Protective effect of berberine against myocardial ischemia reperfusion injury: Role of Notch1/Hes1-PTEN/Akt signaling

Apoptosis

Volumn 20, Issue 6, 2015, Pages 796-810

  Yu, Liming ^a   Li, Feijiang ^b   Zhao, Guolong ^c   Yang, Yang ^a,b   Jin, Zhenxiao ^a   Zhai, Mengen ^a   Yu, Wenjun ^a   Zhao, Lin ^a   Chen, Wensheng ^a   Duan, Weixun ^a   Yu, Shiqiang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c NINGXIA MEDICAL UNIVERSITY   (China)

Author keywords

Akt; Anti apoptosis; Berberine; Myocardial ischemia reperfusion; Notch1

Indexed keywords

2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BERBERINE; CHROMONE DERIVATIVE; ENZYME INHIBITOR; HES1 PROTEIN, RAT; HOMEODOMAIN PROTEIN; MORPHOLINE DERIVATIVE; NOTCH1 PROTEIN, RAT; NOTCH1 RECEPTOR; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, RAT; SMALL INTERFERING RNA;

ANIMAL; APOPTOSIS; CELL SURVIVAL; DRUG EFFECTS; HEART MUSCLE; HEART MUSCLE CELL; MALE; METABOLISM; MYOCARDIAL REPERFUSION INJURY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BERBERINE; CELL SURVIVAL; CHROMONES; ENZYME INHIBITORS; HOMEODOMAIN PROTEINS; MALE; MORPHOLINES; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; ONCOGENE PROTEIN V-AKT; PTEN PHOSPHOHYDROLASE; RATS, SPRAGUE-DAWLEY; RECEPTOR, NOTCH1; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84937764222     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-015-1122-4     Document Type: Article

References (45)

