Skip to main content

Advertisement

Log in

Understanding diabetes-induced cardiomyopathy from the perspective of renin angiotensin aldosterone system

  • Invited Review
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Experimental and clinical evidence suggests that diabetic subjects are predisposed to a distinct cardiovascular dysfunction, known as diabetic cardiomyopathy (DCM), which could be an autonomous disease independent of concomitant micro and macrovascular disorders. DCM is one of the prominent causes of global morbidity and mortality and is on a rising trend with the increase in the prevalence of diabetes mellitus (DM). DCM is characterized by an early left ventricle diastolic dysfunction associated with the slow progression of cardiomyocyte hypertrophy leading to heart failure, which still has no effective therapy. Although the well-known “Renin Angiotensin Aldosterone System (RAAS)” inhibition is considered a gold-standard treatment in heart failure, its role in DCM is still unclear. At the cellular level of DCM, RAAS induces various secondary mechanisms, adding complications to poor prognosis and treatment of DCM. This review highlights the importance of RAAS signaling and its major secondary mechanisms involving inflammation, oxidative stress, mitochondrial dysfunction, and autophagy, their role in establishing DCM. In addition, studies lacking in the specific area of DCM are also highlighted. Therefore, understanding the complex role of RAAS in DCM may lead to the identification of better prognosis and therapeutic strategies in treating DCM.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Abdellatif M, Sedej S, Carmona-Gutierrez D, Madeo F, Kroemer G (2018) Autophagy in cardiovascular aging. Circ Res 123:803–824. https://doi.org/10.1161/CIRCRESAHA.118.312208

    Article  PubMed  Google Scholar 

  2. Abel ED, Litwin SE, Sweeney G (2008) Cardiac remodeling in obesity. Physiol Rev 88:389–419. https://doi.org/10.1152/physrev.00017.2007

    Article  PubMed  Google Scholar 

  3. Acar G, Akcay A, Sokmen A, Ozkaya M, Guler E, Sokmen G, Kaya H, Nacar AB, Tuncer C (2009) Assessment of atrial electromechanical delay, diastolic functions, and left atrial mechanical functions in patients with type 1 diabetes mellitus. J Am Soc Echocardiogr 22:732–738. https://doi.org/10.1016/j.echo.2009.03.028

    Article  PubMed  Google Scholar 

  4. Amador N, Encarnacion JD, Rodriguez L, Tello A, Lopez M, Guizar JM (2004) Relationship between left ventricular mass and heart sympathetic activity in male obese subjects. Arch Med Res 35:411–415. https://doi.org/10.1016/j.arcmed.2004.05.003

    Article  PubMed  Google Scholar 

  5. Anderson EJ, Kypson AP, Rodriguez E, Anderson CA, Lehr EJ, Neufer PD (2009) Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol 54:1891–1898. https://doi.org/10.1016/j.jacc.2009.07.031

    Article  PubMed  PubMed Central  Google Scholar 

  6. Andreozzi F, Laratta E, Sciacqua A, Perticone F, Sesti G (2004) Angiotensin II impairs the insulin signaling pathway promoting production of nitric oxide by inducing phosphorylation of insulin receptor substrate-1 on Ser(312) and Ser(616) in human umbilical vein endothelial cells. Circ Res 94:1211–1218. https://doi.org/10.1161/01.Res.0000126501.34994.96

    Article  PubMed  Google Scholar 

  7. Ansley DM, Wang BH (2013) Oxidative stress and myocardial injury in the diabetic heart. Journal of Pathology 229:232–241. https://doi.org/10.1002/path.4113

    Article  PubMed  Google Scholar 

  8. Atlas SA (2007) The renin-angiotensin aldosterone system: pathophysiological role and pharmacologic inhibition. J Manag Care Pharm 13:9–20. https://doi.org/10.18553/jmcp.2007.13.s8-b (2007(13)8:9-20 [pii])

    Article  PubMed  Google Scholar 

  9. Banday AA, Lokhandwala MF (2008) Oxidative stress-induced renal angiotensin AT1 receptor upregulation causes increased stimulation of sodium transporters and hypertension. Am J Physiol Renal Physiol 295:F698-706. https://doi.org/10.1152/ajprenal.90308.2008 (90308.2008[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  10. Banday AA, Lokhandwala MF (2011) Oxidative stress causes renal angiotensin II type 1 receptor upregulation, Na+/H+ exchanger 3 overstimulation, and hypertension. Hypertension 57:452–459. https://doi.org/10.1161/HYPERTENSIONAHA.110.162339 (HYPERTENSIONAHA.110.162339[pii])

    Article  PubMed  Google Scholar 

  11. Benigni A, Corna D, Zoja C, Sonzogni A, Latini R, Salio M, Conti S, Rottoli D, Longaretti L, Cassis P, Morigi M, Coffman TM, Remuzzi G (2009) Disruption of the Ang II type 1 receptor promotes longevity in mice. J Clin Investig 119:524–530. https://doi.org/10.1172/JCI36703

    Article  PubMed  PubMed Central  Google Scholar 

  12. Benter IF, Yousif MH, Cojocel C, Al-Maghrebi M, Diz DI (2007) Angiotensin-(1–7) prevents diabetes-induced cardiovascular dysfunction. Am J Physiol Heart Circ Physiol 292:H666-672. https://doi.org/10.1152/ajpheart.00372.2006

    Article  PubMed  Google Scholar 

  13. Boudina S, Abel ED (2007) Diabetic cardiomyopathy revisited. Circulation 115:3213–3223. https://doi.org/10.1161/CIRCULATIONAHA.106.679597 (115/25/3213[pii])

    Article  PubMed  Google Scholar 

  14. Boudina S, Abel ED (2010) Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 11:31–39. https://doi.org/10.1007/s11154-010-9131-7

    Article  PubMed  PubMed Central  Google Scholar 

  15. Boudina S, Bugger H, Sena S, O’Neill BT, Zaha VG, Ilkun O, Wright JJ, Mazumder PK, Palfreyman E, Tidwell TJ, Theobald H, Khalimonchuk O, Wayment B, Sheng XM, Rodnick KJ, Centini R, Chen D, Litwin SE, Weimer BE, Abel ED (2009) Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 119:1272-U1111. https://doi.org/10.1161/Circulationaha.108.792101

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bugger H, Riehle C, Jaishy B, Wende AR, Tuinei J, Chen D, Soto J, Pires KM, Boudina S, Theobald HA, Luptak I, Wayment B, Wang X, Litwin SE, Weimer BC, Abel ED (2012) Genetic loss of insulin receptors worsens cardiac efficiency in diabetes. J Mol Cell Cardiol 52:1019–1026. https://doi.org/10.1016/j.yjmcc.2012.02.001

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bush E, Maeda N, Kuziel WA, Dawson TC, Wilcox JN, DeLeon H, Taylor WR (2000) CC chemokine receptor 2 is required for macrophage infiltration and vascular hypertrophy in angiotensin II-induced hypertension. Hypertension 36:360–363

    Article  PubMed  Google Scholar 

  18. Byberg L, Melhus H, Gedeborg R, Sundstrom J, Ahlbom A, Zethelius B, Berglund LG, Wolk A, Michaelsson K (2009) Total mortality after changes in leisure time physical activity in 50 year old men: 35 year follow-up of population based cohort. British Medical Journal 338. ARTN b688. https://doi.org/10.1136/bmj.b688

  19. Candido R, Jandeleit-Dahm KA, Cao Z, Nesteroff SP, Burns WC, Twigg SM, Dilley RJ, Cooper ME, Allen TJ (2002) Prevention of accelerated atherosclerosis by angiotensin-converting enzyme inhibition in diabetic apolipoprotein E-deficient mice. Circulation 106:246–253

    Article  PubMed  Google Scholar 

  20. Castoldi G, di Gioia CRT, Roma F, Carletti R, Manzoni G, Stella A, Zerbini G, Perseghin G (2019) Activation of angiotensin type 2 (AT2) receptors prevents myocardial hypertrophy in Zucker diabetic fatty rats. Acta Diabetol 56:97–104. https://doi.org/10.1007/s00592-018-1220-1

    Article  PubMed  Google Scholar 

  21. Chen F, Chen B, Xiao FQ, Wu YT, Wang RH, Sun ZW, Fu GS, Mou Y, Tao W, Hu XS, Hu SJ (2014) Autophagy protects against senescence and apoptosis via the RAS-mitochondria in high-glucose-induced endothelial cells. Cell Physiol Biochem 33:1058–1074. https://doi.org/10.1159/000358676

    Article  PubMed  Google Scholar 

  22. Cheng J, Wang M, Ma H, Li H, Ren J, Wang R (2015) Adiponectin inhibits oxidative stress and modulates TGF-b1 and COL-1 expression via the AMPK pathway in HSC-T6 cells. Zhonghua Gan Zang Bing Za Zhi 23:69–72

    PubMed  Google Scholar 

  23. Cheng Z, Zhang M, Hu J, Lin J, Feng X, Wang S, Wang T, Gao E, Wang H, Sun D (2018) Mst1 knockout enhances cardiomyocyte autophagic flux to alleviate angiotensin II-induced cardiac injury independent of angiotensin II receptors. J Mol Cell Cardiol 125:117–128. https://doi.org/10.1016/j.yjmcc.2018.08.028

    Article  PubMed  Google Scholar 

  24. Chow BSM, Koulis C, Krishnaswamy P, Steckelings UM, Unger T, Cooper ME, Jandeleit-Dahm KA, Allen TJ (2016) The angiotensin II type 2 receptor agonist Compound 21 is protective in experimental diabetes-associated atherosclerosis. Diabetologia 59:1778–1790. https://doi.org/10.1007/s00125-016-3977-5

    Article  PubMed  Google Scholar 

  25. Connelly KA, Kelly DJ, Zhang Y, Prior DL, Martin J, Cox AJ, Thai K, Feneley MP, Tsoporis J, White KE, Krum H, Gilbert RE (2007) Functional, structural and molecular aspects of diastolic heart failure in the diabetic (mRen-2)27 rat. Cardiovasc Res 76:280–291. https://doi.org/10.1016/j.cardiores.2007.06.022

