Molecular and cellular mechanisms of cardiovascular disorders in diabetes

Circulation Research

Volumn 118, Issue 11, 2016, Pages 1808-1829

  Shah, Manasi S ^a   Brownlee, Michael ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

atherosclerosis; diabetes mellitus; heart failure; insulin resistance; myocardial infarction; reactive oxygen species

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); ADENYLATE KINASE; ALDEHYDE REDUCTASE; INFLAMMASOME; METHYLGLYOXAL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN ARGININE DEIMINASE; PROTEIN KINASE C BETA; PROTEIN KINASE C DELTA; PROTEIN KINASE C THETA; REACTIVE OXYGEN METABOLITE; SIRTUIN;

CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CIRCADIAN RHYTHM; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; ENZYME SUBSTRATE; FATTY ACID OXIDATION; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; REVIEW; ANIMAL; ATHEROSCLEROSIS; HEART FAILURE; METABOLISM; MYOCARDIAL INFARCTION; OXIDATIVE STRESS; PATHOLOGY;

ANIMALS; ATHEROSCLEROSIS; DIABETES COMPLICATIONS; HEART FAILURE; HUMANS; INSULIN RESISTANCE; MYOCARDIAL INFARCTION; OXIDATIVE STRESS;

EID: 84971265146     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.306923     Document Type: Review

References (180)

1. Gu K, Cowie CC, Harris MI, Mortality in adults with and without diabetes in a national cohort of the U.S. population, 1971-1993. Diabetes Care 1998 21 1138 1145
2. Virmani R, Burke AP, Kolodgie F, Morphological characteristics of coronary atherosclerosis in diabetes mellitus. Can J Cardiol 2006 22(SUPPL B) 81B 84B
3. Gu K, Cowie CC, Harris MI, Diabetes and decline in heart disease mortality in US adults. JAMA 1999 281 1291 1297
4. Burchfield JS, Xie M, Hill JA, Pathological ventricular remodeling: mechanisms: part 1 of 2. Circulation 2013 128 388 400. doi: 10.1161/CIRCULATIONAHA.113.001878
5. Donahoe SM, Stewart GC, McCabe CH, Mohanavelu S, Murphy SA, Cannon CP, Antman EM, Diabetes and mortality following acute coronary syndromes. JAMA 2007 298 765 775. doi: 10.1001/jama.298.7.765
6. Banerjee PS, Ma J, Hart GW, Diabetes-Associated dysregulation of O-GlcNAcylation in rat cardiac mitochondria. Proc Natl Acad Sci U S A 2015 112 6050 6055. doi: 10.1073/pnas.1424017112
7. Erickson JR, Pereira L, Wang L, Han G, Ferguson A, Dao K, Copeland RJ, Despa F, Hart GW, Ripplinger CM, Bers DM, Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 2013 502 372 376. doi: 10.1038/nature12537
8. Luo M, Guan X, Luczak ED, Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. J Clin Invest 2013 123 1262 1274. doi: 10.1172/JCI65268
9. Vinik AI, Ziegler D, Diabetic cardiovascular autonomic neuropathy. Circulation 2007 115 387 397. doi: 10.1161/CIRCULATIONAHA.106.634949
10. Battiprolu P, Wnag ZV, Hill J A, DK McGuire, N Marx, Diabetic cardiomyopathy mediators and mechanisms. In: Diabetes in Cardiovascular Disease: A Companion to Braunwald's Heart Disease 2015 Philadelphia, PA Saunders 290 320
11. Ramasamy R, Yan SF, Schmidt AM, DK McGuire, N Marx, Vascular biology of atherosclerosis in patients with diabetes. In: Diabetes in Cardiovascular Disease: A Companion to Braunwald's Heart Disease 2015 Philadelphia, PA Saunders 99 110
12. Plutzky J, Zafir B, Brown JD, DK McGuire, N Marx, Vascular biology of atherosclerosis in patients with diabetes. In: Diabetes in Cardiovascular Disease: A Companion to Braunwald's Heart Disease 2015 Philadelphia, PA Saunders 111 126
13. Ramasamy R, Goldberg IJ, Aldose reductase and cardiovascular diseases, creating human-like diabetic complications in an experimental model. Circ Res 2010 106 1449 1458. doi: 10.1161/CIRCRESAHA.109.213447
14. Vedantham S, Noh H, Ananthakrishnan R, Human aldose reductase expression accelerates atherosclerosis in diabetic apolipoprotein E-/- mice. Arterioscler Thromb Vasc Biol 2011 31 1805 1813. doi: 10.1161/ATVBAHA.111.226902
15. Vedantham S, Thiagarajan D, Ananthakrishnan R, Wang L, Rosario R, Zou YS, Goldberg I, Yan SF, Schmidt AM, Ramasamy R, Aldose reductase drives hyperacetylation of Egr-1 in hyperglycemia and consequent upregulation of proinflammatory and prothrombotic signals. Diabetes 2014 63 761 774. doi: 10.2337/db13-0032
16. Srivastava S, Vladykovskaya E, Barski OA, Spite M, Kaiserova K, Petrash JM, Chung SS, Hunt G, Dawn B, Bhatnagar A, Aldose reductase protects against early atherosclerotic lesion formation in apolipoprotein E-null mice. Circ Res 2009 105 793 802. doi: 10.1161/CIRCRESAHA.109.200568
17. Thornalley PJ, Battah S, Ahmed N, Karachalias N, Agalou S, Babaei-Jadidi R, Dawnay A, Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 2003 375 581 592. doi: 10.1042/BJ20030763
18. Thornalley PJ, The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 1990 269 1 11
19. Yao D, Brownlee M, Hyperglycemia-induced reactive oxygen species increase expression of the receptor for advanced glycation end products (RAGE) and RAGE ligands. Diabetes 2010 59 249 255. doi: 10.2337/db09-0801
20. Rong LL, Gooch C, Szabolcs M, Herold KC, Lalla E, Hays AP, Yan SF, Yan SS, Schmidt AM, RAGE: A journey from the complications of diabetes to disorders of the nervous system-striking a fine balance between injury and repair. Restor Neurol Neurosci 2005 23 355 365
