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Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 8024857, 18 pages
https://doi.org/10.1155/2017/8024857
Research Article

Exercise Combined with Rhodiola sacra Supplementation Improves Exercise Capacity and Ameliorates Exhaustive Exercise-Induced Muscle Damage through Enhancement of Mitochondrial Quality Control

Cardiac Rehabilitation Center, Department of Rehabilitation, Xiangya Hospital of Central South University, Changsha 410008, China

Correspondence should be addressed to Suixin Liu; moc.621@nixiustraeh

Received 22 June 2017; Accepted 1 October 2017; Published 22 November 2017

Academic Editor: Aditya Sen

Copyright © 2017 Yaoshan Dun 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. R. Lozano, M. Naghavi, K. Foreman et al., “Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010,” The Lancet, vol. 380, no. 9859, pp. 2095–2128, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Korpelainen, J. Lämsä, K. M. Kaikkonen et al., “Exercise capacity and mortality – a follow-up study of 3033 subjects referred to clinical exercise testing,” Annals of Medicine, vol. 48, no. 5, pp. 359–366, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. D. L. Swift, C. J. Lavie, N. M. Johannsen et al., “Physical activity, cardiorespiratory fitness, and exercise training in primary and secondary coronary prevention,” Circulation Journal, vol. 77, no. 2, pp. 281–292, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Myers, P. McAuley, C. J. Lavie, J. P. Despres, R. Arena, and P. Kokkinos, “Physical activity and cardiorespiratory fitness as major markers of cardiovascular risk: their independent and interwoven importance to health status,” Progress in Cardiovascular Diseases, vol. 57, no. 4, pp. 306–314, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Ross, S. N. Blair, R. Arena et al., “Importance of assessing cardiorespiratory fitness in clinical practice: a case for fitness as a clinical vital sign: a scientific statement from the American Heart Association,” Circulation, vol. 134, no. 24, pp. e653–e699, 2016. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Du, D. Zhang, Y. Yin et al., “The personality and psychological stress predict major adverse cardiovascular events in patients with coronary heart disease after percutaneous coronary intervention for five years,” Medicine, vol. 95, no. 15, article e3364, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Dominguez-Rodriguez, S. Rodríguez, P. Abreu-Gonzalez, P. Avanzas, and R. A. Juarez-Prera, “Black carbon exposure, oxidative stress markers and major adverse cardiovascular events in patients with acute coronary syndromes,” International Journal of Cardiology, vol. 188, pp. 47–49, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Vassalle, S. Bianchi, D. Battaglia, P. Landi, F. Bianchi, and C. Carpeggiani, “Elevated levels of oxidative stress as a prognostic predictor of major adverse cardiovascular events in patients with coronary artery disease,” Journal of Atherosclerosis and Thrombosis, vol. 19, no. 8, pp. 712–717, 2012. View at Publisher · View at Google Scholar
  9. P. D. Addison, P. C. Neligan, H. Ashrafpour et al., “Noninvasive remote ischemic preconditioning for global protection of skeletal muscle against infarction,” American Journal of Physiology - Heart and Circulatory Physiology, vol. 285, no. 4, pp. H1435–H1443, 2003. View at Publisher · View at Google Scholar
