Oxidative DNA damage in kidneys and heart of hypertensive mice is prevented by blocking angiotensin II and aldosterone receptors

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Brand, Susanne ^a   Amann, Kerstin ^c   Mandel, Philipp ^a   Zimnol, Anna ^b   Schupp, Nicole ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALDOSTERONE RECEPTOR; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; CANDESARTAN; EPLERENONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TEMPOL; TRANSCRIPTION FACTOR NRF2; 8-HYDROXYGUANOSINE; 8-OXO-7-HYDRODEOXYGUANOSINE; ALDOSTERONE; AMINE OXIDE; ANGIOTENSIN 1 RECEPTOR ANTAGONIST; ANTIOXIDANT; BENZIMIDAZOLE DERIVATIVE; DEOXYGUANOSINE; GUANOSINE; MINERALOCORTICOID ANTAGONIST; NFE2L2 PROTEIN, MOUSE; REACTIVE OXYGEN METABOLITE; SPIN LABEL; SPIRONOLACTONE; TETRAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; BLOOD PRESSURE REGULATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DRUG EFFICACY; HISTOPATHOLOGY; HYPERTENSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KIDNEY INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; BLOOD PRESSURE; C57BL MOUSE; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; HEART; KIDNEY; METABOLISM; PATHOPHYSIOLOGY; SPIN LABELS; URINE;

ANIMALIA; MUS;

ALDOSTERONE; ANGIOTENSIN II; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; ANTIOXIDANTS; BENZIMIDAZOLES; BLOOD PRESSURE; CYCLIC N-OXIDES; DEOXYGUANOSINE; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; GUANOSINE; HEART; HYPERTENSION; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MINERALOCORTICOID RECEPTOR ANTAGONISTS; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RENIN-ANGIOTENSIN SYSTEM; SPIN LABELS; SPIRONOLACTONE; TETRAZOLES;

EID: 84938412180     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115715     Document Type: Article

References (81)

1. Grossman E, Messerli FH, Boyko V, Goldbourt U (2002) Is there an association between hypertension and cancer mortality? Am J Med 112: 479-486.
2. Ljungberg B, Campbell SC, Choi HY, Jacqmin D, Lee JE, et al. (2011) The epidemiology of renal cell carcinoma. Eur Urol 60: 615-621.
3. Weikert S, Boeing H, Pischon T, Weikert C, Olsen A, et al. (2008) Blood pressure and risk of renal cell carcinoma in the European prospective investigation into cancer and nutrition. Am J Epidemiol 167: 438-446.
4. Haggstrom C, Stocks T, Rapp K, Bjorge T, Lindkvist B, et al. (2011) Metabolic syndrome and risk of bladder cancer: prospective cohort study in the metabolic syndrome and cancer project (Me-Can). Int J Cancer 128: 1890-1898.
5. Martin RM, Vatten L, Gunnell D, Romundstad P (2010) Blood pressure and risk of prostate cancer: Cohort Norway (CONOR). Cancer Causes Control 21: 463-472.
6. Kabat GC, Kim M, Chlebowski RT, Khandekar J, Ko MG, et al. (2009) A longitudinal study of the metabolic syndrome and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 18: 2046-2053.
7. Andreotti G, Boffetta P, Rosenberg PS, Berndt SI, Karami S, et al. (2010) Variants in blood pressure genes and the risk of renal cell carcinoma. Carcinogenesis 31: 614-620.
8. Schupp N, Schmid U, Rutkowski P, Lakner U, Kanase N, et al. (2007) Angiotensin II-induced genomic damage in renal cells can be prevented by angiotensin II type 1 receptor blockage or radical scavenging. Am J Physiol Renal Physiol 292: F1427-1434.
9. Schupp N, Queisser N, Wolf M, Kolkhof P, Bärfacker L, et al. (2010) Aldosterone causes DNA strand breaks and chromosomal damage in renal cells, which are prevented by mineralocorticoid receptor antagonists. Horm Metab Res 42: 458-465.
10. Schmid U, Stopper H, Schweda F, Queisser N, Schupp N (2008) Angiotensin II induces DNA damage in the kidney. Cancer Res 68: 9239-9246.
