Modulation of the sympathetic nervous system by renal denervation prevents reduction of aortic distensibility in atherosclerosis prone ApoE-deficient rats

Journal of Translational Medicine

Volumn 14, Issue 1, 2016, Pages

  Hohl, Mathias ^a   Linz, Dominik ^a   Fries, Peter ^a   Müller, Andreas ^a   Stroeder, Jonas ^a   Urban, Daniel ^a   Speer, Thimoteus ^a   Geisel, Jürgen ^a   Hummel, Björn ^a   Laufs, Ulrich ^a   Schirmer, Stephan H ^a   Böhm, Michael ^a   Mahfoud, Felix ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Aortic distensibility; ApoE deficient rats; Hypercholesterolemia; Renal sympathetic denervation

Indexed keywords

ALDOSTERONE; APOLIPOPROTEIN E; COLLAGEN; NORADRENALIN; CARBACHOL; GLYCERYL TRINITRATE;

ADRENERGIC SYSTEM; ALDOSTERONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA MEDIA; AORTIC RING (SLICE); ARTERY COMPLIANCE; ARTERY DILATATION; ARTICLE; ASCENDING AORTA; ATHEROSCLEROSIS; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FIBROSIS; HYPERCHOLESTEROLEMIA; KIDNEY DENERVATION; NEUROMODULATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RAT; ANIMAL; AORTA; BLOOD PRESSURE; BODY WEIGHT; DEFICIENCY; DENERVATION; DISEASE COURSE; DRUG EFFECTS; HEART FUNCTION TEST; IN VITRO STUDY; INFLAMMATION; INNERVATION; KIDNEY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SPRAGUE DAWLEY RAT; VASCULAR ENDOTHELIUM; VASODILATATION;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOOD PRESSURE; BODY WEIGHT; CARBACHOL; DENERVATION; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; FIBROSIS; HEART FUNCTION TESTS; IN VITRO TECHNIQUES; INFLAMMATION; KIDNEY; NITROGLYCERIN; NOREPINEPHRINE; RATS, SPRAGUE-DAWLEY; RENIN-ANGIOTENSIN SYSTEM; SYMPATHETIC NERVOUS SYSTEM; VASODILATION;

EID: 84975745665     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-016-0914-9     Document Type: Article

References (39)

1. Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol. 2011. doi: 10.1016/j.jacc.2010.12.017.
2. Wang YX, Halks-Miller M, Vergona R, Sullivan ME, Fitch R, Mallari C, Martin-McNulty B, da Cunha V, Freay A, Rubanyi GM, Kauser K. Increased aortic stiffness assessed by pulse wave velocity in apolipoprotein E-deficient mice. Am J Physiol Heart Circ Physiol. 2000. doi: 10.1161/HYPERTENSIONAHA.114.04648.
3. Levenson J, Del Pino M, Razavian M, Merli I, Filitti V, Simon A. Hypercholesterolaemia alters arterial and blood factors related to atherosclerosis in hypertension. Atherosclerosis. 1992;95:171-9.
4. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD, Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res. 1998. doi: 10.1161/01.RES.82.12.1298.
5. Zieman SJ, Melenovsky V, Kass DA. Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol. 2005. doi: 10.1161/01.ATV.0000160548.78317.29.
6. Wassmann S, Stumpf M, Strehlow K, Schmid A, Schieffer B, Böhm M, Nickenig G. Interleukin-6 induces oxidative stress and endothelial dysfunction by overexpression of the angiotensin II type 1 receptor. Circ Res. 2004. doi: 10.1161/01.RES.0000115557.25127.8D.
7. Dinenno FA, Jones PP, Seals DR, Tanaka H. Age-associated arterial wall thickening is related to elevations in sympathetic activity in healthy humans. Am J Physiol Heart Circ Physiol. 2000;278:1205-10.
8. Pauletto P, Scannapieco G, Pessina AC. Sympathetic drive and vascular damage in hypertension and atherosclerosis. Hypertension. 1991;17(Suppl 4):III75-81.
9. Azizi M, Sapoval M, Gosse P, Monge M, Bobrie G, Delsart P, Midulla M, Mounier-Véhier C, Courand PY, Lantelme P, Denolle T, Dourmap-Collas C, Trillaud H, Pereira H, Plouin PF, Chatellier G. Renal denervation for hypertension (DENERHTN) investigators. Optimum and stepped care standardised antihypertensive treatment with or without renal denervation for resistant hypertension (DENERHTN): a multicentre, open-label, randomised controlled trial. Lancet. 2015. doi: 10.1016/S0140-6736(14)61942-5.
10. Krum H, Schlaich MP, Sobotka PA, Böhm M, Mahfoud F, Rocha-Singh K, Katholi R, Esler MD. Percutaneous renal denervation in patients with treatment-resistant hypertension: final 3-year report of the symplicity HTN-1 study. Lancet. 2014. doi: 10.1016/S0140-6736(13)62192-3.
11. Mahfoud F, Schlaich M, Kindermann I, Ukena C, Cremers B, Brandt MC, Hoppe UC, Vonend O, Rump LC, Sobotka PA, Krum H, Esler M, Böhm M. Effect of renal sympathetic denervation on glucose metabolism in patients with resistant hypertension: a pilot study. Circulation. 2011. doi: 10.1161/CIRCULATIONAHA.110.991869.
12. Kopp UC, Jones SY, DiBona GF. Afferent renal denervation impairs baroreflex control of efferent renal sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol. 2008. doi: 10.1152/ajpregu.90529.2008.
13. Böhm M, Linz D, Urban D, Mahfoud F, Ukena C. Renal sympathetic denervation: applications in hypertension and beyond. Nat Rev Cardiol. 2013. doi: 10.1038/nrcardio.2013.89.
14. Linz D, Ukena C, Mahfoud F, Neuberger HR, Böhm M. Atrial autonomic innervation: a target for interventional antiarrhythmic therapy? J Am Coll Cardiol. 2014. doi: 10.1016/j.jacc.2013.09.020.
15. Brandt MC, Reda S, Mahfoud F, Lenski M, Böhm M, Hoppe UC. Effects of renal sympathetic denervation on arterial stiffness and central hemodynamics in patients with resistant hypertension. J Am Coll Cardiol. 2012. doi: 10.1016/j.jacc.2012.08.959.
16. Linz D, Hohl M, Schütze J, Mahfoud F, Speer T, Linz B, Hübschle T, Juretschke HP, Dechend R, Geisel J, Rütten H, Böhm M. Progression of kidney injury and cardiac remodeling in obese spontaneously hypertensive rats: the role of renal sympathetic innervation. Am J Hypertens. 2015. doi: 10.1093/ajh/hpu123.
17. Linz D, van Hunnik A, Hohl M, Mahfoud F, Wolf M, Neuberger HR, Casadei B, Reilly SN, Verheule S, Böhm M, Schotten U. Catheter-based renal denervation reduces atrial nerve sprouting and complexity of atrial fibrillation in goats. Circ Arrhythm Electrophysiol. 2015. doi: 10.1161/CIRCEP.114.002453.
18. Wang H, Wang J, Guo C, Luo W, Kleiman K, Eitzman DT. Renal denervation attenuates progression of atherosclerosis in apolipoprotein E-deficient mice independent of blood pressure lowering. Hypertension. 2015. doi: 10.1161/HYPERTENSIONAHA.114.04648.
19. Tomofuji T, Ekuni D, Azuma T, Irie K, Endo Y, Kasuyama K, Yoneda T, Morita M. Involvement of toll-like receptor 2 and 4 in association between dyslipidemia and osteoclast differentiation in apolipoprotein E deficient rat periodontium. Lipids Health Dis. 2013. doi: 10.1186/1476-511X-12-1.