  10. M. R. Schmidt, M. Smerup, I. E. Konstantinov et al., “Intermittent peripheral tissue ischemia during coronary ischemia reduces myocardial infarction through a KATP-dependent mechanism: first demonstration of remote ischemic perconditioning,” American Journal of Physiology - Heart and Circulatory Physiology, vol. 292, no. 4, pp. H1883–H1890, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Malhotra, B. P. Dhakal, A. S. Eisman et al., “Pulmonary vascular distensibility predicts pulmonary hypertension severity, exercise capacity, and survival in heart failure,” Circulation: Heart Failure, vol. 9, no. 6, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. J. I. Blomster, S. Svedlund, H. U. Westergren, and L. M. Gan, “Coronary flow reserve as a link between exercise capacity, cardiac systolic and diastolic function,” International Journal of Cardiology, vol. 217, pp. 161–166, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Van Remoortel, E. De Buck, V. Compernolle, L. Deldicque, and P. Vandekerckhove, “The effect of a standard whole blood donation on oxygen uptake and exercise capacity: a systematic review and meta-analysis,” Transfusion, vol. 57, no. 2, pp. 451–462, 2017. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. T. Wu, S. B. Wu, and Y. H. Wei, “Roles of sirtuins in the regulation of antioxidant defense and bioenergetic function of mitochondria under oxidative stress,” Free Radical Research, vol. 48, no. 9, pp. 1070–1084, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. T. Figge, H. D. Osiewacz, and A. S. Reichert, “Quality control of mitochondria during aging: is there a good and a bad side of mitochondrial dynamics?” BioEssays, vol. 35, no. 4, pp. 314–322, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. D. H. Cho, T. Nakamura, J. Fang et al., “S-nitrosylation of Drp1 mediates β-amyloid-related mitochondrial fission and neuronal injury,” Science, vol. 324, no. 5923, pp. 102–105, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. Y. Zhu, S. Massen, M. Terenzio et al., “Modulation of serines 17 and 24 in the LC3-interacting region of Bnip3 determines pro-survival mitophagy versus apoptosis,” Journal of Biological Chemistry, vol. 288, no. 2, pp. 1099–1113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Pankiv, T. H. Clausen, T. Lamark et al., “p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy,” Journal of Biological Chemistry, vol. 282, no. 33, pp. 24131–24145, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Jäger, C. Handschin, J. St-Pierre, and B. M. Spiegelman, “AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 29, pp. 12017–12022, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. H. N. Carter, C. C. Chen, and D. A. Hood, “Mitochondria, muscle health, and exercise with advancing age,” Physiology, vol. 30, no. 3, pp. 208–223, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Koltai, N. Hart, A. W. Taylor et al., “Age-associated declines in mitochondrial biogenesis and protein quality control factors are minimized by exercise training,” American Journal of Physiology - Regulatory, Integrative and Comparative Physiology, vol. 303, no. 2, pp. R127–R134, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. E. Ferraro, A. M. Giammarioli, S. Chiandotto, I. Spoletini, and G. Rosano, “Exercise-induced skeletal muscle remodeling and metabolic adaptation: redox signaling and role of autophagy,” Antioxidants & Redox Signaling, vol. 21, no. 1, pp. 154–176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. C. W. Taylor, S. A. Ingham, J. E. Hunt, N. R. Martin, J. S. Pringle, and R. A. Ferguson, “Exercise duration-matched interval and continuous sprint cycling induce similar increases in AMPK phosphorylation, PGC-1α and VEGF mRNA expression in trained individuals,” European Journal of Applied Physiology, vol. 116, no. 8, pp. 1445–1454, 2016. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Li, L. Xiao, Y. Hou et al., “Sestrin2 silencing exacerbates cerebral ischemia/reperfusion injury by decreasing mitochondrial biogenesis through the AMPK/PGC-1α pathway in rats,” Scientific Reports, vol. 6, article 30272, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Marongiu and A. Crisafulli, “Cardioprotection acquired through exercise: the role of ischemic preconditioning,” Current Cardiology Reviews, vol. 10, no. 4, pp. 336–348, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. A. J. Smuder, A. N. Kavazis, K. Min, and S. K. Powers, “Exercise protects against doxorubicin-induced oxidative stress and proteolysis in skeletal muscle,” Journal of Applied Physiology, vol. 110, no. 4, pp. 935–942, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. G. S. Kelly, “Rhodiola rosea: a possible plant adaptogen,” Alternative Medicine Review, vol. 6, no. 3, pp. 293–302, 2001. View at Google Scholar
