Renal denervation reduces atrial remodeling in hypertensive rats with metabolic syndrome.


Journal

Basic research in cardiology
ISSN: 1435-1803
Titre abrégé: Basic Res Cardiol
Pays: Germany
ID NLM: 0360342

Informations de publication

Date de publication:
14 07 2022
Historique:
received: 21 01 2021
accepted: 26 06 2022
revised: 22 06 2022
entrez: 14 7 2022
pubmed: 15 7 2022
medline: 19 7 2022
Statut: epublish

Résumé

Atrial fibrillation (AF) is highly prevalent in hypertensive patients with metabolic syndrome and is related to inflammation and activation of the sympathoadrenergic system. The multi-ligand Receptor-for-Advanced-Glycation-End-products (RAGE) activates inflammation-associated tissue remodeling and is regulated by the sympathetic nervous system. Its counterpart, soluble RAGE (sRAGE), serves as anti-inflammatory decoy receptor with protective properties. We investigated the effect of sympathetic modulation by renal denervation (RDN) on atrial remodeling, RAGE/sRAGE and RAGE ligands in metabolic syndrome. RDN was performed in spontaneously hypertensive obese rats (SHRob) with metabolic syndrome compared with lean spontaneously hypertensive rats (SHR) and with normotensive non-obese control rats. Blood pressure and heart rate were measured by telemetry. The animals were killed 12 weeks after RDN. Left atrial (LA) and right atrial (RA) remodeling was assessed by histological analysis and collagen types. Sympathetic innervation was measured by tyrosine hydroxylase staining of atrial nerve fibers, RAGE/sRAGE, RAGE ligands, cytokine expressions and inflammatory infiltrates were analyzed by Western blot and immunofluorescence staining. LA sympathetic nerve fiber density was higher in SHRob (+44%) versus controls and reduced after RDN (-64% versus SHRob). RAGE was increased (+718%) and sRAGE decreased (- 62%) in SHRob as compared with controls. RDN reduced RAGE expression (- 61% versus SHRob), significantly increased sRAGE levels (+162%) and induced a significant decrease in RAGE ligand levels in SHRob (- 57% CML and - 51% HMGB1) with reduced pro-inflammatory NFkB activation (- 96%), IL-6 production (- 55%) and reduced inflammatory infiltrates. This led to a reduction in atrial fibrosis (- 33%), collagen type I content (- 72%), accompanied by reduced LA myocyte hypertrophy (- 21%). Transfection experiments on H9C2 cardiomyoblasts demonstrated that RAGE is directly involved in fibrosis formation by influencing cellular production of collagen type I. In conclusion, suppression of renal sympathetic nerve activity by RDN prevents atrial remodeling in metabolic syndrome by reducing atrial sympathetic innervation and by modulating RAGE/sRAGE balance and reducing pro-inflammatory and pro-fibrotic RAGE ligands, which provides a potential therapeutic mechanism to reduce the development of AF.

Identifiants

pubmed: 35834066
doi: 10.1007/s00395-022-00943-6
pii: 10.1007/s00395-022-00943-6
pmc: PMC9283368
doi:

Substances chimiques

Ager protein, rat 0
Collagen Type I 0
Ligands 0
Receptor for Advanced Glycation End Products 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

36

Informations de copyright

© 2022. The Author(s).

