Adverse cardiac effects of exogenous angiotensin 1-7 in rats with subtotal nephrectomy are prevented by ACE inhibition

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Burrell, Louise M ^a   Gayed, Daniel ^a   Griggs, Karen ^a   Patel, Sheila K ^a   Velkoska, Elena ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN[1-7]; CREATININE; DIPEPTIDYL CARBOXYPEPTIDASE; RAMIPRIL; ANGIOTENSIN I; ANGIOTENSIN I (1-7); DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; PEPTIDE FRAGMENT;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CARDIOVASCULAR EFFECT; COMBINATION DRUG THERAPY; CONTROLLED STUDY; CORRELATIONAL STUDY; CREATININE BLOOD LEVEL; DIASTOLIC DYSFUNCTION; DRUG EFFECT; DRUG MECHANISM; ENZYME BINDING; ENZYME INHIBITION; EXPERIMENTAL RENAL FAILURE; HEART LEFT VENTRICLE CONTRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; KIDNEY FUNCTION; KIDNEY HYPERTROPHY; MALE; NEPHRECTOMY; NONHUMAN; PROTEIN BLOOD LEVEL; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SPRAGUE DAWLEY RAT; SUBTOTAL NEPHRECTOMY; SYSTOLIC BLOOD PRESSURE; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; BLOOD PRESSURE; CARDIAC MUSCLE; CARDIOMEGALY; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYMOLOGY; HEART; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; RENAL INSUFFICIENCY;

ANALYSIS OF VARIANCE; ANGIOTENSIN I; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANIMALS; BLOOD PRESSURE; CARDIOMEGALY; HEART; HYPERTENSION; MALE; MYOCARDIUM; NEPHRECTOMY; PEPTIDE FRAGMENTS; PEPTIDYL-DIPEPTIDASE A; RAMIPRIL; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY;

EID: 85012930137     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171975     Document Type: Article

References (42)

1. Velez JC. The importance of the intrarenal renin-Angiotensin system. Nat Clin Pract Nephrol. 2009; 5 (2):89-100. doi:10.1038/ncpneph1015 PMID: 19065132.
2. Donoghue M, Hsieh F, Baronas E, Godbout K, Gosselin M, Stagliano N, et al. A novel angiotensin-converting enzyme-related carboxypeptidase (ACE2) converts angiotensin I to angiotensin 1-9. Circ Res. 2000; 87(5):E1-E9. PMID: 10969042.
3. Tipnis SR, Hooper NM, Hyde R, Karran E, Christie G, Turner AJ. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captopril-insensitive carboxypeptidase. J Biol Chem. 2000; 275(43):33238-43. doi:10.1074/jbc.M002615200PMID: 10924499.
4. Ferrario CM, Averill DB, Brosnihan KB, Chappell MC, Iskandar SS, Dean RH, et al. Vasopeptidase inhibition and Ang-(1-7) in the spontaneously hypertensive rat. Kidney Int. 2002; 62(4):1349-57. doi:10.1111/j.1523-1755.2002.kid559.x PMID: 12234305.
5. Burrell LM, Johnston CI, Tikellis C, Cooper ME. ACE2, a new regulator of the renin-Angiotensin system. Trends Endocrinol Metab. 2004; 15(4):166-9. doi:10.1016/j.tem.2004.03.001 PMID: 15109615.
6. Santos RA, Simoes e Silva AC, Maric C, Silva DM, Machado RP, de Buhr I, et al. Angiotensin-(1-7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci U S A. 2003; 100 (14):8258-63. doi:10.1073/pnas.1432869100 PMID: 12829792.
7. Loot AE, Roks AJ, Henning RH, Tio RA, Suurmeijer AJ, Boomsma F, et al. Angiotensin-(1±7) attenuates the development of heart failure after myocardial infarction in rats. Circulation. 2002; 105 (13):1548-50. PMID: 11927520.
