Upregulation of angiotensin (1-7)-mediated signaling preserves endothelial function through reducing oxidative stress in diabetes

Antioxidants and Redox Signaling

Volumn 23, Issue 11, 2015, Pages 880-892

  Zhang, Yang ^a   Liu, Jian ^a   Luo, Jiang Yun ^a   Tian, Xiao Yu ^a   Cheang, Wai San ^a   Xu, Jian ^a   Lau, Chi Wai ^a   Wang, Li ^a   Wong, Wing Tak ^a,b   Wong, Chi Ming ^a   Lan, Hui Yao ^a   Yao, Xiaoqiang ^a   Raizada, Mohan K ^c   Huang, Yu ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7]; DIMINAZENE ACETURATE; ENDOTHELIUM DERIVED RELAXING FACTOR; HYDROETHIDINE; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 2; ACETYLCHOLINE; ANGIOTENSIN I; ANGIOTENSIN I (1-7); DIMINAZENE; DIPEPTIDYL CARBOXYPEPTIDASE; PEPTIDE FRAGMENT; VASODILATOR AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHEMOLUMINESCENCE; CONTROLLED STUDY; FLUORESCENCE IMAGING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KIDNEY ARTERY; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSMOTIC PUMP; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; UPREGULATION; AGED; ANIMAL; AORTA; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; FEMALE; MALE; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL;

ACETYLCHOLINE; AGED; ANGIOTENSIN I; ANIMALS; AORTA; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIMINAZENE; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE, INBRED C57BL; MIDDLE AGED; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; REACTIVE OXYGEN SPECIES; RENAL ARTERY; UP-REGULATION; VASODILATOR AGENTS;

EID: 84944871698     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2014.6070     Document Type: Article

References (61)

1. Benter IF, Yousif MH, Dhaunsi GS, Kaur J, Chappell MC, and Diz DI. Angiotensin-(1-7) prevents activation of NADPH oxidase and renal vascular dysfunction in diabetic hypertensive rats. Am J Nephrol 28: 25-33, 2008
2. Bindom SM, Hans CP, Xia H, Boulares AH, and Lazartigues E. Angiotensin I-converting enzyme type 2 (ACE2) gene therapy improves glycemic control in diabetic mice. Diabetes 59: 2540-2548, 2010
3. Brosnihan KB, Li P, and Ferrario CM. Angiotensin-(1-7) dilates canine coronary arteries through kinins and nitric oxide. Hypertension 27: 523-528, 1996
4. Castro CH, Santos RA, Ferreira AJ, Bader M, Alenina N, and Almeida AP. Evidence for a functional interaction of the angiotensin-(1-7) receptor Mas with AT1 and AT2 receptors in the mouse heart. Hypertension 46: 937-942, 2005
5. Chen J, Xiao X, Chen S, Zhang C, Chen J, Yi D, Shenoy V, Raizada MK, Zhao B, and Chen Y. Angiotensin-converting enzyme 2 priming enhances the function of endothelial progenitor cells and their therapeutic efficacy. Hypertension 61: 681-689, 2013
6. Cosentino F and Luscher TF. Endothelial dysfunction in diabetes mellitus. J Cardiovasc Pharmacol 32 Suppl 3: S54-S61, 1998
7. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J, Ferrario CM, Manoukian AS, Chappell MC, Backx PH, Yagil Y, and Penninger JM. Angiotensinconverting enzyme 2 is an essential regulator of heart function. Nature 417: 822-828, 2002
8. 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, and Zhang Y. 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, 2012
9. Donoghue M, Wakimoto H, Maguire CT, Acton S, Hales P, Stagliano N, Fairchild-Huntress V, Xu J, Lorenz JN, Kadambi V, Berul CI, and Breitbart RE. Heart block, ventricular tachycardia, and sudden death in ACE2 transgenic mice with downregulated connexins. J Mol Cell Cardiol 35: 1043-1053, 2003
10. Feng Y, Yue X, Xia H, Bindom SM, Hickman PJ, Filipeanu CM, Wu G, and Lazartigues E. Angiotensin-converting enzyme 2 overexpression in the subfornical organ prevents the angiotensin II-mediated pressor and drinking responses and is associated with angiotensin II type 1 receptor downregulation. Circ Res 102: 729-736, 2008
11. Fraga-Silva RA, Costa-Fraga FP, Murca TM, Moraes PL, Martins Lima A, Lautner RQ, Castro CH, Soares CM, Borges CL, Nadu AP, Oliveira ML, Shenoy V, Katovich MJ, Santos RA, Raizada MK, and Ferreira AJ. Angiotensin-converting enzyme 2 activation improves endothelial function. Hypertension 61: 1233-1238, 2013
12. Gava E, Samad-Zadeh A, Zimpelmann J, Bahramifarid N, Kitten GT, Santos RA, Touyz RM, and Burns KD. Angiotensin-(1-7) activates a tyrosine phosphatase and inhibits glucose-induced signalling in proximal tubular cells. Nephrol Dial Transplant 24: 1766-1773, 2009
13. Gjymishka A, Kulemina LV, Shenoy V, Katovich MJ, Ostrov DA, and Raizada MK. Diminazene Aceturate Is an ACE2 Activator and a Novel Antihypertensive Drug. Faseb J 24: 1032-1033, 2010
14. Gwathmey TM, Pendergrass KD, Reid SD, Rose JC, Diz DI, and Chappell MC. Angiotensin-(1-7)-angiotensinconverting enzyme 2 attenuates reactive oxygen species formation to angiotensin II within the cell nucleus. Hypertension 55: 166-171, 2010
15. Heitsch H, Brovkovych S, Malinski T, and Wiemer G. Angiotensin-(1-7)-stimulated nitric oxide and superoxide release from endothelial cells. Hypertension 37: 72-76, 2001
16. Higashi Y, Noma K, Yoshizumi M, and Kihara Y. Endothelial function and oxidative stress in cardiovascular diseases. Circ J 73: 411-418, 2009
17. Iusuf D, Henning RH, Van Gilst WH, and Roks AJ. Angiotensin-(1-7): pharmacological properties and pharmacotherapeutic perspectives. Eur J Pharmacol 585: 303-312, 2008
18. Jarajapu YP, Bhatwadekar AD, Caballero S, Hazra S, Shenoy V, Medina R, Kent D, Stitt AW, Thut C, Finney EM, Raizada MK, and Grant MB. Activation of the ACE2/angiotensin-(1-7)/Mas receptor axis enhances the reparative function of dysfunctional diabetic endothelial progenitors. Diabetes 62: 1258-1269, 2013
19. Jin HY, Song B, Oudit GY, Davidge ST, Yu HM, Jiang YY, Gao PJ, Zhu DL, Ning G, Kassiri Z, Penninger JM, and Zhong JC. ACE2 deficiency enhances angiotensin IImediated aortic profilin-1 expression, inflammation and peroxynitrite production. PLoS One 7: e38502, 2012.