Références

Azizi M, Schmieder RE, Mahfoud F, Weber MA, Daemen J, Davies J, Basile J, Kirtane AJ, Wang Y, Lobo MD, Saxena M, Feyz L, Rader F, Lurz P, Sayer J, Sapoval M, Levy T, Sanghvi K, Abraham J, Sharp ASP, Fisher NDL, Bloch MJ, Reeve-Stoffer H, Coleman L, Mullin C, Mauri L, Investigators RADIANCE-HTN (2018) Endovascular ultrasound renal denervation to treat hypertension (RADIANCE-HTN SOLO): a multicentre, international, single-blind, randomised, sham-controlled trial. Lancet 391:2335–2345. https://doi.org/10.1016/S0140-6736(18)31082-1
doi: 10.1016/S0140-6736(18)31082-1
Baumann M, Stehouwer C, Scheijen J, Heemann U, Struijker Boudier H, Schalkwijk C (2008) N epsilon-(carboxymethyl)lysine during the early development of hypertension. Ann NY Acad Sci 1126:201–204. https://doi.org/10.1196/annals.1433.004
doi: 10.1196/annals.1433.004
Begieneman MP, Rijvers L, Kubat B, Paulus WJ, Vonk AB, van Rossum AC, Schalkwijk CG, Stooker W, Niessen HW, Krijnen PA (2015) Atrial fibrillation coincides with the advanced glycation end product N(ε)-(carboxymethyl)lysine in the atrium. Am J Pathol 185:2096–2104. https://doi.org/10.1016/j.ajpath.2015.04.018
doi: 10.1016/j.ajpath.2015.04.018
Böhm M, Linz D, Urban D, Mahfoud F, Ukena C (2013) Renal sympathetic denervation: applications in hypertension and beyond. Nat Rev Cardiol 10:465–476. https://doi.org/10.1038/nrcardio.2013.89
doi: 10.1038/nrcardio.2013.89
Böhm M, Mahfoud F, Ukena C, Hoppe UC, Narkiewicz K, Negoita M, Ruilope L, Schlaich MP, Schmieder RE, Whitbourn R, Williams B, Zeymer U, Zirlik A, Mancia G, Investigators GSR (2015) First report of the Global SYMPLICITY registry on the effect of renal artery denervation in patients with uncontrolled hypertension. Hypertension 65:766–774. https://doi.org/10.1161/HYPERTENSIONAHA.114.05010
doi: 10.1161/HYPERTENSIONAHA.114.05010
Carnagarin R, Kiuchi MG, Ho JK, Matthews VB, Schlaich MP (2019) Sympathetic nervous system activation and its modulation: role in atrial fibrillation. Front Neurosci 12:1058. https://doi.org/10.3389/fnins.2018.01058
doi: 10.3389/fnins.2018.01058
Chung MK, Martin DO, Sprecher D, Wazni O, Kanderian A, Carnes CA, Bauer JA, Tchou PJ, Niebauer MJ, Natale A, Van Wagoner DR (2001) C-reactive protein elevation in patients with atrial arrhythmias: inflammatory mechanisms and persistence of atrial fibrillation. Circulation 104:2886–2891. https://doi.org/10.1161/hc4901.101760
doi: 10.1161/hc4901.101760
Donazzan L, Mahfoud F, Ewen S, Ukena C, Cremers B, Kirsch CM, Hellwig D, Eweiwi T, Ezziddin S, Esler M, Böhm M (2016) Effects of catheter-based renal denervation on cardiac sympathetic activity and innervation in patients with resistant hypertension. Clin Res Cardiol 105:364–371. https://doi.org/10.1007/s00392-015-0930-4
doi: 10.1007/s00392-015-0930-4
Dörr O, Liebetrau C, Möllmann H, Gaede L, Troidl C, Rixe J, Hamm C, Nef H (2014) Soluble fms-like tyrosine kinase-1 and endothelial adhesion molecules (intercellular cell adhesion molecule-1 and vascular cell adhesion molecule-1) as predictive markers for blood pressure reduction after renal sympathetic denervation. Hypertension 63:984–990