    Article  PubMed  Google Scholar 

  26. Conti V, Izzo V, Corbi G, Russomanno G, Manzo V, De Lise F, Di Donato A, Filippelli A (2016) Antioxidant supplementation in the treatment of aging-associated diseases. Frontiers in Pharmacology 7. Artn 24. https://doi.org/10.3389/Fphar.2016.00024

  27. Crabos M, Roth M, Hahn AWA, Erne P (1994) Characterization of angiotensin-ii receptors in cultured adult-rat cardiac fibroblasts - coupling to signaling systems and gene-expression. J Clin Investig 93:2372–2378. https://doi.org/10.1172/Jci117243

    Article  PubMed  PubMed Central  Google Scholar 

  28. Crowley SD, Coffman TM (2012) Recent advances involving the renin-angiotensin system. Exp Cell Res 318:1049–1056. https://doi.org/10.1016/j.yexcr.2012.02.023

    Article  PubMed  PubMed Central  Google Scholar 

  29. Dai Q, Xu M, Yao M, Sun B (2007) Angiotensin AT1 receptor antagonists exert antiinflammatory effects in spontaneously hypertensive rats. Br J Pharmacol 152:1042–1048. https://doi.org/10.1038/sj.bjp.0707454

    Article  PubMed  PubMed Central  Google Scholar 

  30. Daly CA, Fox KM, Remme WJ, Bertrand ME, Ferrari R, Simoons ML (2005) The effect of perindopril on cardiovascular morbidity and mortality in patients with diabetes in the EUROPA study: results from the PERSUADE substudy. Eur Heart J 26:1369–1378. https://doi.org/10.1093/eurheartj/ehi225 (ehi225[pii])

    Article  PubMed  Google Scholar 

  31. Dandamudi S, Slusser J, Mahoney DW, Redfield MM, Rodeheffer RJ, Chen HH (2014) The prevalence of diabetic cardiomyopathy: a population-based study in Olmsted County, Minnesota. J Cardiac Fail 20:304–309. https://doi.org/10.1016/j.cardfail.2014.02.007

    Article  Google Scholar 

  32. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T (2000) International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol Rev 52:415–472

    PubMed  Google Scholar 

  33. De Mello WC (2004) Angiotensin (1–7) re-establishes impulse conduction in cardiac muscle during ischaemia-reperfusion. The role of the sodium pump. J Renin-Angiotensin-Aldosterone Syst 5:203–208. https://doi.org/10.3317/jraas.2004.041

  34. De Mello WC (2014) Angiotensin (1–7) re-establishes heart cell communication previously impaired by cell swelling: Implications for myocardial ischemia. Exp Cell Res 323:359–365. https://doi.org/10.1016/j.yexcr.2014.03.006

    Article  PubMed  Google Scholar 

  35. De Mello WC, Danser AHJ (2000) Angiotensin II and the heart - on the intracrine renin-angiotensin system. Hypertension 35:1183–1188

    Article  PubMed  Google Scholar 

  36. De Mello WC, Gerena Y (2010) Further studies on the effects of intracrine and extracellular angiotensin II on the regulation of heart cell volume. On the influence of aldosterone and spironolactone. Regul Pept 165:200–205. https://doi.org/10.1016/j.regpep.2010.07.165

    Article  PubMed  Google Scholar 

  37. Deng G, Long Y, Yu YR, Li MR (2010) Adiponectin directly improves endothelial dysfunction in obese rats through the AMPK-eNOS Pathway. Int J Obes 34:165–171. https://doi.org/10.1038/ijo.2009.205

    Article  Google Scholar 

  38. Di Marco E, Gray SP, Jandeleit-Dahm K (2013) Diabetes alters activation and repression of pro- and anti-inflammatory signaling pathways in the vasculature. Front Endocrinol (Lausanne) 4:68. https://doi.org/10.3389/fendo.2013.00068

    Article  Google Scholar 

  39. Diamant M, Lamb HJ, Groeneveld Y, Endert EL, Smit JWA, Bax JJ, Romijn JA, de Roos A, Radder JK (2003) Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. J Am Coll Cardiol 42:328–335. https://doi.org/10.1016/S0735-1097(03)00625-9

    Article  PubMed  Google Scholar 

  40. Dias-Peixoto MF, Santos RAS, Gomes ERM, Alves MNM, Almeida PWM, Greco L, Rosa M, Fauler B, Bader M, Alenina N, Guatimosim S (2008) Molecular mechanisms involved in the angiotensin-(1–7)/Mas signaling pathway in cardiomyocytes. Hypertension 52:542–548. https://doi.org/10.1161/Hypertensionaha.108.114280

    Article  PubMed  Google Scholar 

  41. Dinh W, Futh R, Nickl W, Krahn T, Ellinghaus P, Scheffold T, Bansemir L, Bufe A, Barroso MC, Lankisch M (2009) Elevated plasma levels of TNF-alpha and Interleukin-6 in patients with diastolic dysfunction and glucose metabolism disorders. Cardiovascular Diabetology 8. Artn 58. https://doi.org/10.1186/1475-2840-8-58

  42. Donath MY, Storling J, Maedler K, Mandrup-Poulsen T (2003) Inflammatory mediators and islet beta-cell failure: a link between type 1 and type 2 diabetes. J Mol Med (Berl) 81:455–470. https://doi.org/10.1007/s00109-003-0450-y

    Article  Google Scholar 

  43. Doughan AK, Harrison DG, Dikalov SI (2008) Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction. Circ Res 102:488–496. https://doi.org/10.1161/CIRCRESAHA.107.162800

    Article  PubMed  Google Scholar 

  44. Durand MJ, Zinkevich NS, Riedel M, Gutterman DD, Nasci VL, Salato VK, Hijjawi JB, Reuben CF, North PE, Beyer AM (2016) Vascular actions of angiotensin 1–7 in the human microcirculation novel role for telomerase. Arterioscler Thromb Vasc Biol 36:1254-+. https://doi.org/10.1161/Atvbaha.116.307518

  45. Dzau V (2005) The cardiovascular continuum and renin-angiotensin-aldosterone system blockade. J Hypertens 23:S9–S17. https://doi.org/10.1097/01.hjh.0000165623.72310.dd

    Article  Google Scholar 

  46. Ebermann L, Spillmann F, Sidiropoulos M, Escher F, Heringer-Walther S, Schultheiss HP, Tschope C, Walther T (2008) The angiotensin-(1–7) receptor agonist AVE0991 is cardioprotective in diabetic rats. Eur J Pharmacol 590:276–280. https://doi.org/10.1016/j.ejphar.2008.05.024

    Article  PubMed  Google Scholar 

  47. Eckel RH (2008) Nonsurgical management of obesity in adults. N Engl J Med 358:1941–1950. https://doi.org/10.1056/Nejmcp0801652

    Article  PubMed  Google Scholar 

  48. Essick EE, Wilson RM, Pimentel DR, Shimano M, Baid S, Ouchi N, Sam F (2013) Adiponectin modulates oxidative stress-induced autophagy in cardiomyocytes. Plos One 8. UNSP e68697. https://doi.org/10.1371/journal.pone.0068697

  49. Fang ZY, Prins JB, Marwick TH (2004) Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 25:543–567. https://doi.org/10.1210/er.2003-0012.25/4/543[pii]

    Article  PubMed  Google Scholar 

  50. Fenger M (2013) The enigma of adiponectin. Atherosclerosis 227:226–227. https://doi.org/10.1016/j.atherosclerosis.2012.11.018

    Article  PubMed  Google Scholar 

  51. Finckenberg P, Eriksson O, Baumann M, Merasto S, Lalowski MM, Levijoki J, Haasio K, Kyto V, Muller DN, Luft FC, Oresic M, Mervaala E (2012) Caloric restriction ameliorates angiotensin II-induced mitochondrial remodeling and cardiac hypertrophy. Hypertension 59:76–84. https://doi.org/10.1161/HYPERTENSIONAHA.111.179457

    Article  PubMed  Google Scholar 

  52. Fiordaliso F, Cuccovillo I, Bianchi R, Bai A, Doni M, Salio M, De Angelis N, Ghezzi P, Latini R, Masson S (2006) Cardiovascular oxidative stress is reduced by an ACE inhibitor in a rat model of streptozotocin-induced diabetes. Life Sci 79:121–129. https://doi.org/10.1016/j.lfs.2005.12.036

    Article  PubMed  Google Scholar 

  53. Flather MD, Yusuf S, Kober L, Pfeffer M, Hall A, Murray G, Torp-Pedersen C, Ball S, Pogue J, Moye L, Braunwald E, C AIMI, (2000) Long-term ACE-inhibitor therapy in patients with heart failure or left-ventricular dysfunction: a systematic overview of data from individual patients. Lancet 355:1575–1581. https://doi.org/10.1016/S0140-6736(00)02212-1

    Article  PubMed  Google Scholar 

  54. Frustaci A, Kajstura J, Chimenti C, Jakoniuk I, Leri A, Maseri A, Nadal-Ginard B, Anversa P (2000) Myocardial cell death in human diabetes. Circ Res 87:1123–1132

    Article  PubMed  Google Scholar 

  55. Fukuda T, Ahearn M, Roberts A, Mattaliano RJ, Zaal K, Ralston E, Plotz PH, Raben N (2006) Autophagy and mistargeting of therapeutic enzyme in skeletal muscle in Pompe disease. Mol Ther 14:831–839. https://doi.org/10.1016/j.ymthe.2006.08.009

    Article  PubMed  Google Scholar 

  56. Galderisi M, Anderson KM, Wilson PW, Levy D (1991) Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol 68:85–89 (0002-9149(91)90716-X[pii])

    Article  PubMed  Google Scholar 

  57. Gamez-Mendez AM, Vargas-Robles H, Rios A, Escalante B (2015) Oxidative stress-dependent coronary endothelial dysfunction in obese mice. Plos One 10. ARTN e0138609. https://doi.org/10.1371/journal.pone.0138609