1. Hausenloy DJ, Yellon DM (2013) Myocardial ischemia-reperfusion injury: a neglected therapeutic target. J Clin Investig 123(1):92-100. doi: 10.1172/jci62874
2. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. New Engl J Med 357(11):1121-1135. doi: 10.1056/NEJMra071667
3. Remppis A, Bea F, Greten HJ, Buttler A, Wang H, Zhou Q, Preusch MR, Enk R, Ehehalt R, Katus H, Blessing E (2010) Rhizoma Coptidis inhibits LPS-induced MCP-1/CCL2 production in murine macrophages via an AP-1 and NFkappaB-dependent pathway. Mediat Inflamm 2010:194896. doi: 10.1155/2010/194896
4. Liu F, Liang HL, Xu KH, Tong LL, Tang B (2007) Supramolecular interaction of ethylenediamine linked beta-cyclodextrin dimer and berberine hydrochloride by spectrofluorimetry and its analytical application. Talanta 74(1):140-145. doi: 10.1016/j.talanta.2007.05.048
5. Chen K, Li G, Geng F, Zhang Z, Li J, Yang M, Dong L, Gao F (2014) Berberine reduces ischemia/reperfusion-induced myocardial apoptosis via activating AMPK and PI3K-Akt signaling in diabetic rats. Apoptosis Int J Program Cell Death 19(6):946-957. doi: 10.1007/s10495-014-0977-0
6. Chang W, Zhang M, Li J, Meng Z, Xiao D, Wei S, Chen L, Wang C, Hatch GM (2012) Berberine attenuates ischemia-reperfusion injury via regulation of adenosine-5′-monophosphate kinase activity in both non-ischemic and ischemic areas of the rat heart. Cardiovas Drugs Therapy 26(6):467-478. doi: 10.1007/s10557-012-6422-0
7. Zeng XH, Zeng XJ, Li YY (2003) Efficacy and safety of berberine for congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy. Am J Cardiol 92(2):173-176
8. Piazzi G, Bazzoli F, Ricciardiello L (2012) Epigenetic silencing of Notch signaling in gastrointestinal cancers. Cell Cycle 11(23):4323-4327. doi: 10.4161/cc.22388
9. Marignol L, Rivera-Figueroa K, Lynch T, Hollywood D (2013) Hypoxia, notch signalling, and prostate cancer. Nat Rev Urol 10(7):405-413. doi: 10.1038/nrurol.2013.110
10. Nakagawa O, McFadden DG, Nakagawa M, Yanagisawa H, Hu T, Srivastava D, Olson EN (2000) Members of the HRT family of basic helix-loop-helix proteins act as transcriptional repressors downstream of Notch signaling. Proc Natl Acad Sci USA 97(25):13655-13660. doi: 10.1073/pnas.250485597
11. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R (1997) PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science (New York, NY) 275(5308):1943-1947
12. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DH, Tavtigian SV (1997) Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 15(4):356-362. doi: 10.1038/ng0497-356
13. Salmena L, Carracedo A, Pandolfi PP (2008) Tenets of PTEN tumor suppression. Cell 133(3):403-414. doi: 10.1016/j.cell.2008.04.013
14. Downward J (2004) PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 15(2):177-182
15. Pei H, Yu Q, Xue Q, Guo Y, Sun L, Hong Z, Han H, Gao E, Qu Y, Tao L (2013) Notch1 cardioprotection in myocardial ischemia/reperfusion involves reduction of oxidative/nitrative stress. Basic Res Cardiol 108(5):373. doi: 10.1007/s00395-013-0373-x
16. Park SH, Sung JH, Chung N (2014) Berberine diminishes side population and down-regulates stem cell-associated genes in the pancreatic cancer cell lines PANC-1 and MIA PaCa-2. Mol Cell Biochem 394(1-2):209-215. doi: 10.1007/s11010-014-2096-1
17. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, Hohnen-Behrens C, Gosby A, Kraegen EW, James DE, Kim JB (2006) Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55(8):2256-2264. doi: 10.2337/db06-0006
18. Kong W, Wei J, Abidi P, Lin M, Inaba S, Li C, Wang Y, Wang Z, Si S, Pan H, Wang S, Wu J, Wang Y, Li Z, Liu J, Jiang JD (2004) Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins. Nat Med 10(12):1344-1351. doi: 10.1038/nm1135
19. Wang C, Li J, Lv X, Zhang M, Song Y, Chen L, Liu Y (2009) Ameliorative effect of berberine on endothelial dysfunction in diabetic rats induced by high-fat diet and streptozotocin. Eur J Pharmacol 620(1-3):131-137. doi: 10.1016/j.ejphar.2009.07.027
20. Cui G, Qin X, Zhang Y, Gong Z, Ge B, Zang YQ (2009) Berberine differentially modulates the activities of ERK, p38 MAPK, and JNK to suppress Th17 and Th1 T cell differentiation in type 1 diabetic mice. J Biol Chem 284(41):28420-28429. doi: 10.1074/jbc.M109.012674
21. Yin J, Hu R, Chen M, Tang J, Li F, Yang Y, Chen J (2002) Effects of berberine on glucose metabolism in vitro. Metab Clin Exp 51(11):1439-1443
22. Yu L, Sun Y, Cheng L, Jin Z, Yang Y, Zhai M, Pei H, Wang X, Zhang H, Meng Q, Zhang Y, Yu S, Duan W (2014) Melatonin receptor-mediated protection against myocardial ischemia/reperfusion injury: role of SIRT1. J Pineal Res 57(2):228-238. doi: 10.1111/jpi.12161
23. Oshima Y, Ouchi N, Sato K, Izumiya Y, Pimentel DR, Walsh K (2008) Follistatin-like 1 is an Akt-regulated cardioprotective factor that is secreted by the heart. Circulation 117(24):3099-3108. doi: 10.1161/circulationaha.108.767673