20. Schlimmer N, Kratz M, Böhm M, Baumhäkel M. Telmisartan, ramipril and their combination improve endothelial function in different tissues in a murine model of cholesterol-induced atherosclerosis. Br J Pharmacol. 2011. doi: 10.1111/j.1476-5381.2011.01267.
21. Kannel WB. Office assessment of coronary candidates and risk factor insights from the Framingham study. J Hypertension. 1991;9:13-9.
22. Schlaich MP, Lambert E, Kaye DM, Krozowski Z, Campbell DJ, Lambert G, Hastings J, Aggarwal A, Esler MD. Sympathetic augmentation in hypertension: role of nerve firing, norepinephrine reuptake, and Angiotensin neuromodulation. Hypertension. 2004. doi: 10.1161/01.HYP.0000103160.35395.9E.
23. Atlas SA. The renin-angiotensin aldosterone system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm. 2007;13(Suppl 8B):9-20.
24. Imanishi M, Tomita S, Ishizawa K, Kihira Y, Ueno M, Izawa-Ishizawa Y, Ikeda Y, Yamano N, Tsuchiya K, Tamaki T. Smooth muscle cell-specific Hif-1α deficiency suppresses angiotensin II-induced vascular remodelling in mice. Cardiovasc Res. 2014. doi: 10.1093/cvr/cvu061.
25. Lin CX, Rhaleb NE, Yang XP, Liao TD, D'Ambrosio MA, Carretero OA. Prevention of aortic fibrosis by N-acetyl-seryl-aspartyl-lysyl-proline in angiotensin II-induced hypertension. Am J Physiol Heart Circ Physiol. 2008. doi: 10.1152/ajpheart.00481.2008.
26. Takai S, Jin D, Muramatsu M, Kirimura K, Sakonjo H, Miyazaki M. Eplerenone inhibits atherosclerosis in nonhuman primates. Hypertension. 2005. doi: 10.1161/01.HYP.0000184640.81730.22.
27. Keidar S, Hayek T, Kaplan M, Pavlotzky E, Hamoud S, Coleman R, Aviram M. Effect of eplerenone, a selective aldosterone blocker, on blood pressure, serum and macrophage oxidative stress, and atherosclerosis in apolipoprotein E-deficient mice. J Cardiovasc Pharmacol. 2003;41:955-63.
28. Fitch RM, Rutledge JC, Wang YX, Powers AF, Tseng JL, Clary T, Rubanyi GM. Synergistic effect of angiotensin II and nitric oxide synthase inhibitor in increasing aortic stiffness in mice. Am J Physiol Heart Circ Physiol. 2006. doi: 10.1152/ajpheart.00327.2005.
29. Harrison DG. Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest. 1997. doi: 10.1172/JCI119751.
30. Wilkinson IB, Qasem A, McEniery CM, Webb DJ, Avolio AP, Cockcroft JR. Nitric oxide regulates local arterial distensibility in vivo. Circulation. 2002. doi: 10.1161/hc0202.101970.
31. Mollnau H, Wendt M, Szöcs K, Lassègue B, Schulz E, Oelze M, Li H, Bodenschatz M, August M, Kleschyov AL, Tsilimingas N, Walter U, Förstermann U, Meinertz T, Griendling K, Münzel T. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ Res. 2002;90:E58-65. doi: 10.1161/01.RES.0000012569.55432.02.
32. Libby P. Inflammation in atherosclerosis. Nature. 2002. doi: 10.1038/nature01323.
33. Viel EC, Lemarié CA, Benkirane K, Paradis P, Schiffrin EL. Immune regulation and vascular inflammation in genetic hypertension. Am J Physiol Heart Circ Physiol. 2010. doi: 10.1152/ajpheart.00707.2009.
34. Steinberg D. Hypercholesterolemia and inflammation in atherogenesis: two sides of the same coin. Mol Nutr Food Res. 2005. doi: 10.1002/mnfr.200500081.
35. Bhatt DL, Kandzari DE, O'Neill WW, D'Agostino R, Flack JM, Katzen BT, Leon MB, Liu M, Mauri L, Negoita M, Cohen SA, Oparil S, Rocha-Singh K, Townsend RR, Bakris GL. SYMPLICITY HTN-3 investigators. A controlled trial of renal denervation for resistant hypertension. N Engl J Med. 2014. doi: 10.1056/NEJMoa1402670.
36. Mahfoud F, Urban D, Teller D, Linz D, Stawowy P, Hassel JH, Fries P, Dreysse S, Wellnhofer E, Schneider G, Buecker A, Schneeweis C, Doltra A, Schlaich MP, Esler MD, Fleck E, Böhm M, Kelle S. Effect of renal denervation on left ventricular mass and function in patients with resistant hypertension: data from a multi-centre cardiovascular magnetic resonance imaging trial. Eur Heart J. 2014. doi: 10.1093/eurheartj/ehu093.
37. Linz D, Hohl M, Nickel A, Mahfoud F, Wagner M, Ewen S, Schotten U, Maack C, Wirth K, Böhm M. Effect of renal denervation on neurohumoral activation triggering atrial fibrillation in obstructive sleep apnea. Hypertension. 2013. doi: 10.1161/HYPERTENSIONAHA.113.01728.
38. Smithwick RH, Thompson JE. Splanchnicectomy for essential hypertension. JAMA. 1953;152:1501-4.
39. Nishikawa T, Suematsu S, Saito J, Soyama A, Ito H, Kino T, Chrousos G. Human renal mesangial cells produce aldosterone in response to low-density lipoprotein (LDL). J Steroid Biochem Mol Biol. 2005;96:309-16.