  28. A. Parisi, E. Tranchita, G. Duranti et al., “Effects of chronic Rhodiola rosea supplementation on sport performance and antioxidant capacity in trained male: preliminary results,” Journal of Sports Medicine and Physical Fitness, vol. 50, no. 1, pp. 57–63, 2010. View at Google Scholar
  29. M. Jafari, J. S. Felgner, I. I. Bussel et al., “Rhodiola: a promising anti-aging Chinese herb,” Rejuvenation Research, vol. 10, no. 4, pp. 587–602, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Chen, J. Song, M. Chen et al., “Rhodiola rosea extends lifespan and improves stress tolerance in silkworm, Bombyx mori,” Biogerontology, vol. 17, no. 2, pp. 373–381, 2016. View at Publisher · View at Google Scholar · View at Scopus
  31. S. C. Huang, F. T. Lee, T. Y. Kuo, J. H. Yang, and C. T. Chien, “Attenuation of long-term Rhodiola rosea supplementation on exhaustive swimming-evoked oxidative stress in the rat,” The Chinese Journal of Physiology, vol. 52, no. 5, pp. 316–324, 2009. View at Google Scholar
  32. Z. Liu, X. Li, A. R. Simoneau, M. Jafari, and X. Zi, “Rhodiola rosea extracts and salidroside decrease the growth of bladder cancer cell lines via inhibition of the mTOR pathway and induction of autophagy,” Molecular Carcinogenesis, vol. 51, no. 3, pp. 257–267, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Xing, X. Yang, W. Li et al., “Salidroside stimulates mitochondrial biogenesis and protects against H2O2-induced endothelial dysfunction,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 904834, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Matsumoto, K. Ishihara, K. Tanaka, K. Inoue, and T. Fushiki, “An adjustable-current swimming pool for the evaluation of endurance capacity of mice,” Journal of Applied Physiology, vol. 81, no. 4, pp. 1843–1849, 1996. View at Google Scholar
  35. T. S. Yeh, H. L. Chuang, W. C. Huang, Y. M. Chen, C. C. Huang, and M. C. Hsu, “Astragalus membranaceus improves exercise performance and ameliorates exercise-induced fatigue in trained mice,” Molecules, vol. 19, no. 3, pp. 2793–2807, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. T. L. Cheng, C. C. Liao, W. H. Tsai et al., “Identification and characterization of the mitochondrial targeting sequence and mechanism in human citrate synthase,” Journal of Cellular Biochemistry, vol. 107, no. 5, pp. 1002–1015, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. S. J. Moat, T. Korpimäki, P. Furu et al., “Characterization of a blood spot creatine kinase skeletal muscle isoform immunoassay for high-throughput newborn screening of Duchenne muscular dystrophy,” Clinical Chemistry, vol. 63, no. 4, pp. 908–914, 2017. View at Publisher · View at Google Scholar
  38. T. Zhang, L. Xue, L. Li et al., “BNIP3 protein suppresses PINK1 kinase proteolytic cleavage to promote mitophagy,” Journal of Biological Chemistry, vol. 291, no. 41, pp. 21616–21629, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. N. A. Sobol, K. Hoffmann, K. S. Frederiksen et al., “Effect of aerobic exercise on physical performance in patients with Alzheimer’s disease,” Alzheimer’s & Dementia, vol. 12, no. 12, pp. 1207–1215, 2016. View at Publisher · View at Google Scholar · View at Scopus
