Angiotensin II-induced hypertension dose-dependently leads to oxidative stress and DNA damage in mouse kidneys and hearts

Journal of Hypertension

Volumn 31, Issue 2, 2013, Pages 333-344

  Brand, Susanne ^a   Amann, Kerstin ^b   Schupp, Nicole ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

8 oxodG; DNA double strand breaks; reactive oxygen species; renin angiotensin system; tempol

Indexed keywords

8 HYDROXYGUANINE; ANGIOTENSIN II; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA MODIFICATION; DOUBLE STRANDED DNA BREAK; GENOTOXICITY; HEART INJURY; HYPERTENSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; KIDNEY INJURY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SYSTOLIC BLOOD PRESSURE;

EID: 84872831417     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0b013e32835ba77e     Document Type: Article

References (62)

1. Grossman E, Messerli FH, Boyko V, Goldbourt U. Is there an association between hypertension and cancer mortality? Am J Med 2002; 112:479-486.
2. Corrao G, Scotti L, Bagnardi V, Sega R. Hypertension, antihypertensive therapy and renal-cell cancer: a meta-analysis. Curr Drug Safety 2007; 2:125-133.
3. Sipahi I, Debanne SM, Rowland DY, Simon DI, Fang JC. Angiotensinreceptor blockade and risk of cancer: meta-analysis of randomised controlled trials. Lancet Oncol 2010; 11:627-636.
4. Bangalore S, Kumar S, Kjeldsen SE, Makani H, Grossman E, Wetterslev J, et al. Antihypertensive drugs and risk of cancer: network metaanalyses and trial sequential analyses of 324 168 participants from randomised trials. Lancet Oncol 2011; 12:65-82.
5. Pasternak B, Svanstrom H, Callreus T, Melbye M, Hviid A. Use of angiotensin receptor blockers and the risk of cancer. Circulation 2011; 123:1729-1736.
6. The ARB Trialists Collaboration. Effects of telmisartan, irbesartan, valsartan, candesartan, and losartan on cancers in 15 trials enrolling 138 769 individuals. J Hypertens 2011; 29:623-635.
7. Fryzek JP, Poulsen AH, Johnsen SP, McLaughlin JK, Sorensen HT, Friis S. A cohort study of antihypertensive treatments and risk of renal cell cancer. Br J Cancer 2005; 92:1302-1306.
8. Shapiro JA, Williams MA, Weiss NS, Stergachis A, LaCroix AZ, Barlow WE. Hypertension, antihypertensive medication use, and risk of renal cell carcinoma. Am J Epidemiol 1999; 149: 521-530.
9. Laragh JH, Lewis K. Dahl Memorial Lecture. The renin system and four lines of hypertension research. Nephron heterogeneity, the calcium connection, the prorenin vasodilator limb, and plasma renin and heart attack. Hypertension 1992; 20:267-279.
10. Carey RM, Siragy HM. Newly recognized components of the reninangiotensin system: potential roles in cardiovascular and renal regulation. Endocr Rev 2003; 24:261-271.
11. MacKenzie SM, Fraser R, Connell JM, Davies E. Local renin-angiotensin systems and their interactions with extra-adrenal corticosteroid production. J Renin Angiotensin Aldosterone Syst 2002; 3: 214-221.
12. Agarwal R, Campbell RC, Warnock DG. Oxidative stress in hypertension and chronic kidney disease: role of angiotensin II. Semin Nephrol 2004; 24:101-114.
13. Sadoshima J. Cytokine actions of angiotensin II. Circ Res 2000; 86:1187-1189.
14. Deshayes F, Nahmias C. Angiotensin receptors: a new role in cancer? Trends Endocrinol Metab 2005; 16:293-299.
15. Queisser N, Fazeli G, Schupp N. Superoxide anion and hydrogen peroxide-induced signaling and damage in angiotensin II and aldosterone action. Biol Chem 2010; 391:1265-1279.
16. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care 2008; 31 (Suppl 2):S170-S180.
17. Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 2004; 122:339-352.
18. Welch WJ. Intrarenal oxygen and hypertension. Clin Exp Pharmacol Physiol 2006; 33:1002-1005.
19. Biswas SK, de Faria JB. Which comes first: renal inflammation or oxidative stress in spontaneously hypertensive rats? Free Radic Res 2007; 41:216-224.
