Intermedin1-53 Attenuates Abdominal Aortic Aneurysm by Inhibiting Oxidative Stress

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 11, 2016, Pages 2176-2190

  Lu, Wei Wei ^a,b   Jia, Li Xin ^a   Ni, Xian Qiang ^a,b   Zhao, Lei ^a,b   Chang, Jin Rui ^a,b   Zhang, Jin Sheng ^a,b   Hou, Yue Long ^a,b   Zhu, Yi ^a,b   Guan, You Fei ^a,b   Yu, Yan Rong ^a,b   Du, Jie ^a   Tang, Chao Shu ^a,b   Qi, Yong Fen ^a,b  

^a CAPITAL MEDICAL UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

abdominal aortic aneurysm; angiotensin II; NAD(P)H oxidase; oxidative stress

Indexed keywords

ANGIOTENSIN II; APOCYNIN; CALCITONIN RECEPTOR LIKE RECEPTOR; CALCIUM CHLORIDE; CD68 ANTIGEN; ELASTIN; GAMMA INTERFERON; INTERLEUKIN 6; INTERMEDIN; INTERMEDIN[1-53]; MATRIX METALLOPROTEINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P47; PROTEIN P53; REACTIVE OXYGEN METABOLITE; RECEPTOR ACTIVITY MODIFYING PROTEIN 1; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; RECEPTOR ACTIVITY MODIFYING PROTEIN 3; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ADM2 PROTEIN, HUMAN; ADRENOMEDULLIN; ANTIOXIDANT; APOLIPOPROTEIN E; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; INTERMEDIN PROTEIN, MOUSE; INTERMEDIN PROTEIN, RAT; NEUROPEPTIDE; PEPTIDE HORMONE;

ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; AORTA MEDIA; APOPTOSIS; ARTERY DIAMETER; ARTICLE; CONTROLLED STUDY; ECHOGRAPHY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE SILENCING; HYPERLIPIDEMIA; IN VITRO STUDY; INFLAMMATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SYSTOLIC BLOOD PRESSURE; VASCULAR SMOOTH MUSCLE CELL; ABDOMINAL AORTA; ANIMAL; AORTIC ANEURYSM, ABDOMINAL; C57BL MOUSE; CELL CULTURE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; GENOTYPE; HUMAN; KNOCKOUT MOUSE; LESIONS AND DEFECTS; METABOLISM; PATHOLOGY; PHENOTYPE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; SPRAGUE DAWLEY RAT; TIME FACTOR; VASCULAR SMOOTH MUSCLE;

ADRENOMEDULLIN; ANGIOTENSIN II; ANIMALS; ANTIOXIDANTS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; APOPTOSIS; CALCIUM CHLORIDE; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; GENOTYPE; HUMANS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; NEUROPEPTIDES; OXIDATIVE STRESS; PEPTIDE HORMONES; PHENOTYPE; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84987879250     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.307825     Document Type: Article

References (48)