11. Queisser N, Oteiza PI, Stopper H, Oli RG, Schupp N (2011) Aldosterone induces oxidative stress, oxidative DNA damage and NF-kappaB-activation in kidney tubule cells. Mol Carcinog 50: 123-135.
12. Brand S, Amann K, Schupp N (2013) Angiotensin II-induced hypertension dose-dependently leads to oxidative stress and DNA damage in mouse kidneys and hearts. J Hypertens 31: 333-344.
13. Queisser N, Amann K, Hey V, Habib SL, Schupp N (2013) Blood pressure has only minor influence on aldosterone-induced oxidative stress and DNA damage in vivo. Free Radic Biol Med 54: 17-25.
14. Fazeli G, Stopper H, Schinzel R, Ni CW, Jo H, et al. (2012) Angiotensin II induces DNA damage via AT1 receptor and NADPH oxidase isoform Nox4. Mutagenesis 27: 673-681.
15. Lamprecht MR, Sabatini DM, Carpenter AE (2007) CellProfiler: free, versatile software for automated biological image analysis. Biotechniques 42: 71-75.
16. Westhoff JH, Hilgers KF, Steinbach MP, Hartner A, Klanke B, et al. (2008) Hypertension induces somatic cellular senescence in rats and humans by induction of cell cycle inhibitor p16INK4a. Hypertension 52: 123-129.
17. Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, et al. (1998) DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci U S A 95: 288-293.
18. Bogdanov MB, Beal MF, McCabe DR, Griffin RM, Matson WR (1999) A carbon column-based liquid chromatography electrochemical approach to routine 8-hydroxy-2′-deoxyguanosine measurements in urine and other biologic matrices: a one-year evaluation of methods. Free Radic Biol Med 27: 647-666.
19. Liao TD, Yang XP, Liu YH, Shesely EG, Cavasin MA, et al. (2008) Role of inflammation in the development of renal damage and dysfunction in angiotensin II-induced hypertension. Hypertension 52: 256-263.
20. Lassegue B, San Martin A, Griendling KK (2012) Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res 110: 1364-1390.
21. Simao S, Gomes P, Pinto V, Silva E, Amaral JS, et al. (2011) Age-related changes in renal expression of oxidant and antioxidant enzymes and oxidative stress markers in male SHR and WKY rats. Exp Gerontol 46: 468-474.
22. Zhang J, Chandrashekar K, Lu Y, Duan Y, Qu P, et al. (2014) Enhanced expression and activity of Nox2 and Nox4 in the macula densa in ANG II-induced hypertensive mice. Am J Physiol Renal Physiol 306: F344-350.
23. Briones AM, Tabet F, Callera GE, Montezano AC, Yogi A, et al. (2011) Differential regulation of Nox1, Nox2 and Nox4 in vascular smooth muscle cells from WKY and SHR. J Am Soc Hypertens 5: 137-153.
24. Babelova A, Avaniadi D, Jung O, Fork C, Beckmann J, et al. (2012) Role of Nox4 in murine models of kidney disease. Free Radic Biol Med 53: 842-853.
25. Sirker A, Zhang M, Shah AM (2011) NADPH oxidases in cardiovascular disease: insights from in vivo models and clinical studies. Basic Res Cardiol 106: 735-747.
26. Li H, Horke S, Forstermann U (2013) Oxidative stress in vascular disease and its pharmacological prevention. Trends Pharmacol Sci 34: 313-319.
27. de Jong JW, Schoemaker RG, de Jonge R, Bernocchi P, Keijzer E, et al. (2000) Enhanced expression and activity of xanthine oxidoreductase in the failing heart. J Mol Cell Cardiol 32: 2083-2089.
28. Yamamoto E, Kataoka K, Yamashita T, Tokutomi Y, Dong YF, et al. (2007) Role of xanthine oxidoreductase in the reversal of diastolic heart failure by candesartan in the salt-sensitive hypertensive rat. Hypertension 50: 657-662.
29. Surh YJ, Kundu JK, Na HK (2008) Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med 74: 1526-1539.
30. Gomez-Guzman M, Jimenez R, Sanchez M, Zarzuelo MJ, Galindo P, et al. (2012) Epicatechin lowers blood pressure, restores endothelial function, and decreases oxidative stress and endothelin-1 and NADPH oxidase activity in DOCA-salt hypertension. Free Radic Biol Med 52: 70-79.