20. Kulemina LV and Ostrov DA. Prediction of off-target effects on angiotensin-converting enzyme 2. J Biomol Screen 16: 878-885, 2011
21. Lau YS, Tian XY, Mustafa MR, Murugan D, Liu J, Zhang Y, Lau CW, and Huang Y. Boldine improves endothelial function in diabetic db/db mice through inhibition of angiotensin II-mediated BMP4-oxidative stress cascade. Br J Pharmacol 170: 1190-1198, 2013
22. Lely AT, Hamming I, Van Goor H, and Navis GJ. Renal ACE2 expression in human kidney disease. J Pathol 204: 587-593, 2004
23. Li G, Xu YL, Ling F, Liu AJ, Wang D, Wang Q, and Liu YL. Angiotensin-converting enzyme 2 activation protects against pulmonary arterial hypertension through improving early endothelial function and mediating cytokines levels. Chin Med J (Engl) 125: 1381-1388, 2012
24. Li Y, Wu J, He Q, Shou Z, Zhang P, Pen W, Zhu Y, and Chen J. Angiotensin (1-7) prevent heart dysfunction and left ventricular remodeling caused by renal dysfunction in 5/6 nephrectomy mice. Hypertens Res 32: 369-374, 2009
25. Liu C, Lv XH, Li HX, Cao X, Zhang F, Wang L, Yu M, and Yang JK. Angiotensin-(1-7) suppresses oxidative stress and improves glucose uptake via Mas receptor in adipocytes. Acta Diabetol 49: 291-299, 2012
26. Liu CX, Hu Q, Wang Y, Zhang W, Ma ZY, Feng JB, Wang R, Wang XP, Dong B, Gao F, Zhang MX, and Zhang Y. Angiotensin-converting enzyme (ACE) 2 overexpression ameliorates glomerular injury in a rat model of diabetic nephropathy: a comparison with ACE inhibition. Mol Med 17: 59-69, 2011
27. Liu L, Liu J, Tian XY, Wong WT, Lau CW, Xu A, Xu G, Ng CF, Yao X, Gao Y, and Huang Y. Uncoupling protein-2 mediates DPP-4 inhibitor-induced restoration of endothelial function in hypertension through reducing oxidative stress. Antioxid Redox Signal 21: 1571-1581, 2014
28. Loot AE, Roks AJ, Henning RH, Tio RA, Suurmeijer AJ, Boomsma F, and Van Gilst WH. Angiotensin-(1-7) attenuates the development of heart failure after myocardial infarction in rats. Circulation 105: 1548-1550, 2002
29. Lovren F, Pan Y, Quan A, Teoh H, Wang G, Shukla PC, Levitt KS, Oudit GY, Al-Omran M, Stewart DJ, Slutsky AS, Peterson MD, Backx PH, Penninger JM, and Verma S. Angiotensin converting enzyme-2 confers endothelial protection and attenuates atherosclerosis. Am J Physiol Heart Circ Physiol 295: H1377-H1384, 2008
30. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, Sharff KA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, and He TC. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2: 1236-1247, 2007
31. Masson R, Nicklin SA, Craig MA, McBride M, Gilday K, Gregorevic P, Allen JM, Chamberlain JS, Smith G, Graham D, Dominiczak AF, Napoli C, and Baker AH. Onset of experimental severe cardiac fibrosis is mediated by overexpression of Angiotensin-converting enzyme 2. Hypertension 53: 694-700, 2009
32. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ, Santos RA, Walther T, Touyz RM, and Reudelhuber TL. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res 103: 1319-1326, 2008
33. Moon JY, Tanimoto M, Gohda T, Hagiwara S, Yamazaki T, Ohara I, Murakoshi M, Aoki T, Ishikawa Y, Lee SH, Jeong KH, Lee TW, Ihm CG, Lim SJ, and Tomino Y. Attenuating effect of angiotensin-(1-7) on angiotensin IImediated NAD(P)H oxidase activation in type 2 diabetic nephropathy of KK-A(y)/Ta mice. Am J Physiol Renal Physiol 300: F1271-F1282, 2011