1. Davis FM, Rateri DL, Daugherty A. Mechanisms of aortic aneurysm formation: translating preclinical studies into clinical therapies. Heart. 2014; 100: 1498-1505. doi: 10.1136/heartjnl-2014-305648.
2. Michel JB, Martin-Ventura JL, Egido J, Sakalihasan N, Treska V, Lindholt J, Allaire E, Thorsteinsdottir U, Cockerill G, Swedenborg J; FAD EU consortium. Novel aspects of the pathogenesis of aneurysms of the abdominal aorta in humans. Cardiovasc Res. 2011; 90: 18-27. doi: 10.1093/cvr/ cvq337.
3. Yoshimura K, Aoki H. Recent advances in pharmacotherapy development for abdominal aortic aneurysm. Int J Vasc Med. 2012; 2012: 648167. doi: 10.1155/2012/648167.
4. Guzik B, Sagan A, Ludew D, Mrowiecki W, Chwała M, Bujak-Gizycka B, Filip G, Grudzien G, Kapelak B, Zmudka K, Mrowiecki T, Sadowski J, Korbut R, Guzik TJ. Mechanisms of oxidative stress in human aortic aneurysms-association with clinical risk factors for atherosclerosis and disease severity. Int J Cardiol. 2013; 168: 2389-2396. doi: 10.1016/j. ijcard.2013.01.278.
5. Madamanchi NR, Runge MS. Redox signaling in cardiovascular health and disease. Free Radic Biol Med. 2013; 61: 473-501. doi: 10.1016/j. freeradbiomed.2013.04.001.
6. Thomas M, Gavrila D, McCormick ML, Miller FJ Jr, Daugherty A, Cassis LA, Dellsperger KC, Weintraub NL. Deletion of p47phox attenuates angiotensin II-induced abdominal aortic aneurysm formation in apolipoprotein E-deficient mice. Circulation. 2006; 114: 404-413. doi: 10.1161/ CIRCULATIONAHA.105.607168.
7. Gavazzi G, Deffert C, Trocme C, Schäppi M, Herrmann FR, Krause KH. NOX1 deficiency protects from aortic dissection in response to angiotensin II. Hypertension. 2007; 50: 189-196. doi: 10.1161/ HYPERTENSIONAHA.107.089706.
8. Satoh K, Nigro P, Matoba T, O'Dell MR, Cui Z, Shi X, Mohan A, Yan C, Abe J, Illig KA, Berk BC. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med. 2009; 15: 649-656. doi: 10.1038/nm.1958.
9. Raaz U, Toh R, Maegdefessel L, Adam M, Nakagami F, Emrich FC, Spin JM, Tsao PS. Hemodynamic regulation of reactive oxygen species: implications for vascular diseases. Antioxid Redox Signal. 2014; 20: 914-928. doi: 10.1089/ars.2013.5507.
10. Miller FJ Jr, Sharp WJ, Fang X, Oberley LW, Oberley TD, Weintraub NL. Oxidative stress in human abdominal aortic aneurysms: a potential mediator of aneurysmal remodeling. Arterioscler Thromb Vasc Biol. 2002; 22: 560-565.
11. Xiong W, Mactaggart J, Knispel R, Worth J, Zhu Z, Li Y, Sun Y, Baxter BT, Johanning J. Inhibition of reactive oxygen species attenuates aneurysm formation in a murine model. Atherosclerosis. 2009; 202: 128-134. doi: 10.1016/j.atherosclerosis.2008.03.029.
12. Konior A, Schramm A, Czesnikiewicz-Guzik M, Guzik TJ. NADPH oxidases in vascular pathology. Antioxid Redox Signal. 2014; 20: 2794-2814. doi: 10.1089/ars.2013.5607.
13. Kato J, Tsuruda T, Kita T, Kitamura K, Eto T. Adrenomedullin: a protective factor for blood vessels. Arterioscler Thromb Vasc Biol. 2005; 25: 2480-2487. doi: 10.1161/01.ATV.0000184759.91369.f8.
14. Roh J, Chang CL, Bhalla A, Klein C, Hsu SY. Intermedin is a calcitonin/ calcitonin gene-related peptide family peptide acting through the calcitonin receptor-like receptor/receptor activity-modifying protein receptor complexes. J Biol Chem. 2004; 279: 7264-7274. doi: 10.1074/jbc.M305332200.
15. Bell D, McDermott BJ. Intermedin (adrenomedullin-2): a novel counter- regulatory peptide in the cardiovascular and renal systems. Br J Pharmacol. 2008; 153(suppl 1): S247-S262. doi: 10.1038/sj.bjp.0707494.
16. Morimoto R, Satoh F, Murakami O, Totsune K, Suzuki T, Sasano H, Ito S, Takahashi K. Expression of adrenomedullin2/intermedin in human brain, heart, and kidney. Peptides. 2007; 28: 1095-1103. doi: 10.1016/j. peptides.2007.01.018.
