High-salt intake enhances superoxide activity in enos knockout mice leading to the development of salt sensitivity

American Journal of Physiology - Renal Physiology

Volumn 299, Issue 3, 2010, Pages

  Kopkan, Libor ^a,b,c   Hess, Arthur ^a   Husková, Zuzana ^b,c   Červenka, Luděk ^b,c,d   Navar, L Gabriel ^a   Majid, Dewan S A ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

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

^c Center for Cardiovascular Research   (Czech Republic)

^d CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

8-EPI-PROSTAGLANDIN F2ALPHA; ACETOPHENONE DERIVATIVE; AMINE OXIDE; ANTIOXIDANT; APOCYNIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NOS3 PROTEIN, MOUSE; PROSTAGLANDIN F2 ALPHA; SALT INTAKE; SPIN LABELING; SUPEROXIDE; TEMPOL;

ANALOGS AND DERIVATIVES; ANIMAL; BLOOD PRESSURE; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; HYPERTENSION; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; SALT INTAKE; SPIN LABELING; URINE;

ACETOPHENONES; ANIMALS; ANTIOXIDANTS; BLOOD PRESSURE; CYCLIC N-OXIDES; DINOPROST; DISEASE MODELS, ANIMAL; HYPERTENSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE III; SODIUM CHLORIDE, DIETARY; SPIN LABELS; SUPEROXIDES;

EID: 77956480688     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00047.2010     Document Type: Article

References (51)