34. Muthalif MM, Benter IF, Uddin MR, Harper JL, and Malik KU. Signal transduction mechanisms involved in angiotensin-(1-7)-stimulated arachidonic acid release and prostanoid synthesis in rabbit aortic smooth muscle cells. J Pharmacol Exp Ther 284: 388-398, 1998
35. Niu MJ, Yang JK, Lin SS, Ji XJ, and Guo LM. Loss of angiotensin-converting enzyme 2 leads to impaired glucose homeostasis in mice. Endocrine 34: 56-61, 2008
36. Ohshima K, Mogi M, Nakaoka H, Iwanami J, Min LJ, Kanno H, Tsukuda K, Chisaka T, Bai HY, Wang XL, Ogimoto A, Higaki J, and Horiuchi M. Possible role of angiotensin-converting enzyme 2 and activation of angiotensin II type 2 receptor by angiotensin-(1-7) in improvement of vascular remodeling by angiotensin II type 1 receptor blockade. Hypertension 63: e53-e59, 2014
37. Oudit GY, Liu GC, Zhong J, Basu R, Chow FL, Zhou J, Loibner H, Janzek E, Schuster M, Penninger JM, Herzenberg AM, Kassiri Z, and Scholey JW. Human recombinant ACE2 reduces the progression of diabetic nephropathy. Diabetes 59: 529-538, 2010
38. Patel VB, Bodiga S, Basu R, Das SK, Wang W, Wang Z, Lo J, Grant MB, Zhong J, Kassiri Z, and Oudit GY. Loss of angiotensin-converting enzyme-2 exacerbates diabetic cardiovascular complications and leads to systolic and vascular dysfunction: a critical role of the angiotensin II/AT1 receptor axis. Circ Res 110: 1322-1335, 2012
39. Pena Silva RA, Chu Y, Miller JD, Mitchell IJ, Penninger JM, Faraci FM, and Heistad DD. Impact of ACE2 deficiency and oxidative stress on cerebrovascular function with aging. Stroke 43: 3358-3363, 2012
40. Qi Y, Zhang J, Cole-Jeffrey CT, Shenoy V, Espejo A, Hanna M, Song C, Pepine CJ, Katovich MJ, and Raizada MK. Diminazene aceturate enhances angiotensin-converting enzyme 2 activity and attenuates ischemia-induced cardiac pathophysiology. Hypertension 62: 746-752, 2013
41. Raffai G, Durand MJ, and Lombard JH. Acute and chronic angiotensin-(1-7) restores vasodilation and reduces oxidative stress in mesenteric arteries of salt-fed rats. Am J Physiol Heart Circ Physiol 301: H1341-H1352, 2011
42. Ren Y, Garvin JL, and Carretero OA. Vasodilator action of angiotensin-(1-7) on isolated rabbit afferent arterioles. Hypertension 39: 799-802, 2002
43. Rentzsch B, Todiras M, Iliescu R, Popova E, Campos LA, Oliveira ML, Baltatu OC, Santos RA, and Bader M. Transgenic angiotensin-converting enzyme 2 overexpression in vessels of SHRSP rats reduces blood pressure and improves endothelial function. Hypertension 52: 967-973, 2008
44. Sampaio WO, Henrique De Castro C, Santos RA, Schiffrin EL, and Touyz RM. Angiotensin-(1-7) counterregulates angiotensin II signaling in human endothelial cells. Hypertension 50: 1093-1098, 2007
45. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, and Touyz RM. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49: 185-192, 2007
46. Shenoy V, Gjymishka A, Jarajapu YP, Qi Y, Afzal A, Rigatto K, Ferreira AJ, Fraga-Silva RA, Kearns P, Douglas JY, Agarwal D, Mubarak KK, Bradford C, Kennedy WR, Jun JY, Rathinasabapathy A, Bruce E, Gupta D, Cardounel AJ, Mocco J, Patel JM, Francis J, Grant MB, Katovich MJ, and Raizada MK. Diminazene attenuates pulmonary hypertension and improves angiogenic progenitor cell functions in experimental models. Am J Respir Crit Care Med 187: 648-657, 2013
47. Shiota A, Yamamoto K, Ohishi M, Tatara Y, Ohnishi M, Maekawa Y, Iwamoto Y, Takeda M, and Rakugi H. Loss of ACE2 accelerates time-dependent glomerular and tubulointerstitial damage in streptozotocin-induced diabetic mice. Hypertens Res 33: 298-307, 2010