  40. E. E. Noreen, J. G. Buckley, S. L. Lewis, J. Brandauer, and K. J. Stuempfle, “The effects of an acute dose of Rhodiola rosea on endurance exercise performance,” Journal of Strength and Conditioning Research, vol. 27, no. 3, pp. 839–847, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. A. P. Russell, V. C. Foletta, R. J. Snow, and G. D. Wadley, “Skeletal muscle mitochondria: a major player in exercise, health and disease,” Biochimica et Biophysica Acta (BBA) - General Subjects, vol. 1840, no. 4, pp. 1276–1284, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Vainshtein, L. D. Tryon, M. Pauly, and D. A. Hood, “Role of PGC-1α during acute exercise-induced autophagy and mitophagy in skeletal muscle,” American Journal of Physiology - Cell Physiology, vol. 308, no. 9, pp. C710–C719, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. V. D. Petkov, D. Yonkov, A. Mosharoff et al., “Effects of alcohol aqueous extract from Rhodiola rosea L. roots on learning and memory,” Acta Physiologica et Pharmacologica Bulgarica, vol. 12, no. 1, pp. 3–16, 1986. View at Google Scholar
  44. X. T. Zheng, Z. H. Wu, Y. Wei et al., “Induction of autophagy by salidroside through the AMPK-mTOR pathway protects vascular endothelial cells from oxidative stress-induced apoptosis,” Molecular and Cellular Biochemistry, vol. 425, no. 1-2, pp. 125–138, 2017. View at Publisher · View at Google Scholar · View at Scopus
  45. Z. Ping, L. F. Zhang, Y. J. Cui et al., “The protective effects of salidroside from exhaustive exercise-induced heart injury by enhancing the PGC-1α–NRF1/NRF2 pathway and mitochondrial respiratory function in rats,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 876825, 9 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  46. K. T. Lin, S. W. Hsu, F. Y. Lai, T. C. Chang, L. S. Shi, and S. Y. Lee, “Rhodiola crenulata extract regulates hepatic glycogen and lipid metabolism via activation of the AMPK pathway,” BMC Complementary and Alternative Medicine, vol. 16, no. 1, p. 127, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Li, W. Miao, J. Ma et al., “Acute exercise-induced mitochondrial stress triggers an inflammatory response in the myocardium via NLRP3 inflammasome activation with mitophagy,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 1987149, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  48. L. M. Popovic, N. R. Mitic, I. Radic et al., “The effect of exhaustive exercise on oxidative stress generation and antioxidant defense in guinea pigs,” Advances in Clinical and Experimental Medicine, vol. 21, no. 3, pp. 313–320, 2012. View at Google Scholar
  49. M. A. Kluge, J. L. Fetterman, and J. A. Vita, “Mitochondria and endothelial function,” Circulation Research, vol. 112, no. 8, pp. 1171–1188, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. K. Palikaras, E. Lionaki, and N. Tavernarakis, “Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans,” Nature, vol. 521, no. 7553, pp. 525–528, 2015. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Ascensão, J. Lumini-Oliveira, P. J. Oliveira, and J. Magalhães, “Mitochondria as a target for exercise-induced cardioprotection,” Current Drug Targets, vol. 12, no. 6, pp. 860–871, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Hernández-Santana, V. Pérez-López, J. M. Zubeldia, and M. Jiménez-del-Rio, “A Rhodiola rosea root extract protects skeletal muscle cells against chemically induced oxidative stress by modulating heat shock protein 70 (HSP70) expression,” Phytotherapy Research, vol. 28, no. 4, pp. 623–628, 2014. View at Publisher · View at Google Scholar · View at Scopus
  53. V. Gupta, S. S. Lahiri, S. Sultana, R. K. Tulsawani, and R. Kumar, “Anti-oxidative effect of Rhodiola imbricata root extract in rats during cold, hypoxia and restraint (C–H–R) exposure and post-stress recovery,” Food and Chemical Toxicology, vol. 48, no. 4, pp. 1019–1025, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Abidov, F. Crendal, S. Grachev, R. Seifulla, and T. Ziegenfuss, “Effect of extracts from Rhodiola rosea and Rhodiola crenulata (Crassulaceae) roots on ATP content in mitochondria of skeletal muscles,” Bulletin of Experimental Biology and Medicine, vol. 136, no. 6, pp. 585–587, 2003. View at Publisher · View at Google Scholar · View at Scopus