20. Schupp N, Schmid U, Rutkowski P, Lakner U, Kanase N, Heidland A, et al. 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 2007; 292:F1427-F1434.
21. Schmid U, Stopper H, Schweda F, Queisser N, Schupp N. Angiotensin II induces DNA damage in the kidney. Cancer Res 2008; 68:9239-9246.
22. Westhoff JH, Hilgers KF, Steinbach MP, Hartner A, Klanke B, Amann K, et al. Hypertension induces somatic cellular senescence in rats and humans by induction of cell cycle inhibitor p16INK4a. Hypertension 2008; 52:123-129.
23. Oli RG, Fazeli G, Kuhn W, Walitza S, Gerlach M, Stopper H. No increased chromosomal damage in L-DOPA-treated patients with Parkinson's disease: a pilot study. J Neural Transm 2010; 117:737-746.
24. Schupp N, Kolkhof P, Queisser N, Gartner S, Schmid U, Kretschmer A, et al. Mineralocorticoid receptor-mediated DNA damage in kidneys of DOCA-salt hypertensive rats. FASEB J 2011; 25:968-978.
25. Kawada N, Imai E, Karber A, Welch WJ, Wilcox CS. A mouse model of angiotensin II slow pressor response: role of oxidative stress. J Am Soc Nephrol 2002; 13:2860-2868.
26. Francois H, Athirakul K, Mao L, Rockman H, Coffman TM. Role for thromboxane receptors in angiotensin-II-induced hypertension. Hypertension 2004; 43:364-369.
27. Liao TD, Yang XP, Liu YH, Shesely EG, Cavasin MA, Kuziel WA, et al. Role of inflammation in the development of renal damage and dysfunction in angiotensin II-induced hypertension. Hypertension 2008; 52:256-263.
28. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, et al. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 2005; 112:2677-2685.
29. Wesseling S, Ishola DA Jr, Joles JA, Bluyssen HA, Koomans HA, Braam B. Resistance to oxidative stress by chronic infusion of angiotensin II in mouse kidney is not mediated by the AT2 receptor. Am J Physiol Renal Physiol 2005; 288:F1191-1200.
30. Zimmerman MC, Lazartigues E, Sharma RV, Davisson RL. Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 2004; 95:210-216.
31. Queisser N, Oteiza PI, Stopper H, Oli RG, Schupp N. Aldosterone induces oxidative stress, oxidative DNA damage and NF-kappaBactivation in kidney tubule cells. Mol Carcinog 2011; 50:123-135.
32. Ding H, He Y, Li K, Yang J, Li X, Lu R, et al. Urinary neutrophil gelatinase-associated lipocalin (NGAL) is an early biomarker for renal tubulointerstitial injury in IgA nephropathy. Clin Immunol 2007; 123:227-234.
33. Kuwabara T, Mori K, Mukoyama M, Kasahara M, Yokoi H, Saito Y, et al. Urinary neutrophil gelatinase-associated lipocalin levels reflect damage to glomeruli, proximal tubules, and distal nephrons. Kidney Int 2009; 75:285-294.
34. Fazeli G, Stopper H, Schinzel R, Ni CW, Jo H, Schupp N. Angiotensin II induces DNA damage via AT1 receptor and NADPH oxidase isoform Nox4. Mutagenesis 2012; 27:673-681.
35. Zhong J, Guo D, Chen CB, Wang W, Schuster M, Loibner H, et al. Prevention of angiotensin II-mediated renal oxidative stress, inflammation, and fibrosis by angiotensin-converting enzyme 2. Hypertension 2010; 57:314-322.
36. Polichnowski AJ, Lu L, Cowley AW Jr. Renal injury in angiotensin II\+L-NAME-induced hypertensive rats is independent of elevated blood pressure. Am J Physiol Renal Physiol 2011; 300: F1008-F1016.
37. Inagi R. Oxidative stress in cardiovascular disease: a new avenue toward future therapeutic approaches. Recent Pat Cardiovasc Drug Discov 2006; 1:151-159.
38. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-20-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2009; 27:120-139.
39. Kovacs G, Akhtar M, Beckwith BJ, Bugert P, Cooper CS, Delahunt B, et al. The Heidelberg classification of renal cell tumours. J Pathol 1997; 183:131-133.
40. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, et al. GammaH2AX and cancer. Nat Rev Cancer 2008; 8: 957-967.
41. Huang X, Halicka HD, Traganos F, Tanaka T, Kurose A, Darzynkiewicz Z. Cytometric assessment of DNA damage in relation to cell cycle phase and apoptosis. Cell Prolif 2005; 38:223-243.
