Cholesterol induces renal vasoconstriction and anti-natriuresis by inhibiting nitric oxide production in anesthetized rats

American Journal of Physiology - Renal Physiology

Volumn 297, Issue 6, 2009, Pages

  Kopkan, Libor ^a,c   Khan, Md Abdul H ^a   Lis, Agnieszka ^b   Awayda, Mouhamed S ^b   Majid, Dewan S A ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c INSTITUTE FOR CLINICAL AND EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

Cholesterol; Epithelial Na+ channel; Na+ K+ 2Cl cotransport; Nitric oxide; Renal hemodynamics; Sodium excretion; Superoxide

Indexed keywords

CHOLESTEROL; NITRATE; NITRIC OXIDE; NITRITE; SODIUM; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY CONSTRICTION; ARTICLE; CONTROLLED STUDY; GLOMERULUS FILTRATION RATE; HYPERCHOLESTEROLEMIA; KIDNEY BLOOD FLOW; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RENAL ARTERY; SODIUM ABSORPTION; SODIUM EXCRETION;

EID: 71449088250     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90743.2008     Document Type: Article

References (41)

1. Attia DM, Feron O, Goldschmeding R, Radermakers LH, Vaziri ND, Boer P, Balligand JL, Koomans HA, Joles JA. Hypercholesterolemia in rats induces podocyte stress and decreases renal cortical nitric oxide synthesis via an angiotensin II type 1 receptor-sensitive mechanism. J Am Soc Nephrol 15: 949-957, 2004. (Pubitemid 38375314)
2. Attia DM, Ni ZN, Boer P, Attia MA, Goldschmeding R, Koomans HA, Vaziri ND, Joles JA. Proteinuria is preceded by decreased nitric oxide synthesis and prevented by a NO donor in cholesterol-fed rats. Kidney Int 61: 1776-1787, 2002. (Pubitemid 34437931)
3. Awayda MS, Shao W, Guo F, Zeidel M, Hill WG. ENaC-membrane interactions: regulation of channel activity by membrane order. J Gen Physiol 123: 709-727, 2004. (Pubitemid 38781376)
4. Badzynska B, Grzelec-Mojzesowicz M, Sadowski J. Prostaglandins but not nitric oxide protect renal medullary perfusion in anaesthetized rats receiving angiotensin II. J Physiol 548: 875-880, 2003. (Pubitemid 36592780)
5. + transport in A6 renal epithelia. Am J Physiol Cell Physiol 290: C87-C94, 2006.
6. Barenholz Y. Cholesterol and other membrane active sterols: from membrane evolution to "rafts". Prog Lipid Res 41: 1-5, 2002.
7. Bligh EG, Dryer WJ. A rapid method for total lipid extraction and purification. Can J Bioch Physiol 37: 911-917, 1959.
8. Chade AR, Bentley MD, Zhu X, Rodriguez-Porcel M, Niemeyer S, Amores-Arriaga B, Napoli C, Ritman EL, Lerman A, Lerman LO. Antioxidant intervention prevents renal neovascularization in hypercholesterolemic pigs. J Am Soc Nephrol 15: 1816-1825, 2004.
9. Chade AR, Zhu XY, Grande JP, Krier JD, Lerman A, Lerman LO. Simvastatin abates development of renal fibrosis in experimental renovascular disease. J Hypertens 26: 1651-1660, 2008.
10. Endemann DH, Schiffrin EL. Endothelial dysfunction. J Am Soc Nephrol 15: 1983-1992, 2004.
11. Feron O, Dessy C, Moniotte S, Desager JP, Balligand JL. Hypercholesterolemia decreases nitric oxide production by promoting the interac- tion of caveolin and endothelial nitric oxide synthase. J Clin Invest 103: 897-905, 1999. (Pubitemid 29152636)
12. Feron O, Kelly RA. The caveolar paradox: suppressing, inducing, and terminating eNOS signaling. Circ Res 88: 129-131, 2001. (Pubitemid 32147297)
13. Herrera M, Ortiz PA, Garvin JL. Regulation of thick ascending limb transport: role of nitric oxide. Am J Physiol Renal Physiol 290: F1279-F1284, 2006. (Pubitemid 43830750)
14. Hill WG, An B, Johnson JP. Endogenously expressed epithelial sodium channel is present in lipid rafts in A6 cells. J Biol Chem 277: 33541-33544, 2002.
15. John S, Schmieder RE. Impaired endothelial function in arterial hypertension and hypercholesterolemia: potential mechanisms and differences. J Hypertens 18: 363-374, 2000. (Pubitemid 30209715)
16. Kawano H, Motoyama T, Hirai N, Kugiyama K, Yasue H, Ogawa H. Endothelial dysfunction in hypercholesterolemia is improved by L-arginine administration: possible role of oxidative stress. Atherosclerosis 161: 375-380, 2002. (Pubitemid 34219190)
17. Keane WF, O'Donnell MP, Kasiske BL, Schmitz PG. Lipids and the progression of renal disease. J Am Soc Nephrol 1: S69-S74, 1990.
18. Kopkan L, Castillo A, Navar LG, Majid DS. Enhanced superoxide generation modulates renal function in ANG II-induced hypertensive rats. Am J Physiol Renal Physiol 290: F80-F86, 2006.