31. Queisser N, Oteiza PI, Link S, Hey V, Stopper H, et al. (2014) Aldosterone Activates Transcription Factor Nrf2 in Kidney Cells Both In Vitro and In Vivo. Antioxid Redox Signal.
32. Wu L, Noyan Ashraf MH, Facci M, Wang R, Paterson PG, et al. (2004) Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci U S A 101: 7094-7099.
33. Kim HJ, Vaziri ND (2010) Contribution of impaired Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am J Physiol Renal Physiol 298: F662-671.
34. Aminzadeh MA, Nicholas SB, Norris KC, Vaziri ND (2013) Role of impaired Nrf2 activation in the pathogenesis of oxidative stress and inflammation in chronic tubulo-interstitial nephropathy. Nephrol Dial Transplant doi: 10.1093/ndt/gft022.
35. Kang SJ, You A, Kwak MK (2011) Suppression of Nrf2 signaling by angiotensin II in murine renal epithelial cells. Arch Pharm Res 34: 829-836.
36. Aizawa T, Ishizaka N, Taguchi J, Nagai R, Mori I, et al. (2000) Heme oxygenase-1 is upregulated in the kidney of angiotensin II-induced hypertensive rats: possible role in renoprotection. Hypertension 35: 800-806.
37. Ishizaka N, Aizawa T, Mori I, Taguchi J, Yazaki Y, et al. (2000) Heme oxygenase-1 is upregulated in the rat heart in response to chronic administration of angiotensin II. Am J Physiol Heart Circ Physiol 279: H672-678.
38. Esteban V, Ruperez M, Vita JR, Lopez ES, Mezzano S, et al. (2003) Effect of simultaneous blockade of AT1 and AT2 receptors on the NFkappaB pathway and renal inflammatory response. Kidney Int Suppl: S33-38.
39. Kim HJ, Sato T, Rodriguez-Iturbe B, Vaziri ND (2011) Role of intrarenal angiotensin system activation, oxidative stress, inflammation, and impaired nuclear factor-erythroid-2-related factor 2 activity in the progression of focal glomerulosclerosis. J Pharmacol Exp Ther 337: 583-590.
40. Kowala MC, Murugesan N, Tellew J, Carlson K, Monshizadegan H, et al. (2004) Novel dual action AT1 and ETA receptor antagonists reduce blood pressure in experimental hypertension. J Pharmacol Exp Ther 309: 275-284.
41. Kim DK, Cho ES, Lee BR, Um HD (2001) NF-kappa B mediates the adaptation of human U937 cells to hydrogen peroxide. Free Radic Biol Med 30: 563-571.
42. Xu S, Zhi H, Hou X, Cohen RA, Jiang B (2011) IkappaBbeta attenuates angiotensin II-induced cardiovascular inflammation and fibrosis in mice. Hypertension 58: 310-316.
43. Kawano S, Kubota T, Monden Y, Kawamura N, Tsutsui H, et al. (2005) Blockade of NF-kappaB ameliorates myocardial hypertrophy in response to chronic infusion of angiotensin II. Cardiovasc Res 67: 689-698.
44. Chen Y, Arrigo AP, Currie RW (2004) Heat shock treatment suppresses angiotensin II-induced activation of NF-kappaB pathway and heart inflammation: a role for IKK depletion by heat shock? Am J Physiol Heart Circ Physiol 287: H1104-1114.
45. Grew IS, Cejvanovic V, Broedbaek K, Henriksen T, Petersen M, et al. (2014) Diurnal variation of urinary markers of nucleic acid oxidation. Scand J Clin Lab Invest 74: 336-343.
46. Poulsen HE, Nadal LL, Broedbaek K, Nielsen PE, Weimann A (2014) Detection and interpretation of 8-oxodG and 8-oxoGua in urine, plasma and cerebrospinal fluid. Biochim Biophys Acta 1840: 801-808.
47. Mendes B, Silva P, Mendonca I, Pereira J, Camara JS (2013) A new and fast methodology to assess oxidative damage in cardiovascular diseases risk development through eVol-MEPS-UHPLC analysis of four urinary biomarkers. Talanta 116: 164-172.
