Upregulation of connexin 43 and apoptosis-associated protein expression by high glucose in H9c2 cells was improved by resveratrol via the autophagy signaling pathway

Molecular Medicine Reports

Volumn 16, Issue 3, 2017, Pages 3262-3268

  Wang, Guang Yu ^a   Bi, Ya Guang ^a   Liu, Xiang Dong ^a   Han, Jun Feng ^a   Wei, Meng ^a   Zhang, Qing Yong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Autophagy; Connexin43; H9c2 cells; High glucose; Resveratrol

Indexed keywords

BECLIN 1; CHLOROQUINE; CONNEXIN 43; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LACTATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 I; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3 II; PROTEIN BAX; PROTEIN BCL 2; RESVERATROL; SEQUESTOSOME 1; UNCLASSIFIED DRUG; STILBENE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CARDIAC MUSCLE CELL; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG MECHANISM; H9C2 CELL LINE; HYPERGLYCEMIA; MTT ASSAY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; MOUSE; PATHOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE; CELL SURVIVAL; CHLOROQUINE; CONNEXIN 43; DOWN-REGULATION; GLUCOSE; HYPERGLYCEMIA; L-LACTATE DEHYDROGENASE; MICE; SIGNAL TRANSDUCTION; STILBENES; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 85025596166     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2017.6953     Document Type: Article

References (38)