  58. Gao XM, Tsai A, Al-Sharea A, Su Y, Moore S, Han LP, Kiriazis H, Dart AM, Murphy AJ, Du XJ (2017) Inhibition of the renin-angiotensin system post myocardial infarction prevents inflammation-associated acute cardiac rupture. Cardiovasc Drugs Ther 31:145–156. https://doi.org/10.1007/s10557-017-6717-2[pii]

    Article  PubMed  Google Scholar 

  59. Gao YL, Kang L, Li CM, Wang XY, Sun CF, Li QZ, Liu RH, Wang JP (2016) Resveratrol ameliorates diabetes-induced cardiac dysfunction through AT1R-ERK/p38 MAPK signaling pathway. Cardiovasc Toxicol 16:130–137. https://doi.org/10.1007/s12012-015-9321-3

    Article  PubMed  Google Scholar 

  60. Giani JF, Gironacci MM, Munoz MC, Pena C, Turyn D, Dominici FP (2007) Angiotensin-(1 7) stimulates the phosphorylation of JAK2, IRS-1 and Akt in rat heart in vivo: role of the AT1 and Mas receptors. Am J Physiol Heart Circ Physiol 293:H1154-1163. https://doi.org/10.1152/ajpheart.01395.2006 (01395.2006[pii])

    Article  PubMed  Google Scholar 

  61. Giani JF, Mayer MA, Munoz MC, Silberman EA, Hocht C, Taira CA, Gironacci MM, Turyn D, Dominici FP (2009) Chronic infusion of angiotensin-(1–7) improves insulin resistance and hypertension induced by a high-fructose diet in rats. Am J Physiol Endocrinol Metab 296:E262-271. https://doi.org/10.1152/ajpendo.90678.2008 (90678.2008[pii])

    Article  PubMed  Google Scholar 

  62. Goldin A, Beckman JA, Schmidt AM, Creager MA (2006) Advanced glycation end products - sparking the development of diabetic vascular injury. Circulation 114:597–605. https://doi.org/10.1161/Circulationaha.106.621854

    Article  PubMed  Google Scholar 

  63. Grobe JL, Mecca AP, Lingis M, Shenoy V, Bolton TA, Machado JM, Speth RC, Raizada MK, Katovich MJ (2007) Prevention of angiotensin II-induced cardiac remodeling by angiotensin-(1–7). Am J Physiol Heart Circ Physiol 292:H736-742. https://doi.org/10.1152/ajpheart.00937.2006

    Article  PubMed  Google Scholar 

  64. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE (2014) Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 103:137–149. https://doi.org/10.1016/j.diabres.2013.11.002 (S0168-8227(13)00385-9[pii])

    Article  PubMed  Google Scholar 

  65. Ha H, Hwang IA, Park JH, Lee HB (2008) Role of reactive oxygen species in the pathogenesis of diabetic nephropathy. Diabetes Res Clin Pract 82:S42–S45. https://doi.org/10.1016/j.diabres.2008.09.017

    Article  PubMed  Google Scholar 

  66. Ha JW, Lee HC, Kang ES, Ahn CM, Kim JM, Ahn JA, Lee SW, Choi EY, Rim SJ, Oh JK, Chung N (2007) Abnormal left ventricular longitudinal functional reserve in patients with diabetes mellitus: implication for detecting subclinical myocardial dysfunction using exercise tissue Doppler echocardiography. Heart 93:1571–1576. https://doi.org/10.1136/hrt.2006.101667 (hrt.2006.101667[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  67. Haffner SM (2006) The metabolic syndrome: inflammation, diabetes mellitus, and cardiovascular disease. Am J Cardiol 97:3A-11A. https://doi.org/10.1016/j.amjcard.2005.11.010 (S0002-9149(05)02028-X[pii])

    Article  PubMed  Google Scholar 

  68. Hao PP, Yang JM, Zhang MX, Zhang K, Chen YG, Zhang C, Zhang Y (2015) Angiotensin-(1–7) treatment mitigates right ventricular fibrosis as a distinctive feature of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 308:H1007-1019. https://doi.org/10.1152/ajpheart.00563.2014

    Article  PubMed  Google Scholar 

  69. Hayat SA, Patel B, Khattar RS, Malik RA (2004) Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci 107:539–557

    Article  Google Scholar 

  70. Heart Outcomes Prevention Evaluation Study Investigators (2000) Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy. Lancet 355(9200):253–9. https://doi.org/10.1016/S0140-6736(99)12323-7

  71. Hussein SA, El-Wadood HM, Abdallah MA, Khorshed AA (2015) HPTLC with fluorescence densitometry for simultaneous determination of some angiotensin II receptor blockers in tablets and plasma. J AOAC Int 98:354–360. https://doi.org/10.5740/jaoacint.14-179

    Article  PubMed  Google Scholar 

  72. Huynh K, Kiriazis H, Du XJ, Love JE, Jandeleit-Dahm KA, Forbes JM, McMullen JR, Ritchie RH (2012) Coenzyme Q10 attenuates diastolic dysfunction, cardiomyocyte hypertrophy and cardiac fibrosis in the db/db mouse model of type 2 diabetes. Diabetologia 55:1544–1553. https://doi.org/10.1007/s00125-012-2495-3

    Article  PubMed  Google Scholar 

  73. Ibsen H, Lindholm LH, Pedersen OL, Dahlof B, Kjeldsen S (2003) The effect of losartan versus atenolol on cardiovascular morbidity and mortality in patients with diabetes mellitus in the LIFE-study. Ugeskr Laeger 165:459–462

    PubMed  Google Scholar 

  74. Jager J, Gremeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF (2007) Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 148:241–251. https://doi.org/10.1210/en.2006-0692 (en.2006-0692[pii])

    Article  PubMed  Google Scholar 

  75. Jia G, DeMarco VG, Sowers JR (2016) Insulin resistance and hyperinsulinaemia in diabetic cardiomyopathy. Nat Rev Endocrinol 12:144–153. https://doi.org/10.1038/nrendo.2015.216

    Article  PubMed  Google Scholar 

  76. Jia G, Whaley-Connell A, Sowers JR (2018) Diabetic cardiomyopathy: a hyperglycaemia- and insulin-resistance-induced heart disease. Diabetologia 61:21–28. https://doi.org/10.1007/s00125-017-4390-4

    Article  PubMed  Google Scholar 

  77. Jiang F, Yang J, Zhang Y, Dong M, Wang S, Zhang Q, Liu FF, Zhang K, Zhang C (2014) Angiotensin-converting enzyme 2 and angiotensin 1–7: novel therapeutic targets. Nat Rev Cardiol 11:413–426. https://doi.org/10.1038/nrcardio.2014.59 (nrcardio.2014.59[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  78. Kadoguchi T, Kinugawa S, Takada S, Fukushima A, Furihata T, Homma T, Masaki Y, Mizushima W, Nishikawa M, Takahashi M, Yokota T, Matsushima S, Okita K, Tsutsui H (2015) Angiotensin II can directly induce mitochondrial dysfunction, decrease oxidative fibre number and induce atrophy in mouse hindlimb skeletal muscle. Exp Physiol 100:312–322. https://doi.org/10.1113/expphysiol.2014.084095

    Article  PubMed  Google Scholar 

  79. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Investig 116:1784–1792. https://doi.org/10.1172/JCI29126

    Article  PubMed  PubMed Central  Google Scholar 

  80. Kajstura J, Fiordaliso F, Andreoli AM, Li B, Chimenti S, Medow MS, Limana F, Nadal-Ginard B, Leri A, Anversa P (2001) IGF-1 overexpression inhibits the development of diabetic cardiomyopathy and angiotensin II-mediated oxidative stress. Diabetes 50:1414–1424. https://doi.org/10.2337/diabetes.50.6.1414

    Article  PubMed  Google Scholar 

  81. Kalil GZ, Haynes WG (2012) Sympathetic nervous system in obesity-related hypertension: mechanisms and clinical implications. Hypertens Res 35:4–16. https://doi.org/10.1038/hr.2011.173

    Article  PubMed  Google Scholar 

  82. Kanamori H, Takemura G, Goto K, Tsujimoto A, Mikami A, Ogino A, Watanabe T, Morishita K, Okada H, Kawasaki M, Seishima M, Minatoguchi S (2015) Autophagic adaptations in diabetic cardiomyopathy differ between type 1 and type 2 diabetes. Autophagy 11:1146–1160. https://doi.org/10.1080/15548627.2015.1051295

    Article  PubMed  PubMed Central  Google Scholar 

  83. Karam JG, McFarlane SI (2011) Update on the prevention of type 2 diabetes. Curr DiabRep 11:56–63. https://doi.org/10.1007/s11892-010-0163-x

    Article  Google Scholar 

  84. Kassiri Z, Zhong JC, Guo D, Basu R, Wang XH, Liu PP, Scholey JW, Penninger JM, Oudit GY (2009) Loss of angiotensin-converting enzyme 2 accelerates maladaptive left ventricular remodeling in response to myocardial infarction. Circulation-Heart Failure 2:446–455. https://doi.org/10.1161/Circheartfailure.108.840124

    Article  PubMed  Google Scholar 

  85. Kayama Y, Raaz U, Jagger A, Adam M, Schellinger IN, Sakamoto M, Suzuki H, Toyama K, Spin JM, Tsao PS (2015) Diabetic cardiovascular disease induced by oxidative stress. Int J Mol Sci 16:25234–25263. https://doi.org/10.3390/ijms161025234

    Article  PubMed  PubMed Central  Google Scholar 

  86. Khullar M, Al-Shudiefat AA, Ludke A, Binepal G, Singal PK (2010) Oxidative stress: a key contributor to diabetic cardiomyopathy. Can J Physiol Pharmacol 88:233–240. https://doi.org/10.1139/Y10-016 (y10-016[pii])

