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Early Aerobic Exercise Combined with Hydrogen-Rich Saline as Preconditioning Protects Myocardial Injury Induced by Acute Myocardial Infarction in Rats

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Abstract

It has been reported that hydrogen-rich saline (HRS) water reduces oxidative stress, and early aerobic exercise (eAE) acts an efficient exercise preconditioning (EP) against cardiac I/R injury. However, whether early aerobic exercise combined with hydrogen-rich saline (eAE-HRS) water can more effectively protect myocardial damage induced by acute myocardial infarction (MI) is still unknown. This study was aimed to evaluate the effect of eAE-HRS in preventing MI-induced myocardial damage and explore the possible underlying mechanisms. After Sprague-Dawley (SD) rats were given a intragastric administration of HRS (1.6 ppm) at a dosage of 10 mL/kg weight daily for 3 weeks and/or the SD rats were performed a eAE program with 3 weeks running training, the left anterior descending coronary artery was ligated to induce MI. We assessed the effects of eAE-HRS on myocardial injury and oxidative damage in the MI model of rats and detected the effects of eAE-HRS on the expressions of cardiac OGG1 and Tom40, Tom20, and Tim23. The eAE-HRS increased significantly left ventricular systolic pressure, reduced left ventricular end-diastolic pressure, and potentiated + dp/dtmax, −dp/dtmax, heart coefficient and pH after MI injury. The eAE-HRS reduced MI-induced CK-MB level, c-Tnl level, h-FABP level, infarct size. The eAE-HRS enhanced MI-induced levels of the superoxide dismutase and total antioxidant capacity, attenuated MI-induced levels of malondialdehyde and catalase. The eAE-HRS increased expressions of OGG1, Tom20 and Tim23 proteins after MI injury, but not Tom40. The eAE-HRS has the potential to be a novel precautionary measure to protect myocardial injury after MI via partially regulating expressions of antioxidant-related proteins and mitochondrial-associated proteins.

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Abbreviations

CAT:

catalase

CK-MB:

creatine kinase isoenzyme

cTn-I:

cardiac troponin I

eAE:

early aerobic exercise

eAE-HRS:

early aerobic exercise combined with hydrogen-rich saline

ECG:

electrocardiogram

ELISA:

enzyme-linked immunosorbent assay

GAPDH:

glyceraldehyde-3-phosphate dehydrogenase

GSH-PX:

glutathione peroxidase

H&E:

hematoxylin and eosin

h-FABP:

heart type fatty acid binding protein

HRP:

horseradish peroxidase

HRS:

hydrogen-rich saline

LVEDP:

left ventricular end-diastolic pressure

LVSP:

left ventricular systolic pressure

HC:

heart coefficient

MDA:

malondialdehyde

MI:

myocardial infarction

mtDNA:

mitochondrial DNA

OGG1:

8-oxoguanine DNA glycosylase

T-AOC:

total antioxidant capacity

Tim23:

translocase of inner mitochondrial membrane 23

Tom20:

translocase of outer membrane 20

Tom40:

translocase of the outer mitochondrial membrane 40

T-SOD:

superoxide dismutase

TTC:

2,3,5-triphenyl tetrazolium chloride

RNS:

reactive nitrogen species

ROS:

reactive oxygen species

8-OHdG:

8-hydroxydeoxyguanosine

References

  1. Adeneye, A. A., Awodele, O., Aiyeola, S. A., & Benebo, A. S. (2015). Modulatory potentials of the aqueous stem bark extract of Mangifera indica on carbon tetrachloride-induced hepatotoxicity in rats. Journal of Traditional and Complementary Medicine, 5(2), 106–115.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Alessio, H. M., Hagerman, A. E., Fulkerson, B. K., Ambrose, J., Rice, R. E., & Wiley, R. L. (2000). Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Medicine and Science in Sports and Exercise, 32(9), 1576–1581.

    Article  CAS  PubMed  Google Scholar 

  3. Antman, E. M., Tanasijevic, M. J., Thompson, B., Schactman, M., McCabe, C. H., Cannon, C. P., Fischer, G. A., Fung, A. Y., Thompson, C., Wybenga, D., & Braunwald, E. (1996). Cardiac-specific troponin I levels to predict the risk of mortality in patients with acute coronary syndromes. The New England Journal of Medicine, 335(18), 1342–1349.

