Atrial overexpression of angiotensin-converting enzyme 2 improves the canine rapid atrial pacing-induced structural and electrical remodeling: Fan, ACE2 improves atrial substrate remodeling

Basic Research in Cardiology

Volumn 110, Issue 4, 2015, Pages

  Fan, Jinqi ^a   Zou, Lili ^a   Cui, Kun ^a   Woo, Kamsang ^b   Du, Huaan ^a   Chen, Shaojie ^a   Ling, Zhiyu ^a   Zhang, Quanjun ^a   Zhang, Bo ^a   Lan, Xianbin ^a   Su, Li ^a   Zrenner, Bernhard ^c   Yin, Yuehui ^a  

^a THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c Krankenhaus Landshut Achdorf   (Germany)

Author keywords

Angiotensin converting enzyme 2; Atrial fibrillation; Atrial remodeling; Gene therapy; Renin angiotensin system

Indexed keywords

ADENOVIRUS VECTOR; ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; ANGIOTENSIN[1-7]; COLLAGEN TYPE 1; COLLAGEN TYPE 3; CONNEXIN 40; CONNEXIN 43; ENHANCED GREEN FLUORESCENT PROTEIN; KV4.2 PROTEIN; KV4.3 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; DIPEPTIDYL CARBOXYPEPTIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE DURATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION REGULATION; GENE THERAPY; GENE TRANSFER; HEART ATRIUM PACING; HEART ATRIUM REMODELING; HEART MUSCLE FIBROSIS; HEART RATE; IN VIVO STUDY; MALE; MONGREL DOG; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SHAM PROCEDURE; UPREGULATION; ADENOVIRIDAE; ANIMAL; ATRIAL FIBRILLATION; DOG; GENETICS; HEART ATRIUM; HEART PACING; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADENOVIRIDAE; ANIMALS; ATRIAL FIBRILLATION; ATRIAL REMODELING; CARDIAC PACING, ARTIFICIAL; DOGS; DUAL SPECIFICITY PHOSPHATASE 1; FEMALE; GENETIC THERAPY; HEART ATRIA; MALE; MAP KINASE SIGNALING SYSTEM; PEPTIDYL-DIPEPTIDASE A; RENIN-ANGIOTENSIN SYSTEM;

EID: 84937564343     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0499-0     Document Type: Article

References (43)

