Renal denervation prevents stroke and brain injury via attenuation of oxidative stress in hypertensive rats

Journal of the American Heart Association

Volumn 2, Issue 5, 2013, Pages

  Nakagawa, Takashi ^a   Hasegawa, Yu ^a   Uekawa, Ken ^a   Ma, Mingjie ^a   Katayama, Tetsuji ^a   Sueta, Daisuke ^a   Toyama, Kensuke ^a   Kataoka, Keiichiro ^a   Koibuchi, Nobutaka ^a   Maeda, Masanobu ^b   Kuratsu, Jun Ichi ^a   Kim Mitsuyama, Shokei ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

Hypertension; Oxidative stress; Renal denervation; Stroke; Sympathetic nerve

Indexed keywords

HYDRALAZINE; PROTEIN P67; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD PRESSURE REGULATION; BRAIN BLOOD FLOW; BRAIN INJURY; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; DEATH; ENDOTHELIAL DYSFUNCTION; HEART DISEASE; HYPERTENSION; KIDNEY DENERVATION; MACROPHAGE MIGRATION; MALE; MICROGLIA; NERVE CELL STIMULATION; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; RAT; SHAM PROCEDURE; STROKE PRONE SPONTANEOUSLY HYPERTENSIVE RAT; VASCULAR ENDOTHELIUM; WHITE MATTER LESION; ANIMAL; BLOOD PRESSURE; BRAIN DISEASE; DENERVATION; INNERVATION; KIDNEY; METABOLISM; SPONTANEOUSLY HYPERTENSIVE RAT; SYMPATHETIC NERVE; BRAIN DISEASES; COMPLICATION; STROKE; SURGERY;

HYPERTENSION; OXIDATIVE STRESS; RENAL DENERVATION; STROKE; SYMPATHETIC NERVE;

ANIMALS; BLOOD PRESSURE; BRAIN DISEASES; DENERVATION; HYPERTENSION; KIDNEY; MALE; OXIDATIVE STRESS; RATS, INBRED SHR; STROKE;

EID: 84891699355     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.113.000375     Document Type: Article

References (43)