24. Song CL, Liu B, Diao HY, Shi YF, Li YX, Zhang JC, Lu Y, Wang G, Liu J, Yu YP, Guo ZY, Wang JP, Zhao Z, Liu JG, Liu YH, Liu ZX, Cai D, Li Q (2014) The protective effect of microRNA-320 on left ventricular remodeling after myocardial ischemia-reperfusion injury in the rat model. Int J Mol Sci 15(10):17442-17456. doi: 10.3390/ijms151017442
25. Yang Y, Duan W, Jin Z, Yi W, Yan J, Zhang S, Wang N, Liang Z, Li Y, Chen W, Yi D, Yu S (2013) JAK2/STAT3 activation by melatonin attenuates the mitochondrial oxidative damage induced by myocardial ischemia/reperfusion injury. J Pineal Res 55(3):275-286. doi: 10.1111/jpi.12070
26. Duan W, Yang Y, Yi W, Yan J, Liang Z, Wang N, Li Y, Chen W, Yu S, Jin Z, Yi D (2013) New role of JAK2/STAT3 signaling in endothelial cell oxidative stress injury and protective effect of melatonin. PLoS One 8(3):e57941. doi: 10.1371/journal.pone.0057941
27. Yang Y, Duan W, Liang Z, Yi W, Yan J, Wang N, Li Y, Chen W, Yu S, Jin Z, Yi D (2013) Curcumin attenuates endothelial cell oxidative stress injury through Notch signaling inhibition. Cell Signal 25(3):615-629. doi: 10.1016/j.cellsig.2012.11.025
28. Song JQ, Teng X, Cai Y, Tang CS, Qi YF (2009) Activation of Akt/GSK-3beta signaling pathway is involved in intermedin(1-53) protection against myocardial apoptosis induced by ischemia/reperfusion. Apoptosis Int J Program Cell Death 14(9):1061-1069. doi: 10.1007/s10495-009-0382-2
29. Gao F, Tao L, Yan W, Gao E, Liu HR, Lopez BL, Christopher TA, Ma XL (2004) Early anti-apoptosis treatment reduces myocardial infarct size after a prolonged reperfusion. Apoptosis Int J Program Cell Death 9(5):553-559. doi: 10.1023/B:APPT.0000038035.75845.ab
30. Xing W, Yan W, Fu F, Jin Y, Ji L, Liu W, Wang L, Lv A, Duan Y, Zhang J, Zhang H, Gao F (2009) Insulin inhibits myocardial ischemia-induced apoptosis and alleviates chronic adverse changes in post-ischemic cardiac structure and function. Apoptosis Int J Program Cell Death 14(9):1050-1060. doi: 10.1007/s10495-009-0378-y
31. Zhang T, Yang S, Du J (2014) Protective Effects of Berberine on Isoproterenol-Induced Acute Myocardial Ischemia in Rats through Regulating HMGB1-TLR4 Axis. Evid-Based Complement Altern Med 2014:849783. doi: 10.1155/2014/849783
32. Kratsios P, Catela C, Salimova E, Huth M, Berno V, Rosenthal N, Mourkioti F (2010) Distinct roles for cell-autonomous Notch signaling in cardiomyocytes of the embryonic and adult heart. Circ Res 106(3):559-572. doi: 10.1161/circresaha.109.203034
33. Miele L (2006) Notch signaling. Clin Cancer Res 12(4):1074-1079. doi: 10.1158/1078-0432.ccr-05-2570
34. Niessen K, Karsan A (2007) Notch signaling in the developing cardiovascular system. Am J Physiol Cell Physiol 293(1):C1-C11. doi: 10.1152/ajpcell.00415.2006
35. High FA, Epstein JA (2008) The multifaceted role of Notch in cardiac development and disease. Nat Rev Genet 9(1):49-61. doi: 10.1038/nrg2279
36. Campa VM, Gutierrez-Lanza R, Cerignoli F, Diaz-Trelles R, Nelson B, Tsuji T, Barcova M, Jiang W, Mercola M (2008) Notch activates cell cycle reentry and progression in quiescent cardiomyocytes. J Cell Biol 183(1):129-141. doi: 10.1083/jcb.200806104
37. Collesi C, Zentilin L, Sinagra G, Giacca M (2008) Notch1 signaling stimulates proliferation of immature cardiomyocytes. J Cell Biol 183(1):117-128. doi: 10.1083/jcb.200806091
38. Gude NA, Emmanuel G, Wu W, Cottage CT, Fischer K, Quijada P, Muraski JA, Alvarez R, Rubio M, Schaefer E, Sussman MA (2008) Activation of Notch-mediated protective signaling in the myocardium. Circ Res 102(9):1025-1035. doi: 10.1161/circresaha.107.164749
39. Dror V, Nguyen V, Walia P, Kalynyak TB, Hill JA, Johnson JD (2007) Notch signalling suppresses apoptosis in adult human and mouse pancreatic islet cells. Diabetologia 50(12):2504-2515. doi: 10.1007/s00125-007-0835-5
40. Zhou XL, Wan L, Xu QR, Zhao Y, Liu JC (2013) Notch signaling activation contributes to cardioprotection provided by ischemic preconditioning and postconditioning. J Transl Med 11:251. doi: 10.1186/1479-5876-11-251
41. Luo HR, Hattori H, Hossain MA, Hester L, Huang Y, Lee-Kwon W, Donowitz M, Nagata E, Snyder SH (2003) Akt as a mediator of cell death. Proc Natl Acad Sci USA 100(20):11712-11717. doi: 10.1073/pnas.1634990100
42. Qian J, Ling S, Castillo AC, Long B, Birnbaum Y, Ye Y (2012) Regulation of phosphatase and tensin homolog on chromosome 10 in response to hypoxia. Am J Physiol Heart Circ Physiol 302(9):H1806-H1817. doi: 10.1152/ajpheart.00929.2011
43. Zhou XL, Wan L, Liu JC (2013) Activated Notch1 reduces myocardial ischemia reperfusion injury in vitro during ischemic postconditioning by crosstalk with the RISK signaling pathway. Chin Med J 126(23):4545-4551
44. Hsu YY, Chen CS, Wu SN, Jong YJ, Lo YC (2012) Berberine activates Nrf2 nuclear translocation and protects against oxidative damage via a phosphatidylinositol 3-kinase/Akt-dependent mechanism in NSC34 motor neuron-like cells. Eur J Pharmaceut Sci 46(5):415-425. doi: 10.1016/j.ejps.2012.03.004
45. Xiao M, Men LN, Xu MG, Wang GB, Lv HT, Liu C (2014) Berberine protects endothelial progenitor cell from damage of TNF-alpha via the PI3K/AKT/eNOS signaling pathway. Eur J Pharmacol 743:11-16. doi: 10.1016/j.ejphar.2014.09.024