doi: 10.1161/HYPERTENSIONAHA.113.02266
Dyer MR, Chen Q, Haldeman S, Yazdani H, Hoffman R, Loughran P, Tsung A, Zuckerbraun BS, Simmons RL, Neal MD (2018) Deep vein thrombosis in mice is regulated by platelet HMGB1 through release of neutrophil-extracellular traps and DNA. Sci Rep 8:2068. https://doi.org/10.1038/s41598-018-20479-x
doi: 10.1038/s41598-018-20479-x
Egaña-Gorroño L, López-Díez R, Yepuri G, Ramirez LS, Reverdatto S, Gugger PF, Shekhtman A, Ramasamy R, Schmidt AM (2020) Receptor for Advanced Glycation End Products (RAGE) and mechanisms and therapeutic opportunities in diabetes and cardiovascular disease: insights from human subjects and animal models. Front Cardiovasc Med 10(7):37. https://doi.org/10.3389/fcvm.2020.00037
doi: 10.3389/fcvm.2020.00037
Eiros R, Romero-González G, Gavira JJ, Beloqui O, Colina I, Fortún Landecho M, López B, González A, Díez J, Ravassa S (2020) Does chronic kidney disease facilitate malignant myocardial fibrosis in heart failure with preserved ejection fraction of hypertensive origin? J Clin Med. https://doi.org/10.3390/jcm9020404
doi: 10.3390/jcm9020404
Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stern DM, Schmidt AM (2001) Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 159:513–525. https://doi.org/10.1016/S0002-9440(10)61723-3
doi: 10.1016/S0002-9440(10)61723-3
Grammer JB, Böhm J, Dufour A, Benz M, Lange R, Bauernschmitt R (2005) Atrial fibrosis in heart surgery patients: decreased collagen III/I ratio in postoperative atrial fibrillation. Basic Res Cardiol 100:288–294. https://doi.org/10.1007/s00395-005-0515-x
doi: 10.1007/s00395-005-0515-x
Hohl M, Lau DH, Müller A, Elliott AD, Linz B, Mahajan R, Hendriks JML, Böhm M, Schotten U, Sanders P, Linz D (2017) Concomitant obesity and metabolic syndrome add to the atrial arrhythmogenic phenotype in male hypertensive rats. J Am Heart Assoc 6:e006717. https://doi.org/10.1161/JAHA.117.006717
doi: 10.1161/JAHA.117.006717
Huang QT, Zhang M, Zhong M, Yu YH, Liang WZ, Hang LL, Gao YF, Huang LP, Wang ZJ (2013) Advanced glycation end products as an upstream molecule triggers ROS-induced sFlt-1 production in extravillous trophoblasts: a novel bridge between oxidative stress and preeclampsia. Placenta 34:1177–1182
doi: 10.1016/j.placenta.2013.09.017
Hudson BI, Lippman ME (2018) Targeting RAGE signaling in inflammatory disease. Annu Rev Med 69:349–364. https://doi.org/10.1146/annurev-med-041316-085215
doi: 10.1146/annurev-med-041316-085215
Huiliang Q, Chunlan J, Wei L, Yuchi W, Zhaoyu L, Qizhan L, Zheng X, Xusheng L, Huanlin W, Wei J, Chuan Z (2018) Chronic kidney disease increases atrial fibrillation inducibility: involvement of inflammation, atrial fibrosis, and connexins. Front Physiol 9:1726. https://doi.org/10.3389/fphys.2018.01726
doi: 10.3389/fphys.2018.01726
Huo JY, Jiang WY, Geng J, Chen C, Zhu L, Chen R, Ge TT, Chang Q, Jiang ZX, Shan QJ (2019) Renal denervation attenuates pressure overload-induced cardiac remodelling in rats with biphasic regulation of autophagy. Acta Physiol (Oxf) 226:e13272. https://doi.org/10.1111/apha.13272
doi: 10.1111/apha.13272