19. Kopkan L, Husková Z, VanourkováZ, Thumová M, Skaroupková P, Cervenka L, Majid DS. Superoxide and its interaction with nitric oxide modulates renal function in prehypertensive Ren-2 transgenic rats. J Hypertens 25: 2257-2265, 2007. (Pubitemid 47537919)
20. Kopkan L, Majid DS. Enhanced superoxide activity modulates renal function in NO-deficient hypertensive rats. Hypertension 47: 568-572, 2006. (Pubitemid 43843877)
21. Lopez B, Salom MG, Arregui B, Valero F, Fenoy FJ. Role of superoxide in modulating the renal effects of angiotensin II. Hypertension 42: 1150-1156, 2003. (Pubitemid 37549070)
22. Majid DS, Kopkan L. Nitric oxide and superoxide interactions in the kidney and their implication in the development of salt-sensitive hypertension. Clin Exp Pharmacol Physiol 34: 946-952, 2007. (Pubitemid 47083962)
23. Majid DS, Navar LG. Blockade of distal nephron sodium transport attenuates pressure natriuresis in dogs. Hypertension 23: 1040-1045, 1994.
24. Majid DS, Navar LG. Nitric oxide in the control of renal hemodynamics and excretory function. Am J Hypertens 14: 74S-82S, 2001.
25. Majid DSA, Nishiyama A. Nitric oxide blockade enhances renal reponses to superoxide dismutase inhibition in dogs. Hypertension 39: 293-297, 2002. (Pubitemid 34165231)
26. Majid DSA, Nishiyama A, Jackson KE, Castillo A. Inhibition of nitric oxide synthase enhances superoxide activity in canine kidney. Am J Physiol Regul Integr Comp Physiol 287: R27-R32, 2004. (Pubitemid 38856307)
27. Majid DS, Nishiyama A, Jackson KE, Castillo A. Superoxide scavenging attenuates renal responses to ANG II during nitric oxide synthase inhibition in anesthetized dogs. Am J Physiol Renal Physiol 288: F412-F419, 2005. (Pubitemid 40105401)
28. Miersch S, Espey MG, Chaube R, Akarca A, Tweten R, Ananvoranich S, Mutus B. Plasma membrane cholesterol content affects nitric oxide diffusion dynamics and signaling. J Biol Chem 283: 18513-18521, 2008.
29. Novak J, Reckelhoff J, Bumgarner L, Cockrell K, Kassab S, Granger JP. Reduced sensitivity of the renal circulation to angiotensin II in pregnant rats. Hypertension 30: 580-584. 1997. (Pubitemid 27444235)
30. Rahman MM, Varghese Z, Moorhead JF. Paradoxical increase in nitric oxide synthase activity in hypercholesterolaemic rats with impaired renal function and decreased activity of nitric oxide. Nephrol Dial Transplant 16: 262-268, 2001. (Pubitemid 32123912)
31. Romero JC, Reckelhoff JF. Role of angiotensin and oxidative stress in essential hypertension. Hypertension 34: 943-949, 1999. (Pubitemid 29501328)
32. Sato SB, Ishii K, Makino A, Iwabuchi K, Yamaji-Hasegawa A, Senoh Y, Nagaoka I, Sakuraba H, Kobayashi T. Distribution and transport of cholesterol-rich membrane domains monitored by a membrane-impermeant fluorescent polyethylene glycol-derivatized cholesterol. J Biol Chem 279: 23790-23796, 2004. (Pubitemid 38685696)
33. Stulak JM, Lerman A, Caccitolo JA, Wilson SH, Romero JC, Schaff HV, Rodriguez Porcel M, Lerman LO. Impaired renal vascular endothelial function in vitro in experimental hypercholesterolemia. Atherosclerosis 154: 195-201, 2001. (Pubitemid 32008581)
34. Tasset C, Preat V, Bernard A, Roland M. Comparison of nephrotoxicities of different polyoxyethyleneglycol formulations of amphotericin B in rats. Antimicrob Agents Chemother 36: 1525-1531, 1992.
35. Varela M, Garvin JL. Acute and chronic regulation of thick ascending limb endothelial nitric oxide synthase by statins. J Am Soc Nephrol 15: 269-275, 2004. (Pubitemid 38140767)
36. Wang J, Zhang ZR, Chou CF, Liang YY, Gu Y, Ma HP. Cyclosporine stimulates the renal epithelial sodium channel by elevating cholesterol. Am J Physiol Renal Physiol 296: F284-F290, 2009.
37. Wei SP, Li XQ, Chou CF, Liang YY, Peng JB, Warnock DG, Ma HP. Membrane tension modulates the effects of apical cholesterol on the renal epithelial sodium channel. J Membr Biol 220: 21-31, 2007.
38. West A, Blazer-Yost B. Modulation of basal and peptide hormone-stimulated Na transport by membrane cholesterol content in the A6 epithelial cell line. Cell Physiol Biochem 16: 263-270, 2005. (Pubitemid 41643026)
39. Wilcox CS. Reactive oxygen species: roles in blood pressure and kidney function. Curr Hypertens Rep 4: 160-166, 2002.
40. Xu Y, Buikema H, van Gilst WH, Henning RH. Caveolae and endothelial dysfunction: filling the caves in cardiovascular disease. Eur J Pharmacol 585: 256-260, 2008.
41. Zicha J, Kunes J, Devynck MA. Abnormalities of membrane function and lipid metabolism in hypertension: a review. Am J Hypertens 12: 315-331, 1999. (Pubitemid 29147359)