1. Beswick RA, Dorrance AM, Leite R, Webb RC. NADH/NADPH oxidase and enhanced superoxide production in the mineralocorticoid hypertensive rat. Hypertension 38: 1107-1111, 2001. (Pubitemid 34252814)
2. Cervenka L, Vanecková I, Husková Z, Vanourková Z, Erbanová M, Thumová M, Skaroupková P, Opocenský M, Malý J, Chábová VC, Tesar V, Bürgelová M, Viklický O, Teplan V, Zelízko M, Kramer HJ, Navar LG. Pivotal role of angiotensin II receptor subtype 1A in the development of two-kidney, one-clip hypertension: study in angiotensin II receptor subtype 1A knockout mice. J Hypertens 26: 1379-1389, 2008.
3. Evans RG, Majid DS, Eppel GA. Mechanisms mediating pressure natriuresis: what we know and what we need to find out. Clin Exp Pharmacol Physiol 32: 400-409, 2005.
4. Franco V, Oparil S. Salt sensitivity, a determinant of blood pressure, cardiovascular disease and survival. J Am Coll Nutr 25, 3 Suppl: 247S-255S, 2006.
5. Gonzalez-Villalobos RA, Satou R, Seth DM, Semprun-Prieto LC, Katsurada A, Kobori H, Navar LG. Angiotensin-converting enzyme-derived angiotensin II formation during angiotensin II-induced hypertension. Hypertension 53: 351-355, 2009.
6. Harrison CB, Drummond GR, Sobey CG, Selemidis S. Evidence that nitric oxide inhibits vascular inflammation and superoxide production via a p47-dependent mechanism in mice. Clin Exp Pharmacol Physiol 37: 429-434, 2010.
7. 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.
8. Herrera M, Silva G, Garvin JL. A high-salt diet dissociates NO synthase-3 expression and NO production by the thick ascending limb. Hypertension 47: 95-101, 2006. (Pubitemid 43177821)
9. Heumuller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schroder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an oxidant. Hypertension 51: 211-217, 2008.
10. Kitiyakara C, Chabrashvili T, Chen Y, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS. Salt intake, oxidative stress, and renal expression of NADPH oxidase and superoxide dismutase. J Am Soc Nephrol 14: 2775-2782, 2003.
11. Kone BC. Nitric oxide synthesis in the kidney: isoforms, biosynthesis, and functions in health. Semin Nephrol 24: 299-315, 2004.
12. Kopkan L, Husková Z, Vanourková Z, Thumová M, Skaroupková P, Malý J, Kramer HJ, Dvorák P, Cervenka L. Reduction of oxidative stress does not attenuate the development of angiotensin II-dependent hypertension in Ren-2 transgenic rats. Vascul Pharmacol 51: 175-181, 2009.
13. Kopkan L, Majid DS. Enhanced superoxide activity modulates renal function in NO-deficient hypertensive rats. Hypertension 47: 568-572, 2006.
14. Kopkan L, Majid DS. Superoxide contributes to development of salt sensitivity and hypertension induced by nitric oxide deficiency. Hypertension 46: 1026-1031, 2005.
15. Lefer DJ, Scalia R, Campbell B, Nossuli T, Hayward R, Salamon M, Grayson J, Lefer AM. Peroxynitrite inhibits leukocyte-endothelial cell interactions and protects against ischemia-reperfusion injury in rats. J Clin Invest 99: 684-691, 1997.
16. Leonard AM, Chafe LL, Montani JP, Van Vliet BN. Increased salt sensitivity in endothelial nitric oxide synthase-knockout mice. Am J Hypertens 19: 1264-1269, 2006. (Pubitemid 44856255)
17. Liu R, Ren Y, Garvin JL, Carretero OA. Superoxide enhances tubuloglomerular feedback by constricting the afferent arteriole. Kidney Int 66: 268-274, 2004.
18. Majid DS, Kopkan L. Nitric oxide and superoxide interaction in the kidney and its implication in the development of salt-sensitive hypertension. Clin Exp Pharmacol Physiol 34: 946-952, 2007.
19. Majid DS, Navar LG. Nitric oxide in the control of renal hemodynamics and excretory function. Am J Hypertens 14, Suppl 3: 74S-82S, 2001.
20. Majid DS, 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)
21. Majid DS, Nishiyama A. Nitric oxide blockade enhances renal reponses to superoxide dismutase inhibition in dogs. Hypertension 39: 293-297, 2002.
22. Manning RD Jr, Hu L, Tan DY, Meng S. Role of abnormal nitric oxide systems in salt-sensitive hypertension. Am J Hypertens 14, Suppl 3: 68S-73S, 2001.
23. Massion PB, Balligand JL. Modulation of cardiac contraction, relaxation and rate by the endothelial nitric oxide synthase (eNOS): lessons from genetically modified mice. J Physiol 546: 63-75, 2003.
24. Matavelli LC, Kadowitz PJ, Navar LG, Majid DS. Renal hemodynamic and excretory responses to intra-arterial infusion of peroxynitrite in anesthetized rats. Am J Physiol Renal Physiol 296: F170-F176, 2009.
25. Mattson DL, Maeda CY, Bachman TD, Cowley AW Jr. Inducible nitric oxide synthase and blood pressure. Hypertension 31: 15-20, 1998.
26. Mattson DL, Meister CJ. Sodium sensitivity of arterial blood pressure in L-NAME hypertensive but not eNOS knockout mice. Am J Hypertens 19: 327-329, 2006.
27. Mendoza MG, Castillo-Henkel C, Medina-Santillan R, Jarillo Luna RA, Robles HV, Romo E, Rios A, Escalante B. Kidney damage after renal ablation is worsened in endothelial nitric oxide synthase -/- mice and improved by combined administration of L-arginine and antioxidants. Nephrology 13: 218-227, 2008.