21. Tikellis C, Pickering RJ, Tsorotes D, Huet O, Cooper ME, Jandeleit-Dahm K, Thomas MC, Dicarbonyl stress in the absence of hyperglycemia increases endothelial inflammation and atherogenesis similar to that observed in diabetes. Diabetes 2014 63 3915 3925. doi: 10.2337/db13-0932
22. Hanssen NM, Wouters K, Huijberts MS, Gijbels MJ, Sluimer JC, Scheijen JL, Heeneman S, Biessen EA, Daemen MJ, Brownlee M, de Kleijn DP, Stehouwer CD, Pasterkamp G, Schalkwijk CG, Higher levels of advanced glycation endproducts in human carotid atherosclerotic plaques are associated with a rupture-prone phenotype. Eur Heart J 2014 35 1137 1146. doi: 10.1093/eurheartj/eht402
23. Tian C, Alomar F, Moore CJ, Shao CH, Kutty S, Singh J, Bidasee KR, Reactive carbonyl species and their roles in sarcoplasmic reticulum Ca2+ cycling defect in the diabetic heart. Heart Fail Rev 2014 19 101 112. doi: 10.1007/s10741-013-9384-9
24. Molgat AS, Tilokee EL, Rafatian G, Vulesevic B, Ruel M, Milne R, Suuronen EJ, Davis DR, Hyperglycemia inhibits cardiac stem cell-mediated cardiac repair and angiogenic capacity. Circulation 2014 130 S70 S76. doi: 10.1161/CIRCULATIONAHA.113.007908
25. Vulesevic B, McNeill B, Geoffrion M, Kuraitis D, McBane JE, Lochhead M, Vanderhyden BC, Korbutt GS, Milne RW, Suuronen EJ, Glyoxalase-1 overexpression in bone marrow cells reverses defective neovascularization in STZ-induced diabetic mice. Cardiovasc Res 2014 101 306 316. doi: 10.1093/cvr/cvt259
26. Nam DH, Han JH, Lee TJ, Shishido T, Lim JH, Kim GY, Woo CH, CHOP deficiency prevents methylglyoxal-induced myocyte apoptosis and cardiac dysfunction. J Mol Cell Cardiol 2015 85 168 177. doi: 10.1016/j.yjmcc.2015.05.016
27. Thorp E, Li G, Seimon TA, Kuriakose G, Ron D, Tabas I, Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP. Cell Metab 2009 9 474 481. doi: 10.1016/j.cmet.2009.03.003
28. Vulesevic B, McNeill B, Giacco F, Maeda K, Blackburn NJ, Brownlee M, Milne RW, Suuronen EJ, Methylglyoxal-induced endothelial cell loss and inflammation contribute to the development of diabetic cardiomyopathy [published online ahead of print March 8, 2016] Diabetes. doi:10.2337/db15-0568
29. Parodi EM, Kuhn B, Signalling between microvascular endothelium and cardiomyocytes through neuregulin. Cardiovasc Res 2014 102 194 204. doi: 10.1093/cvr/cvu021
30. Craven PA, Davidson CM, DeRubertis FR, Increase in diacylglycerol mass in isolated glomeruli by glucose from de novo synthesis of glycerolipids. Diabetes 1990 39 667 674
31. Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL, Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci U S A 1992 89 11059 11063
32. Shiba T, Inoguchi T, Sportsman JR, Heath WF, Bursell S, King GL, Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol 1993 265 E783 E793
33. Cosentino-Gomes D, Rocco-Machado N, Meyer-Fernandes JR, Cell signaling through protein kinase C oxidation and activation. Int J Mol Sci 2012 13 10697 10721. doi: 10.3390/ijms130910697
34. Geraldes P, King GL, Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res 2010 106 1319 1331. doi: 10.1161/CIRCRESAHA.110.217117
35. Kong L, Shen X, Lin L, Leitges M, Rosario R, Zou YS, Yan SF, PKCβ promotes vascular inflammation and acceleration of atherosclerosis in diabetic ApoE null mice. Arterioscler Thromb Vasc Biol 2013 33 1779 1787. doi: 10.1161/ATVBAHA.112.301113
36. Durpès MC, Morin C, Paquin-Veillet J, Beland R, Paré M, Guimond MO, Rekhter M, King GL, Geraldes P, PKC-β activation inhibits IL-18-binding protein causing endothelial dysfunction and diabetic atherosclerosis. Cardiovasc Res 2015 106 303 313. doi: 10.1093/cvr/cvv107
37. Li Q, Park K, Li C, Rask-Madsen C, Mima A, Qi W, Mizutani K, Huang P, King GL, Induction of vascular insulin resistance and endothelin-1 expression and acceleration of atherosclerosis by the overexpression of protein kinase C-β isoform in the endothelium. Circ Res 2013 113 418 427. doi: 10.1161/CIRCRESAHA.113.301074
38. Way KJ, Isshiki K, Suzuma K, Yokota T, Zvagelsky D, Schoen FJ, Sandusky GE, Pechous PA, Vlahos CJ, Wakasaki H, King GL, Expression of connective tissue growth factor is increased in injured myocardium associated with protein kinase C beta2 activation and diabetes. Diabetes 2002 51 2709 2718
39. Verma SK, Deshmukh V, Liu P, Nutter CA, Espejo R, Hung ML, Wang GS, Yeo GW, Kuyumcu-Martinez MN, Reactivation of fetal splicing programs in diabetic hearts is mediated by protein kinase C signaling. J Biol Chem 2013 288 35372 35386. doi: 10.1074/jbc.M113.507426
40. Rask-Madsen C, King GL, Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab 2013 17 20 33. doi: 10.1016/j.cmet.2012.11.012
41. Hardivillé S, Hart GW, Nutrient regulation of signaling, transcription, and cell physiology by O-GlcNAcylation. Cell Metab 2014 20 208 213. doi: 10.1016/j.cmet.2014.07.014
42. Bond MR, Hanover JA, A little sugar goes a long way: the cell biology of O-GlcNAc. J Cell Biol 2015 208 869 880. doi: 10.1083/jcb.201501101
43. Marsh SA, Collins HE, Chatham JC, Protein O-GlcNAcylation and cardiovascular (patho)physiology. J Biol Chem 2014 289 34449 34456. doi: 10.1074/jbc.R114.585984
44. Makino A, Dai A, Han Y, Youssef KD, Wang W, Donthamsetty R, Scott BT, Wang H, Dillmann WH, O-GlcNAcase overexpression reverses coronary endothelial cell dysfunction in type 1 diabetic mice. Am J Physiol Cell Physiol 2015 309 C593 C599. doi: 10.1152/ajpcell.00069.2015