    Article  PubMed  Google Scholar 

  87. Kim S, Iwao H (2000) Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. Pharmacol Rev 52:11–34

    PubMed  Google Scholar 

  88. Kimura S, Zhang GX, Nishiyama A, Shokoji T, Yao L, Fan YY, Rahman M, Abe Y (2005) Mitochondria-derived reactive oxygen species and vascular MAP kinases: comparison of angiotensin II and diazoxide. Hypertension 45:438–444. https://doi.org/10.1161/01.HYP.0000157169.27818.ae

    Article  PubMed  Google Scholar 

  89. Kleinschmidt TL, Oltman CL (2014) Progression and reversal of coronary and mesenteric vascular dysfunction associated with obesity. Obesity 22:2193–2200. https://doi.org/10.1002/oby.20837

    Article  PubMed  Google Scholar 

  90. Kobori H, Mori H, Masaki T, Nishiyama A (2013) Angiotensin II blockade and renal protection. Curr Pharm Des 19:3033–3042

    Article  PubMed  PubMed Central  Google Scholar 

  91. Kritchevsky SB, Cesari M, Pahor M (2005) Inflammatory markers and cardiovascular health in older adults. Cardiovasc Res 66:265–275. https://doi.org/10.1016/j.cardiores.2004.12.026

    Article  PubMed  Google Scholar 

  92. Lakshmanan AP, Harima M, Sukumaran V, Soetikno V, Thandavarayan RA, Suzuki K, Kodama M, Nagata M, Takagi R, Watanabe K (2012) Modulation of AT-1R/AMPK-MAPK cascade plays crucial role for the pathogenesis of diabetic cardiomyopathy in transgenic type 2 diabetic (Spontaneous Diabetic Toni) rats. Biochem Pharmacol 83:653–660. https://doi.org/10.1016/j.bcp.2011.11.018

    Article  PubMed  Google Scholar 

  93. Lautner RQ, Villela DC, Fraga-Silva RA, Silva N, Verano-Braga T, Costa-Fraga F, Jankowski J, Jankowski V, Sousa F, Alzamora A, Soares E, Barbosa C, Kjeldsen F, Oliveira A, Braga J, Savergnini S, Maia G, Peluso AB, Passos-Silva D, Ferreira A, Alves F, Martins A, Raizada M, Paula R, Motta-Santos D, Kemplin F, Pimenta A, Alenina N, Sinisterra R, Bader M, Campagnole-Santos MJ, Santos RAS (2013) Discovery and characterization of alamandine a novel component of the renin-angiotensin system. Circ Res 112:1104-+. https://doi.org/10.1161/Circresaha.113.301077

    Article  PubMed  Google Scholar 

  94. Lee J (2013) Adipose tissue macrophages in the development of obesity-induced inflammation, insulin resistance and type 2 Diabetes. Arch Pharmacal Res 36:208–222. https://doi.org/10.1007/s12272-013-0023-8

    Article  Google Scholar 

  95. Lei SQ, Li YA, Liu HM, Yu H, Wang H, Xia ZY (2012) Effects of N-acetylcysteine on nicotinamide dinucleotide phosphate oxidase activation and antioxidant status in heart, lung, liver and kidney in streptozotocin-induced diabetic rats. Yonsei Med J 53:294–303. https://doi.org/10.3349/ymj.2012.53.2.294

    Article  PubMed  PubMed Central  Google Scholar 

  96. Lim HS, MacFadyen RJ, Lip GY (2004) Diabetes mellitus, the renin-angiotensin-aldosterone system, and the heart. Arch Intern Med 164:1737–1748. https://doi.org/10.1001/archinte.164.16.1737.164/16/1737[pii]

    Article  PubMed  Google Scholar 

  97. Lin L, Liu X, Xu J, Weng L, Ren J, Ge J, Zou Y (2016) Mas receptor mediates cardioprotection of angiotensin-(1–7) against angiotensin II-induced cardiomyocyte autophagy and cardiac remodelling through inhibition of oxidative stress. J Cell Mol Med 20:48–57. https://doi.org/10.1111/jcmm.12687

    Article  PubMed  Google Scholar 

  98. Lindholm LH, Ibsen H, Dahlof B, Devereux RB, Beevers G, de Faire U, Fyhrquist F, Julius S, Kjeldsen SE, Kristiansson K, Lederballe-Pedersen O, Nieminen MS, Omvik P, Oparil S, Wedel H, Aurup P, Edelman J, Snapinn S, grp Ls, (2002) Cardiovascular morbidity and mortality in patients with diabetes in the Losartan Intervention For Endpoint reduction in hypertension study (LIFE): a randomised trial against atenolol. Lancet 359:1004–1010. https://doi.org/10.1016/S0140-6736(02)08090-X

    Article  PubMed  Google Scholar 

  99. Lohmeier TE, Iliescu R (2013) The sympathetic nervous system in obesity hypertension. Curr Hypertens Rep 15:409–416. https://doi.org/10.1007/s11906-013-0356-1

    Article  PubMed  PubMed Central  Google Scholar 

  100. Low Wang CC, Hess CN, Hiatt WR, Goldfine AB (2016) Clinical update: cardiovascular disease in diabetes mellitus: atherosclerotic cardiovascular disease and heart failure in type 2 diabetes mellitus - mechanisms, management, and clinical considerations. Circulation 133:2459–2502. https://doi.org/10.1161/CIRCULATIONAHA.116.022194 (CIRCULATIONAHA.116.022194[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  101. Luong KVQ, Nguyen LTH (2013) The beneficial role of vitamin D in obesity: possible genetic and cell signaling mechanisms. Nutrition Journal 12. Artn 89. https://doi.org/10.1186/1475-2891-12-89

  102. Ma H, Li SY, Xu PS, Babcock SA, Dolence EK, Brownlee M, Li J, Ren J (2009) Advanced glycation endproduct (AGE) accumulation and AGE receptor (RAGE) up-regulation contribute to the onset of diabetic cardiomyopathy. J Cell Mol Med 13:1751–1764. https://doi.org/10.1111/j.1582-4934.2008.00547.x

    Article  PubMed  Google Scholar 

  103. Ma TK, Kam KK, Yan BP, Lam YY (2010) Renin-angiotensin-aldosterone system blockade for cardiovascular diseases: current status. Br J Pharmacol 160:1273–1292. https://doi.org/10.1111/j.1476-5381.2010.00750.x (BPH750[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  104. Maalouf RM, Eid AA, Gorin YC, Block K, Escobar GP, Bailey S, Abboud HE (2012) Nox4-derived reactive oxygen species mediate cardiomyocyte injury in early type 1 diabetes. Am J Physiol Cell Physiol 302:C597–C604. https://doi.org/10.1152/ajpcell.00331.2011

    Article  PubMed  Google Scholar 

  105. Makino A, Dai A, Han Y, Youssef KD, Wang W, Donthamsetty R, Scott BT, Wang H, Dillmann WH (2015) O-GlcNAcase overexpression reverses coronary endothelial cell dysfunction in type 1 diabetic mice. Am J Physiol Cell Physiol 309:C593-599. https://doi.org/10.1152/ajpcell.00069.2015

    Article  PubMed  PubMed Central  Google Scholar 

  106. Mapanga RF, Essop MF (2016) Damaging effects of hyperglycemia on cardiovascular function: spotlight on glucose metabolic pathways. American Journal of Physiology-Heart and Circulatory Physiology 310:H153–H173. https://doi.org/10.1152/ajpheart.00206.2015

    Article  PubMed  Google Scholar 

  107. Mariappan N, Elks CM, Sriramula S, Guggilam A, Liu Z, Borkhsenious O, Francis J (2010) NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 85:473–483. https://doi.org/10.1093/cvr/cvp305 (cvp305[pii])

    Article  PubMed  Google Scholar 

  108. Martin-Timon I, Sevillano-Collantes C, Segura-Galindo A, Del Canizo-Gomez FJ (2014) Type 2 diabetes and cardiovascular disease: have all risk factors the same strength? World J Diabetes 5:444–470. https://doi.org/10.4239/wjd.v5.i4.444

    Article  PubMed  PubMed Central  Google Scholar 

  109. Matsusaka H, Kinugawa S, Ide T, Matsushima S, Shiomi T, Kubota T, Sunagawa K, Tsutsui H (2006) Angiotensin II type 1 receptor blocker attenuates exacerbated left ventricular remodeling and failure in diabetes-associated myocardial infarction. J Cardiovasc Pharmacol 48:95–102. https://doi.org/10.1097/01.fjc.0000245405.41317.60

    Article  PubMed  Google Scholar 

  110. Mehta PK, Griendling KK (2007) Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292:C82–C97. https://doi.org/10.1152/ajpcell.00287.2006

    Article  PubMed  Google Scholar 

  111. Miki T, Yuda S, Kouzu H, Miura T (2013) Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev 18:149–166. https://doi.org/10.1007/s10741-012-9313-3

    Article  PubMed  Google Scholar 

  112. Montezano AC, Touyz RM (2014) Reactive oxygen species, vascular noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal 20:164–182. https://doi.org/10.1089/ars.2013.5302

    Article  PubMed  PubMed Central  Google Scholar 

  113. Mori J, Patel VB, Alrob OA, Basu R, Altamimi T, DesAulniers J, Wagg CS, Kassiri Z, Lopaschuk GD, Oudit GY (2014) Angiotensin 1–7 ameliorates diabetic cardiomyopathy and diastolic dysfunction in db/db mice by reducing lipotoxicity and inflammation. Circulation-Heart Failure 7:327–339. https://doi.org/10.1161/Circheartfailure.113.000672

    Article  PubMed  Google Scholar 

  114. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, Neschen S, White MF, Bilz S, Sono S, Pypaert M, Shulman GI (2005) Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest 115:3587–3593. https://doi.org/10.1172/JCI25151