1. Campese VM. A new model of neurogenic hypertension caused by renal injury: pathophysiology and therapeutic implications. Clin Exp Nephrol. 2003;7: 167-171.
2. Campese VM, Kogosov E, Koss M. Renal afferent denervation prevents the progression of renal disease in the renal ablation model of chronic renal failure in the rat. Am J Kidney Dis. 1995;26:861-865.
3. Dampney RA. Functional organization of central pathways regulating the cardiovascular system. Physiol Rev. 1994;74:323-364.
4. DiBona GF, Kopp UC. Neural control of renal function. Physiol Rev. 1997;77:75-197.
5. Schlaich MP, Sobotka PA, Krum H, Whitbourn R, Walton A, Esler MD. Renal denervation as a therapeutic approach for hypertension: novel implications for an old concept. Hypertension. 2009;54:1195-1201.
6. Campese VM, Kogosov E. Renal afferent denervation prevents hypertension in rats with chronic renal failure. Hypertension. 1995;25:878-882.
7. Krum H, Schlaich M, Whitbourn R, Sobotka PA, Sadowski J, Bartus K, Kapelak B, Walton A, Sievert H, Thambar S, Abraham WT, Esler M. Catheter-based renal sympathetic denervation for resistant hypertension: a multicentre safety and proof-of-principle cohort study. Lancet. 2009;373:1275-1281.
8. Symplicity HTNI, Esler MD, Krum H, Sobotka PA, Schlaich MP, Schmieder RE, Bohm M. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial. Lancet. 2010;376:1903-1909.
9. Schlaich MP, Sobotka PA, Krum H, Lambert E, Esler MD. Renal sympatheticnerve ablation for uncontrolled hypertension. N Engl J Med. 2009;361: 932-934.
10. Brandt MC, Mahfoud F, Reda S, Schirmer SH, Erdmann E, Bohm M, Hoppe UC. Renal sympathetic denervation reduces left ventricular hypertrophy and improves cardiac function in patients with resistant hypertension. J Am Coll Cardiol. 2012;59:901-909.
11. Linz D, Mahfoud F, Schotten U, Ukena C, Hohl M, Neuberger HR, Wirth K, Bohm M. Renal sympathetic denervation provides ventricular rate control but does not prevent atrial electrical remodeling during atrial fibrillation. Hypertension. 2013;61:225-231.
12. Nakamura T, Yamamoto E, Kataoka K, Yamashita T, Tokutomi Y, Dong YF, Matsuba S, Ogawa H, Kim-Mitsuyama S. Pioglitazone exerts protective effects against stroke in stroke-prone spontaneously hypertensive rats, independently of blood pressure. Stroke. 2007;38:3016-3022.
13. Luippold G, Beilharz M, Muhlbauer B. Chronic renal denervation prevents glomerular hyperfiltration in diabetic rats. Nephrol Dial Transplant. 2004; 19:342-347.
14. Sueta D, Kataoka K, Koibuchi N, Toyama K, Uekawa K, Katayama T, Mingjie M, Nakagawa T, Waki H, Maeda M, Yasuda O, Matsui K, Ogawa H, Kim-Mitsuyama S. Novel mechanism for disrupted circadian blood pressure rhythm in a rat model of metabolic syndrome-the critical role of angiotensin II. J Am Heart Assoc. 2013;2:e000035.
15. Dong YF, Kataoka K, Tokutomi Y, Nako H, Nakamura T, Toyama K, Sueta D, Koibuchi N, Yamamoto E, Ogawa H, Kim-Mitsuyama S. Beneficial effects of combination of valsartan and amlodipine on salt-induced brain injury in hypertensive rats. J Pharmacol Exp Ther. 2011;339:358-366.
16. Wakita H, Tomimoto H, Akiguchi I, Kimura J. Glial activation and white matter changes in the rat brain induced by chronic cerebral hypoperfusion: an immunohistochemical study. Acta Neuropathol. 1994;87:484-492.
17. Richmon JD, Fukuda K, Maida N, Sato M, Bergeron M, Sharp FR, Panter SS, Noble LJ. Induction of heme oxygenase-1 after hyperosmotic opening of the blood-brain barrier. Brain Res. 1998;780:108-118.
18. Tsubokawa T, Solaroglu I, Yatsushige H, Cahill J, Yata K, Zhang JH. Cathepsin and calpain inhibitor E64D attenuates matrix metalloproteinase-9 activity after focal cerebral ischemia in rats. Stroke. 2006;37:1888-1894.
19. Yamamoto E, Yamashita T, Tanaka T, Kataoka K, Tokutomi Y, Lai ZF, Dong YF, Matsuba S, Ogawa H, Kim-Mitsuyama S. Pravastatin enhances beneficial effects of olmesartan on vascular injury of salt-sensitive hypertensive rats, via pleiotropic effects. Arterioscler Thromb Vasc Biol. 2007; 27:556-563.
20. Yamamoto E, Tamamaki N, Nakamura T, Kataoka K, Tokutomi Y, Dong YF, Fukuda M, Matsuba S, Ogawa H, Kim-Mitsuyama S. Excess salt causes cerebral neuronal apoptosis and inflammation in stroke-prone hypertensive rats through angiotensin II-induced NADPH oxidase activation. Stroke. 2008; 39:3049-3056.
