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Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 2370617, 13 pages
https://doi.org/10.1155/2018/2370617
Research Article

Ginkgo biloba Leaf Extract Protects against Myocardial Injury via Attenuation of Endoplasmic Reticulum Stress in Streptozotocin-Induced Diabetic ApoE−/− Mice

1Department of Cardiology, Beijing Anzhen Hospital, Capital Medical University, Beijing 100029, China
2Beijing Institute of Heart, Lung and Blood Vessel Diseases, Beijing 100029, China
3Cardiovascular Disease Center, Xiyuan Hospital, China Academy of Chinese Medical Sciences, Beijing 100091, China
4Graduate School, Beijing University of Chinese Medicine, Beijing 100029, China

Correspondence should be addressed to Yue Liu; moc.liamtoh@traeheuyuil and Shuzheng Lyu; nc.moc.liamdem@gnehzuhs

Received 23 September 2017; Revised 26 November 2017; Accepted 26 December 2017; Published 25 February 2018

Academic Editor: Paola Rizzo

Copyright © 2018 Jinfan Tian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Huynh, B. C. Bernardo, J. R. McMullen, and R. H. Ritchie, “Diabetic cardiomyopathy: mechanisms and new treatment strategies targeting antioxidant signaling pathways,” Pharmacology & Therapeutics, vol. 142, no. 3, pp. 375–415, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. X. Palomer, L. Salvadó, E. Barroso, and M. Vázquez-Carrera, “An overview of the crosstalk between inflammatory processes and metabolic dysregulation during diabetic cardiomyopathy,” International Journal of Cardiology, vol. 168, no. 4, pp. 3160–3172, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Falcão-Pires and A. F. Leite-Moreira, “Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment,” Heart Failure Reviews, vol. 17, no. 3, pp. 325–344, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. Z. Li, T. Zhang, H. Dai et al., “Endoplasmic reticulum stress is involved in myocardial apoptosis of streptozocin-induced diabetic rats,” The Journal of Endocrinology, vol. 196, no. 3, pp. 565–572, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Papa, F. Zazzeroni, C. G. Pham, C. Bubici, and G. Franzoso, “Linking JNK signaling to NF-κB: a key to survival,” Journal of Cell Science, vol. 117, no. 22, pp. 5197–5208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Su, L. Zhou, X. Kong et al., “Endoplasmic reticulum is at the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in the pathogenesis of diabetes mellitus,” Journal of Diabetes Research, vol. 2013, Article ID 193461, 6 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. H. L. Wen, Z. S. Liang, R. Zhang, and K. Yang, “Anti-inflammatory effects of triptolide improve left ventricular function in a rat model of diabetic cardiomyopathy,” Cardiovascular Diabetology, vol. 12, no. 1, p. 50, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Tosaki, T. Pali, and M. T. Droy-Lefaix, “Effects of Ginkgo biloba extract and preconditioning on the diabetic rat myocardium,” Diabetologia, vol. 39, no. 11, pp. 1255–1262, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Cheng, B. Liang, and Y. Li, “Antihyperglycemic effect of Ginkgo biloba extract in streptozotocin-induced diabetes in rats,” BioMed Research International, vol. 2013, Article ID 162724, 7 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. K. J. Rhee, C. G. Lee, S. W. Kim, D. H. Gim, H. C. Kim, and B. D. Jung, “Extract of Ginkgo biloba ameliorates streptozotocin-induced type 1 diabetes mellitus and high-fat diet-induced type 2 diabetes mellitus in mice,” International Journal of Medical Sciences, vol. 12, no. 12, pp. 987–994, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. R. M. Banin, B. K. S. Hirata, I. S. Andrade et al., “Beneficial effects of Ginkgo biloba extract on insulin signaling cascade, dyslipidemia, and body adiposity of diet-induced obese rats,” Brazilian Journal of Medical and Biological Research, vol. 47, no. 9, pp. 780–788, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. Q. Lu, X. X. Yin, J. Y. Wang, Y. Y. Gao, and Y. M. Pan, “Effects of Ginkgo biloba on prevention of development of experimental diabetic nephropathy in rats,” Acta Pharmacologica Sinica, vol. 28, no. 6, pp. 818–828, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Geoffrion, X. Du, Z. Irshad et al., “Differential effects of glyoxalase 1 overexpression on diabetic atherosclerosis and renal dysfunction in streptozotocin‐treated, apolipoprotein E‐deficient mice,” Physiological Reports, vol. 2, no. 6, article e12043, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Pan, Y. Wang, Y. Zhao et al., “Inhibition of JNK phosphorylation by a novel curcumin analog prevents high glucose–induced inflammation and apoptosis in cardiomyocytes and the development of diabetic cardiomyopathy,” Diabetes, vol. 63, no. 10, pp. 3497–3511, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. X.-m. Ren, G.-f. Zuo, W. Wu et al., “Atorvastatin alleviates experimental diabetic cardiomyopathy by regulating the GSK-3β-PP2Ac-NF-κB signaling Axis,” PLoS One, vol. 11, no. 11, article e0166740, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Quidgley, N. Cruz, and M. J. Crespo, “Atorvastatin improves systolic function, but does not prevent the development of dilated cardiomyopathy in streptozotocin-induced diabetic rats,” Therapeutic Advances in Cardiovascular Disease, vol. 8, no. 4, pp. 133–144, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Y. Qiao, J. H. Huang, J. W. Ma et al., “Ginkgo biloba extract reducing myocardium cells apoptosis by regulating apoptotic related proteins expression in myocardium tissues,” Molecular Biology Reports, vol. 41, no. 1, pp. 347–353, 2014. View at Publisher · View at Google Scholar · View at Scopus