    Article  PubMed  PubMed Central  Google Scholar 

  115. Mozaffarian D, Benjamin EJ, Go AS, Arnett DK, Blaha MJ, Cushman M, Das SR, de Ferranti S, Despres JP, Fullerton HJ, Howard VJ, Huffman MD, Isasi CR, Jimenez MC, Judd SE, Kissela BM, Lichtman JH, Lisabeth LD, Liu S, Mackey RH, Magid DJ, McGuire DK, Mohler ER 3rd, Moy CS, Muntner P, Mussolino ME, Nasir K, Neumar RW, Nichol G, Palaniappan L, Pandey DK, Reeves MJ, Rodriguez CJ, Rosamond W, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Woo D, Yeh RW, Turner MB (2016) Heart Disease And Stroke Statistics-2016 update: a report from the American Heart Association. Circulation 133:e38-360. https://doi.org/10.1161/CIR.0000000000000350 (CIR.0000000000000350[pii])

    Article  PubMed  Google Scholar 

  116. Mozaffarian D, Kamineni A, Carnethon M, Djousse L, Mukamal KJ, Siscovick D (2009) Lifestyle risk factors and new-onset diabetes mellitus in older adults the cardiovascular health study. Arch Intern Med 169:798–807

    Article  PubMed  PubMed Central  Google Scholar 

  117. Muhammad Z, Hashmi A (2013) Frequency of diabetic cardiomyopathy among type-2 diabetics presenting as heart failure. Jcpsp-J Coll Physicians Surg Pakistan 23:538–542

    Google Scholar 

  118. Munoz MC, Giani JF, Dominici FP (2010) Angiotensin-(1–7) stimulates the phosphorylation of Akt in rat extracardiac tissues in vivo via receptor Mas. Regul Pept 161:1–7. https://doi.org/10.1016/j.regpep.2010.02.001

    Article  PubMed  Google Scholar 

  119. Murase T, Hattori T, Ohtake M, Abe M, Amakusa Y, Takatsu M, Murohara T, Nagata K (2012) Cardiac remodeling and diastolic dysfunction in DahlS.Z-Lepr(fa)/Lepr(fa) rats: a new animal model of metabolic syndrome. Hypertens Res 35:186–193. https://doi.org/10.1038/hr.2011.157

    Article  PubMed  Google Scholar 

  120. Naito T, Ma LJ, Yang HC, Zuo YQ, Tang YW, Han JY, Kon V, Fogo AB (2010) Angiotensin type 2 receptor actions contribute to angiotensin type 1 receptor blocker effects on kidney fibrosis. Am J Physiol-Renal Physiol 298:F683–F691. https://doi.org/10.1152/ajprenal.00503.2009

    Article  PubMed  Google Scholar 

  121. Nagatomo Y, Meguro T, Ito H, Koide K, Anzai T, Fukuda K, Ogawa S, Yoshikawa T (2014) Significance of AT1 receptor independent activation of mineralocorticoid receptor in murine diabetic cardiomyopathy. PLoS One 9:e93145. https://doi.org/10.1371/journal.pone.0093145

  122. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K (2007) The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13:619–624. https://doi.org/10.1038/nm1574

    Article  PubMed  Google Scholar 

  123. Nenna A, Nappi F, Avtaar Singh SS, Sutherland FW, Di Domenico F, Chello M, Spadaccio C (2015) Pharmacologic approaches against advanced glycation end products (AGEs) in diabetic cardiovascular disease. Res Cardiovasc Med 4:e26949. https://doi.org/10.5812/cardiovascmed.4(2)2015.26949

    Article  PubMed  PubMed Central  Google Scholar 

  124. Neri Serneri GG, Boddi M, Modesti PA, Coppo M, Cecioni I, Toscano T, Papa ML, Bandinelli M, Lisi GF, Chiavarelli M (2004) Cardiac angiotensin II participates in coronary microvessel inflammation of unstable angina and strengthens the immunomediated component. Circ Res 94:1630–1637. https://doi.org/10.1161/01.RES.0000130944.49657.b8 (01.RES.0000130944.49657.b8[pii])

    Article  PubMed  Google Scholar 

  125. Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T, Mora M, Riggs JE, Oh SJ, Koga Y, Sue CM, Yamamoto A, Murakami N, Shanske S, Byrne E, Bonilla E, Nonaka I, DiMauro S, Hirano M (2000) Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 406:906–910. https://doi.org/10.1038/35022604

    Article  PubMed  Google Scholar 

  126. Nosarev AV, Smagliy LV, Anfinogenova Y, Popov SV, Kapilevich LV (2014) Exercise and NO production: relevance and implications in the cardiopulmonary system. Front Cell Dev Biol 2:73. https://doi.org/10.3389/fcell.2014.00073

    Article  PubMed  Google Scholar 

  127. Oak JH, Cai H (2007) Attenuation of angiotensin II signaling recouples eNOS and inhibits nonendothelial NOX activity in diabetic mice. Diabetes 56:118–126. https://doi.org/10.2337/db06-0288 (56/1/118[pii])

    Article  PubMed  Google Scholar 

  128. Oka T, Hikoso S, Yamaguchi O, Taneike M, Takeda T, Tamai T, Oyabu J, Murakawa T, Nakayama H, Nishida K, Akira S, Yamamoto A, Komuro I, Otsu K (2012) Mitochondrial DNA that escapes from autophagy causes inflammation and heart failure. Nature 485:251-U142. https://doi.org/10.1038/nature10992

    Article  PubMed  PubMed Central  Google Scholar 

  129. Olefsky JM, Glass CK (2010) Macrophages, inflammation, and insulin resistance. Annu Rev Physiol 72:219–246. https://doi.org/10.1146/annurev-physiol-021909-135846

    Article  PubMed  Google Scholar 

  130. Oudit GY, Kassiri Z, Patel MP, Chappell M, Butany J, Backx PH, Tsushima RG, Scholey JW, Khokha R, Penninger JM (2007) Angiotensin II-mediated oxidative stress and inflammation mediate the age-dependent cardiomyopathy in ACE2 null mice. Cardiovasc Res 75:29–39. https://doi.org/10.1016/j.cardiores.2007.04.007

    Article  PubMed  Google Scholar 

  131. Papinska AM, Mordwinkin NM, Meeks CJ, Jadhav SS, Rodgers KE (2015) Angiotensin-(1–7) administration benefits cardiac, renal and progenitor cell function in db/db mice. Br J Pharmacol 172:4443–4453. https://doi.org/10.1111/bph.13225

    Article  PubMed  PubMed Central  Google Scholar 

  132. Papinska AM, Soto M, Meeks CJ, Rodgers KE (2016) 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 107:372–380. https://doi.org/10.1016/j.phrs.2016.02.026

    Article  PubMed  PubMed Central  Google Scholar 

  133. Parving HH, Brenner BM, McMurray JJ, de Zeeuw D, Haffner SM, Solomon SD, Chaturvedi N, Persson F, Desai AS, Nicolaides M, Richard A, Xiang Z, Brunel P, Pfeffer MA (2012) Cardiorenal end points in a trial of aliskiren for type 2 diabetes. N Engl J Med 367:2204–2213. https://doi.org/10.1056/NEJMoa1208799

    Article  PubMed  Google Scholar 

  134. Patel VB, Bodiga S, Fan D, Das SK, Wang ZC, Wang W, Basu R, Zhong JC, Kassiri Z, Oudit GY (2012) Cardioprotective effects mediated by angiotensin II type 1 receptor blockade and enhancing angiotensin 1–7 in experimental heart failure in angiotensin-converting enzyme 2-null mice. Hypertension 59:1195-U1303. https://doi.org/10.1161/Hypertensionaha.112.191650

    Article  PubMed  Google Scholar 

  135. Patel VB, Mori J, McLean BA, Basu R, Das SK, Ramprasath T, Parajuli N, Penninger JM, Grant MB, Lopaschuk GD, Oudit GY (2016) ACE2 deficiency worsens epicardial adipose tissue inflammation and cardiac dysfunction in response to diet-induced obesity. Diabetes 65:85–95. https://doi.org/10.2337/db15-0399 (db15-0399[pii])

    Article  PubMed  Google Scholar 

  136. Pereira RI, Snell-Bergeon JK, Erickson C, Schauer IE, Bergman BC, Rewers M, Maahs DM (2012) Adiponectin dysregulation and insulin resistance in type 1 diabetes. J Clin Endocrinol Metab 97:E642–E647. https://doi.org/10.1210/jc.2011-2542

    Article  PubMed  PubMed Central  Google Scholar 

  137. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350:664–671. https://doi.org/10.1056/NEJMoa031314.350/7/664[pii]

    Article  PubMed  PubMed Central  Google Scholar 

  138. Pitocco D, Tesauro M, Alessandro R, Ghirlanda G, Cardillo C (2013) Oxidative stress in diabetes: implications for vascular and other complications. Int J Mol Sci 14:21525–21550. https://doi.org/10.3390/ijms141121525

    Article  PubMed  PubMed Central  Google Scholar 

  139. Pittaluga M, Sgadari A, Dimauro I, Tavazzi B, Parisi P, Caporossi D (2015) Physical exercise and redox balance in type 2 diabetics: effects of moderate training on biomarkers of oxidative stress and DNA damage evaluated through comet assay. Oxidative Medicine and Cellular Longevity. Artn 981242. https://doi.org/10.1155/2015/981242

  140. Porrello ER, D’Amore A, Curl CL, Allen AM, Harrap SB, Thomas WG, Delbridge LM (2009) Angiotensin II type 2 receptor antagonizes angiotensin II type 1 receptor-mediated cardiomyocyte autophagy. Hypertension 53:1032–1040. https://doi.org/10.1161/HYPERTENSIONAHA.108.128488 (HYPERTENSIONAHA.108.128488[pii])

    Article  PubMed  Google Scholar 

  141. Porrello ER, Delbridge LM (2009) Cardiomyocyte autophagy is regulated by angiotensin II type 1 and type 2 receptors. Autophagy 5:1215–1216. https://doi.org/10.4161/auto.5.8.10153