    Article  CAS  PubMed  Google Scholar 

  4. Bassuk, S. S., & Manson, J. E. (2005). Epidemiological evidence for the role of physical activity in reducing risk of type 2 diabetes and cardiovascular disease. Journal of Applied Physiology (1985), 99(3), 1193–1204.

    Article  Google Scholar 

  5. Bloomer, R. J., Goldfarb, A. H., & McKenzie, M. J. (2006). Oxidative stress response to aerobic exercise: comparison of antioxidant supplements. Medicine and Science in Sports and Exercise, 38(6), 1098–1105.

    Article  CAS  PubMed  Google Scholar 

  6. Chen, F., Zhang, T., Xiong, J., Guo, W., Pan, X., Shen, C., Song, Y., Jia, S., & Liu, J. (2014). Suppression of abdominal aortic aneurysm by hydrogen through chemokine-like factor1. Zhonghua Yi Xue Za Zhi, 94(1), 59–61.

    CAS  PubMed  Google Scholar 

  7. Chen, H., Sun, Y. P., Hu, P. F., Liu, W. W., Xiang, H. G., Li, Y., Yan, R. L., Su, N., Ruan, C. P., Sun, X. J., & Wang, Q. (2011). The effects of hydrogen-rich saline on the contractile and structural changes of intestine induced by ischemia-reperfusion in rats. Journal of Surgical Research, 167(2), 316–322.

    Article  CAS  PubMed  Google Scholar 

  8. Eijsvogels, T. M., Molossi, S., Lee, D. C., Emery, M. S., & Thompson, P. D. (2016). Exercise at the extremes: the amount of exercise to reduce cardiovascular events. Journal of the American College of Cardiology, 67(3), 316–329.

    Article  PubMed  Google Scholar 

  9. Ferrari, R., Ceconi, C., Curello, S., Cargnoni, A., Alfieri, O., Pardini, A., Marzollo, P., & Visioli, O. (1991). Oxygen free radicals and myocardial damage: protective role of thiol-containing agents. American Journal of Medicine, 91(3C), 95S–105S.

    Article  CAS  PubMed  Google Scholar 

  10. Gaschler, M. M., & Stockwell, B. R. (2017). Lipid peroxidation in cell death. Biochemical and Biophysical Research Communications, 482(3), 419–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ide, T., Tsutsui, H., Hayashidani, S., Kang, D., Suematsu, N., Nakamura, K., Utsumi, H., Hamasaki, N., & Takeshita, A. (2001). Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circulation Research, 88(5), 529–535.

    Article  CAS  PubMed  Google Scholar 

  12. Imai, H., Matsuoka, M., Kumagai, T., Sakamoto, T., & Koumura, T. (2017). Lipid peroxidation-dependent cell death regulated by GPx4 and Ferroptosis. Current Topics in Microbiology and Immunology, 403, 143–170.

    CAS  PubMed  Google Scholar 

  13. Jiang, D., Wu, D., Zhang, Y., Xu, B., Sun, X., & Li, Z. (2012). Protective effects of hydrogen rich saline solution on experimental testicular ischemia-reperfusion injury in rats. Journal of Urology, 187(6), 2249–2253.

    Article  CAS  PubMed  Google Scholar 

  14. Kannel, W. B., Wilson, P., & Blair, S. N. (1985). Epidemiological assessment of the role of physical activity and fitness in development of cardiovascular disease. American Heart Journal, 109(4), 876–885.

    Article  CAS  PubMed  Google Scholar 

  15. Khaket, T. P., & Ahmad, R. (2011). Biochemical studies on hemoglobin modified with reactive oxygen species (ROS). Applied Biochemistry and Biotechnology, 164(8), 1422–1430.

    Article  CAS  PubMed  Google Scholar 

  16. LeBlanc, P. J., Peters, S. J., Tunstall, R. J., Cameron-Smith, D., & Heigenhauser, G. J. (2004). Effects of aerobic training on pyruvate dehydrogenase and pyruvate dehydrogenase kinase in human skeletal muscle. Journal of Physiology, 557(Pt 2), 559–570.

