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Evidence-Based Complementary and Alternative Medicine
Volume 2013, Article ID 924128, 14 pages
http://dx.doi.org/10.1155/2013/924128
Research Article

Ursolic-Acid-Enriched Herba Cynomorii Extract Protects against Oxidant Injury in H9c2 Cells and Rat Myocardium by Increasing Mitochondrial ATP Generation Capacity and Enhancing Cellular Glutathione Redox Cycling, Possibly through Mitochondrial Uncoupling

Division of Life Science, Hong Kong University of Science & Technology, Clear Water Bay, Hong Kong

Received 2 January 2013; Accepted 11 March 2013

Academic Editor: Tanawan Kummalue

Copyright © 2013 Jihang Chen and Kam Ming Ko. 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. S. Judge and C. Leeuwenburgh, “Cardiac mitochondrial bioenergetics, oxidative stress, and aging,” American Journal of Physiology, vol. 292, no. 6, pp. C1983–C1992, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. H. Cui, Y. Kong, and H. Zhang, “Oxidative stress, mitochondrial dysfunction, and aging,” Journal of Signal Transduction, vol. 2012, Article ID 646354, 13 pages, 2012. View at Publisher · View at Google Scholar
  3. W. C. Stanley, F. A. Recchia, and G. D. Lopaschuk, “Myocardial substrate metabolism in the normal and failing heart,” Physiological Reviews, vol. 85, no. 3, pp. 1093–1129, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Yao and R. D. Brinton, “Targeting mitochondrial bioenergetics for Alzheimer's prevention and treatment,” Current Pharmaceutical Design, vol. 17, no. 31, pp. 3474–3479, 2011. View at Publisher · View at Google Scholar
  5. A. Trifunovic and N. G. Larsson, “Mitochondrial dysfunction as a cause of ageing,” Journal of Internal Medicine, vol. 263, no. 2, pp. 167–178, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Kumaran, M. Subathra, M. Balu, and C. Panneerselvam, “Age-associated decreased activities of mitochondrial electron transport chain complexes in heart and skeletal muscle: role of L-carnitine,” Chemico-Biological Interactions, vol. 148, no. 1-2, pp. 11–18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. K. M. Ko, N. Chen, H. Y. Leung, E. P. K. Leong, M. K. T. Poon, and P. Y. Chiu, “Long-term schisandrin B treatment mitigates age-related impairments in mitochondrial antioxidant status and functional ability in various tissues, and improves the survival of aging C57BL/6J mice,” Biofactors, vol. 34, no. 4, pp. 331–342, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Terzioglu and N. G. Larsson, “Mitochondrial dysfunction in mammalian ageing,” Novartis Foundation Symposium, vol. 287, pp. 197–208, 2007. View at Google Scholar · View at Scopus
  9. Q. Meng, Y. T. Wong, J. Chen, and R. Ruan, “Age-related changes in mitochondrial function and antioxidative enzyme activity in fischer 344 rats,” Mechanisms of Ageing and Development, vol. 128, no. 3, pp. 286–292, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. E. J. Lesnefsky, S. Moghaddas, B. Tandler, J. Kerner, and C. L. Hoppel, “Mitochondrial dysfunction in cardiac disease: ischemia—reperfusion, aging, and heart failure,” Journal of Molecular and Cellular Cardiology, vol. 33, no. 6, pp. 1065–1089, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. C. C. Preston, A. S. Oberlin, E. L. Holmuhamedov et al., “Aging-induced alterations in gene transcripts and functional activity of mitochondrial oxidative phosphorylation complexes in the heart,” Mechanisms of Ageing and Development, vol. 129, no. 6, pp. 304–312, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. T. K. Yim, K. M. Ko, and R. Ko, “Antioxidant and immunomodulatory activities of Chinese tonifying herbs,” Pharmaceutical Biology, vol. 40, no. 5, pp. 329–335, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. K. M. Ko, T. Y. Y. Leon, D. H. F. Mak, P. Y. Chiu, Y. Du, and M. K. T. Poon, “A characteristic pharmacological action of “Yang-invigorating” Chinese tonifying herbs: enhancement of myocardial ATP-generation capacity,” Phytomedicine, vol. 13, no. 9-10, pp. 636–642, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Y. Leung, P. Y. Chiu, M. K. T. Poon, and K. M. Ko, “A Yang-invigorating Chinese herbal formula enhances mitochondrial functional ability and antioxidant