45. Aicher A, Heeschen C, Mildner-Rihm C, Urbich C, Ihling C, Technau-Ihling K, Zeiher AM, Dimmeler S, Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003 9 1370 1376. doi: 10.1038/nm948
46. Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M, Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 2001 108 1341 1348. doi: 10.1172/JCI11235
47. Qian J, Fulton D, Post-Translational regulation of endothelial nitric oxide synthase in vascular endothelium. Front Physiol 2013 4 347. doi: 10.3389/fphys.2013.00347
48. Federici M, Menghini R, Mauriello A, Hribal ML, Ferrelli F, Lauro D, Sbraccia P, Spagnoli LG, Sesti G, Lauro R, Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 2002 106 466 472
49. Shrikhande GV, Scali ST, da Silva CG, O-glycosylation regulates ubiquitination and degradation of the anti-inflammatory protein A20 to accelerate atherosclerosis in diabetic ApoE-null mice. PLoS One 2010 5 e14240. doi: 10.1371/journal.pone.0014240
50. Clark RJ, McDonough PM, Swanson E, Trost SU, Suzuki M, Fukuda M, Dillmann WH, Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 2003 278 44230 44237. doi: 10.1074/jbc.M303810200
51. Daniels L, Bell JR, Delbridge LM, McDonald FJ, Lamberts RR, Erickson JR, The role of CaMKII in diabetic heart dysfunction. Heart Fail Rev 2015 20 589 600. doi: 10.1007/s10741-015-9498-3
52. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M, Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000 404 787 790. doi: 10.1038/35008121
53. Brownlee M, Biochemistry and molecular cell biology of diabetic complications. Nature 2001 414 813 820. doi: 10.1038/414813a.
54. Brownlee M, The pathobiology of diabetic complications: A unifying mechanism. Diabetes 2005 54 1615 1625
55. Rosca MG, Vazquez EJ, Chen Q, Kerner J, Kern TS, Hoppel CL, Oxidation of fatty acids is the source of increased mitochondrial reactive oxygen species production in kidney cortical tubules in early diabetes. Diabetes 2012 61 2074 2083. doi: 10.2337/db11-1437
56. Crabtree MJ, Tatham AL, Al-Wakeel Y, Warrick N, Hale AB, Cai S, Channon KM, Alp NJ, Quantitative regulation of intracellular endothelial nitric-oxide synthase (eNOS) coupling by both tetrahydrobiopterin-eNOS stoichiometry and biopterin redox status: insights from cells with tet-regulated GTP cyclohydrolase I expression. J Biol Chem 2009 284 1136 1144. doi: 10.1074/jbc.M805403200.
57. Aghajanian A, Wittchen ES, Campbell SL, Burridge K, Direct activation of RhoA by reactive oxygen species requires a redox-sensitive motif. PLoS One 2009 4 e8045. doi: 10.1371/journal.pone.0008045
58. Wang W, Wang Y, Long J, Wang J, Haudek SB, Overbeek P, Chang BH, Schumacker PT, Danesh FR, Mitochondrial fission triggered by hyperglycemia is mediated by ROCK1 activation in podocytes and endothelial cells. Cell Metab 2012 15 186 200. doi: 10.1016/j.cmet.2012.01.009
59. Giacco F, Du X, Carratú A, Gerfen GJ, D'Apolito M, Giardino I, Rasola A, Marin O, Divakaruni AS, Murphy AN, Shah MS, Brownlee M, GLP-1 cleavage product reverses persistent ROS generation after transient hyperglycemia by disrupting an ROS-generating feedback loop. Diabetes 2015 64 3273 3284. doi: 10.2337/db15-0084
60. Schaffer SW, Jong CJ, Mozaffari M, Role of oxidative stress in diabetes-mediated vascular dysfunction: unifying hypothesis of diabetes revisited. Vascul Pharmacol 2012 57 139 149. doi: 10.1016/j.vph.2012.03.005
61. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, Channon KM, Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 2002 105 1656 1662
62. Zou MH, Shi C, Cohen RA, High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin H(2) receptor-mediated apoptosis and adhesion molecule expression in cultured human aortic endothelial cells. Diabetes 2002 51 198 203
63. Wang Y, Wang GZ, Rabinovitch PS, Tabas I, Macrophage mitochondrial oxidative stress promotes atherosclerosis and nuclear factor-κB-mediated inflammation in macrophages. Circ Res 2014 114 421 433. doi: 10.1161/CIRCRESAHA.114.302153
64. Maalouf RM, Eid AA, Gorin YC, Block K, Escobar GP, Bailey S, Abboud HE, Nox4-derived reactive oxygen species mediate cardiomyocyte injury in early type 1 diabetes. Am J Physiol Cell Physiol 2012 302 C597 C604. doi: 10.1152/ajpcell.00331.2011
65. Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM, Cave AC, Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 2006 113 1235 1243. doi: 10.1161/CIRCULATIONAHA.105.581397
66. Shen X, Zheng S, Metreveli NS, Epstein PN, Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 2006 55 798 805
67. Ye G, Metreveli NS, Donthi RV, Xia S, Xu M, Carlson EC, Epstein PN, Catalase protects cardiomyocyte function in models of type 1 and type 2 diabetes. Diabetes 2004 53 1336 1343
68. Finkel T, Signal transduction by reactive oxygen species. J Cell Biol 2011 194 7 15. doi: 10.1083/jcb.201102095
69. Burgoyne JR, Mongue-Din H, Eaton P, Shah AM, Redox signaling in cardiac physiology and pathology. Circ Res 2012 111 1091 1106. doi: 10.1161/CIRCRESAHA.111.255216
70. Liu Y, Zhao H, Li H, Kalyanaraman B, Nicolosi AC, Gutterman DD, Mitochondrial sources of H2O2 generation play a key role in flow-mediated dilation in human coronary resistance arteries. Circ Res 2003 93 573 580. doi: 10.1161/01.RES.0000091261.19387.AE.
71. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom-Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, Shah AM, Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol 2011 31 1368 1376. doi: 10.1161/ATVBAHA.110.219238
72. Schmelter M, Ateghang B, Helmig S, Wartenberg M, Sauer H, Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB J 2006 20 1182 1184. doi: 10.1096/fj.05-4723fje
73. Heo JS, Lee JC, β-Catenin mediates cyclic strain-stimulated cardiomyogenesis in mouse embryonic stem cells through ROS-dependent and integrin-mediated PI3K/Akt pathways. J Cell Biochem 2011 112 1880 1889. doi: 10.1002/jcb.23108
74. Prosser BL, Ward CW, Lederer WJ, X-ROS signaling: rapid mechano-chemo transduction in heart. Science 2011 333 1440 1445. doi: 10.1126/science.1202768
75. Nathan C, Cunningham-Bussel A, Beyond oxidative stress: An immunologist's guide to reactive oxygen species. Nat Rev Immunol 2013 13 349 361. doi: 10.1038/nri3423
76. Ma Q, Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 2013 53 401 426. doi: 10.1146/annurev-pharmtox-011112-140320
77. Xue M, Rabbani N, Momiji H, Imbasi P, Anwar MM, Kitteringham N, Park BK, Souma T, Moriguchi T, Yamamoto M, Thornalley PJ, Transcriptional control of glyoxalase 1 by Nrf2 provides a stress-responsive defence against dicarbonyl glycation. Biochem J 2012 443 213 222. doi: 10.1042/BJ20111648
78. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, Brownlee M, Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 2003 9 294 299. doi: 10.1038/nm834
79. Du Y, Kowluru A, Kern TS, PP2A contributes to endothelial death in high glucose: inhibition by benfotiamine. Am J Physiol Regul Integr Comp Physiol 2010 299 R1610 R1617. doi: 10.1152/ajpregu.00676.2009
80. Katare RG, Caporali A, Oikawa A, Meloni M, Emanueli C, Madeddu P, Vitamin B1 analog benfotiamine prevents diabetes-induced diastolic dysfunction and heart failure through Akt/Pim-1-mediated survival pathway. Circ Heart Fail 2010 3 294 305. doi: 10.1161/CIRCHEARTFAILURE.109.903450
81. Niture SK, Khatri R, Jaiswal AK, Regulation of Nrf2-An update. Free Radic Biol Med 2014 66 36 44. doi: 10.1016/j.freeradbiomed.2013.02.008
82. Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A, SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011 31 1121 1133. doi: 10.1128/MCB.01204-10
83. Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ, Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes 2008 57 2809 2817. doi: 10.2337/db06-1003
84. Wang Y, Zhang Z, Sun W, Tan Y, Liu Y, Zheng Y, Liu Q, Cai L, Sun J, Sulforaphane attenuation of type 2 diabetes-induced aortic damage was associated with the upregulation of Nrf2 expression and function. Oxid Med Cell Longev 2014 2014 123963. doi: 10.1155/2014/123963
85. Zhang Z, Wang S, Zhou S, Yan X, Wang Y, Chen J, Mellen N, Kong M, Gu J, Tan Y, Zheng Y, Cai L, Sulforaphane prevents the development of cardiomyopathy in type 2 diabetic mice probably by reversing oxidative stress-induced inhibition of LKB1/AMPK pathway. J Mol Cell Cardiol 2014 77 42 52. doi: 10.1016/j.yjmcc.2014.09.022
86. Tan Y, Ichikawa T, Li J, Si Q, Yang H, Chen X, Goldblatt CS, Meyer CJ, Li X, Cai L, Cui T, Diabetic downregulation of Nrf2 activity via ERK contributes to oxidative stress-induced insulin resistance in cardiac cells in vitro and in vivo. Diabetes 2011 60 625 633. doi: 10.2337/db10-1164
87. Hogan PG, Chen L, Nardone J, Rao A, Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev 2003 17 2205 2232. doi: 10.1101/gad.1102703
88. Olabisi OA, Soto-Nieves N, Nieves E, Yang TT, Yang X, Yu RY, Suk HY, Macian F, Chow CW, Regulation of transcription factor NFAT by ADP-ribosylation. Mol Cell Biol 2008 28 2860 2871. doi: 10.1128/MCB.01746-07
89. Nilsson-Berglund LM, Zetterqvist AV, Nilsson-Ohman J, Sigvardsson M, González Bosc LV, Smith ML, Salehi A, Agardh E, Fredrikson GN, Agardh CD, Nilsson J, Wamhoff BR, Hultgårdh-Nilsson A, Gomez MF, Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetes-induced hyperglycemia. Arterioscler Thromb Vasc Biol 2010 30 218 224. doi: 10.1161/ATVBAHA.109.199299
90. Zetterqvist AV, Berglund LM, Blanco F, Garcia-Vaz E, Wigren M, Dunér P, Andersson AM, To F, Spegel P, Nilsson J, Bengtsson E, Gomez MF, Inhibition of nuclear factor of activated T-cells (NFAT) suppresses accelerated atherosclerosis in diabetic mice. PLoS One 2014 8 e65020. doi: 10.1371/journal.pone.0065020