    Article  PubMed  Google Scholar 

  142. Privratsky JR, Wold LE, Sowers JR, Quinn MT, Ren J (2003) AT1 blockade prevents glucose-induced cardiac dysfunction in ventricular myocytes: role of the AT1 receptor and NADPH oxidase. Hypertension 42:206–212. https://doi.org/10.1161/01.HYP.0000082814.62655.85 (01.HYP.0000082814.62655.85[pii])

    Article  PubMed  Google Scholar 

  143. Putnam K, Shoemaker R, Yiannikouris F, Cassis LA (2012) The renin-angiotensin system: a target of and contributor to dyslipidemias, altered glucose homeostasis, and hypertension of the metabolic syndrome. Am J Physiol-Heart Circ Physiol 302:H1219–H1230. https://doi.org/10.1152/ajpheart.00796.2011

    Article  PubMed  PubMed Central  Google Scholar 

  144. Qi Y, Xu Z, Zhu Q, Thomas C, Kumar R, Feng H, Dostal DE, White MF, Baker KM, Guo S (2013) Myocardial loss of IRS1 and IRS2 causes heart failure and is controlled by p38alpha MAPK during insulin resistance. Diabetes 62:3887–3900. https://doi.org/10.2337/db13-0095

    Article  PubMed  PubMed Central  Google Scholar 

  145. Rajesh M, Mukhopadhyay P, Batkai S, Patel V, Saito K, Matsumoto S, Kashiwaya Y, Horvath B, Mukhopadhyay B, Becker L, Hasko G, Liaudet L, Wink DA, Veves A, Mechoulam R, Pacher P (2010) Cannabidiol attenuates cardiac dysfunction, oxidative stress, fibrosis, and inflammatory and cell death signaling pathways in diabetic cardiomyopathy. J Am Coll Cardiol 56:2115–2125. https://doi.org/10.1016/j.jacc.2010.07.033

    Article  PubMed  PubMed Central  Google Scholar 

  146. Rees K, Hartley L, Day C, Flowers N, Clarke A, Stranges S (2013) Selenium supplementation for the primary prevention of cardiovascular disease (Review). Cochrane Database of Systematic Reviews. Artn Cd009671. https://doi.org/10.1002/14651858.Cd009671.Pub2

  147. Riehle C, Wende AR, Sena S, Pires KM, Pereira RO, Zhu Y, Bugger H, Frank D, Bevins J, Chen D, Perry CN, Dong XC, Valdez S, Rech M, Sheng X, Weimer BC, Gottlieb RA, White MF, Abel ED (2013) Insulin receptor substrate signaling suppresses neonatal autophagy in the heart. J Clin Invest 123:5319–5333. https://doi.org/10.1172/JCI71171 (71171[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  148. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, Stumvoll M, Kahn CR, Bluher M (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci USA 106:8665–8670. https://doi.org/10.1073/pnas.0903485106

    Article  PubMed  PubMed Central  Google Scholar 

  149. Russo C, Jin ZZ, Homma S, Rundek T, Elkind MSV, Sacco RL, Di Tullio MR (2010) Effect of diabetes and hypertension on left ventricular diastolic function in a high-risk population without evidence of heart disease. Eur J Heart Fail 12:454–461. https://doi.org/10.1093/eurjhf/hfq022

    Article  PubMed  PubMed Central  Google Scholar 

  150. Saito T, Asai K, Sato S, Hayashi M, Adachi A, Sasaki Y, Takano H, Mizuno K, Shimizu W (2016) Autophagic vacuoles in cardiomyocytes of dilated cardiomyopathy with initially decompensated heart failure predict improved prognosis. Autophagy 12:579–587. https://doi.org/10.1080/15548627.2016.1145326

    Article  PubMed  PubMed Central  Google Scholar 

  151. Sampaio WO, de Castro CH, Santos RAS, Schiffrin EL, Touyz RM (2007) Angiotensin-(1–7) counterregulates angiotensin II signaling in human endothelial cells. Hypertension 50:1093–1098. https://doi.org/10.1161/Hypertensionaha.106.084848

    Article  PubMed  Google Scholar 

  152. Sampaio WO, dos Santos RAS, Faria-Silva R, Machado LTD, Schiffrin EL, Touyz RM (2007) Angiotensin-(1–7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49:185–192. https://doi.org/10.1161/01.Hyp.0000251865.35728.2f

    Article  PubMed  Google Scholar 

  153. Santos RA (2014) Angiotensin-(1–7). Hypertension 63:1138–1147. https://doi.org/10.1161/HYPERTENSIONAHA.113.01274

    Article  PubMed  Google Scholar 

  154. Santos RAS, Ferreira AJ, Verano-Braga T, Bader M (2013) Angiotensin-converting enzyme 2, angiotensin-(1–7) and Mas: new players of the renin-angiotensin system. J Endocrinol 216:R1–R17. https://doi.org/10.1530/Joe-12-0341

    Article  PubMed  Google Scholar 

  155. Satoh M, Fujimoto S, Arakawa S, Yada T, Namikoshi T, Haruna Y, Horike H, Sasaki T, Kashihara N (2008) Angiotensin II type 1 receptor blocker ameliorates uncoupled endothelial nitric oxide synthase in rats with experimental diabetic nephropathy. Nephrol Dial Transplant 23:3806–3813. https://doi.org/10.1093/ndt/gfn357

    Article  PubMed  PubMed Central  Google Scholar 

  156. Savini I, Catani MV, Evangelista D, Gasperi V, Avigliano L (2013) Obesity-associated oxidative stress: strategies finalized to improve redox state. Int J Mol Sci 14:10497–10538. https://doi.org/10.3390/ijms140510497

    Article  PubMed  PubMed Central  Google Scholar 

  157. Schannwell CM, Schneppenheim M, Perings S, Plehn G, Strauer BE (2002) Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology 98:33–39 (64682[pii]64682)

    Article  PubMed  Google Scholar 

  158. Sciarretta S, Maejima Y, Zablocki D, Sadoshima J (2018) The role of autophagy in the heart. Annu Rev Physiol 80:1–26. https://doi.org/10.1146/annurev-physiol-021317-121427

    Article  PubMed  Google Scholar 

  159. Shah GN, Morofuji Y, Banks WA, Price TO (2013) High glucose-induced mitochondrial respiration and reactive oxygen species in mouse cerebral pericytes is reversed by pharmacological inhibition of mitochondrial carbonic anhydrases: Implications for cerebral microvascular disease in diabetes. Biochem Biophys Res Commun 440:354–358. https://doi.org/10.1016/j.bbrc.2013.09.086

    Article  PubMed  Google Scholar 

  160. Shahveisi K, Mousavi SH, Hosseini M, Rad AK, Jalali SA, Rajaei Z, Sadeghnia HR, Hadjzadeh MAR (2014) The role of local renin-angiotensin system on high glucose-induced cell toxicity, apoptosis and reactive oxygen species production in PC12 cells. Iran J Basic Med Sci 17:613–621

    PubMed  PubMed Central  Google Scholar 

  161. Shirakabe A, Zhai PY, Ikeda Y, Saito T, Maejima Y, Hsu CP, Nomura M, Egashira K, Levine B, Sadoshima J (2016) Drp1-dependent mitochondrial autophagy plays a protective role against pressure overload-induced mitochondrial dysfunction and heart failure. Circulation 133:1249–1263. https://doi.org/10.1161/Circulationaha.115.020502

    Article  PubMed  PubMed Central  Google Scholar 

  162. Singh K, Singh T, Sharma PL (2011) Beneficial effects of angiotensin (1–7) in diabetic rats with cardiomyopathy. Ther Adv Cardiovasc Dis 5:159–167. https://doi.org/10.1177/1753944711409281

    Article  PubMed  Google Scholar 

  163. Singh VP, Bali A, Singh N, Jaggi AS (2014) Advanced glycation end products and diabetic complications. Korean J Physiol Pharmacol 18:1–14. https://doi.org/10.4196/kjpp.2014.18.1.1

    Article  PubMed  PubMed Central  Google Scholar 

  164. Singh VP, Le B, Khode R, Baker KM, Kumar R (2008) Intracellular angiotensin II production in diabetic rats is correlated with cardiomyocyte apoptosis, oxidative stress, and cardiac fibrosis. Diabetes 57:3297–3306. https://doi.org/10.2337/db08-0805

    Article  PubMed  PubMed Central  Google Scholar 

  165. Soetikno V, Sari FR, Sukumaran V, Lakshmanan AP, Harima M, Suzuki K, Kawachi H, Watanabe K (2013) Curcumin decreases renal triglyceride accumulation through AMPK-SREBP signaling pathway in streptozotocin-induced type 1 diabetic rats. J Nutr Biochem 24:796–802. https://doi.org/10.1016/j.jnutbio.2012.04.013

    Article  PubMed  Google Scholar 

  166. Soetikno V, Sari FR, Sukumaran V, Lakshmanan AP, Mito S, Harima M, Thandavarayan RA, Suzuki K, Nagata M, Takagi R, Watanabe K (2012) Curcumin prevents diabetic cardiomyopathy in streptozotocin-induced diabetic rats: possible involvement of PKC-MAPK signaling pathway. Eur J Pharm Sci 47:604–614. https://doi.org/10.1016/j.ejps.2012.04.018

    Article  PubMed  Google Scholar 

  167. Stas S, Whaley-Connell A, Habibi J, Appesh L, Hayden MR, Karuparthi PR, Qazi M, Morris EM, Cooper SA, Link CD, Stump C, Hay M, Ferrario C, Sowers JR (2007) Mineralocorticoid receptor blockade attenuates chronic overexpression of the renin-angiotensin-aldosterone system stimulation of reduced nicotinamide adenine dinucleotide phosphate oxidase and cardiac remodeling. Endocrinology 148:3773–3780. https://doi.org/10.1210/en.2006-1691

    Article  PubMed  Google Scholar 

  168. Stiefel P, Vallejo-Vaz AJ, Garcia Morillo S, Villar J (2011) Role of the renin-angiotensin system and aldosterone on cardiometabolic syndrome. Int J Hypertens 2011:685238. https://doi.org/10.4061/2011/685238