Jalife J, Kaur K (2015) Atrial remodeling, fibrosis, and atrial fibrillation. Trends Cardiovasc Med 25:475–484. https://doi.org/10.1016/j.tcm.2014.12.015
doi: 10.1016/j.tcm.2014.12.015
Kandzari DE, Böhm M, Mahfoud F, Townsend RR, Weber MA, Pocock S, Tsioufis K, Tousoulis D, Choi JW, East C, Brar S, Cohen SA, Fahy M, Pilcher G, Kario K, Trial Investigators SPYRALHTN-ONMED (2018) Effect of renal denervation on blood pressure in the presence of antihypertensive drugs: 6-month efficacy and safety results from the SPYRAL HTN-ON MED proof-of-concept randomised trial. Lancet 391:2346–2355. https://doi.org/10.1016/S0140-6736(18)30951-6
doi: 10.1016/S0140-6736(18)30951-6
Kato T, Yamashita T, Sekiguchi A, Tsuneda T, Sagara K, Takamura M, Kaneko S, Aizawa T, Fu LT (2008) AGEs-RAGE system mediates atrial structural remodeling in the diabetic rat. J Cardiovasc Electrophysiol 19:415–420. https://doi.org/10.1111/j.1540-8167.2007.01037.x
doi: 10.1111/j.1540-8167.2007.01037.x
Katsurada K, Nandi SS, Sharma NM, Patel KP (2021) Enhanced expression and function of renal SGLT2 (Sodium-Glucose Cotransporter 2) in heart failure: role of renal nerves. Circ Heart Fail 14:e008365. https://doi.org/10.1161/CIRCHEARTFAILURE.121.008365
doi: 10.1161/CIRCHEARTFAILURE.121.008365
Katsurada K, Nandi SS, Zheng H, Liu X, Sharma NM, Patel KP (2020) GLP-1 mediated diuresis and natriuresis are blunted in heart failure and restored by selective afferent renal denervation. Cardiovasc Diabetol 19:57. https://doi.org/10.1186/s12933-020-01029-0
doi: 10.1186/s12933-020-01029-0
Lancefield TF, Patel SK, Freeman M, Velkoska E, Wai B, Srivastava PM, Horrigan M, Farouque O, Burrell LM (2016) The receptor for advanced glycation end products (RAGE) is associated with persistent atrial fibrillation. PLoS One 11:e0161715. https://doi.org/10.1371/journal.pone.0161715
doi: 10.1371/journal.pone.0161715
Lau DH, Shipp NJ, Kelly DJ, Thanigaimani S, Neo M, Kuklik P, Lim HS, Zhang Y, Drury K, Wong CX, Chia NH, Brooks AG, Dimitri H, Saint DA, Brown L, Sanders P (2013) Atrial arrhythmia in ageing spontaneously hypertensive rats: unraveling the substrate in hypertension and ageing. PLoS One 8:e72416. https://doi.org/10.1371/journal.pone.0072416
doi: 10.1371/journal.pone.0072416
Linz D, Hohl M, Mahfoud F, Reil JC, Linz W, HeubschleT JHP, Neumann H, Aflin C, Reutten H, Böhm M (2012) Cardiac remodeling and myocardial dysfunction in obese spontaneously hypertensive rats. J Transl Med 10:187. https://doi.org/10.1186/1479-5876-10-187
doi: 10.1186/1479-5876-10-187
Linz D, Hohl M, Nickel A, Mahfoud F, Wagner M, Ewen S, Schotten U, Maack C, Wirth K, Böhm M (2013) Effect of renal denervation on neurohumoral activation triggering atrial fibrillation in obstructive sleep apnea. Hypertension 62:767–774. https://doi.org/10.1161/HYPERTENSIONAHA.113.01728
doi: 10.1161/HYPERTENSIONAHA.113.01728
Linz D, Hohl M, Schutze J, Mahfoud F, Speer T, Linz B, Hubschle T, Juretschke HP, Dechend R, Geisel J, Rutten H, Böhm M (2014) Progression of kidney injury and cardiac remodeling in obese spontaneously hypertensive rats: the role of renal sympathetic innervation. Am J Hypertens 28:256–265. https://doi.org/10.1093/ajh/hpu123