1. He C, Zhu H, Li H, Zou MH and Xie Z: Dissociation of Bcl-2-Beclin1 complex by activated AMPK enhances cardiac autophagy and protects against cardiomyocyte apoptosis in diabetes. Diabetes 62: 1270-1281, 2013.
2. Xie Z, Lau K, Eby B, Lozano P, He C, Pennington B, Li H, Rathi S, Dong Y, Tian R, et al: Improvement of cardiac functions by chronic metformin treatment is associated with enhanced cardiac autophagy in diabetic OVE26 mice. Diabetes 60: 1770-1778, 2011.
3. Martins-Marques T, Catarino S, Marques C, Pereira P and Girão H: To beat or not to beat: Degradation of Cx43 imposes the heart rhythm. Biochem Soc Trans 43: 476-481, 2015.
4. Rohr S: Role of gap junctions in the propagation of the cardiac action potential. Cardiovasc Res 62: 309-322, 2004.
5. Vozzi C, Dupont E, Coppen SR, Yeh HI and Severs NJ: Chamber-related differences in connexin expression in the human heart. J Mol Cell Cardiol 31: 991-1003, 1999.
6. Zhou P, Zhang SM, Wang QL, Wu Q, Chen M and Pei JM: Anti-arrhythmic effect of verapamil is accompanied by preservation of cx43 protein in rat heart. PLoS One 8: e71567, 2013.
7. Rutledge CA, Ng FS, Sulkin MS, Greener ID, Sergeyenko AM, Liu H, Gemel J, Beyer EC, Sovari AA, Efimov IR and Dudley SC: c-Src kinase inhibition reduces arrhythmia inducibility and connexin43 dysregulation after myocardial infarction. J Am Coll Cardiol 63: 928-934, 2014.
8. Hesketh GG, Shah MH, Halperin VL, Cooke CA, Akar FG, Yen TE, Kass DA, Machamer CE, Van Eyk JE and Tomaselli GF: Ultrastructure and regulation of lateralized connexin43 in the failing heart. Circ Res 106: 1153-1163, 2010.
9. Zhang W, Zhao G, Hu X, Wang M, Li H, Ye Y, Du Q, Yao J, Bao Z, Hong W, et al: Aliskiren-attenuated myocardium apoptosis via regulation of autophagy and connexin-43 in aged spontaneously hypertensive rats. J Cell Mol Med 18: 1247-1256, 2014.
10. Lin H, Ogawa K, Imanaga I and Tribulova N: Remodeling of connexin 43 in the diabetic rat heart. Mol Cell Biochem 290: 69-78, 2006.
11. Howarth FC, Nowotny N, Zilahi E, El Haj MA and Lei M: Altered expression of gap junction connexin proteins may partly underlie heart rhythm disturbances in the streptozotocin-induced diabetic rat heart. Mol Cell Biochem 305: 145-151, 2007.
12. Howarth FC, Chandler NJ, Kharche S, Tellez JO, Greener ID, Yamanushi TT, Billeter R, Boyett MR, Zhang H and Dobrzynski H: Effects of streptozotocin-induced diabetes on connexin43 mRNA and protein expression in ventricular muscle. Mol Cell Biochem 319: 105-114, 2008.
13. Fong JT, Kells RM, Gumpert AM, Marzillier JY, Davidson MW and Falk MM: Internalized gap junctions are degraded by autophagy. Autophagy 8: 794-811, 2012.
14. Martins-Marques T, Catarino S, Zuzarte M, Marques C, Matafome P, Pereira P and Girão H: Ischaemia-induced autophagy leads to degradation of gap junction protein connexin43 in cardiomyocytes. Biochem J 467: 231-245, 2015.
15. Wei H, Liu L and Chen Q: Selective removal of mitochondria via mitophagy: Distinct pathways for different mitochondrial stresses. Biochim Biophys Acta 1853: 2784-2790, 2015.
16. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B and Sadoshima J: Distinct roles of autophagy in the heart during ischemia and reperfusion: Roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res 100: 914-922, 2007.
17. Lichtenstein A, Minogue PJ, Beyer EC and Berthoud VM: Autophagy: A pathway that contributes to connexin degradation. J Cell Sci 124: 910-920, 2011.
18. Kanamori H, Takemura G, Goto K, Tsujimoto A, Mikami A, Ogino A, Watanabe T, Morishita K, Okada H, Kawasaki M, et al: Autophagic adaptations in diabetic cardiomyopathy differ between type 1 and type 2 diabetes. Autophagy 11: 1146-1160, 2015.
19. Liu Y, Palanivel R, Rai E, Park M, Gabor TV, Scheid MP, Xu A and Sweeney G: Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice. Diabetes 64: 36-48, 2015.
20. Wang B, Yang Q, Sun YY, Xing YF, Wang YB, Lu XT, Bai WW, Liu XQ and Zhao YX: Resveratrol-enhanced autophagic flux ameliorates myocardial oxidative stress injury in diabetic mice. J Cell Mol Med 18: 1599-1611, 2014.
21. Gurusamy N, Lekli I, Mukherjee S, Ray D, Ahsan MK, Gherghiceanu M, Popescu LM and Das DK: Cardioprotection by resveratrol: A novel mechanism via autophagy involving the mTORC2 pathway. Cardiovasc Res 86: 103-112, 2010.
22. Kanamori H, Takemura G, Goto K, Tsujimoto A, Ogino A, Takeyama T, Kawaguchi T, Watanabe T, Morishita K, Kawasaki M, et al: Resveratrol reverses remodeling in hearts with large, old myocardial infarctions through enhanced autophagy-activating AMP kinase pathway. Am J Pathol 182: 701-713, 2013.
23. Guo R and Ren J: Deficiency in AMPK attenuates ethanol-induced cardiac contractile dysfunction through inhibition of autophagosome formation. Cardiovasc Res 94: 480-491, 2012.
24. Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Øvervatn A, Bjørkøy G and Johansen T: p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 282: 24131-24145, 2007.
25. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y and Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728, 2000.
26. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al: Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12: 1-222, 2016.
27. Wang R, Liu YY, Liu XY, Jia SW, Zhao J, Cui D and Wang L: Resveratrol protects neurons and the myocardium by reducing oxidative stress and ameliorating mitochondria damage in a cerebral ischemia rat model. Cell Physiol Biochem 34: 854-864, 2014.
28. Vilar S, Quezada E, Santana L, Uriarte E, Yánez M, Fraiz N, Alcaide C, Cano E and Orallo F: Design, synthesis, and vasorelaxant and platelet antiaggregatory activities of coumarin-resveratrol hybrids. Bioorg Med Chem Lett 16: 257-261, 2006.
29. Liu PL, Chong IW, Lee YC, Tsai JR, Wang HM, Hsieh CC, Kuo HF, Liu WL, Chen YH and Chen HL: Anti-inflammatory effects of resveratrol on Hypoxia/Reoxygenation-induced alveolar epithelial cell dysfunction. J Agric Food Chem 63: 9480-9487, 2015.
30. Ghaly HA, Boyle PM, Vigmond EJ, Shimoni Y and Nygren A: Simulations of reduced conduction reserve in the diabetic rat heart: Response to uncoupling and reduced excitability. Ann Biomed Eng 38: 1415-1425, 2010.
31. Okruhlicova L, Tribulova N, Misejkova M, Kucka M, Stetka R, Slezak J and Manoach M: Gap junction remodelling is involved in the susceptibility of diabetic rats to hypokalemia-induced ventricular fibrillation. Acta Histochem 104: 387-391, 2002.
32. Santos-Almeida FM, Girão H, da Silva CA, Salgado HC and Fazan R Jr: Cholinergic stimulation with pyridostigmine protects myocardial infarcted rats against ischemic-induced arrhythmias and preserves connexin43 protein. Am J Physiol Heart Circ Physiol 308: H101-H107, 2015.
33. Greener ID, Sasano T, Wan X, Igarashi T, Strom M, Rosenbaum DS and Donahue JK: Connexin43 gene transfer reduces ventricular tachycardia susceptibility after myocardial infarction. J Am Coll Cardiol 60: 1103-1110, 2012.
34. Fernandes R, Girão H and Pereira P: High glucose down-regulates intercellular communication in retinal endothelial cells by enhancing degradation of connexin 43 by a proteasome-dependent mechanism. J Biol Chem 279: 27219-27224, 2004.
35. Yu L, Zhao Y, Fan Y, Wang M, Xu S and Fu G: Epigallocatechin-3 gallate, a green tea catechin, attenuated the downregulation of the cardiac gap junction induced by high glucose in neonatal rat cardiomyocytes. Cell physiol Biochem 26: 403-412, 2010.
36. Kanno S, Kovacs A, Yamada KA and Saffitz JE: Connexin43 as a determinant of myocardial infarct size following coronary occlusion in mice. J Am Coll Cardiol 41: 681-686, 2003.
37. Colosetti P, Puissant A, Robert G, Luciano F, Jacquel A, Gounon P, Cassuto JP and Auberger P: Autophagy is an important event for megakaryocytic differentiation of the chronic myelogenous leukemia K562 cell line. Autophagy 5: 1092-1098, 2009.
38. Zheng Q, Su H, Ranek MJ and Wang X: Autophagy and p62 in cardiac proteinopathy. Circ Res 109: 296-308, 2011.