  18. Y. Liu, Y. F. Liu, J. F. Tian, C. G. Fu, and K. J. Cheng, “The effect and mechanism of extract of Ginkgo biloba (EGb) on cardiovascular protection on the rat model of type 2 diabetes after myocardial infarction,” Chinese Journal of Integrated Traditional and Western Medicine, vol. 37, no. 9, pp. 1100–1104, 2017. View at Google Scholar
  19. A. A. M. Abdel-Hamid and A. E.-D. L. Firgany, “Atorvastatin alleviates experimental diabetic cardiomyopathy by suppressing apoptosis and oxidative stress,” Journal of Molecular Histology, vol. 46, no. 4-5, pp. 337–345, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Packard and A. G. Olsson, “Management of hypercholesterolaemia in the patient with diabetes,” International Journal of Clinical Practice Supplement, vol. 130, pp. 27–32, 2002. View at Google Scholar
  21. K. K. Wu and Y. Huan, “Diabetic atherosclerosis mouse models,” Atherosclerosis, vol. 191, no. 2, pp. 241–249, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Huang, Z. Shi, L. Chen, Y. Zhang, J. Li, and Y. An, “Rutin alleviates diabetic cardiomyopathy and improves cardiac function in diabetic ApoEknockout mice,” European Journal of Pharmacology, vol. 814, pp. 151–160, 2017. View at Publisher · View at Google Scholar · View at Scopus
  23. W. Li, Q. Fang, P. Zhong et al., “EGFR inhibition blocks palmitic acid-induced inflammation in cardiomyocytes and prevents hyperlipidemia-induced cardiac injury in mice,” Scientific Reports, vol. 6, no. 1, article 24580, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Van Linthout, A. Riad, N. Dhayat et al., “Anti-inflammatory effects of atorvastatin improve left ventricular function in experimental diabetic cardiomyopathy,” Diabetologia, vol. 50, no. 9, pp. 1977–1986, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Yoneda, K. Imaizumi, K. Oono et al., “Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress,” The Journal of Biological Chemistry, vol. 276, no. 17, pp. 13935–13940, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Morishima, K. Nakanishi, H. Takenouchi, T. Shibata, and Y. Yasuhiko, “An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12,” The Journal of Biological Chemistry, vol. 277, no. 37, pp. 34287–34294, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. J. Xu, Q. Zhou, W. Xu, and L. Cai, “Endoplasmic reticulum stress and diabetic cardiomyopathy,” Experimental Diabetes Research, vol. 2012, Article ID 827971, 12 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. G. Fitzl, R. Martin, D. Dettmer, V. Hermsdorf, H. Drews, and K. Welt, “Protective effects of Gingko biloba extract EGb 761 on myocardium of experimentally diabetic rats: I: ultrastructural and biochemical investigation on cardiomyocytes,” Experimental and Toxicologic Pathology, vol. 51, no. 3, pp. 189–198, 1999. View at Publisher · View at Google Scholar
  29. H. Yamazaki, N. Hiramatsu, K. Hayakawa et al., “Activation of the Akt-NF-κB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response,” The Journal of Immunology, vol. 183, no. 2, pp. 1480–1487, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. J. J. Kim, S. B. Lee, J. K. Park, and Y. D. Yoo, “TNF-α-induced ROS production triggering apoptosis is directly linked to Romo1 and Bcl-XL,” Cell Death & Differentiation, vol. 17, no. 9, pp. 1420–1434, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Z. Hasnain, R. Lourie, I. Das, A. C.-H. Chen, and M. A. McGuckin, “The interplay between endoplasmic reticulum stress and inflammation,” Immunology & Cell Biology, vol. 90, no. 3, pp. 260–270, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. A. S. Saini, R. Taliyan, and P. L. Sharma, “Protective effect and mechanism of Ginkgo biloba extract-EGb 761 on STZ-induced diabetic cardiomyopathy in rats,” Pharmacognosy Magazine, vol. 10, no. 38, pp. 172–178, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. C. C. Chen, A. N. Chiang, H. N. Liu, and Y. T. Chang, “EGb-761 prevents ultraviolet B-induced photoaging via inactivation of mitogen-activated protein kinases and proinflammatory cytokine expression,” Journal of Dermatological Science, vol. 75, no. 1, pp. 55–62, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. Q. Zhang, G.-J. Wang, J.-Y. A et al., “Application of GC/MS-based metabonomic profiling in studying the lipid-regulating effects of Ginkgo biloba extract on diet-induced hyperlipidemia in rats,” Acta Pharmacologica Sinica, vol. 30, no. 12, pp. 1674–1687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Yao, F. Song, K. Li et al., “Ginkgo biloba extract prevents ethanol induced dyslipidemia,” The American Journal of Chinese Medicine, vol. 35, no. 4, pp. 643–652, 2007. View at Publisher · View at Google Scholar · View at Scopus