91. Friedman JK, Nitta CH, Henderson KM, Codianni SJ, Sanchez L, Ramiro-Diaz JM, Howard TA, Giermakowska W, Kanagy NL, Gonzalez Bosc LV, Intermittent hypoxia-induced increases in reactive oxygen species activate NFATc3 increasing endothelin-1 vasoconstrictor reactivity. Vascul Pharmacol 2014 60 17 24. doi: 10.1016/j.vph.2013.11.001
92. Letavernier E, Zafrani L, Perez J, Letavernier B, Haymann JP, Baud L, The role of calpains in myocardial remodelling and heart failure. Cardiovasc Res 2012 96 38 45. doi: 10.1093/cvr/cvs099
93. Bourajjaj M, Armand AS, da Costa Martins PA, Weijts B, van der Nagel R, Heeneman S, Wehrens XH, De Windt LJ, NFATc2 is a necessary mediator of calcineurin-dependent cardiac hypertrophy and heart failure. J Biol Chem 2008 283 22295 22303. doi: 10.1074/jbc.M801296200
94. Li Y, Ma J, Zhu H, Singh M, Hill D, Greer PA, Arnold JM, Abel ED, Peng T, Targeted inhibition of calpain reduces myocardial hypertrophy and fibrosis in mouse models of type 1 diabetes. Diabetes 2011 60 2985 2994. doi: 10.2337/db10-1333
95. Wang JC, Zhao Y, Li XD, Zhou NN, Sun H, Sun YY, Proteolysis by endogenous calpain I leads to the activation of calcineurin in human heart. Clin Lab 2012 58 1145 1152
96. Weber C, Noels H, Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011 17 1410 1422. doi: 10.1038/nm.2538
97. Warnatsch A, Ioannou M, Wang Q, Papayannopoulos V, Inflammation. Neutrophil extracellular traps license macrophages for cytokine production in atherosclerosis. Science 2015 349 316 320. doi: 10.1126/science.aaa8064
98. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A, Neutrophil extracellular traps kill bacteria. Science 2004 303 1532 1535. doi: 10.1126/science.1092385
99. Fadini GP, Menegazzo L, Scattolini V, Gintoli M, Albiero M, Avogaro A, A perspective on NETosis in diabetes and cardiometabolic disorders. Nutr Metab Cardiovasc Dis 2016 26 1 8. doi: 10.1016/j.numecd.2015.11.008
100. Nahrendorf M, Swirski FK, Immunology. Neutrophil-macrophage communication in inflammation and atherosclerosis. Science 2015 349 237 238. doi: 10.1126/science.aac7801
101. Rohrbach AS, Slade DJ, Thompson PR, Mowen KA, Activation of PAD4 in NET formation. Front Immunol 2012 3 360. doi: 10.3389/fimmu.2012.00360
102. Wong SL, Demers M, Martinod K, Gallant M, Wang Y, Goldfine AB, Kahn CR, Wagner DD, Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med 2015 21 815 819. doi: 10.1038/nm.3887
103. Abbas AK, Le K, Pimmett VL, Bell DA, Cairns E, Dekoter RP, Negative regulation of the peptidylarginine deiminase type IV promoter by NF-κB in human myeloid cells. Gene 2014 533 123 131. doi: 10.1016/j.gene.2013.09.108
104. Bierhaus A, Schiekofer S, Schwaninger M, Diabetes-Associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 2001 50 2792 2808
105. Serhan CN, Savill J, Resolution of inflammation: the beginning programs the end. Nat Immunol 2005 6 1191 1197. doi: 10.1038/ni1276
106. Lee HM, Kim JJ, Kim HJ, Shong M, Ku BJ, Jo EK, Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes 2013 62 194 204. doi: 10.2337/db12-0420
107. Luo B, Li B, Wang W, Liu X, Xia Y, Zhang C, Zhang M, Zhang Y, An F, NLRP3 gene silencing ameliorates diabetic cardiomyopathy in a type 2 diabetes rat model. PLoS One 2014 9 e104771. doi: 10.1371/journal.pone.0104771
108. Shao BZ, Xu ZQ, Han BZ, Su DF, Liu C, NLRP3 inflammasome and its inhibitors: A review. Front Pharmacol 2015 6 262. doi: 10.3389/fphar.2015.00262
109. Guo H, Callaway JB, Ting JP, Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 2015 21 677 687. doi: 10.1038/nm.3893
110. Misawa T, Takahama M, Kozaki T, Lee H, Zou J, Saitoh T, Akira S, Microtubule-driven spatial arrangement of mitochondria promotes activation of the NLRP3 inflammasome. Nat Immunol 2013 14 454 460. doi: 10.1038/ni.2550
111. Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z, Olivier AK, Sadler JJ, Knepper-Adrian V, Han R, Qiao L, Eisenbarth SC, Nauseef WM, Cassel SL, Sutterwala FS, Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 2013 39 311 323. doi: 10.1016/j.immuni.2013.08.001