17. Cai Y, Xu MJ, Teng X, Zhou YB, Chen L, Zhu Y, Wang X, Tang CS, Qi YF. Intermedin inhibits vascular calcification by increasing the level of matrix gamma-carboxyglutamic acid protein. Cardiovasc Res. 2010; 85: 864-873. doi: 10.1093/cvr/cvp366.
18. Dai XY, Cai Y, Mao DD, Qi YF, Tang C, Xu Q, Zhu Y, Xu MJ, Wang X. Increased stability of phosphatase and tensin homolog by intermedin leading to scavenger receptor A inhibition of macrophages reduces atherosclerosis in apolipoprotein E-deficient mice. J Mol Cell Cardiol. 2012; 53: 509-520. doi: 10.1016/j.yjmcc.2012.07.006.
19. Hong Y, Hay DL, Quirion R, Poyner DR. The pharmacology of adrenomedullin 2/intermedin. Br J Pharmacol. 2012; 166: 110-120. doi: 10.1111/j.1476-5381.2011.01530.x.
20. Hagiwara M, Bledsoe G, Yang ZR, Smith RS Jr, Chao L, Chao J. Intermedin ameliorates vascular and renal injury by inhibition of oxidative stress. Am J Physiol Renal Physiol. 2008; 295: F1735-F1743. doi: 10.1152/ ajprenal.90427.2008.
21. Zhao L, Peng DQ, Zhang J, Song JQ, Teng X, Yu YR, Tang CS, Qi YF. Extracellular signal-regulated kinase 1/2 activation is involved in intermedin1-53 attenuating myocardial oxidative stress injury induced by ischemia/ reperfusion. Peptides. 2012; 33: 329-335. doi: 10.1016/j.peptides.2011.12.016.
22. Liu Z, Luo H, Zhang L, Huang Y, Liu B, Ma K, Feng J, Xie J, Zheng J, Hu J, Zhan S, Zhu Y, Xu Q, Kong W, Wang X. Hyperhomocysteinemia exaggerates adventitial inflammation and angiotensin II-induced abdominal aortic aneurysm in mice. Circ Res. 2012; 111: 1261-1273. doi: 10.1161/ CIRCRESAHA.112.270520.
23. Rowe VL, Stevens SL, Reddick TT, Freeman MB, Donnell R, Carroll RC, Goldman MH. Vascular smooth muscle cell apoptosis in aneurysmal, occlusive, and normal human aortas. J Vasc Surg. 2000; 31: 567-576.
24. Muslin AJ. MAPK signalling in cardiovascular health and disease: molecular mechanisms and therapeutic targets. Clin Sci (Lond). 2008; 115: 203-218. doi: 10.1042/CS20070430.
25. Naik P, Murumkar P, Giridhar R, Yadav MR. Angiotensin II receptor type 1 (AT1) selective nonpeptidic antagonists - A perspective. Bioorg Med Chem. 2010; 18: 8418-8456. doi: 10.1016/j.bmc.2010.10.043.
26. McCormick ML, Gavrila D, Weintraub NL. Role of oxidative stress in the pathogenesis of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2007; 27: 461-469. doi: 10.1161/01.ATV.0000257552.94483.14.
27. Daugherty A, Cassis LA. Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2004; 24: 429-434. doi: 10.1161/01. ATV.0000118013.72016.ea.
28. Daugherty A, Rateri DL, Cassis LA. Role of the renin-angiotensin system in the development of abdominal aortic aneurysms in animals and humans. Ann N Y Acad Sci. 2006; 1085: 82-91. doi: 10.1196/annals.1383.035.
29. Chiou AC, Chiu B, Pearce WH. Murine aortic aneurysm produced by periarterial application of calcium chloride. J Surg Res. 2001; 99: 371-376. doi: 10.1006/jsre.2001.6207.
30. Chen H, Wang X, Tong M, Wu D, Wu S, Chen J, Wang X, Wang X, Kang Y, Tang H, Tang C, Jiang W. Intermedin suppresses pressure overload cardiac hypertrophy through activation of autophagy. PLoS One. 2013; 8: e64757. doi: 10.1371/journal.pone.0064757.
31. Bao W, Morimoto K, Hasegawa T, Sasaki N, Yamashita T, Hirata K, Okita Y, Okada K. Orally administered dipeptidyl peptidase-4 inhibitor (alogliptin) prevents abdominal aortic aneurysm formation through an antioxidant effect in rats. J Vasc Surg. 2014; 59: 1098-1108. doi: 10.1016/j. jvs.2013.04.048.
32. Morimoto K, Hasegawa T, Tanaka A, Wulan B, Yu J, Morimoto N, Okita Y, Okada K. Free-radical scavenger edaravone inhibits both formation and development of abdominal aortic aneurysm in rats. J Vasc Surg. 2012; 55: 1749-1758. doi: 10.1016/j.jvs.2011.11.059.