    Article  CAS  PubMed  Google Scholar 

  17. Li, J., Wang, C., Zhang, J. H., Cai, J. M., Cao, Y. P., & Sun, X. J. (2010). Hydrogen-rich saline improves memory function in a rat model of amyloid-beta-induced Alzheimer's disease by reduction of oxidative stress. Brain Research, 1328, 152–161.

    Article  CAS  PubMed  Google Scholar 

  18. Mao, Y. F., Zheng, X. F., Cai, J. M., You, X. M., Deng, X. M., Zhang, J. H., Jiang, L., & Sun, X. J. (2009). Hydrogen-rich saline reduces lung injury induced by intestinal ischemia/reperfusion in rats. Biochemical and Biophysical Research Communications, 381(4), 602–605.

    Article  CAS  PubMed  Google Scholar 

  19. Nagata, K., Nakashima-Kamimura, N., Mikami, T., Ohsawa, I., & Ohta, S. (2009). Consumption of molecular hydrogen prevents the stress-induced impairments in hippocampus-dependent learning tasks during chronic physical restraint in mice. Neuropsychopharmacology, 34(2), 501–508.

    Article  CAS  PubMed  Google Scholar 

  20. Ohsawa, I., Ishikawa, M., Takahashi, K., Watanabe, M., Nishimaki, K., Yamagata, K., Katsura, K., Katayama, Y., Asoh, S., & Ohta, S. (2007). Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nature Medicine, 13(6), 688–694.

    Article  CAS  PubMed  Google Scholar 

  21. Omland, T., Aakvaag, A., & Vik-Mo, H. (1996). Plasma cardiac natriuretic peptide determination as a screening test for the detection of patients with mild left ventricular impairment. Heart, 76(3), 232–237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pfanner, N., & Geissler, A. (2001). Versatility of the mitochondrial protein import machinery. Nature Reviews. Molecular Cell Biology, 2(5), 339–349.

    Article  CAS  PubMed  Google Scholar 

  23. Poulsen, S. H. (2001). Clinical aspects of left ventricular diastolic function assessed by Doppler echocardiography following acute myocardial infarction. Danish Medical Bulletin, 48(4), 199–210.

    CAS  PubMed  Google Scholar 

  24. Saravanan, R., & Shanmugam, A. (2010). Preventive effect of low molecular weight glycosaminoglycan from Amussium pleuronectus (Linne) on oxidative injury and cellular abnormalities in isoproterenol-induced cardiotoxicity in Wistar rats. Applied Biochemistry and Biotechnology, 162(1), 43–51.

    Article  CAS  PubMed  Google Scholar 

  25. Schleiff, E., Shore, G. C., & Goping, I. S. (1997). Human mitochondrial import receptor, Tom20p. Use of glutathione to reveal specific interactions between Tom20-glutathione S-transferase and mitochondrial precursor proteins. FEBS Letters, 404(2–3), 314–318.

    Article  CAS  PubMed  Google Scholar 

  26. Sheikh, I. N., & Roberts, W. C. (2017). Relation of left ventricular free wall rupture and/or aneurysm with acute myocardial infarction in patients with aortic stenosis. Proceedings (Baylor University Medical Center), 30(2), 161–162.

    Article  Google Scholar 

  27. Suhara, T., Baba, Y., Shimada, B. K., Higa, J. K., & Matsui, T. (2017). The mTOR signaling pathway in myocardial dysfunction in type 2 diabetes mellitus. Current Diabetes Reports, 17(6), 38.

    Article  CAS  PubMed  Google Scholar 

  28. Sun, Q., Kang, Z., Cai, J., Liu, W., Liu, Y., Zhang, J. H., Denoble, P. J., Tao, H., & Sun, X. (2009). Hydrogen-rich saline protects myocardium against ischemia/reperfusion injury in rats. Experimental Biology and Medicine (Maywood, N.J.), 234(10), 1212–1219.

    Article  CAS  Google Scholar 

  29. Tsutsui, H., Kinugawa, S., & Matsushima, S. (2009). Mitochondrial oxidative stress and dysfunction in myocardial remodelling. Cardiovascular Research, 81(3), 449–456.