112. Li J, Romestaing C, Han X, Li Y, Hao X, Wu Y, Sun C, Liu X, Jefferson LS, Xiong J, Lanoue KF, Chang Z, Lynch CJ, Wang H, Shi Y, Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity. Cell Metab 2010 12 154 165. doi: 10.1016/j.cmet.2010.07.003
113. He Q, Han X, Cardiolipin remodeling in diabetic heart. Chem Phys Lipids 2014 179 75 81. doi: 10.1016/j.chemphyslip.2013.10.007
114. Wang JX, Gao J, Ding SL, Oxidative modification of miR-184 enables it to target Bcl-xL and Bcl-w. Mol Cell 2015 59 50 61. doi: 10.1016/j.molcel.2015.05.003
115. Wagschal A, Najafi-Shoushtari SH, Wang L, Genome-wide identification of microRNAs regulating cholesterol and triglyceride homeostasis. Nat Med 2015 21 1290 1297. doi: 10.1038/nm.3980
116. Zhou Q, Lv D, Chen P, Xu T, Fu S, Li J, Bei Y, MicroRNAs in diabetic cardiomyopathy and clinical perspectives. Front Genet 2014 5 185. doi: 10.3389/fgene.2014.00185
117. Friedman RC, Farh KK, Burge CB, Bartel DP, Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009 19 92 105. doi:10.1101/gr.082701.108
118. Matkovich SJ, Wang W, Tu Y, Eschenbacher WH, Dorn LE, Condorelli G, Diwan A, Nerbonne JM, Dorn GW II, MicroRNA-133a protects against myocardial fibrosis and modulates electrical repolarization without affecting hypertrophy in pressure-overloaded adult hearts. Circ Res 2010 106 166 175. doi: 10.1161/CIRCRESAHA.109.202176
119. Choi SE, Fu T, Seok S, Kim DH, Yu E, Lee KW, Kang Y, Li X, Kemper B, Kemper JK, Elevated microRNA-34a in obesity reduces NAD+ levels and SIRT1 activity by directly targeting NAMPT. Aging Cell 2013 12 1062 1072. doi: 10.1111/acel.12135
120. Li Y, Xu S, Jiang B, Cohen RA, Zang M, Activation of sterol regulatory element binding protein and NLRP3 inflammasome in atherosclerotic lesion development in diabetic pigs. PLoS One 2013 8 e67532. doi: 10.1371/journal.pone.0067532
121. Kuwabara Y, Horie T, Baba O, Watanabe S, Nishiga M, Usami S, Izuhara M, Nakao T, Nishino T, Otsu K, Kita T, Kimura T, Ono K, MicroRNA-451 exacerbates lipotoxicity in cardiac myocytes and high-fat diet-induced cardiac hypertrophy in mice through suppression of the LKB1/AMPK pathway. Circ Res 2015 116 279 288. doi: 10.1161/CIRCRESAHA.116.304707
122. Im SS, Yousef L, Blaschitz C, Liu JZ, Edwards RA, Young SG, Raffatellu M, Osborne TF, Linking lipid metabolism to the innate immune response in macrophages through sterol regulatory element binding protein-1a. Cell Metab 2011 13 540 549. doi: 10.1016/j.cmet.2011.04.001
123. Taniguchi CM, Emanuelli B, Kahn CR, Critical nodes in signalling pathways: insights into insulin action. Nat Rev Mol Cell Biol 2006 7 85 96. doi: 10.1038/nrm1837
124. Boucher J, Kleinridders A, Kahn CR, Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harb Perspect Biol 2014 6 1 23
125. Nolan CJ, Ruderman NB, Kahn SE, Pedersen O, Prentki M, Insulin resistance as a physiological defense against metabolic stress: implications for the management of subsets of type 2 diabetes. Diabetes 2015 64 673 686. doi: 10.2337/db14-0694
126. Brown MS, Goldstein JL, Selective versus total insulin resistance: A pathogenic paradox. Cell Metab 2008 7 95 96. doi: 10.1016/j.cmet.2007.12.009
127. Muoio DM, Metabolic inflexibility: when mitochondrial indecision leads to metabolic gridlock. Cell 2014 159 1253 1262. doi: 10.1016/j.cell.2014.11.034
128. Du X, Edelstein D, Obici S, Higham N, Zou MH, Brownlee M, Insulin resistance reduces arterial prostacyclin synthase and eNOS activities by increasing endothelial fatty acid oxidation. J Clin Invest 2006 116 1071 1080. doi: 10.1172/JCI23354
129. Jiang ZY, Lin YW, Clemont A, Feener EP, Hein KD, Igarashi M, Yamauchi T, White MF, King GL, Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest 1999 104 447 457. doi: 10.1172/JCI5971
130. Calnan DR, Brunet A, The FoxO code. Oncogene 2008 27 2276 2288. doi: 10.1038/onc.2008.21
131. Tabit CE, Shenouda SM, Holbrook M, Fetterman JL, Kiani S, Frame AA, Kluge MA, Held A, Dohadwala MM, Gokce N, Farb MG, Rosenzweig J, Ruderman N, Vita JA, Hamburg NM, Protein kinase C-β contributes to impaired endothelial insulin signaling in humans with diabetes mellitus. Circulation 2013 127 86 95. doi: 10.1161/CIRCULATIONAHA.112.127514
132. Li H, Forstermann U, Pharmacological prevention of eNOS uncoupling. Curr Pharm Des 2014 20 3595 3606