48. Subash P, Gurumurthy P, Sarasabharathi A, Cherian KM (2010) Urinary 8-OHdG: A marker of oxidative stress to DNA and total antioxidant status in essential hypertension with South Indian population. Indian J Clin Biochem 25: 127-132.
49. Redon J, Oliva MR, Tormos C, Giner V, Chaves J, et al. (2003) Antioxidant activities and oxidative stress byproducts in human hypertension. Hypertension 41: 1096-1101.
50. Negishi H, Ikeda K, Kuga S, Noguchi T, Kanda T, et al. (2001) The relation of oxidative DNA damage to hypertension and other cardiovascular risk factors in Tanzania. J Hypertens 19: 529-533.
51. Mels CM, Schutte AE, Schutte R, Pretorius PJ, Smith W, et al. (2014) 8-Oxo-7,8-dihydro-2′-deoxyguanosine, reactive oxygen species and ambulatory blood pressure in African and Caucasian men: The SABPA study. Free Radic Res 48: 1291-1299.
52. Kushiro T, Fujita H, Hisaki R, Asai T, Ichiyama I, et al. (2005) Oxidative stress in the Dahl salt-sensitive hypertensive rat. Clin Exp Hypertens 27: 9-15.
53. Yamamoto M, Suzuki A, Jokura H, Yamamoto N, Hase T (2008) Glucosyl hesperidin prevents endothelial dysfunction and oxidative stress in spontaneously hypertensive rats. Nutrition 24: 470-476.
54. Peixoto EB, Pessoa BS, Biswas SK, Lopes de Faria JB (2009) Antioxidant SOD mimetic prevents NADPH oxidase-induced oxidative stress and renal damage in the early stage of experimental diabetes and hypertension. Am J Nephrol 29: 309-318.
55. Rocha R, Martin-Berger CL, Yang P, Scherrer R, Delyani J, et al. (2002) Selective aldosterone blockade prevents angiotensin II/salt-induced vascular inflammation in the rat heart. Endocrinology 143: 4828-4836.
56. Nishioka T, Suzuki M, Onishi K, Takakura N, Inada H, et al. (2007) Eplerenone attenuates myocardial fibrosis in the angiotensin II-induced hypertensive mouse: involvement of tenascin-C induced by aldosterone-mediated inflammation. J Cardiovasc Pharmacol 49: 261-268.
57. Rocha R, Chander PN, Khanna K, Zuckerman A, Stier CT, Jr. (1998) Mineralocorticoid blockade reduces vascular injury in stroke-prone hypertensive rats. Hypertension 31: 451-458.
58. Bianchi S, Bigazzi R, Campese VM (2006) Long-term effects of spironolactone on proteinuria and kidney function in patients with chronic kidney disease. Kidney Int 70: 2116-2123.
59. Lea WB, Kwak ES, Luther JM, Fowler SM, Wang Z, et al. (2009) Aldosterone antagonism or synthase inhibition reduces end-organ damage induced by treatment with angiotensin and high salt. Kidney Int 75: 936-944.
60. Shibata S, Nagase M, Yoshida S, Kawachi H, Fujita T (2007) Podocyte as the target for aldosterone: roles of oxidative stress and Sgk1. Hypertension 49: 355-364.
61. Durvasula RV, Petermann AT, Hiromura K, Blonski M, Pippin J, et al. (2004) Activation of a local tissue angiotensin system in podocytes by mechanical strain. Kidney Int 65: 30-39.
62. Klanke B, Cordasic N, Hartner A, Schmieder RE, Veelken R, et al. (2008) Blood pressure versus direct mineralocorticoid effects on kidney inflammation and fibrosis in DOCA-salt hypertension. Nephrol Dial Transplant 23: 3456-3463.
63. Brown NJ, Nakamura S, Ma L, Nakamura I, Donnert E, et al. (2000) Aldosterone modulates plasminogen activator inhibitor-1 and glomerulosclerosis in vivo. Kidney Int 58: 1219-1227.
64. Ikeda H, Tsuruya K, Toyonaga J, Masutani K, Hayashida H, et al. (2009) Spironolactone suppresses inflammation and prevents L-NAME-induced renal injury in rats. Kidney Int 75: 147-155.