1. Adam O, Lohfelm B, Thum T, Gupta SK, Puhl SL, Schafers HJ, Bohm M, Laufs U (2012) Role of miR-21 in the pathogenesis of atrial fibrosis. Basic Res Cardiol 107:278. doi:10.1007/s00395-012-0278-0
2. Amit G, Kikuchi K, Greener ID, Yang L, Novack V, Donahue JK (2010) Selective molecular potassium channel blockade prevents atrial fibrillation. Circulation 121:2263–2270. doi:10.1161/CIRCULATIONAHA.109.911156
3. Bolderman RW, Bruin P, Hermans JJ, Boerakker MJ, Dias AA, van der Veen FH, Maessen JG (2010) Atrium-targeted drug delivery through an amiodarone-eluting bilayered patch. J Thorac Cardiovasc Surg 140:904–910. doi:10.1016/j.jtcvs.2010.01.021
4. Bosch RF, Scherer CR, Rub N, Wohrl S, Steinmeyer K, Haase H, Busch AE, Seipel L, Kuhlkamp V (2003) Molecular mechanisms of early electrical remodeling: transcriptional downregulation of ion channel subunits reduces I(Ca, L) and I(to) in rapid atrial pacing in rabbits. J Am Coll Cardiol 41:858–869
5. Caunt CJ, Keyse SM (2013) Dual-specificity MAP kinase phosphatases (MKPs): shaping the outcome of MAP kinase signalling. FEBS J 280:489–504. doi:10.1111/j.1742-4658.2012.08716.x
6. Choudhary R, Palm-Leis A, Scott RR, Guleria RS, Rachut E, Baker KM, Pan J (2008) All-trans retinoic acid prevents development of cardiac remodeling in aortic banded rats by inhibiting the renin–angiotensin system. Am J Physiol Heart Circ Physiol 294:H633–H644. doi:10.1152/ajpheart.01301.2007
7. Coutinho DCO, Monnerat-Cahli G, Ferreira AJ, Medei E (2014) Activation of angiotensin-converting enzyme 2 improves cardiac electrical changes in ventricular repolarization in streptozotocin-induced hyperglycaemic rats. EUROPACE 16:1689–1696. doi:10.1093/europace/euu070
8. Cui K, Fan J, Kao G, Ling Z, Yin Y, Su L (2011) A Method for Highly Effective Gene Transfer into Atrial Myocardium by “Painting” on Atrial Epicardial in Canine. Chinese Journal of Biochemistry and Molecular Biology. 27:1167–1173
9. Dobrev D, Carlsson L, Nattel S (2012) Novel molecular targets for atrial fibrillation therapy. NAT REV DRUG DISCOV 11:275–291. doi:10.1038/nrd3682
10. Dobrev D, Nattel S (2011) New insights into the molecular basis of atrial fibrillation: mechanistic and therapeutic implications. Cardiovasc Res 89:689–691. doi:10.1093/cvr/cvr021
11. Dong B, Yu QT, Dai HY, Gao YY, Zhou ZL, Zhang L, Jiang H, Gao F, Li SY, Zhang YH, Bian HJ, Liu CX, Wang N, Xu H, Pan CM, Song HD, Zhang C, Zhang Y (2012) Angiotensin-converting enzyme-2 overexpression improves left ventricular remodeling and function in a rat model of diabetic cardiomyopathy. J Am Coll Cardiol 59:739–747. doi:10.1016/j.jacc.2011.09.071
12. Donoghue M, Wakimoto H, Maguire CT, Acton S, Hales P, Stagliano N, Fairchild-Huntress V, Xu J, Lorenz JN, Kadambi V, Berul CI, Breitbart RE (2003) Heart block, ventricular tachycardia, and sudden death in ACE2 transgenic mice with downregulated connexins. J Mol Cell Cardiol 35:1043–1053
13. Ehrlich JR, Hohnloser SH, Nattel S (2006) Role of angiotensin system and effects of its inhibition in atrial fibrillation: clinical and experimental evidence. Eur Heart J 27:512–518. doi:10.1093/eurheartj/ehi668
14. Ferreira AJ, Santos RA, Almeida AP (2001) Angiotensin-(1–7): cardioprotective effect in myocardial ischemia/reperfusion. Hypertension 38:665–668. doi:10.1161/01.HYP.38.3.665
15. Ferreira AJ, Shenoy V, Qi Y, Fraga-Silva RA, Santos RA, Katovich MJ, Raizada MK (2011) Angiotensin-converting enzyme 2 activation protects against hypertension-induced cardiac fibrosis involving extracellular signal-regulated kinases. Exp Physiol 96:287–294. doi:10.1113/expphysiol.2010.055277