    Article  PubMed  PubMed Central  Google Scholar 

  169. Straznicky NE, Lambert EA, Nestel PJ, McGrane MT, Dawood T, Schlaich MP, Masuo K, Eikelis N, de Courten B, Mariani JA, Esler MD, Socratous F, Chopra R, Sari CI, Paul E, Lambert GW (2010) Sympathetic neural adaptation to hypocaloric diet with or without exercise training in obese metabolic syndrome subjects. Diabetes 59:71–79. https://doi.org/10.2337/db09-0934

    Article  PubMed  Google Scholar 

  170. Sukumaran V, Veeraveedu PT, Gurusamy N, Yamaguchi K, Lakshmanan AP, Ma M, Suzuki K, Kodama M, Watanabe K (2011) Cardioprotective effects of telmisartan against heart failure in rats induced by experimental autoimmune myocarditis through the modulation of angiotensin-converting enzyme-2/angiotensin 1–7/mas receptor axis. Int J Biol Sci 7:1077–1092. https://doi.org/10.7150/ijbs.7.1077

    Article  PubMed  PubMed Central  Google Scholar 

  171. Sukumaran V, Veeraveedu PT, Gurusamy N, Lakshmanan AP, Yamaguchi K, Ma M, Suzuki K, Nagata M, Takagi R, Kodama M, Watanabe K (2012) Olmesartan attenuates the development of heart failure after experimental autoimmune myocarditis in rats through the modulation of ANG 1–7 mas receptor. Mol Cell Endocrinol 351:208–219. https://doi.org/10.1016/j.mce.2011.12.010

    Article  PubMed  Google Scholar 

  172. Sukumaran V, Watanabe K, Veeraveedu PT, Gurusamy N, Ma M, Thandavarayan RA, Lakshmanan AP, Yamaguchi K, Suzuki K, Kodama M (2011) Olmesartan, an AT1 antagonist, attenuates oxidative stress, endoplasmic reticulum stress and cardiac inflammatory mediators in rats with heart failure induced by experimental autoimmune myocarditis. Int J Biol Sci 7:154–167

    Article  PubMed  PubMed Central  Google Scholar 

  173. Sukumaran V, Watanabe K, Veeraveedu PT, Ma ML, Gurusamy N, Rajavel V, Suzuki K, Yamaguchi K, Kodama M, Aizawa Y (2011) Telmisartan ameliorates experimental autoimmune myocarditis associated with inhibition of inflammation and oxidative stress. Eur J Pharmacol 652:126–135. https://doi.org/10.1016/j.ejphar.2010.10.081

    Article  PubMed  Google Scholar 

  174. Sun M, Dawood F, Wen WH, Chen M, Dixon I, Kirshenbaum LA, Liu PP (2004) Excessive tumor necrosis factor activation after infarction contributes to susceptibility of myocardial rupture and left ventricular dysfunction. Circulation 110:3221–3228. https://doi.org/10.1161/01.CIR.0000147233.10318.23 (01.CIR.0000147233.10318.23[pii])

    Article  PubMed  Google Scholar 

  175. Sun Y, Weber KT (1996) Angiotensin converting enzyme and myofibroblasts during tissue repair in the rat heart. J Mol Cell Cardiol 28:851–858. https://doi.org/10.1006/jmcc.1996.0080

    Article  PubMed  Google Scholar 

  176. Symeonides P, Koulouris S, Vratsista E, Triantafyllou K, Ioannidis G, Thalassinos N, Katritsis D (2007) Both ramipril and telmisartan reverse indices of early diabetic cardiomyopathy: a comparative study. Eur J Echocardiogr 8:480–486. https://doi.org/10.1016/j.euje.2006.09.005

    Article  PubMed  Google Scholar 

  177. Takahashi H, Yoshika M, Komiyama Y, Nishimura M (2011) The central mechanism underlying hypertension: a review of the roles of sodium ions, epithelial sodium channels, the renin-angiotensin-aldosterone system, oxidative stress and endogenous digitalis in the brain. Hypertens Res 34:1147–1160. https://doi.org/10.1038/hr.2011.105

    Article  PubMed  PubMed Central  Google Scholar 

  178. Takeda M, Yamamoto K, Takemura Y, Takeshita H, Hongyo K, Kawai T, Hanasaki-Yamamoto H, Oguro R, Takami Y, Tatara Y, Takeya Y, Sugimoto K, Kamide K, Ohishi M, Rakugi H (2013) Loss of ACE2 exaggerates high-calorie diet induced insulin resistance by reduction of GLUT4 in mice. Diabetes 62:223–233. https://doi.org/10.2337/db12-0177

    Article  PubMed  Google Scholar 

  179. Tassone EJ, Sciacqua A, Andreozzi F, Presta I, Perticone M, Carnevale D, Casaburo M, Hribal ML, Sesti G, Perticone F (2013) Angiotensin (1–7) counteracts the negative effect of angiotensin II on insulin signalling in HUVECs. Cardiovasc Res 99:129–136. https://doi.org/10.1093/cvr/cvt065 (cvt065[pii])

    Article  PubMed  Google Scholar 

  180. Teshima Y, Takahashi N, Nishio S, Saito S, Kondo H, Fukui A, Aoki K, Yufu K, Nakagawa M, Saikawa T (2014) Production of reactive oxygen species in the diabetic heart - roles of mitochondria and NADPH oxidase -. Circ J 78:300–306. https://doi.org/10.1253/circj.CJ-13-1187

    Article  PubMed  Google Scholar 

  181. Tetzner A, Gebolys K, Meinert C, Klein S, Uhlich A, Trebicka J, Villacanas O, Walther T (2016) G-protein-coupled receptor MrgD is a receptor for angiotensin-(1–7) involving adenylyl cyclase, cAMP, and phosphokinase A. Hypertension 68:185–194. https://doi.org/10.1161/Hypertensionaha.116.07572

    Article  PubMed  Google Scholar 

  182. Than A, Leow MKS, Chen P (2013) Control of adipogenesis by the autocrine interplays between angiotensin 1–7/Mas receptor and angiotensin II/AT(1) receptor signaling pathways. J Biol Chem 288:15520–15531. https://doi.org/10.1074/jbc.M113.459792

    Article  PubMed  PubMed Central  Google Scholar 

  183. Thomas CM, Yong QC, Seqqat R, Chandel N, Feldman DL, Baker KM, Kumar R (2013) Direct renin inhibition prevents cardiac dysfunction in a diabetic mouse model: comparison with an angiotensin receptor antagonist and angiotensin-converting enzyme inhibitor. Clin Sci (Lond) 124:529–541. https://doi.org/10.1042/CS20120448

    Article  Google Scholar 

  184. Tsutsui H, Kinugawa S, Matsushima S (2008) Oxidative stress and mitochondrial DNA damage in heart failure. Circ J 72 Suppl A:A31–37. JST.JSTAGE/circj/CJ-08–0014 [pii]

  185. Tsutsui H, Kinugawa S, Matsushima S, Yokota T (2011) Oxidative stress in cardiac and skeletal muscle dysfunction associated with diabetes mellitus. J Clin Biochem Nutr 48:68–71. https://doi.org/10.3164/jcbn.11-012FR

    Article  PubMed  Google Scholar 

  186. Tziakas DN, Chalikias GK, Kaski JC (2005) Epidemiology of the diabetic heart. Coron Artery Dis 16(Suppl 1):S3–S10 (00019501-200511001-00002[pii])

    Article  PubMed  Google Scholar 

  187. Van Gaal LF, Maggioni AP (2014) Overweight, obesity, and outcomes: fat mass and beyond. Lancet 383:935–936. https://doi.org/10.1016/S0140-6736(13)62076-0

    Article  PubMed  Google Scholar 

  188. van Thiel BS, van der Pluijm I, Riet LT, Essers J, Danser AHJ (2015) The renin-angiotensin system and its involvement in vascular disease. Eur J Pharmacol 763:3–14. https://doi.org/10.1016/j.ejphar.2015.03.090

    Article  PubMed  Google Scholar 

  189. Varga ZV, Giricz Z, Liaudet L, Hasko G, Ferdinandy P, Pacher P (2015) Interplay of oxidative, nitrosative/nitrative stress, inflammation, cell death and autophagy in diabetic cardiomyopathy. Biochim Biophys Acta 1852:232–242. https://doi.org/10.1016/j.bbadis.2014.06.030 (S0925-4439(14)00207-5[pii])

    Article  PubMed  Google Scholar 

  190. Villela D, Leonhardt J, Patel N, Joseph J, Kirsch S, Hallberg A, Unger T, Bader M, Santos RA, Sumners C, Steckelings UM (2015) Angiotensin type 2 receptor (AT2R) and receptor Mas: a complex liaison. Clin Sci (Lond) 128:227–234. https://doi.org/10.1042/CS20130515 (CS20130515[pii])

    Article  Google Scholar 

  191. Waddingham MT, Edgley AJ, Tsuchimochi H, Kelly DJ, Shirai M, Pearson JT (2015) Contractile apparatus dysfunction early in the pathophysiology of diabetic cardiomyopathy. World J Diabetes 6:943–960. https://doi.org/10.4239/wjd.v6.i7.943

    Article  PubMed  PubMed Central  Google Scholar 

  192. Wang L, Lu K, Hao H, Li X, Wang J, Wang K, Yan Z, Zhang S, Du Y, Liu H (2013) Decreased autophagy in rat heart induced by anti-beta1-adrenergic receptor autoantibodies contributes to the decline in mitochondrial membrane potential. PLoS ONE 8:e81296. https://doi.org/10.1371/journal.pone.0081296 (PONE-D-12-29873[pii])

    Article  PubMed  PubMed Central  Google Scholar 

  193. Watanabe R, Suzuki J, Wakayama K, Kumagai H, Ikeda Y, Akazawa H, Komuro I, Isobe M (2016) Angiotensin II receptor blocker irbesartan attenuates cardiac dysfunction induced by myocardial infarction in the presence of renal failure. Hypertens Res 39:237–244. https://doi.org/10.1038/hr.2015.141

