithium countertransport. J Hypertens 11:S256-S257
Rosskopf D, Dusing R, Siffert W (1993) Membrane sodium-proton exchange and primary hypertension. Hypertension 21:607–617
Sang KHLQ, Mazeaud M, Astarie C, Duranthon FD, Devynck MA (1993) Plasma lipids and platelet membrane fluidity in essential hypertension. Thromb Haemost 69:70–76
Sauerheber RD, Esgate JA, Kuhn CE (1982) Alcohols inhibit adipocyte basal and insulin-stimulated glucose uptake and increase the membrane lipid fluidity. Biochim Biophys Acta 691:115–124
Sharp PA, Debnam ES (1994) The role of cyclic AMP in the control of sugar transport across the brush border and basolateral membranes of rat jejunal enterocytes. Exp Physiol 79:203–214
Shirazi-Beechey SP, Davies AG, Dyer TJ, Ellis A, Taylor CJ, Fairclough P, Beechey RB (1990) Preparation and properties of brush-border membrane vesicles from human small intestine. Gastroenterology 98:676–685
Stochmal A, Goldsztajn P, Hartwich M, Wenhrynowicz O, Rajzer M, Kawecka-Jaszcz K, Dembinska-Kiéc A (1993) Very-low-density lipoprotein composition and endogenous insulin response in primary hypertension. J Hypertens 11: S278-S279
Swarts HGP, Bonting SL, De Pont JJHHM, Stekhoven FMAHS, Thien TA, Vant Laar A (1981) Cation fluxes and (Na+-K+)-activated ATPase activity in erythocytes of patients with essential hypertension. Clin Exp Hypertens 3:831–849
Takase S, Goda T (1990) Effects of medium-chain triglycerides on brush border membrane-bound enzyme activity in rat small intestine. J Nutr 120:969–976
Watanabe Y, Huang Y-S, Simmons A, Horrobin DF (1989) The effect of dietary n-6 and n-3 polyunsaturated fatty acids on blood pressure and tissue fatty acid composition in spontaneously hypertensive rats. Lipids 24:638–644
Zanetti R, Santa-Maria C, Vázquez CM, Ruiz-Gutierrez V (1994) Increased sodium-dependent D-glucose transport in the jejunal brush-border membrane of SHR. Fifth Spanish Portuguesse Congress of Biochemistry PHI, 45. Salamanca, Spain
Zicha J, Bin Talib HK, Duhm J (1991) Na+ and K+ transport alterations in hypertension. Physiol Res 40:555–576
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Vázquez, C.M., Coleto, R., Zanetti, R. et al. Increased sodium-dependent D-glucose transport in the jejunal brush-border membrane of spontaneously hypertensive rat. Pflugers Arch. 432, 329–335 (1996). https://doi.org/10.1007/s004240050140
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s004240050140