    Article  CAS  PubMed  Google Scholar 

  30. van den Bos, E. J., Mees, B. M., de Waard, M. C., de Crom, R., & Duncker, D. J. (2005). A novel model of cryoinjury-induced myocardial infarction in the mouse: a comparison with coronary artery ligation. American Journal of Physiology. Heart and Circulatory Physiology, 289(3), H1291–H1300.

    Article  CAS  PubMed  Google Scholar 

  31. Wang, Y., Li, Y., Song, L., Li, Y., Jiang, S., & Zhang, S. (2016). The transplantation of Akt-overexpressing amniotic fluid-derived mesenchymal stem cells protects the heart against ischemia-reperfusion injury in rabbits. Molecular Medicine Reports, 14(1), 234–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Xi, Y., Gong, D. W., & Tian, Z. (2016). FSTL1 as a potential mediator of exercise-induced cardioprotection in post-myocardial infarction rats. Scientific Reports, 6, 32424.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yamashita, N., Hoshida, S., Otsu, K., Asahi, M., Kuzuya, T., & Hori, M. (1999). Exercise provides direct biphasic cardioprotection via manganese superoxide dismutase activation. The Journal of Experimental Medicine, 189(11), 1699–1706.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Yiadom, M. Y., Jarolim, P., Jenkins, C., Melanson, S. E., Conrad, M., & Kosowsky, J. M. (2015). Diagnostic implications of an elevated troponin in the emergency department. Disease Markers, 2015, 157812.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhan, K. Y., Yu, P. L., Liu, C. H., Luo, J. H., & Yang, W. (2016). Detrimental or beneficial: the role of TRPM2 in ischemia/reperfusion injury. Acta Pharmacologica Sinica, 37(1), 4–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zhang, K. R., Liu, H. T., Zhang, H. F., Zhang, Q. J., Li, Q. X., Yu, Q. J., Guo, W. Y., Wang, H. C., & Gao, F. (2007). Long-term aerobic exercise protects the heart against ischemia/reperfusion injury via PI3 kinase-dependent and Akt-mediated mechanism. Apoptosis, 12(9), 1579–1588.

    Article  CAS  PubMed  Google Scholar 

  37. Zheng, X., Mao, Y., Cai, J., Li, Y., Liu, W., Sun, P., Zhang, J. H., Sun, X., & Yuan, H. (2009). Hydrogen-rich saline protects against intestinal ischemia/reperfusion injury in rats. Free Radical Research, 43(5), 478–484.

    Article  CAS  PubMed  Google Scholar 

  38. Zhou, L., Wang, X., Xue, W., Xie, K., Huang, Y., Chen, H., Gong, G., & Zeng, Y. (2013). Beneficial effects of hydrogen-rich saline against spinal cord ischemia-reperfusion injury in rabbits. Brain Research, 1517, 150–160.

    Article  CAS  PubMed  Google Scholar 

  39. Zhou, X., Xu, M., Wang, L., Mu, Y., Feng, R., Dong, Z., Pan, Y., Chen, X., Liu, Y., Zheng, S., Anthony, D. D., Ma, J., Isaacs, W. B., & Xu, X. (2016). Liver-specific NG37 overexpression leads to diet-dependent fatty liver disease accompanied by cardiac dysfunction. Genes & Nutrition, 11, 14.

    Article  CAS  Google Scholar 

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Funding

This work was supported by the Outstanding Doctoral Thesis fund of Shaanxi Normal University (Grant No. X2014YB02).

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TZJ conceived of the study. FR and CMX performed the experiments and collected and analyzed all data. TZJ, FR, and WXD prepared the manuscript, and all the authors edited the manuscript. All the authors contributed to the writing of the manuscript.

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Correspondence to Zhenjun Tian.

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Feng, R., Cai, M., Wang, X. et al. Early Aerobic Exercise Combined with Hydrogen-Rich Saline as Preconditioning Protects Myocardial Injury Induced by Acute Myocardial Infarction in Rats. Appl Biochem Biotechnol 187, 663–676 (2019). https://doi.org/10.1007/s12010-018-2841-0

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