8. Benter IF, Yousif MH, Anim JT, Cojocel C, Diz DI. Angiotensin-(1-7) prevents development of severe hypertension and end-organ damage in spontaneously hypertensive rats treated with L-NAME. Am J Physiol Heart Circ Physiol. 2006; 290(2):H684-91. doi:10.1152/ajpheart.00632.2005 PMID: 16403946.
9. Liu E, Yang S, Xu Z, Li J, Yang W, Li G. Angiotensin-(1-7) prevents atrial fibrosis and atrial fibrillation in long-Term atrial tachycardia dogs. Regul Pept. 2010; 162(1-3):73-8. doi:10.1016/j.regpep.2009.12.020 PMID: 20074590.
10. Fraga-Silva RA, Savergnini SQ, Montecucco F, Nencioni A, Caffa I, Soncini D, et al. Treatment with Angiotensin-(1-7) reduces inflammation in carotid atherosclerotic plaques. Thromb Haemost. 2014; 111(4):736-47. Epub 2014/02/07. doi:10.1160/TH13-06-0448 PMID: 24499778.
11. Papinska AM, Mordwinkin NM, Meeks CJ, Jadhav SS, Rodgers KE. Angiotensin-(1-7) administration benefits cardiac, renal, and progenitor cell function in db/db mice. Br J Pharmacol. 2015. Epub 2015/06/16.
12. Papinska AM, Soto M, Meeks CJ, Rodgers KE. Long-Term administration of angiotensin (1-7) prevents heart and lung dysfunction in a mouse model of type 2 diabetes (db/db) by reducing oxidative stress, inflammation and pathological remodeling. Pharmacol Res. 2016. Epub 2016/03/10.
13. Shi Y, Lo CS, Padda R, Abdo S, Chenier I, Filep JG, et al. Angiotensin-(1-7) prevents systemic hypertension, attenuates oxidative stress and tubulointerstitial fibrosis, and normalizes renal angiotensin-converting enzyme 2 and Mas receptor expression in diabetic mice. Clin Sci (Lond). 2015; 128(10):649-63.
14. Shao Y, He M, Zhou L, Yao T, Huang Y, Lu LM. Chronic angiotensin (1-7) injection accelerates STZinduced diabetic renal injury. Acta Pharmacol Sin. 2008; 29(7):829-37. doi:10.1111/j.1745-7254.2008.00812.x PMID: 18565281.
15. Velkoska E, Dean RG, Griggs K, Burchill LJ, Burrell LM. Angiotensin 1-7 infusion is associated with increased blood pressure and adverse cardiac remodelling in rats with subtotal nephrectomy. Clin Sci (Lond). 2011; 120(8):335-45. Epub 2010/11/26.
16. Esteban V, Heringer-Walther S, Sterner-Kock A, de Bruin R, van den Engel S, Wang Y, et al. Angiotensin-( 1-7) and the G protein-coupled receptor Mas are key players in renal inflammation. PLoS One. 2009; 4(4):e5406. Epub 2009/05/01. doi:10.1371/journal.pone.0005406 PMID: 19404405.
17. Zimmerman DL, Zimpelmann J, Xiao F, Gutsol A, Touyz R, Burns KD. The effect of angiotensin-(1-7) in mouse unilateral ureteral obstruction. Am J Pathol. 2015; 185(3):729-40. Epub 2015/01/28. doi:10.1016/j.ajpath.2014.11.013 PMID: 25625676.
18. Velez JC, Janech MG, Hicks MP, Morinelli TA, Rodgers J, Self SE, et al. Lack of renoprotective effect of chronic intravenous angiotensin-(1-7) or angiotensin-(2-10) in a rat model of focal segmental glomerulosclerosis. PLoS One. 2014; 9(10):e110083. Epub 2014/10/23. PubMed Central PMCID: PMC4206519. doi:10.1371/journal.pone.0110083 PMID: 25337950.