doi: 10.1093/ajh/hpu123
Linz D, van Hunnik A, Hohl M, Mahfoud F, Wolf M, Neuberger HR, Casadei B, Reilly SN, Verheule S, Böhm M, Schotten U (2015) Catheter-based renal denervation reduces atrial nerve sprouting and complexity of atrial fibrillation in goats. Circ Arrhythm Electrophysiol 8:466–474. https://doi.org/10.1161/CIRCEP.114.002453
doi: 10.1161/CIRCEP.114.002453
Linz D, Ukena C, Mahfoud F, Neuberger HR, Böhm M (2013) Atrial autonomic innervation: a target for interventional antiarrhythmic therapy? J Am Coll Cardiol 63:215–224. https://doi.org/10.1016/j.jacc.2013.09.020
doi: 10.1016/j.jacc.2013.09.020
Liu Q, Zhang Q, Wang K, Wang S, Lu D, Li Z, Geng J, Fang P, Wang Y, Shan Q (2015) Renal denervation findings on cardiac and renal fibrosis in rats with isoproterenol induced cardiomyopathy. Sci Rep 5:18582. https://doi.org/10.1038/srep18582
doi: 10.1038/srep18582
Lotze MT, Tracey KJ (2005) High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 5:331–342. https://doi.org/10.1038/nri1594
doi: 10.1038/nri1594
Mahajan R, Lau DH, Brooks AG, Shipp NJ, Manavis J, Wood JP, Finnie JW, Samuel CS, Royce SG, Twomey DJ, Thanigaimani S, Kalman JM, Sanders P (2015) Electrophysiological, electroanatomical, and structural remodeling of the atria as consequences of sustained obesity. J Am Coll Cardiol 66:1–11. https://doi.org/10.1016/j.jacc.2015.04.058
doi: 10.1016/j.jacc.2015.04.058
McManus DD, Saczynski JS, Ward JA, Jaggi K, Bourrell P, Darling C, Goldberg RJ (2012) The relationship between atrial fibrillation and chronic kidney disease: epidemiologic and pathophysiologic considerations for a dual epidemic. J Atr Fibrill 5:442. https://doi.org/10.4022/jafib.442
doi: 10.4022/jafib.442
Pathak RK, Middeldorp ME, Lau DH, Mehta AB, Mahajan R, Twomey D, Alasady M, Hanley L, Antic NA, McEvoy RD, Kalman JM, Abhayaratna WP, Sanders P (2014) Aggressive risk factor reduction study for atrial fibrillation and implications for the outcome of ablation: the ARREST-AF cohort study. J Am Coll Cardiol 64:2222–2231. https://doi.org/10.1016/j.jacc.2014.09.028
doi: 10.1016/j.jacc.2014.09.028
Pathak RK, Middeldorp ME, Meredith M, Mehta AB, Mahajan R, Wong CX, Twomey D, Elliott AD, Kalman JM, Abhayaratna WP, Lau DH, Sanders P (2015) Long term effect of goal-directed weight management in an atrial fibrillation cohort: a long-term follow-up study (LEGACY). J Am Coll Cardiol 65:2159–2169. https://doi.org/10.1016/j.jacc.2015.03.002
doi: 10.1016/j.jacc.2015.03.002
Peng Y, Kim JM, Park HS, Yang A, Islam C, Lakatta EG, Lin L (2016) AGE-RAGE signal generates a specific NF-κB RelA “barcode” that directs collagen I expression. Sci Rep 6:18822. https://doi.org/10.1038/srep18822
doi: 10.1038/srep18822
Polhemus DJ, Trivedi RK, Gao J, Li Z, Scarborough AL, Goodchild TT, Varner KJ, Xia H, Smart FW, Kapusta DR, Lefer DJ (2017) Renal sympathetic denervation protects the failing heart via inhibition of neprilysin activity in the kidney. J Am Coll Cardiol 70:2139–2153. https://doi.org/10.1016/j.jacc.2017.08.056
doi: 10.1016/j.jacc.2017.08.056
Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME (2008) A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 22:3716–3727. https://doi.org/10.1096/fj.08-109033
doi: 10.1096/fj.08-109033
Santilli F, Blardi P, Scapellato C, Bocchia M, Guazzi G, Terzuoli L, Tabucchi A, Silvietti A, Lucani B, Gioffrè WR, Scarpini F, Fazio F, Davì G (2015) Decreased plasma endogenous soluble RAGE, and enhanced adipokine secretion, oxidative stress and platelet/coagulative activation identify non-alcoholic fatty liver disease among patients with familial combined hyperlipidemia and/or metabolic syndrome. Vascul Pharmacol 72:16–24. https://doi.org/10.1016/j.vph.2015.04.004
doi: 10.1016/j.vph.2015.04.004
Sárkány Z, Ikonen TP, Ferreira-da-Silva F, Saraiva MJ, Svergun D, Damas AM (2011) Solution structure of the soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 286:37525–37534. https://doi.org/10.1074/jbc.M111.223438
doi: 10.1074/jbc.M111.223438
Schleicher ED, Wagner E, Nerlich AG (1997) Increased accumulation of the glycoxidation product N(epsilon)-(carboxymethyl)lysine in human tissues in diabetes and aging. J Clin Invest 99:457–468. https://doi.org/10.1172/JCI119180
doi: 10.1172/JCI119180
Schotten U, Verheule S, Kirchhof P, Goette A (2011) Pathophysiological mechanisms of atrial fibrillation: a translational appraisal. Physiol Rev 91:265–325. https://doi.org/10.1152/physrev.00031.2009
doi: 10.1152/physrev.00031.2009
Selejan SR, Linz D, Tatu AM, Hohl M, Speer T, Ewen S, Mahfoud F, Kindermann I, Zamyatkin O, Kazakov A, Laufs U, Böhm M (2018) Sympathoadrenergic suppression improves heart function by upregulating the ratio of sRAGE/RAGE in hypertension with metabolic syndrome. J Mol Cell Cardiol 122:34–46. https://doi.org/10.1016/j.yjmcc.2018.08.003
doi: 10.1016/j.yjmcc.2018.08.003
Shimizu T, Yamakuchi M, Biswas KK, Aryal B, Yamada S, Hashiguchi T, Maruyama I (2016) HMGB1 is secreted by 3T3-L1 adipocytes through JNK signaling and the secretion is partially inhibited by adiponectin. Obesity (Silver Spring) 24:1913–1921. https://doi.org/10.1002/oby.21549
doi: 10.1002/oby.21549
Soliman EZ, Prineas RJ, Go AS, Xie D, Lash JP, Rahman M, Ojo A, Teal VL, Jensvold NG, Robinson NL, Dries DL, Bazzano L, Mohler ER, Wright JT, Feldman HI, Chronic Renal Insufficiency Cohort (CRIC) Study Group (2010) Chronic kidney disease and prevalent atrial fibrillation: the Chronic Renal Insufficiency Cohort (CRIC). Am Heart J 159:1102–1107. https://doi.org/10.1016/j.ahj.2010.03.027
doi: 10.1016/j.ahj.2010.03.027
Steinberg JS, Shabanov V, Ponomarev D, Losik D, Ivanickiy E, Kropotkin E, Polyakov K, Ptaszynski P, Keweloh B, Yao CJ, Pokushalov EA, Romanov AB (2020) Effect of renal denervation and catheter ablation vs catheter ablation alone on atrial fibrillation recurrence among patients with paroxysmal atrial fibrillation and hypertension: the ERADICATE-AF randomized clinical trial. JAMA 323:248–255. https://doi.org/10.1001/jama.2019.21187
doi: 10.1001/jama.2019.21187
Sun X, Wei Z, Li Y, Wang J, Hu J, Yin Y, Xie J, Xu B (2020) Renal denervation restrains the inflammatory response in myocardial ischemia-reperfusion injury. Basic Res Cardiol 115:15. https://doi.org/10.1007/s00395-020-0776-4