133. Bayeva M, Sawicki KT, Ardehali H, Taking diabetes to heart-deregulation of myocardial lipid metabolism in diabetic cardiomyopathy. J Am Heart Assoc 2013 2 e000433. doi: 10.1161/JAHA.113.000433
134. Jia G, DeMarco VG, Sowers JR, Insulin resistance and hyperinsulinaemia in diabetic cardiomyopathy. Nat Rev Endocrinol 2016 12 144 153. doi: 10.1038/nrendo.2015.216
135. Pulinilkunnil T, Rodrigues B, Cardiac lipoprotein lipase: metabolic basis for diabetic heart disease. Cardiovasc Res 2006 69 329 340. doi: 10.1016/j.cardiores.2005.09.017
136. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ, Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest 2003 111 419 426. doi: 10.1172/JCI16751
137. Greenwalt DE, Scheck SH, Rhinehart-Jones T, Heart CD36 expression is increased in murine models of diabetes and in mice fed a high fat diet. J Clin Invest 1995 96 1382 1388. doi: 10.1172/JCI118173
138. Tremblay F, Dubois MJ, Marette A, Regulation of GLUT4 traffic and function by insulin and contraction in skeletal muscle. Front Biosci 2003 8 d1072 d1084
139. Doria A, Nosadini R, Avogaro A, Fioretto P, Crepaldi G, Myocardial metabolism in type 1 diabetic patients without coronary artery disease. Diabet Med 1991 8 Spec No S104 S107
140. Camps M, Castelló A, Muñoz P, Monfar M, Testar X, Palacín M, Zorzano A, Effect of diabetes and fasting on GLUT-4 (muscle/fat) glucose-Transporter expression in insulin-sensitive tissues. Heterogeneous response in heart, red and white muscle. Biochem J 1992 282 (pt 3) 765 772
141. Finck BN, Han X, Courtois M, Aimond F, Nerbonne JM, Kovacs A, Gross RW, Kelly DP, A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc Natl Acad Sci U S A 2003 100 1226 1231. doi: 10.1073/pnas.0336724100
142. Madrazo JA, Kelly DP, The PPAR trio: regulators of myocardial energy metabolism in health and disease. J Mol Cell Cardiol 2008 44 968 975. doi: 10.1016/j.yjmcc.2008.03.021
143. Chakravarthy MV, Lodhi IJ, Yin L, Malapaka RR, Xu HE, Turk J, Semenkovich CF, Identification of a physiologically relevant endogenous ligand for PPARalpha in liver. Cell 2009 138 476 488. doi: 10.1016/j.cell.2009.05.036
144. Blanquart C, Mansouri R, Paumelle R, Fruchart JC, Staels B, Glineur C, The protein kinase C signaling pathway regulates a molecular switch between transactivation and transrepression activity of the peroxisome proliferator-Activated receptor alpha. Mol Endocrinol 2004 18 1906 1918. doi: 10.1210/me.2003-0327
145. Quintana MT, He J, Sullivan J, Grevengoed T, Schisler J, Han Y, Hill JA, Yates CC, Stansfield WE, Mapanga RF, Essop MF, Muehlbauer MJ, Newgard CB, Bain JR, Willis MS, Muscle ring finger-3 protects against diabetic cardiomyopathy induced by a high fat diet. BMC Endocr Disord 2015 15 36. doi: 10.1186/s12902-015-0028-z.
146. Chaurasia B, Summers SA, Ceramides-Lipotoxic Inducers of Metabolic Disorders. Trends Endocrinol Metab 2015 26 538 550. doi: 10.1016/j.tem.2015.07.006
147. Park TS, Hu Y, Noh HL, Drosatos K, Okajima K, Buchanan J, Tuinei J, Homma S, Jiang XC, Abel ED, Goldberg IJ, Ceramide is a cardiotoxin in lipotoxic cardiomyopathy. J Lipid Res 2008 49 2101 2112. doi: 10.1194/jlr.M800147-JLR200
148. Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED, Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 2007 56 2457 2466. doi: 10.2337/db07-0481
149. Anderson EJ, Kypson AP, Rodriguez E, Anderson CA, Lehr EJ, Neufer PD, Substrate-specific derangements in mitochondrial metabolism and redox balance in the atrium of the type 2 diabetic human heart. J Am Coll Cardiol 2009 54 1891 1898. doi: 10.1016/j.jacc.2009.07.031
150. Han X, Yang J, Yang K, Zhao Z, Abendschein DR, Gross RW, Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: A shotgun lipidomics study. Biochemistry 2007 46 6417 6428. doi: 10.1021/bi7004015
151. Ren M, Phoon CK, Schlame M, Metabolism and function of mitochondrial cardiolipin. Prog Lipid Res 2014 55 1 16. doi: 10.1016/j.plipres.2014.04.001
152. Paradies G, Paradies V, De Benedictis V, Ruggiero FM, Petrosillo G, Functional role of cardiolipin in mitochondrial bioenergetics. Biochim Biophys Acta 2014 1837 408 417. doi: 10.1016/j.bbabio.2013.10.006
153. Frohman MA, Role of mitochondrial lipids in guiding fission and fusion. J Mol Med (Berl) 2015 93 263 269. doi: 10.1007/s00109-014-1237-z.