28. Mitchell JB, Xavier S, DeLuca AM, Sowers AL, Cook JA, Krishna MC, Hahn SM, Russo A. A low molecular weight antioxidant decreases weight and lowers tumor incidence. Free Radic Biol Med 34: 93-102, 2003.
29. Nishiyama A, Yao L, Nagai Y, Miyata K, Yoshizumi M, Kagami S, Kondo S, Kiyomoto H, Shokoji T, Kimura S, Kohno M, Abe Y. Possible contributions of reactive oxygen species and mitogen-activated protein kinase to renal injury in aldosterone/salt-induced hypertensive rats. Hypertension 43: 841-848, 2004.
30. Nishiyama A, Yoshizumi M, Hitomi H, Kagami S, Kondo S, Miyatake A, Fukunaga M, Tamaki T, Kiyomoto H, Kohno M, Shokoji T, Kimura S, Abe Y. The SOD mimetic tempol ameliorates glomerular injury and reduces mitogen-activated protein kinase activity in Dahl salt-sensitive rats. J Am Soc Nephrol 15: 306-315, 2004.
31. Ortiz PA, Garvin JL. Cardiovascular and renal control in NOS-deficient mouse models. Am J Physiol Regul Integr Comp Physiol 284: R628-R638, 2003. (Pubitemid 36342795)
32. Ortiz PA, Hong NJ, Wang D, Garvin JL. Gene transfer of eNOS to the thick ascending limb of eNOS-KO mice restores the effects of L-arginine on NaCl absorption. Hypertension 42: 674-679, 2003.
33. Pech V, Sikka SC, Sindhu RK, Vaziri ND, Majid DS. Oxidant stress and blood pressure responses to angiotensin II administration in rats fed varying salt diets. Am J Hypertens 19: 534-540, 2006.
34. Rodriguez-Iturbe B, Vaziri ND, Herrera-Acosta J, Johnson RJ. Oxidative stress, renal infiltration of immune cells, and salt-sensitive hypertension: all for one and one for all. Am J Physiol Renal Physiol 286: F606-F616, 2004. (Pubitemid 38365077)
35. Romero JC, Reckelhoff JF. Role of angiotensin and oxidative stress in essential hypertension. Hypertension 34: 943-949, 1999.
36. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin f2alpha. Hypertension 33: 424-428, 1999.
37. Schneider MP, Ge Y, Pollock DM, Pollock JS, Kohan DE. Collecting duct-derived endothelin regulates arterial pressure and Na excretion via nitric oxide. Hypertension 51: 1605-1610, 2008.
38. Silva GB, Ortiz PA, Hong NJ, Garvin JL. Superoxide stimulates NaCl absorption in the thick ascending limb via activation of protein kinase C. Hypertension 48: 467-472, 2006.
39. Tian N, Moore RS, Phillips WE, Lin L, Braddy S, Pryor JS, Stockstill RL, Hughson MD, Manning RD Jr. NADPH oxidase contributes to renal damage and dysfunction in Dahl salt-sensitive hypertension. Am J Physiol Regul Integr Comp Physiol 295: R1858-R1865, 2008.
40. Tolins JP, Shultz PJ. Endogenous nitric oxide synthesis determines sensitivity to the pressor effect of salt. Kidney Int 46: 230-236, 1994.
41. Tsuchiya K, Sakai H, Suzuki N, Iwashima F, Yoshimoto T, Shichiri M, Hirata Y. Chronic blockade of nitric oxide synthesis reduces adiposity and improves insulin resistance in high fat-induced obese mice. Endocrinology 148: 4548-4556, 2007.
42. Uppu RM, Nossaman BD, Greco AJ, Fokin A, Murthy SN, Fonseca VA, Kadowitz PJ. Cardiovascular effects of peroxynitrite. Clin Exp Pharmacol Physiol 34: 933-937, 2007.
43. Virdis A, Neves MF, Amiri F, Touyz RM, Schiffrin EL. Role of NAD(P)H oxidase on vascular alterations in angiotensin II-infused mice. J Hypertens 22: 535-542, 2004. (Pubitemid 38368487)
44. Weinberger MH. Salt sensitivity of blood pressure in humans. Hypertension 27: 481-490, 1996.
45. Wilcox CS. Oxidative stress and nitric oxide deficiency in the kidney: a critical link to hypertension? Am J Physiol Regul Integr Comp Physiol 289: R913-R935, 2005.
46. Wilcox CS. Special feature: cardiovascular-kidney interactions in health and disease. Am J Physiol Regul Integr Comp Physiol 290: R34-R36, 2006.
47. Williams JM, Pollock JS, Pollock DM. Arterial pressure response to the antioxidant tempol and ETB receptor blockade in rats on a high-salt diet. Hypertension 44: 770-775, 2004.
48. Wink DA, Miranda KM, Espey MG, Pluta RM, Hewett SJ, Colton C, Vitek M, Feelisch M, Grisham MB. Mechanisms of the antioxidant effects of nitric oxide. Antioxid Redox Signal 3: 203-213, 2001.
49. Xu H, Fink GD, Galligan JJ. Nitric oxide-independent effects of tempol on sympathetic nerve activity and blood pressure in DOCA-salt rats. Am J Physiol Heart Circ Physiol 283: H885-H892, 2002.
50. Yamada SS, Sassaki AL, Fujihara CK, Malheiros DM, De Nucci G, Zatz R. Effect of salt intake and inhibitor dose on arterial hypertension and renal injury induced by chronic nitric oxide blockade. Hypertension 27: 1165-1172, 1996. (Pubitemid 26140675)
51. Yanes L, Romero D, Iliescu R, Cucchiarelli VE, Fortepiani LA, Santacruz F, Bell W, Zhang H, Reckelhoff JF. Systemic arterial pressure response to two weeks of Tempol therapy in SHR: involvement of NO, the RAS, and oxidative stress. Am J Physiol Regul Integr Comp Physiol 288: R903-R908, 2005.