doi: 10.1007/s00395-020-0776-4
Takaya K, Ogawa Y, Hiraoka J, Hosoda K, Yamori Y, Nakao K, Koletsky RJ (1996) Nonsense mutation of leptin receptor in the obese spontaneously hypertensive Koletsky rat. Nat Genet 14:130–131. https://doi.org/10.1038/ng1096-130
doi: 10.1038/ng1096-130
Veiga GL, Nishi EE, Estrela HF, Lincevicius GS, Gomes GN, Simões Sato AY, Campos RR, Bergamaschi CT (2016) Total renal denervation reduces sympathoexcitation to different target organs in a model of chronic kidney disease. Auton Neurosci pii S1566–0702(16):30269–30277. https://doi.org/10.1016/j.autneu.2016.11.006
doi: 10.1016/j.autneu.2016.11.006
Waldron NH, Fudim M, Mathew JP, Piccini JP (2019) Neuromodulation for the treatment of heart rhythm disorders. JACC Basic Transl Sci 4:546–562. https://doi.org/10.1016/j.jacbts.2019.02.009
doi: 10.1016/j.jacbts.2019.02.009
Wang X, Desai K, Clausen JT, Wu L (2004) Increased methylglyoxal and advanced glycation end products in kidney from spontaneously hypertensive rats. Kidney Int 66:2315–2321
doi: 10.1111/j.1523-1755.2004.66034.x
Wang N, Zheng X, Qian J, Yao W, Bai L, Hou G, Qiu X, Li X, Jiang X (2017) Renal sympathetic denervation alleviates myocardial fibrosis following isoproterenol-induced heart failure. Mol Med Rep 16:5091–5098. https://doi.org/10.3892/mmr.2017.7255
doi: 10.3892/mmr.2017.7255
Wang Y, Zhong J, Zhang X, Liu Z, Yang Y, Gong Q, Ren B (2016) The role of HMGB1 in the pathogenesis of type 2 diabetes. J Diabetes Res 2016:2543268. https://doi.org/10.1155/2016/2543268
doi: 10.1155/2016/2543268
Winkelmayer WC, Patrick AR, Liu J, Brookhart MA, Setoguchi S (2011) The increasing prevalence of atrial fibrillation among hemodialysis patients. J Am Soc Nephrol 22:349–357. https://doi.org/10.1681/ASN.2010050459
doi: 10.1681/ASN.2010050459
Van de Wouw J, Sorop O, Van Drie RWA, Joles JA, Danser AHJ, Verhaar MC, Merkus D, Duncker DJ (2021) Reduced nitric oxide bioavailability impairs myocardial oxygen balance during exercise in swine with multiple risk factors. Basic Res Cardiol 116:50. https://doi.org/10.1007/s00395-021-00890-8
doi: 10.1007/s00395-021-00890-8
Wyatt CM, Textor SC (2018) Emerging evidence on renal denervation for the treatment of hypertension. Kidney Int 94:644–646. https://doi.org/10.1016/j.kint.2018.08.002
doi: 10.1016/j.kint.2018.08.002
Xu Q, Bo L, Hu J, Geng J, Chen Y, Li X, Chen F, Song J (2018) High mobility group box 1 was associated with thrombosis in patients with atrial fibrillation. Medicine (Baltimore) 97:e0132. https://doi.org/10.1097/MD.0000000000010132
doi: 10.1097/MD.0000000000010132
Yamada S, Fong MC, Hsiao YW, Chang SL, Tsai YN, Lo LW, Chao TF, Lin YJ, Hu YF, Chung FP, Liao JN, Chang YT, Li HY, Higa S, Chen SA (2018) Impact of renal denervation on atrial arrhythmogenic substrate in ischemic model of heart failure. J Am Heart Assoc 7:e007312. https://doi.org/10.1161/JAHA.117.007312
doi: 10.1161/JAHA.117.007312
Yang PS, Kim TH, Uhm JS, Park S, Joung B, Lee MH, Pak HN (2016) High plasma level of soluble RAGE is independently associated with a low recurrence of atrial fibrillation after catheter ablation in diabetic patient. Europace 18:1711–1718. https://doi.org/10.1093/europace/euv449