48. Soares De Moura R, Resende AC, Emiliano AF, Tano T, Mendes-Ribeiro AC, Correia ML, and De Carvalho LC. The role of bradykinin, AT2 and angiotensin 1-7 receptors in the EDRF-dependent vasodilator effect of angiotensin II on the isolated mesenteric vascular bed of the rat. Br J Pharmacol 141: 860-866, 2004
49. Soler MJ, Wysocki J, Ye M, Lloveras J, Kanwar Y, and Batlle D. ACE2 inhibition worsens glomerular injury in association with increased ACE expression in streptozotocin-induced diabetic mice. Kidney Int 72: 614-623, 2007
50. Stegbauer J, Oberhauser V, Vonend O, and Rump LC. Angiotensin-(1-7) modulates vascular resistance and sympathetic neurotransmission in kidneys of spontaneously hypertensive rats. Cardiovasc Res 61: 352-359, 2004
51. Stegbauer J, Potthoff SA, Quack I, Mergia E, Clasen T, Friedrich S, Vonend O,Woznowski M, Konigshausen E, Sellin L, and Rump LC. Chronic treatment with angiotensin-(1-7) improves renal endothelial dysfunction in apolipoproteinEdeficient mice. Br J Pharmacol 163: 974-983, 2011
52. Su Z, Zimpelmann J, and Burns KD. Angiotensin-(1-7) inhibits angiotensin II-stimulated phosphorylation of MAP kinases in proximal tubular cells. Kidney Int 69: 2212-2218, 2006
53. Tallant EA and Clark MA. Molecular mechanisms of inhibition of vascular growth by angiotensin-(1-7). Hypertension 42: 574-579, 2003
54. Thatcher SE, Zhang X, Howatt DA, Lu H, Gurley SB, Daugherty A, and Cassis LA. Angiotensin-converting enzyme 2 deficiency in whole body or bone marrow-derived cells increases atherosclerosis in low-density lipoprotein receptor-/- mice. Arterioscler Thromb Vasc Biol 31: 758-765, 2011
55. Thomas MC, Pickering RJ, Tsorotes D, Koitka A, Sheehy K, Bernardi S, Toffoli B, Nguyen-Huu TP, Head GA, Fu Y, Chin-Dusting J, Cooper ME, and Tikellis C. Genetic Ace2 deficiency accentuates vascular inflammation and atherosclerosis in the ApoE knockout mouse. Circ Res 107: 888-897, 2010
56. Tian XY, Wong WT, Wang N, Lu Y, Cheang WS, Liu J, Liu L, Liu Y, Lee SS, Chen ZY, Cooke JP, Yao X, and Huang Y. PPARdelta activation protects endothelial function in diabetic mice. Diabetes 61: 3285-3293, 2012
57. Tian XY, Wong WT, Xu A, Lu Y, Zhang Y, Wang L, Cheang WS, Wang Y, Yao X, and Huang Y. Uncoupling protein-2 protects endothelial function in diet-induced obese mice. Circ Res 110: 1211-1216, 2012
58. Wysocki J, Ye M, Soler MJ, Gurley SB, Xiao HD, Bernstein KE, Coffman TM, Chen S, and Batlle D. ACE and ACE2 activity in diabetic mice. Diabetes 55: 2132-2139, 2006
59. Zhang C, Zhao YX, Zhang YH, Zhu L, Deng BP, Zhou ZL, Li SY, Lu XT, Song LL, Lei XM, Tang WB, Wang N, Pan CM, Song HD, Liu CX, Dong B, Zhang Y, and Cao Y. Angiotensin-converting enzyme 2 attenuates atherosclerotic lesions by targeting vascular cells. Proc Natl Acad Sci U S A 107: 15886-15891, 2010
60. Zhang Y, Liu J, Tian XY, Wong WT, Chen Y, Wang L, Luo J, Cheang WS, Lau CW, Kwan KM, Wang N, Yao X, and Huang Y. Inhibition of bone morphogenic protein 4 restores endothelial function in db/db diabetic mice. Arterioscler Thromb Vasc Biol 34: 152-159, 2014
61. Zhong J, Basu R, Guo D, Chow FL, Byrns S, Schuster M, Loibner H, Wang XH, Penninger JM, Kassiri Z, and Oudit GY. Angiotensin-converting enzyme 2 suppresses pathological hypertrophy, myocardial fibrosis, and cardiac dysfunction. Circulation 122: 717-728, 18 p following 728, 2010