16. Goette A, Lendeckel U (2004) Expression of angiotensin II receptors in human left and right atrial tissue in atrial fibrillation with and without underlying mitral valve disease. J Am Coll Cardiol 43(2363):2363–2364. doi:10.1016/j.jacc.2004.03.026
17. Hall MC, Kirubakaran S, Chowdhury R, Abidin N, Peters NS, Garratt CJ (2010) Effects of angiotensin receptor blockade on atrial electrical remodeling and the ‘second factor’ in a goat burst-paced model of atrial fibrillation. J Renin Angiotensin Aldosterone Syst 11:222–233. doi:10.1177/1470320310369604
18. He X, Gao X, Peng L, Wang S, Zhu Y, Ma H, Lin J, Duan DD (2011) Atrial fibrillation induces myocardial fibrosis through angiotensin II type 1 receptor-specific Arkadia-mediated downregulation of Smad7. Circ Res 108:164–175. doi:10.1161/CIRCRESAHA.110.234369
19. Hussain W, Patel PM, Chowdhury RA, Cabo C, Ciaccio EJ, Lab MJ, Duffy HS, Wit AL, Peters NS (2010) The Renin–Angiotensin system mediates the effects of stretch on conduction velocity, connexin43 expression, and redistribution in intact ventricle. J Cardiovasc Electrophysiol 21:1276–1283. doi:10.1111/j.1540-8167.2010.01802.x
20. Ichiki T, Takeda K, Tokunou T, Funakoshi Y, Ito K, Iino N, Takeshita A (2001) Reactive oxygen species-mediated homologous downregulation of angiotensin II type 1 receptor mRNA by angiotensin II. Hypertension 37:535–540
21. Kikuchi K, McDonald AD, Sasano T, Donahue JK (2005) Targeted modification of atrial electrophysiology by homogeneous transmural atrial gene transfer. Circulation 111:264–270. doi:10.1161/01.CIR.0000153338.47507.83
22. Kumagai K, Nakashima H, Urata H, Gondo N, Arakawa K, Saku K (2003) Effects of angiotensin II type 1 receptor antagonist on electrical and structural remodeling in atrial fibrillation. J Am Coll Cardiol 41:2197–2204. doi:10.1016/S0735-1097(03)00464-9
23. Li D, Shinagawa K, Pang L, Leung TK, Cardin S, Wang Z, Nattel S (2001) Effects of angiotensin-converting enzyme inhibition on the development of the atrial fibrillation substrate in dogs with ventricular tachypacing-induced congestive heart failure. Circulation 104:2608–2614. doi:10.1161/hc4601.099402
24. Li Y, Li WM, Gong YT, Li BX, Liu W, Han W, Dong D, Sheng L, Xue JY, Zhang L, Chu S, Yang BF (2007) The effects of cilazapril and valsartan on the mRNA and protein expressions of atrial calpains and atrial structural remodeling in atrial fibrillation dogs. Basic Res Cardiol 102:245–256. doi:10.1007/s00395-007-0641-8
25. Liang B, Wang X, Zhang N, Yang H, Bai R, Liu M, Bian Y, Xiao C, Yang Z (2015) Angiotensin-(1–7) Attenuates Angiotensin II-Induced ICAM-1, VCAM-1, and MCP-1 Expression via the MAS Receptor Through Suppression of P38 and NF-kappaB Pathways in HUVECs. Cell Physiol Biochem 35:2472–2482. doi:10.1159/000374047
26. Liu E, Yang S, Xu Z, Li J, Yang W, Li G (2010) Angiotensin-(1–7) prevents atrial fibrosis and atrial fibrillation in long-term atrial tachycardia dogs. Regul Pept 162:73–78. doi:10.1016/j.regpep.2009.12.020
27. McCollum LT, Gallagher PE, Ann TE (2012) Angiotensin-(1–7) attenuates angiotensin II-induced cardiac remodeling associated with upregulation of dual-specificity phosphatase 1. Am J Physiol Heart Circ Physiol 302:H801–H810. doi:10.1152/ajpheart.00908.2011
28. McCollum LT, Gallagher PE, Tallant EA (2012) Angiotensin-(1–7) abrogates mitogen-stimulated proliferation of cardiac fibroblasts. Peptides 34:380–388. doi:10.1016/j.peptides.2012.01.020
29. Michael G, Xiao L, Qi XY, Dobrev D, Nattel S (2009) Remodelling of cardiac repolarization: how homeostatic responses can lead to arrhythmogenesis. Cardiovasc Res 81:491–499. doi:10.1093/cvr/cvn266