21. Yamamoto E, Kataoka K, Shintaku H, Yamashita T, Tokutomi Y, Dong YF, Matsuba S, Ichijo H, Ogawa H, Kim-Mitsuyama S. Novel mechanism and role of angiotensin II induced vascular endothelial injury in hypertensive diastolic heart failure. Arterioscler Thromb Vasc Biol. 2007;27: 2569-2575.
22. Symplicity HTNI. Catheter-based renal sympathetic denervation for resistant hypertension: durability of blood pressure reduction out to 24 months. Hypertension. 2011;57:911-917.
23. Kim-Mitsuyama S, Yamamoto E, Tanaka T, Zhan Y, Izumi Y, Izumiya Y, Ioroi T, Wanibuchi H, Iwao H. Critical role of angiotensin II in excess salt-induced brain oxidative stress of stroke-prone spontaneously hypertensive rats. Stroke. 2005;36:1083-1088.
24. He J, Ogden LG, Vupputuri S, Bazzano LA, Loria C, Whelton PK. Dietary sodium intake and subsequent risk of cardiovascular disease in overweight adults. JAMA. 1999;282:2027-2034.
25. Meneton P, Jeunemaitre X, de Wardener HE, MacGregor GA. Links between dietary salt intake, renal salt handling, blood pressure, and cardiovascular diseases. Physiol Rev. 2005;85:679-715.
26. Morimoto A, Uzu T, Fujii T, Nishimura M, Kuroda S, Nakamura S, Inenaga T, Kimura G. Sodium sensitivity and cardiovascular events in patients with essential hypertension. Lancet. 1997;350:1734-1737.
27. Perry IJ, Beevers DG. Salt intake and stroke: a possible direct effect. J Hum Hypertens. 1992;6:23-25.
28. Strazzullo P, D'Elia L, Kandala NB, Cappuccio FP. Salt intake, stroke, and cardiovascular disease: meta-analysis of prospective studies. BMJ. 2009;339: b4567.
29. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis. 2004;16:1-13.
30. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci. 2003;4:399-415.
31. Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab. 2001;21:2-14.
32. Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov. 2011;10:453-471.
33. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol. 2010;87:779-789.
34. Kahles T, Brandes RP. NADPH oxidases as therapeutic targets in ischemic stroke. Cell Mol Life Sci. 2012;69:2345-2363.
35. Dahlof B, Devereux RB, Kjeldsen SE, Julius S, Beevers G, de Faire U, Fyhrquist F, Ibsen H, Kristiansson K, Lederballe-Pedersen O, Lindholm LH, Nieminen MS, Omvik P, Oparil S, Wedel H, Group LS. Cardiovascular morbidity and mortality in the losartan intervention for endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet. 2002;359:995-1003.
36. Schrader J, Luders S, Kulschewski A, Hammersen F, Plate K, Berger J, Zidek W, Dominiak P, Diener HC, Group MS. Morbidity and mortality after stroke, eprosartan compared with nitrendipine for secondary prevention: principal results of a prospective randomized controlled study (MOSES). Stroke. 2005;36:1218-1226.
37. Campese VM. Neurogenic factors and hypertension in renal disease. Kidney Int Suppl. 2000;75:S2-S6.
38. Siddiqi L, Joles JA, Grassi G, Blankestijn PJ. Is kidney ischemia the central mechanism in parallel activation of the renin and sympathetic system? J Hypertens. 2009;27:1341-1349.
39. Ye S, Zhong H, Yanamadala S, Campese VM. Oxidative stress mediates the stimulation of sympathetic nerve activity in the phenol renal injury model of hypertension. Hypertension. 2006;48:309-315.
40. Converse RL Jr, Jacobsen TN, Toto RD, Jost CM, Cosentino F, Fouad-Tarazi F, Victor RG. Sympathetic overactivity in patients with chronic renal failure. N Engl J Med. 1992;327:1912-1918.
41. Ligtenberg G, Blankestijn PJ, Oey PL, Klein IH, Dijkhorst-Oei LT, Boomsma F, Wieneke GH, van Huffelen AC, Koomans HA. Reduction of sympathetic hyperactivity by enalapril in patients with chronic renal failure. N Engl J Med. 1999;340:1321-1328.
42. Hering D, Lambert EA, Marusic P, Walton AS, Krum H, Lambert GW, Esler MD, Schlaich MP. Substantial reduction in single sympathetic nerve firing after renal denervation in patients with resistant hypertension. Hypertension. 2013;61:457-464.
43. Mahfoud F, Schlaich M, Kindermann I, Ukena C, Cremers B, Brandt MC, Hoppe UC, Vonend O, Rump LC, Sobotka PA, Krum H, Esler M, Bohm M. Effect of renal sympathetic denervation on glucose metabolism in patients with resistant hypertension: a pilot study. Circulation. 2011;123:1940-1946.