65. Taira M, Toba H, Murakami M, Iga I, Serizawa R, et al. (2008) Spironolactone exhibits direct renoprotective effects and inhibits renal renin-angiotensin-aldosterone system in diabetic rats. Eur J Pharmacol 589: 264-271.
66. Krug AW, Allenhofer L, Monticone R, Spinetti G, Gekle M, et al. (2010) Elevated mineralocorticoid receptor activity in aged rat vascular smooth muscle cells promotes a proinflammatory phenotype via extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase and epidermal growth factor receptor-dependent pathways. Hypertension 55: 1476-1483.
67. McCurley A, McGraw A, Pruthi D, Jaffe IZ (2013) Smooth muscle cell mineralocorticoid receptors: role in vascular function and contribution to cardiovascular disease. Pflugers Arch 465: 1661-1670.
68. Van Belle E, Bauters C, Wernert N, Hamon M, McFadden EP, et al. (1995) Neointimal thickening after balloon denudation is enhanced by aldosterone and inhibited by spironolactone, and aldosterone antagonist. Cardiovasc Res 29: 27-32.
69. Jin HM, Zhou DC, Gu HF, Qiao QY, Fu SK, et al. (2013) Antioxidant N-acetylcysteine protects pancreatic beta-cells against aldosterone-induced oxidative stress and apoptosis in female db/db mice and insulin-producing MIN6 cells. Endocrinology 154: 4068-4077.
70. Chen H, Sun F, Zhong X, Shao Y, Yoshimura A, et al. (2013) Eplerenone-mediated aldosterone blockade prevents renal fibrosis by reducing renal inflammation, interstitial cell proliferation and oxidative stress. Kidney Blood Press Res 37: 557-566.
71. Kawarazaki H, Ando K, Nagae A, Fujita M, Matsui H, et al. (2010) Mineralocorticoid receptor activation contributes to salt-induced hypertension and renal injury in prepubertal Dahl salt-sensitive rats. Nephrol Dial Transplant 25: 2879-2889.
72. Fukuda S, Horimai C, Harada K, Wakamatsu T, Fukasawa H, et al. (2011) Aldosterone-induced kidney injury is mediated by NFkappaB activation. Clin Exp Nephrol 15: 41-49.
73. Sanz-Rosa D, Oubina MP, Cediel E, de Las Heras N, Vegazo O, et al. (2005) Effect of AT1 receptor antagonism on vascular and circulating inflammatory mediators in SHR: role of NF-kappaB/IkappaB system. Am J Physiol Heart Circ Physiol 288: H111-115.
74. Dikalova A, Clempus R, Lassegue B, Cheng G, McCoy J, et al. (2005) Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 112: 2668-2676.
75. Yagi S, Akaike M, Aihara K, Ishikawa K, Iwase T, et al. (2010) Endothelial nitric oxide synthase-independent protective action of statin against angiotensin II-induced atrial remodeling via reduced oxidant injury. Hypertension 55: 918-923.
76. Ohashi N, Katsurada A, Miyata K, Satou R, Saito T, et al. (2009) Role of activated intrarenal reactive oxygen species and renin-angiotensin system in IgA nephropathy model mice. Clin Exp Pharmacol Physiol 36: 750-755.
77. Wilcox CS, Pearlman A (2008) Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 60: 418-469.
78. Hayden MR, Chowdhury NA, Cooper SA, Whaley-Connell A, Habibi J, et al. (2007) Proximal tubule microvilli remodeling and albuminuria in the Ren2 transgenic rat. Am J Physiol Renal Physiol 292: F861-867.
79. Knight SF, Yuan J, Roy S, Imig JD (2010) Simvastatin and tempol protect against endothelial dysfunction and renal injury in a model of obesity and hypertension. Am J Physiol Renal Physiol 298: F86-94.
80. Rugale C, Delbosc S, Mimran A, Jover B (2007) Simvastatin reverses target organ damage and oxidative stress in Angiotensin II hypertension: comparison with apocynin, tempol, and hydralazine. J Cardiovasc Pharmacol 50: 293-298.
81. Panchal SK, Ward L, Brown L (2013) Ellagic acid attenuates high-carbohydrate, high-fat diet-induced metabolic syndrome in rats. Eur J Nutr 52: 559-568.