30. Nakashima H, Kumagai K, Urata H, Gondo N, Ideishi M, Arakawa K (2000) Angiotensin II antagonist prevents electrical remodeling in atrial fibrillation. Circulation 101:2612–2617
31. Pan CH, Lin JL, Lai LP, Chen CL, Stephen HS, Lin CS (2007) Downregulation of angiotensin converting enzyme II is associated with pacing-induced sustained atrial fibrillation. FEBS Lett 581:526–534. doi:10.1016/j.febslet.2007.01.014
32. Pellman J, Lyon RC, Sheikh F (2010) Extracellular matrix remodeling in atrial fibrosis: mechanisms and implications in atrial fibrillation. J Mol Cell Cardiol 48:461–467. doi:10.1016/j.yjmcc.2009.09.001
33. Polontchouk L, Haefliger JA, Ebelt B, Schaefer T, Stuhlmann D, Mehlhorn U, Kuhn-Regnier F, De Vivie ER, Dhein S (2001) Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J Am Coll Cardiol 38:883–891. doi:10.1016/S0735-1097(01)01443-7
34. Schotten U, Verheule S, Kirchhof P, Goette A (2011) Pathophysiological mechanisms of atrial fibrillation: a translational appraisal. Physiol Rev 91:265–325. doi:10.1152/physrev.00031.2009
35. Sovari AA, Iravanian S, Dolmatova E, Jiao Z, Liu H, Zandieh S, Kumar V, Wang K, Bernstein KE, Bonini MG, Duffy HS, Dudley SC (2011) Inhibition of c-Src tyrosine kinase prevents angiotensin II-mediated connexin-43 remodeling and sudden cardiac death. J Am Coll Cardiol 58:2332–2339. doi:10.1016/j.jacc.2011.07.048
36. Tsai CT, Lai LP, Hwang JJ, Chen WP, Chiang FT, Hsu KL, Tseng CD, Tseng YZ, Lin JL (2008) Renin-angiotensin system component expression in the HL-1 atrial cell line and in a pig model of atrial fibrillation. J Hypertens 26:570–582. doi:10.1097/HJH.0b013e3282f34a4a
37. Tsai CT, Lai LP, Kuo KT, Hwang JJ, Hsieh CS, Hsu KL, Tseng CD, Tseng YZ, Chiang FT, Lin JL (2008) Angiotensin II activates signal transducer and activators of transcription 3 via Rac1 in atrial myocytes and fibroblasts: implication for the therapeutic effect of statin in atrial structural remodeling. Circulation 117:344–355. doi:10.1161/CIRCULATIONAHA.107.695346
38. Tsai CT, Wang DL, Chen WP, Hwang JJ, Hsieh CS, Hsu KL, Tseng CD, Lai LP, Tseng YZ, Chiang FT, Lin JL (2007) Angiotensin II increases expression of alpha1C subunit of L-type calcium channel through a reactive oxygen species and cAMP response element-binding protein-dependent pathway in HL-1 myocytes. Circ Res 100:1476–1485. doi:10.1161/01.RES.0000268497.93085.e1
39. Voigt N, Heijman J, Wang Q, Chiang DY, Li N, Karck M, Wehrens XH, Nattel S, Dobrev D (2014) Cellular and molecular mechanisms of atrial arrhythmogenesis in patients with paroxysmal atrial fibrillation. Circulation 129:145–156. doi:10.1161/CIRCULATIONAHA.113.006641
40. von LD, Kockskamper J, Rubertus SU, Zhu D, Schmitto JD, Schondube FA, Hasenfuss G, Pieske B (2008) Direct pro-arrhythmogenic effects of angiotensin II can be suppressed by AT1 receptor blockade in human atrial myocardium. EUR J HEART FAIL 10:1172–1176. doi:10.1016/j.ejheart.2008.09.014
41. Yue L, Melnyk P, Gaspo R, Wang Z, Nattel S (1999) Molecular mechanisms underlying ionic remodeling in a dog model of atrial fibrillation. Circ Res 84:776–784. doi:10.1161/01.RES.84.7.776
42. Zhao J, Xu W, Yun F, Zhao H, Li W, Gong Y, Yuan Y, Yan S, Zhang S, Ding X, Wang D, Zhang C, Dong D, Xiu C, Yang N, Liu L, Xue J, Li Y (2014) Chronic obstructive sleep apnea causes atrial remodeling in canines: mechanisms and implications. Basic Res Cardiol 109:427. doi:10.1007/s00395-014-0427-8
43. Zhong J, Basu R, Guo D, Chow FL, Byrns S, Schuster M, Loibner H, Wang XH, Penninger JM, Kassiri Z, Oudit GY (2010) Angiotensin-converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation 122(717–728):18–728. doi:10.1161/CIRCULATIONAHA.110.955369