doi: 10.1093/europace/euv449
Zhang L, Bukulin M, Kojro E, Roth A, Metz VV, Fahrenholz F, Nawroth PP, Bierhaus A, Postina R (2008) Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 283:35507–35516. https://doi.org/10.1074/jbc.M806948200
doi: 10.1074/jbc.M806948200
Zhang Q, Li G, Liu T (2013) Receptor for advanced glycation end products (RAGE): novel biomarker and therapeutic target for atrial fibrillation. Int J Cardiol 168:4802–4804. https://doi.org/10.1016/j.ijcard.2013.07.038
doi: 10.1016/j.ijcard.2013.07.038
Zhang J, Zhang L, Zhang S, Yu Q, Xiong F, Huang K, Wang CY, Yang P (2017) HMGB1, an innate alarmin, plays a critical role in chronic inflammation of adipose tissue in obesity. Mol Cell Endocrinol 454:103–111. https://doi.org/10.1016/j.mce.2017.06.012
doi: 10.1016/j.mce.2017.06.012
Zhao J, Randive R, Stewart JA (2014) Molecular mechanisms of AGE/RAGE-mediated fibrosis in the diabetic heart. World J Diabetes 5:860–867. https://doi.org/10.4239/wjd.v5.i6.860
doi: 10.4239/wjd.v5.i6.860
Zheng H, Katsurada K, Liu X, Knuepfer MM, Patel KP (2018) Specific afferent renal denervation prevents reduction in neuronal nitric oxide synthase within the paraventricular nucleus in rats with chronic heart failure. Hypertension 72:667–675. https://doi.org/10.1161/HYPERTENSIONAHA.118.11071
doi: 10.1161/HYPERTENSIONAHA.118.11071
Zheng H, Liu X, Sharma NM, Patel KP (2016) Renal denervation improves cardiac function in rats with chronic heart failure: effects on expression of β-adrenoceptors. Am J Physiol Heart Circ Physiol 311:H337–H346. https://doi.org/10.1152/ajpheart.00999.2015
doi: 10.1152/ajpheart.00999.2015
Zhu W, Tsang S, Browe DM, Woo AY, Huang Y, Xu C, Liu JF, Lv F, Zhang Y, Xiao RP (2016) Interaction of β1-adrenoceptor with RAGE mediates cardiomyopathy via CaMKII signaling. JCI Insight 1:e84969. https://doi.org/10.1172/jci.insight.84969
doi: 10.1172/jci.insight.84969

Auteurs

Simina-Ramona Selejan (SR)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany. simina.selejan@uks.eu.

Dominik Linz (D)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Muriel Mauz (M)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Mathias Hohl (M)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Anh Khoa Dennis Huynh (AKD)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Thimoteus Speer (T)

Klinik für Innere Medizin IV (Nephrologie und Hochdruckkrankheiten), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Homburg/Saar, Germany.

Jan Wintrich (J)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Andrey Kazakov (A)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Christian Werner (C)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Felix Mahfoud (F)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

Michael Böhm (M)

Klinik für Innere Medizin III (Kardiologie, Angiologie und Internistische Intensivmedizin), Universitätsklinikum des Saarlandes und Medizinische Fakultät der Universität des Saarlandes, Kirrbergerstr. 100, Geb. 41.1 (IMED), 66421, Homburg/Saar, Germany.

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