capacity in various tissues of male and female rats,” Rejuvenation Research, vol. 8, no. 4, pp. 238–247, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. A. H. L. Siu and K. M. Ko, “Herba Cistanche extract enhances mitochondrial glutathione status and respiration in rat hearts, with possible induction of uncoupling proteins,” Pharmaceutical Biology, vol. 48, no. 5, pp. 512–517, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Y. Chiu, H. Y. Leung, A. H. L. Siu, N. Chen, M. K. T. Poon, and K. M. Ko, “Long-term treatment with a Yang-invigorating Chinese herbal formula produces generalized tissue protection against oxidative damage in rats,” Rejuvenation Research, vol. 11, no. 1, pp. 43–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. L. Chen, S. H. Tsai, S. P. Ip, K. M. Ko, and C. T. Che, “Long-term treatment with a Yang-invigorating Chinese herbal formula, Wu-Zi-Yan-Zong-Wan, reduces mortality and liver oxidative damage in chronic alcohol-intoxicated rats,” Rejuvenation Research, vol. 13, no. 4, pp. 459–467, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. H. S. Wong, H. Y. Leung, and K. M. Ko, “‘Yang-invigorating’ Chinese tonic herbs enhance mitochondrial ATP generation in H9c2 cardiomyocytes,” Chinese Medicine, vol. 2, pp. 1–5, 2011. View at Google Scholar
  19. H. Y. Leung and K. M. Ko, “Herba cistanche extract enhances mitochondrial ATP generation in rat hearts and H9c2 cells,” Pharmaceutical Biology, vol. 46, no. 6, pp. 418–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. O. W. Griffith, “Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine,” Analytical Biochemistry, vol. 106, no. 1, pp. 207–212, 1980. View at Google Scholar · View at Scopus
  21. P. C. Li, D. H. F. Mak, M. K. T. Poon, S. R. Ip, and K. M. Ko, “Myocardial protective effect of Sheng Mai San (SMS) and a lignan-enriched extract of Fructus Schisandrae, in vivo and ex vivo,” Phytomedicine, vol. 3, no. 2, pp. 217–221, 1996. View at Google Scholar · View at Scopus
  22. P. Y. Chiu, M. H. Tang, D. H. F. Mak, M. K. T. Poon, and K. M. Ko, “Hepatoprotective mechanism of schisandrin B: role of mitochondrial glutathione antioxidant status and heat shock proteins,” Free Radical Biology and Medicine, vol. 35, no. 4, pp. 368–380, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. S. W. Ballinger, “Mitochondrial dysfunction in cardiovascular disease,” Free Radical Biology and Medicine, vol. 38, no. 10, pp. 1278–1295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. M. G. Rosca, E. J. Vazquez, J. Kerner et al., “Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation,” Cardiovascular Research, vol. 80, no. 1, pp. 30–39, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. C. M. Ma, N. Nakamura, H. Miyashiro, M. Hattori, and K. Shimotohno, “Inhibitory effects of ursolic acid derivatives from Cynomorium songaricum, and related triterpenes on human immunodeficiency viral protease,” Phytotherapy Research, vol. 12, no. 1, pp. S138–S142, 1998. View at Google Scholar
  26. C. M. Ma, N. Sato, X. Y. Li, N. Nakamura, and M. Hattori, “Flavan-3-ol contents, anti-oxidative and α-glucosidase inhibitory activities of Cynomorium songaricum,” Food Chemistry, vol. 118, no. 1, pp. 116–119, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. Z. H. Jiang, T. Tanaka, M. Sakamoto, T. Jiang, and I. Kouno, “Studies on a medicinal parasitic plant: lignans from the stems of Cynomorium songaricum,” Chemical and Pharmaceutical Bulletin, vol. 49, no. 8, pp. 1036–1038, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Wang, J. Zhang, B. Zhao, Y. Wu, C. Wang, and Y. Wang, “Structural features and hypoglycaemic effects of Cynomorium songaricum polysaccharides on STZ-induced rats,” Food Chemistry, vol. 120, no. 2, pp. 443–451, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. Q. Chen, E. J. Vazquez, S. Moghaddas, C. L. Hoppel, and E. J. Lesnefsky, “Production of reactive oxygen species by mitochondria: central role of complex III,” Journal of Biological Chemistry, vol. 278, no. 38, pp. 36027–36031, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Gruber, S. Fong, C. B. Chen et al., “Mitochondria-targeted antioxidants and metabolic modulators as pharmacological interventions to slow ageing,” Biotechnology Advances, 2012. View at Publisher · View at Google Scholar