    Article  PubMed  Google Scholar 

  194. Watanabe Y, Nagai Y, Takatsu K (2013) Activation and regulation of the pattern recognition receptors in obesity-induced adipose tissue inflammation and insulin resistance. Nutrients 5:3757–3778. https://doi.org/10.3390/nu5093757

    Article  PubMed  PubMed Central  Google Scholar 

  195. Wei Y, Whaley-Connell AT, Chen K, Habibi J, Uptergrove GM, Clark SE, Stump CS, Ferrario CM, Sowers JR (2007) NADPH oxidase contributes to vascular inflammation, insulin resistance, and remodeling in the transgenic (mRen2) rat. Hypertension 50:384–391. https://doi.org/10.1161/HYPERTENSIONAHA.107.089284

    Article  PubMed  Google Scholar 

  196. Westermann D, Rutschow S, Jager S, Linderer A, Anker S, Riad A, Unger T, Schultheiss HP, Pauschinger M, Tschope C (2007) Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy: the role of angiotensin type 1 receptor antagonism. Diabetes 56:641–646. https://doi.org/10.2337/db06-1163 (56/3/641[pii])

    Article  PubMed  Google Scholar 

  197. Westermann D, Rutschow S, Van Linthout S, Linderer A, Bucker-Gartner C, Sobirey M, Riad A, Pauschinger M, Schultheiss HP, Tschope C (2006) Inhibition of p38 mitogen-activated protein kinase attenuates left ventricular dysfunction by mediating pro-inflammatory cardiac cytokine levels in a mouse model of diabetes mellitus. Diabetologia 49:2507–2513. https://doi.org/10.1007/s00125-006-0385-2

    Article  PubMed  Google Scholar 

  198. Willemsen JM, Westerink JW, Dallinga-Thie GM, van Zonneveld AJ, Gaillard CA, Rabelink TJ, de Koning EJP (2007) Angiotensin II type 1 receptor blockade improves hyperglycemia-induced endothelial dysfunction and reduces proinflammatory cytokine release from leukocytes. J Cardiovasc Pharmacol 49:6–12. https://doi.org/10.1097/Fjc.0b013e31802b31a7

    Article  PubMed  Google Scholar 

  199. Xie ZL, He CY, Zou MH (2011) AMP-activated protein kinase modulates cardiac autophagy in diabetic cardiomyopathy. Autophagy 7:1254–1255. https://doi.org/10.4161/auto.7.10.16740

    Article  PubMed  PubMed Central  Google Scholar 

  200. Xu JJ, Lei SQ, Liu YN, Gao X, Irwin MG, Xia ZY, Hei ZQ, Gan XL, Wang TT, Xia ZY (2013) Antioxidant N-acetylcysteine attenuates the reduction of Brg1 protein expression in the myocardium of type 1 diabetic rats. J Diabetes Res. Artn 716219. https://doi.org/10.1155/2013/716219

  201. Xu XM, Kobayashi S, Chen K, Timm D, Volden P, Huang Y, Gulick J, Yue ZY, Robbins J, Epstein PN, Liang QR (2013) Diminished autophagy limits cardiac injury in mouse models of type 1 diabetes. J Biol Chem 288:18077–18092. https://doi.org/10.1074/jbc.M113.474650

    Article  PubMed  PubMed Central  Google Scholar 

  202. Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, Johnson MR, Kasper EK, Levy WC, Masoudi FA, McBride PE, McMurray JJV, Mitchell JE, Peterson PN, Riegel B, Sam F, Stevenson LW, Tang WHW, Tsai EJ, Wilkoff BL, Anderson JL, Jacobs AK, Halperin JL, Albert NM, Bozkurt B, Brindis RG, Creager MA, Curtis LH, DeMets D, Guyton RA, Hochman JS, Kovacs RJ, Kushner FG, Ohman EM, Pressler SJ, Sellke FW, Shen WK, Stevenson WG, Commi W, Force AAT (2013) 2013 ACCF/AHA Guideline for the Management of Heart Failure A Report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 62:E147–E239. https://doi.org/10.1016/j.jacc.2013.05.019

    Article  PubMed  Google Scholar 

  203. Yaras N, Bilginoglu A, Vassort G, Turan B (2007) Restoration of diabetes-induced abnormal local Ca2+ release in cardiomyocytes by angiotensin II receptor blockade. Am J Physiol Heart Circ Physiol 292:H912-920. https://doi.org/10.1152/ajpheart.00824.2006

    Article  PubMed  Google Scholar 

  204. Yayama K, Okamoto H (2008) Angiotensin II-induced vasodilation via type 2 receptor: role of bradykinin and nitric oxide. Int Immunopharmacol 8:312–318. https://doi.org/10.1016/j.intimp.2007.06.012

    Article  PubMed  Google Scholar 

  205. Ye YZ, Li J, Yuan ZX (2013) Effect of antioxidant vitamin supplementation on cardiovascular outcomes: a meta-analysis of randomized controlled trials. Plos One 8. ARTN e56803. https://doi.org/10.1371/journal.pone.0056803

  206. Yim HE, Yoo KH (2008) Renin-angiotensin system - considerations for hypertension and kidney. Electrolyte Blood Press 6:42–50. https://doi.org/10.5049/EBP.2008.6.1.42

    Article  PubMed  PubMed Central  Google Scholar 

  207. Yokoyama T, Nakano M, Bednarczyk JL, McIntyre BW, Entman M, Mann DL (1997) Tumor necrosis factor-alpha provokes a hypertrophic growth response in adult cardiac myocytes. Circulation 95:1247–1252

    Article  PubMed  Google Scholar 

  208. Yong QC, Thomas CM, Seqqat R, Chandel N, Baker KM, Kumar R (2013) Angiotensin type 1a receptor-deficient mice develop diabetes-induced cardiac dysfunction, which is prevented by renin-angiotensin system inhibitors. Cardiovasc Diabetol 12:169. https://doi.org/10.1186/1475-2840-12-169

    Article  PubMed  PubMed Central  Google Scholar 

  209. Younce CW, Kolattukudy PE (2010) MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein, MCPIP. Biochem J 426:43–53. https://doi.org/10.1042/Bj20090976

    Article  PubMed  Google Scholar 

  210. Yu XY, Chen HM, Liang JL, Lin QX, Tan HH, Fu YH, Liu XY, Shan ZX, Li XH, Yang HZ, Yang M, Li Y, Lin SG (2011) Hyperglycemic myocardial damage is mediated by proinflammatory cytokine: macrophage migration inhibitory factor. PLoS ONE 6:e16239. https://doi.org/10.1371/journal.pone.0016239

    Article  PubMed  PubMed Central  Google Scholar 

  211. Yusuf S, Sleight P, Pogue J, Bosch J, Davies R, Dagenais G (2000) Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. N Engl J Med 342:145–153. https://doi.org/10.1056/NEJM200001203420301

    Article  PubMed  Google Scholar 

  212. Zhang D, Shadrin IY, Lam J, Xian HQ, Snodgrass HR, Bursac N (2013) Tissue-engineered cardiac patch for advanced functional maturation of human ESC-derived cardiomyocytes. Biomaterials 34:5813–5820. https://doi.org/10.1016/j.biomaterials.2013.04.026

    Article  PubMed  PubMed Central  Google Scholar 

  213. Zhang F, Hu YH, Xu QB, Ye S (2010) Different effects of angiotensin ii and angiotensin-(1-7) on vascular smooth muscle cell proliferation and migration. Plos One 5. ARTN e12323. https://doi.org/10.1371/journal.pone.0012323

  214. Zhao W, Ahokas RA, Weber KT, Sun Y (2006) ANG II-induced cardiac molecular and cellular events: role of aldosterone. Am J Physiol Heart Circ Physiol 291:H336-343. https://doi.org/10.1152/ajpheart.01307.2005

    Article  PubMed  Google Scholar 

  215. Zhao W, Li YL, Jia LX, Pan LL, Li HH, Du J (2014) Atg5 deficiency-mediated mitophagy aggravates cardiac inflammation and injury in response to angiotensin II. Free Radical Biol Med 69:108–115. https://doi.org/10.1016/j.freeradbiomed.2014.01.002

    Article  Google Scholar 

  216. Zhou G, Li X, Hein DW, Xiang X, Marshall JP, Prabhu SD, Cai L (2008) Metallothionein suppresses angiotensin II-induced nicotinamide adenine dinucleotide phosphate oxidase activation, nitrosative stress, apoptosis, and pathological remodeling in the diabetic heart. J Am Coll Cardiol 52:655–666. https://doi.org/10.1016/j.jacc.2008.05.019

    Article  PubMed  Google Scholar 

  217. Zhou MS, Schulman IH, Zeng Q (2012) Link between the renin-angiotensin system and insulin resistance: Implications for cardiovascular disease. Vasc Med 17:330–341. https://doi.org/10.1177/1358863X12450094

    Article  PubMed  Google Scholar 

  218. Zuanetti G, Latini R, Maggioni AP, Franzosi M, Santoro L, Tognoni G (1997) Effect of the ACE inhibitor lisinopril on mortality in diabetic patients with acute myocardial infarction: data from the GISSI-3 study. Circulation 96:4239–4245. https://doi.org/10.1161/01.cir.96.12.4239

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was made possible by a Rapid Response Call (RRC) award (RRC2-076) to H. C. Y. from the Qatar National Research Fund (a member of The Qatar Foundation). Venkatesh Sundararajan’s laboratory work is partially supported by the American Heart Association grants (20CDA35260096 and 20TPA3542000)

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vijayakumar Sukumaran.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sukumaran, V., Gurusamy, N., Yalcin, H.C. et al. Understanding diabetes-induced cardiomyopathy from the perspective of renin angiotensin aldosterone system. Pflugers Arch - Eur J Physiol 474, 63–81 (2022). https://doi.org/10.1007/s00424-021-02651-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-021-02651-x

Keywords

Navigation