154. Eijkelenboom A, Burgering BM, FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 2013 14 83 97. doi: 10.1038/nrm3507
155. Ozcan L, Wong CC, Li G, Xu T, Pajvani U, Park SK, Wronska A, Chen BX, Marks AR, Fukamizu A, Backs J, Singer HA, Yates JR III, Accili D, Tabas I, Calcium signaling through CaMKII regulates hepatic glucose production in fasting and obesity. Cell Metab 2012 15 739 751. doi: 10.1016/j.cmet.2012.03.002
156. Battiprolu PK, Hojayev B, Jiang N, Wang ZV, Luo X, Iglewski M, Shelton JM, Gerard RD, Rothermel BA, Gillette TG, Lavandero S, Hill JA, Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J Clin Invest 2012 122 1109 1118. doi: 10.1172/JCI60329
157. Vásquez-Trincado C, García-Carvajal I, Pennanen C, Parra V, Hill JA, Rothermel BA, Lavandero S, Mitochondrial dynamics, mitophagy and cardiovascular disease. J Physiol 2016 594 509 525. doi: 10.1113/JP271301
158. Montaigne D, Marechal X, Coisne A, Myocardial contractile dysfunction is associated with impaired mitochondrial function and dynamics in type 2 diabetic but not in obese patients. Circulation 2014 130 554 564. doi: 10.1161/CIRCULATIONAHA.113.008476
159. Parra V, Verdejo H, del Campo A, Pennanen C, Kuzmicic J, Iglewski M, Hill JA, Rothermel BA, Lavandero S, The complex interplay between mitochondrial dynamics and cardiac metabolism. J Bioenerg Biomembr 2011 43 47 51. doi: 10.1007/s10863-011-9332-0
160. Mishra P, Chan DC, Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 2014 15 634 646. doi: 10.1038/nrm3877
161. Min K, Kwon OS, Smuder AJ, Wiggs MP, Sollanek KJ, Christou DD, Yoo JK, Hwang MH, Szeto HH, Kavazis AN, Powers SK, Increased mitochondrial emission of reactive oxygen species and calpain activation are required for doxorubicin-induced cardiac and skeletal muscle myopathy. J Physiol 2015 593 2017 2036. doi: 10.1113/jphysiol.2014.286518
162. Burkard N, Becher J, Heindl C, Neyses L, Schuh K, Ritter O, Targeted proteolysis sustains calcineurin activation. Circulation 2005 111 1045 1053. doi: 10.1161/01.CIR.0000156458.80515.F7
163. Makino A, Scott BT, Dillmann WH, Mitochondrial fragmentation and superoxide anion production in coronary endothelial cells from a mouse model of type 1 diabetes. Diabetologia 2010 53 1783 1794. doi: 10.1007/s00125-010-1770-4
164. Parra V, Verdejo HE, Iglewski M, Insulin stimulates mitochondrial fusion and function in cardiomyocytes via the Akt-mTOR-NFκB-Opa-1 signaling pathway. Diabetes 2014 63 75 88. doi: 10.2337/db13-0340
165. Bass J, Takahashi JS, Circadian integration of metabolism and energetics. Science 2010 330 1349 1354. doi: 10.1126/science.1195027
166. Liu C, Li S, Liu T, Borjigin J, Lin JD, Transcriptional coactivator PGC-1alpha integrates the mammalian clock and energy metabolism. Nature 2007 447 477 481. doi: 10.1038/nature05767
167. Bass J, Circadian topology of metabolism. Nature 2012 491 348 356. doi: 10.1038/nature11704
168. Hoyle NP, O'Neill JS, Oxidation-reduction cycles of peroxiredoxin proteins and nontranscriptional aspects of timekeeping. Biochemistry 2015 54 184 193. doi: 10.1021/bi5008386
169. Baggs JE, Price TS, DiTacchio L, Panda S, Fitzgerald GA, Hogenesch JB, Network features of the mammalian circadian clock. PLoS Biol 2009 7 e52. doi: 10.1371/journal.pbio.1000052
170. Anea CB, Cheng B, Sharma S, Kumar S, Caldwell RW, Yao L, Ali MI, Merloiu AM, Stepp DW, Black SM, Fulton DJ, Rudic RD, Increased superoxide and endothelial NO synthase uncoupling in blood vessels of Bmal1-knockout mice. Circ Res 2012 111 1157 1165. doi: 10.1161/CIRCRESAHA.111.261750
171. Anea CB, Zhang M, Stepp DW, Simkins GB, Reed G, Fulton DJ, Rudic RD, Vascular disease in mice with a dysfunctional circadian clock. Circulation 2009 119 1510 1517. doi: 10.1161/CIRCULATIONAHA.108.827477
172. Schoenhard JA, Smith LH, Painter CA, Eren M, Johnson CH, Vaughan DE, Regulation of the PAI-1 promoter by circadian clock components: differential activation by BMAL1 and BMAL2. J Mol Cell Cardiol 2003 35 473 481
173. Wang J, Yin L, Lazar MA, The orphan nuclear receptor Rev-erb alpha regulates circadian expression of plasminogen activator inhibitor type 1. J Biol Chem 2006 281 33842 33848. doi: 10.1074/jbc.M607873200
174. Jeyaraj D, Haldar SM, Wan X, Circadian rhythms govern cardiac repolarization and arrhythmogenesis. Nature 2012 483 96 99. doi: 10.1038/nature10852
175. Nishikawa T, Brownlee M, Araki E, Mitochondrial reactive oxygen species in the pathogenesis of early diabetic nephropathy. J Diabetes Investig 2015 6 137 139. doi: 10.1111/jdi.12258
176. He B, Nohara K, Park N, Park YS, Guillory B, Zhao Z, Garcia JM, Koike N, Lee CC, Takahashi JS, Yoo SH, Chen Z, The small molecule nobiletin targets the molecular oscillator to enhance circadian rhythms and protect against metabolic syndrome. Cell Metab 2016 23 610 621. doi: 10.1016/j.cmet.2016.03.007
177. Sovari AA, Rutledge CA, Jeong EM, Dolmatova E, Arasu D, Liu H, Vahdani N, Gu L, Zandieh S, Xiao L, Bonini MG, Duffy HS, Dudley SC Jr, Mitochondria oxidative stress, connexin43 remodeling, and sudden arrhythmic death. Circ Arrhythm Electrophysiol 2013 6 623 631. doi: 10.1161/CIRCEP.112.976787
178. Sun H, Olson KC, Gao C, Catabolic defect of branched-chain amino acids promotes heart failure [published online ahead of print April 8, 2016] Circulation. doi: 10.1161/CIRCULATIONAHA.115.020226. http://circ.ahajournals.org/content/early/2016/04/08/CIRCULATIONAHA.115.020226.abstract
179. Stevens MJ, Dayanikli F, Raffel DM, Allman KC, Sandford T, Feldman EL, Wieland DM, Corbett J, Schwaiger M, Scintigraphic assessment of regionalized defects in myocardial sympathetic innervation and blood flow regulation in diabetic patients with autonomic neuropathy. J Am Coll Cardiol 1998 31 1575 1584
180. Campanucci V, Krishnaswamy A, Cooper E, Diabetes depresses synaptic transmission in sympathetic ganglia by inactivating nAChRs through a conserved intracellular cysteine residue. Neuron 2010 66 827 834. doi: 10.1016/j.neuron.2010.06.010