19. Bi J, Contag SA, Carey LC, Tang L, Valego NK, Chappell MC, et al. Antenatal betamethasone exposure alters renal responses to angiotensin-(1-7) in uninephrectomized adult male sheep. J Renin Angiotensin Aldosterone Syst. 2013; 14(4):290-8. PubMed Central PMCID: PMCPMC4020597. doi:10.1177/1470320312465217PMID: 23161144.
20. Burchill L, Velkoska E, Dean RG, Lew RA, Smith AI, Levidiotis V, et al. Acute kidney injury in the rat causes cardiac remodelling and increases angiotensin-converting enzyme 2 expression. Exp Physiol. 2008; 93(5):622-30. doi:10.1113/expphysiol.2007.040386 PMID: 18223026.
21. Velkoska E, Dean RG, Burchill LJ, Levidiotis V, Burrell LM. Reduction in renal ACE2 expression in subtotal nephrectomy is ameliorated with ACE inhibition. Clin Sci (Lond). 2010; 118(4):269-79. Epub 2009/08/25.
22. Velkoska E, Patel SK, Griggs K, Pickering RJ, Tikellis C, Burrell LM. Short-Term treatment with diminazene aceturate ameliorates the reduction in kidney ACE2 activity in rats with subtotal nephrectomy. PLoS One. 2015; 10(3):e0118758. Epub 2015/03/19. doi:10.1371/journal.pone.0118758 PMID: 25786223.
23. Burrell LM, Burchill L, Dean RG, Griggs K, Patel SK, Velkoska E. Chronic kidney disease: cardiac and renal angiotensin converting enzyme (ACE) 2 expression in rats after subtotal nephrectomy and the effect of ACE inhibition. Exp Physiol. 2012; 97(4):477-85. Epub 2011/12/27. doi:10.1113/expphysiol.2011.063156 PMID: 22198016.
24. Velkoska E, Patel SK, Griggs K, Burrell LM. Diminazene aceturate improves cardiac fibrosis and diastolic dysfunction in rats with kidney disease. PLoS One. 2016; 11(8):e0161760. PubMed Central PMCID: PMCPMC5003360. doi:10.1371/journal.pone.0161760 PMID: 27571511.
25. Kennedy DJ, Elkareh J, Shidyak A, Shapiro AP, Smaili S, Mutgi K, et al. Partial nephrectomy as a model for uremic cardiomyopathy in the mouse. Am J Physiol Renal Physiol. 2008; 294(2):F450-4. doi:10.1152/ajprenal.00472.2007 PMID: 18032546.
26. Candido R, Forbes JM, Thomas MC, Thallas V, Dean RG, Burns WC, et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res. 2003; 92 (7):785-92. doi:10.1161/01.RES.0000065620.39919.20 PMID: 12623881.
27. Burrell LM, Risvanis J, Kubota E, Dean RG, MacDonald PS, Lu S, et al. Myocardial infarction increases ACE2 expression in rat and humans. Eur Heart J. 2005; 26(4):369-75; discussion 22-4. doi:10.1093/eurheartj/ehi114 PMID: 15671045.
28. Dean RG, Balding LC, Candido R, Burns WC, Cao Z, Twigg SM, et al. Connective tissue growth factor and cardiac fibrosis after myocardial infarction. J Histochem Cytochem. 2005; 53(10):1245-56. doi:10.1369/jhc.4A6560.2005 PMID: 15956033.
29. Herath CB, Warner FJ, Lubel JS, Dean RG, Jia Z, Lew RA, et al. Upregulation of hepatic angiotensinconverting enzyme 2 (ACE2) and angiotensin-(1-7) levels in experimental biliary fibrosis. J Hepatol. 2007; 47(3):387-95. doi:10.1016/j.jhep.2007.03.008 PMID: 17532087.
30. Santos RA, Krieger EM, Greene LJ. An improved fluorometric assay of rat serum and plasma converting enzyme. Hypertension. 1985; 7(2):244-52. PMID: 2984118.