42. Solier S, Pommier Y. The apoptotic ring: a novel entity with phosphorylated histones H2AX and H2B and activated DNA damage response kinases. Cell Cycle 2009; 8:1853-1859.
43. Wilcox CS. Effects of tempol and redox-cycling nitroxides in models of oxidative stress. Pharmacol Ther 2010; 126:119-145.
44. Wilcox CS, Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 2008; 60: 418-469.
45. Qin Z, Gongora MC, Ozumi K, Itoh S, Akram K, Ushio-Fukai M, et al. Role of Menkes ATPase in angiotensin II-induced hypertension: a key modulator for extracellular superoxide dismutase function. Hypertension 2008; 52:945-951.
46. Xue B, Zhao Y, Johnson AK, Hay M. Central estrogen inhibition of angiotensin II-induced hypertension in male mice and the role of reactive oxygen species. Am J Physiol Heart Circ Physiol 2008; 295:H1025-H1032.
47. Adams GN, LaRusch GA, Stavrou E, Zhou Y, Nieman MT, Jacobs GH, et al. Murine prolylcarboxypeptidase depletion induces vascular dysfunction with hypertension and faster arterial thrombosis. Blood 2011; 117:3929-3937.
48. Ohashi N, Katsurada A, Miyata K, Satou R, Saito T, Urushihara M, et al. Role of activated intrarenal reactive oxygen species and renin-angiotensin system in IgA nephropathy model mice. Clin Exp Pharmacol Physiol 2009; 36:750-755.
49. Yagi S, Akaike M, Aihara K, Ishikawa K, Iwase T, Ikeda Y, et al. Endothelial nitric oxide synthase-independent protective action of statin against angiotensin II-induced atrial remodeling via reduced oxidant injury. Hypertension 2010; 55:918-923.
50. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, et al. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res 2010; 107:106-116.
51. Nakabeppu Y, Sakumi K, Sakamoto K, Tsuchimoto D, Tsuzuki T, Nakatsu Y. Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids. Biol Chem 2006; 387:373-379.
52. Trapp C, Schwarz M, Epe B. The peroxisome proliferator WY-14 643 promotes hepatocarcinogenesis caused by endogenously generated oxidative DNA base modifications in repair-deficient Csbm/m/Ogg1-/-mice. Cancer Res 2007; 67:5156-5161.
53. Polichnowski AJ, Jin C, Yang C, Cowley AW Jr. Role of renal perfusion pressure versus angiotensin II on renal oxidative stress in angiotensin II-induced hypertensive rats. Hypertension 2010; 55:1425-1430.
54. Park E, Shin JI, Park OJ, Kang MH. Soy isoflavone supplementation alleviates oxidative stress and improves systolic blood pressure in male spontaneously hypertensive rats. J Nutr Sci Vitaminol (Tokyo) 2005; 51:254-259.
55. Yildiz A, Gur M, Yilmaz R, Demirbag R, Celik H, Aslan M, et al. Lymphocyte DNA damage and total antioxidant status in patients with white-coat hypertension and sustained hypertension. Turk Kardiyol Dern Ars 2008; 36:231-238.
56. Negishi H, Ikeda K, Sagara M, Sawamura M, Yamori Y. Increased oxidative DNA damage in stroke-prone spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 1999; 26:482-484.
57. Espinosa O, Jimenez-Almazan J, Chaves FJ, Tormos MC, Clapes S, Iradi A, et al. Urinary 8-oxo-7,8-dihydro-20-deoxyguanosine (8-oxo-dG), a reliable oxidative stress marker in hypertension. Free Radic Res 2007; 41:546-554.
58. Almeida MR, de Oliveira Lima E, da Silva VJ, Campos MG, Antunes LM, Salman AK, et al. Genotoxic studies in hypertensive and normotensive rats treated with amiodarone. Mutat Res 2008; 657:155-159.
59. Bennett WM. Drug interactions and consequences of sodium restriction. Am J Clin Nutr 1997; 65:678S-681S.
60. Iwanami J, Mogi M, Iwai M, Horiuchi M. Inhibition of the reninangiotensin system and target organ protection. Hypertens Res 2009; 32:229-237.
61. Putnam K, Shoemaker R, Yiannikouris F, Cassis LA. The renin-angiotensin system: a target of and contributor to dyslipidemias, altered glucose homeostasis, and hypertension of the metabolic syndrome. Am J Physiol Heart Circ Physiol 2012; 302:H1219-1230.
62. Huang CC, Chan WL, Chen YC, Chen TJ, Lin SJ, Chen JW, et al. Angiotensin II receptor blockers and risk of cancer in patients with systemic hypertension. Am J Cardiol 2011; 107:1028-1033.