  31. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, and P. Walter, “Electron-transport chains and their proton pumps,” in Molecular Biology of the Cell, Garland Science, New York, NY, USA, 4th edition, 2002. View at Google Scholar
  32. J. Liobikas, D. Majiene, S. Trumbeckaite et al., “Uncoupling and antioxidant effects of ursolic acid in isolated rat heart mitochondria,” Journal of Natural Products, vol. 74, no. 7, pp. 1640–1644, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Terada, “Uncouplers of oxidative phosphorylation,” Environmental Health Perspectives, vol. 87, pp. 213–218, 1990. View at Google Scholar · View at Scopus
  34. P. W.-L. Ho, J. W.-M. Ho, H.-M. Tse et al., “Uncoupling protein-4 (UCP4) increases ATP supply by interacting with mitochondrial complex II in neuroblastoma cells,” Plos One, vol. 7, no. 2, Article ID e32810, 2012. View at Publisher · View at Google Scholar
  35. A. C. Y. Chu, P. W. L. Ho, K. H. H. Kwok et al., “Mitochondrial UCP4 attenuates MPP+- and dopamine-induced oxidative stress, mitochondrial depolarization, and ATP deficiency in neurons and is interlinked with UCP2 expression,” Free Radical Biology and Medicine, vol. 46, no. 6, pp. 810–820, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. H. S. Wong and K. M. Ko, “Herba Cistanches stimulates cellular glutathione redox cycling by reactive oxygen species generated from mitochondrial respiration in H9c2 cardiomyocytes,” Pharmaceutical Biology, vol. 51, no. 1, pp. 64–73, 2012. View at Publisher · View at Google Scholar
  37. E. D. Owuor and A. N. T. Kong, “Antioxidants and oxidants regulated signal transduction pathways,” Biochemical Pharmacology, vol. 64, no. 5-6, pp. 765–770, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. C. J. Harvey, R. K. Thimmulappa, A. Singh et al., “Nrf2-regulated glutathione recycling independent of biosynthesis is critical for cell survival during oxidative stress,” Free Radical Biology and Medicine, vol. 46, no. 4, pp. 443–453, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Robin, R. D. Guzy, G. Loor et al., “Oxidant stress during simulated ischemia primes cardiomyocytes for cell death during reperfusion,” Journal of Biological Chemistry, vol. 282, no. 26, pp. 19133–19143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. J. S. Kim, S. Ohshima, P. Pediaditakis, and J. J. Lemasters, “Nitric oxide protects rat hepatocytes against reperfusion injury mediated by the mitochondrial permeability transition,” Hepatology, vol. 39, no. 6, pp. 1533–1543, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Lu, Q. Wang, M. F. Melzig, and K. Jenett-Siems, “Extracts of Cynomorium songaricum protect SK-N-SH human neuroblastoma cells against staurosporine-induced apoptosis potentially through their radical scavenging activity,” Phytotherapy Research, vol. 23, no. 2, pp. 257–261, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Z. Ovesná, K. Kozics, and D. Slameňová, “Protective effects of ursolic acid and oleanolic acid in leukemic cells,” Mutation Research, vol. 600, no. 1-2, pp. 131–137, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Ambrosio, J. L. Zweier, and J. T. Flaherty, “The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion,” Journal of Molecular and Cellular Cardiology, vol. 23, no. 12, pp. 1359–1374, 1991. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Borrás, J. Sastre, D. García-Sala, A. Lloret, F. V. Pallardó, and J. Viña, “Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males,” Free Radical Biology and Medicine, vol. 34, no. 5, pp. 546–552, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Camper-Kirby, S. Welch, A. Walker et al., “Myocardial Akt activation and gender: increased nuclear activity in females versus males,” Circulation Research, vol. 88, no. 10, pp. 1020–1027, 2001. View at Google Scholar · View at Scopus
  46. A. A. Starkov, R. A. Simonyan, V. I. Dedukhova, S. E. Mansurova, L. A. Palamarchuk, and V. P. Skulachev, “Regulation of the energy coupling in mitochondria by some steroid and thyroid hormones,” Biochimica et Biophysica Acta, vol. 1318, no. 1-2, pp. 173–183, 1997. View at Publisher · View at Google Scholar · View at Scopus