31. Yamada K, Iyer SN, Chappell MC, Ganten D, Ferrario CM. Converting enzyme determines plasma clearance of angiotensin-(1-7). Hypertension. 1998; 32(3):496-502. PMID: 9740616.
32. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ, et al. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res. 2008; 103(11):1319-26. doi:10.1161/CIRCRESAHA.108.184911 PMID: 18845809.
33. Benter IF, Yousif MH, Cojocel C, Al-Maghrebi M, Diz DI. Angiotensin-(1-7) prevents diabetes-induced cardiovascular dysfunction. Am J Physiol Heart Circ Physiol. 2007; 292(1):H666-72. doi:10.1152/ajpheart.00372.2006 PMID: 17213482.
34. Grobe JL, Mecca AP, Mao H, Katovich MJ. Chronic angiotensin-(1-7) prevents cardiac fibrosis in DOCA-salt model of hypertension. Am J Physiol Heart Circ Physiol. 2006; 290(6):H2417-23. doi:10.1152/ajpheart.01170.2005 PMID: 16415071.
35. Li Y, Wu J, He Q, Shou Z, Zhang P, Pen W, et al. Angiotensin (1-7) prevent heart dysfunction and left ventricular remodeling caused by renal dysfunction in 5/6 nephrectomy mice. Hypertens Res. 2009; 32 (5):369-74. doi:10.1038/hr.2009.25 PMID: 19325560.
36. Xu C, Ding W, Zhang M, Gu Y. Protective effects of angiotensin-(1-7) administered with an angiotensin receptor blocker in a rat model of chronic kidney disease. Nephrology. 2013; 8(12):761-9.
37. Burgelova M, Vanourkova Z, Thumova M, Dvorak P, Opocensky M, Kramer HJ, et al. Impairment of the angiotensin-converting enzyme 2-Angiotensin-(1-7)-Mas axis contributes to the acceleration of two-kidney, one-clip Goldblatt hypertension. J Hypertens. 2009; 27:1988-2000. doi:10.1097/HJH.0b013e32832f0d06 PMID: 19593210.
38. Dilauro M, Zimpelmann J, Robertson SJ, Genest D, Burns KD. The effect of ACE2 and angiotensin-(1- 7) in a mouse model of early chronic kidney disease. Am J Physiol Renal Physiol. 2010; 298(6):F1523- F32. doi:10.1152/ajprenal.00426.2009 PMID: 20357030.
39. Pinheiro SV, Ferreira AJ, Kitten GT, da Silveira KD, da Silva DA, Santos SH, et al. Genetic deletion of the angiotensin-(1-7) receptor Mas leads to glomerular hyperfiltration and microalbuminuria. Kidney Int. 2009; 75(11):1184-93. Epub 2009/03/06. doi:10.1038/ki.2009.61 PMID: 19262461.
40. Burns WC, Velkoska E, Dean RG, Burrell LM, Thomas MC. Angiotensin II mediates epithelial-To-mesenchymal transformation in tubular cells by Ang1-7/Mas-1 dependent pathways. Am J Physiol Renal Physiol. 2010; 299(3):F585-93. doi:10.1152/ajprenal.00538.2009 PMID: 20554647.
41. Alzayadneh EM, Chappell MC. Angiotensin-(1-7) abolishes AGE-induced cellular hypertrophy and myofibroblast transformation via inhibition of ERK1/2. Cell Signal. 2014; 26(12):3027-35. Epub 2014/09/24. PubMed Central PMCID: PMCPMC4254268. doi:10.1016/j.cellsig.2014.09.010 PMID: 25246357.
42. Kim CS, Kim IJ, Bae EH, Ma SK, Lee J, Kim SW. Angiotensin-(1-7) Attenuates Kidney Injury Due to Obstructive Nephropathy in Rats. PLoS One. 2015; 10(11):e0142664. Epub 2015/11/12. PubMed Central PMCID: PMCPMC4640496. doi:10.1371/journal.pone.0142664 PMID: 26556707.