33. Gavrila D, Li WG, McCormick ML, Thomas M, Daugherty A, Cassis LA, Miller FJ Jr, Oberley LW, Dellsperger KC, Weintraub NL. Vitamin E inhibits abdominal aortic aneurysm formation in angiotensin II-infused apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2005; 25: 1671-1677. doi: 10.1161/01.ATV.0000172631. 50972.0f.
34. Wang L, Cheng X, Li H, Qiu F, Yang N, Wang B, Lu H, Wu H, Shen Y, Wang Y, Jing H. Quercetin reduces oxidative stress and inhibits activation of c-Jun N-terminal kinase/activator protein-1 signaling in an experimental mouse model of abdominal aortic aneurysm. Mol Med Rep. 2014; 9: 435-442. doi: 10.3892/mmr.2013.1846.
35. Parastatidis I, Weiss D, Joseph G, Taylor WR. Overexpression of catalase in vascular smooth muscle cells prevents the formation of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2013; 33: 2389-2396. doi: 10.1161/ATVBAHA.113.302175.
36. Zhang X, Gu L, Chen X, Wang S, Deng X, Liu K, Lv Z, Yang R, He S, Peng Y, Huang D, Jiang W, Wu K. Intermedin ameliorates atherosclerosis in ApoE null mice by modifying lipid profiles. Peptides. 2012; 37: 189-193. doi: 10.1016/j.peptides.2012.07.011.
37. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000; 105: 1605-1612. doi: 10.1172/JCI7818.
38. Nordon IM, Hinchliffe RJ, Holt PJ, Loftus IM, Thompson MM. Review of current theories for abdominal aortic aneurysm pathogenesis. Vascular. 2009; 17: 253-263.
39. Curci JA. Digging in the "soil" of the aorta to understand the growth of abdominal aortic aneurysms. Vascular. 2009; 17(suppl 1): S21-S29.
40. Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB. The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res. 2012; 95: 194-204. doi: 10.1093/cvr/cvs135.
41. Shang T, Liu Z, Liu CJ. Antioxidant Vitamin C attenuates experimental abdominal aortic aneurysm development in an elastase-induced rat model. J Surg Res. 2014; 188: 316-325. doi: 10.1016/j.jss.2013. 11.1105.
42. Chun HJ, Ali ZA, Kojima Y, Kundu RK, Sheikh AY, Agrawal R, Zheng L, Leeper NJ, Pearl NE, Patterson AJ, Anderson JP, Tsao PS, Lenardo MJ, Ashley EA, Quertermous T. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J Clin Invest. 2008; 118: 3343-3354. doi: 10.1172/JCI34871.
43. Yoshimura K, Aoki H, Ikeda Y, Fujii K, Akiyama N, Furutani A, Hoshii Y, Tanaka N, Ricci R, Ishihara T, Esato K, Hamano K, Matsuzaki M. Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase. Nat Med. 2005; 11: 1330-1338. doi: 10.1038/ nm1335.
44. Ghosh A, DiMusto PD, Ehrlichman LK, Sadiq O, McEvoy B, Futchko JS, Henke PK, Eliason JL, Upchurch GR, Jr. The role of extracellular signalrelated kinase during abdominal aortic aneurysm formation. J Am Coll Surg.2012; 215: 668-680 e661.
45. Papaharalambus CA, Griendling KK. Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc Med. 2007; 17: 48-54. doi: 10.1016/j.tcm.2006.11.005.
46. Chang JR, Duan XH, Zhang BH, Teng X, Zhou YB, Liu Y, Yu YR, Zhu Y, Tang CS, Qi YF. Intermedin1-53 attenuates vascular smooth muscle cell calcification by inhibiting endoplasmic reticulum stress via cyclic adenosine monophosphate/protein kinase A pathway. Exp Biol Med (Maywood). 2013; 238: 1136-1146. doi: 10.1177/1535370213502619.
47. Kuivaniemi H, Ryer EJ, Elmore JR, Tromp G. Understanding the pathogenesis of abdominal aortic aneurysms. Expert Rev Cardiovasc Ther. 2015; 13: 975-987. doi: 10.1586/14779072.2015.1074861.
48. Rosenbaugh EG, Savalia KK, Manickam DS, Zimmerman MC. Antioxidant-based therapies for angiotensin II-associated cardiovascular diseases. Am J Physiol Regul Integr Comp Physiol. 2013; 304: R917-R928. doi: 10.1152/ajpregu.00395.2012.