DOI QR코드

DOI QR Code

Sevoflurane Postconditioning Reduces Hypoxia/Reoxygenation Injury in Cardiomyocytes via Upregulation of Heat Shock Protein 70

  • Zhang, Jun (Department of Anesthesiology, The Affiliated Yantai Yuhuangding Hospital of Qingdao University) ;
  • Wang, Haiyan (Department of Anesthesiology, The Affiliated Yantai Yuhuangding Hospital of Qingdao University) ;
  • Sun, Xizhi (Department of Anesthesiology, The Affiliated Yantai Yuhuangding Hospital of Qingdao University)
  • Received : 2021.03.24
  • Accepted : 2021.06.09
  • Published : 2021.08.28

Abstract

Sevoflurane postconditioning (SPostC) has been proved effective in cardioprotection against myocardial ischemia/reperfusion injury. It was also reported that heat shock protein 70 (HSP70) could be induced by sevoflurane, which played a crucial role in hypoxic/reoxygenation (HR) injury of cardiomyocytes. However, the mechanism by which sevoflurane protects cardiomyocytes via HSP70 is still not understood. Here, we aimed to investigate the related mechanisms of SPostC inducing HSP70 expression to reduce the HR injury of cardiomyocytes. After the HR cardiomyocytes model was established, the cells transfected with siRNA for HSP70 (siHSP70) or not were treated with sevoflurane during reoxygenation. The lactate dehydrogenase (LDH) level was detected by colorimetry while cell viability and apoptosis were detected by MTT and flow cytometry. Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) and Western blotting were used to detect HSP70, apoptosis-, cell cycle-associated factors, iNOS, and Cox-2 expressions. Enzyme-linked immuno sorbent assay (ELISA) was used to measure malondialdehyde (MDA) and superoxide dismutase (SOD). SPostC decreased apoptosis, cell injury, oxidative stress and inflammation and increased viability of HR-induced cardiomyocytes. In addition, SPostC downregulated Bax and cleaved caspase-3 levels, while SPostC upregulated Bcl-2, CDK-4, Cyclin D1, and HSP70 levels. SiHSP70 had the opposite effect that SPostC had on HR-induced cardiomyocytes. Moreover, siHSP70 further reversed the effect of SPostC on apoptosis, cell injury, oxidative stress, inflammation, viability and the expressions of HSP70, apoptosis-, and cell cycle-associated factors in HR-induced cardiomyocytes. In conclusion, this study demonstrates that SPostC can reduce the HR injury of cardiomyocytes by inducing HSP70 expression.

Keywords

References

  1. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, et al. 2005. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 11: 367-368. https://doi.org/10.1038/nm0405-367
  2. Fihn SD, Gardin JM, Abrams J, Berra K, Blankenship JC, Dallas AP, et al. 2012. ACCF/AHA/ACP/AATS/PCNA/SCAI/STS guideline for the diagnosis and management of patients with stable ischemic heart disease: executive summary: a report of the American College of Cardiology Foundation/American Heart Association task force on practice guidelines, and the American College of Physicians, American Association for Thoracic Surgery, Preventive Cardiovascular Nurses Association, Society for Cardiovascular Angiography and Interventions, and Society of Thoracic Surgeons. Circulation 126: 3097-3137. https://doi.org/10.1161/CIR.0b013e3182776f83
  3. Vinten-Johansen J, Zhao ZQ, Zatta AJ, Kin H, Halkos ME, Kerendi F. 2005. Postconditioning--A new link in nature's armor against myocardial ischemia-reperfusion injury. Basic Res. Cardiol. 100: 295-310. https://doi.org/10.1007/s00395-005-0523-x
  4. Wang Y, Ouyang M, Wang Q, Jian Z. 2016. MicroRNA-142-3p inhibits hypoxia/reoxygenation-induced apoptosis and fibrosis of cardiomyocytes by targeting high mobility group box 1. Int. J. Mol. Med. 38: 1377-1386. https://doi.org/10.3892/ijmm.2016.2756
  5. Obal D, Dettwiler S, Favoccia C, Scharbatke H, Preckel B, Schlack W. 2005. The influence of mitochondrial KATP-channels in the cardioprotection of preconditioning and postconditioning by sevoflurane in the rat in vivo. Anesth. Analg. 101: 1252-1260. https://doi.org/10.1213/01.ANE.0000181336.96511.32
  6. Wallin RF, Regan BM, Napoli MD, Stern IJ. 1975. Sevoflurane: a new inhalational anesthetic agent. Anesth. Analg. 54: 758-766.
  7. Patel SS, Goa KL. 1996. Sevoflurane. A review of its pharmacodynamic and pharmacokinetic properties and its clinical use in general anaesthesia. Drugs 51: 658-700. https://doi.org/10.2165/00003495-199651040-00009
  8. Fleisher LA, Beckman JA, Brown KA, Calkins H, Chaikof EL, Fleischmann KE, et al. 2009. ACCF/AHA focused update on perioperative beta blockade incorporated into the ACC/AHA 2007 guidelines on perioperative cardiovascular evaluation and care for noncardiac surgery: a report of the American college of cardiology foundation/American heart association task force on practice guidelines. Circulation 120: e169-276. https://doi.org/10.1161/CIRCULATIONAHA.109.192690
  9. Bein B, Renner J, Caliebe D, Scholz J, Paris A, Fraund S, et al. 2005. Sevoflurane but not Propofol preserves myocardial function during minimally invasive direct coronary artery bypass surgery. Anesth. Analg. 100: 610-616. https://doi.org/10.1213/01.ANE.0000145012.27484.A7
  10. Luo Y, Ma D, Ieong E, Sanders RD, Yu B, Hossain M, et al. 2008. Xenon and sevoflurane protect against brain injury in a neonatal asphyxia model. Anesthlogy 109: 782-789. https://doi.org/10.1097/ALN.0b013e3181895f88
  11. Hu X, Wang J, Zhang L, Zhang Q, Duan X, Zhang Y. 2018. Postconditioning with sevoflurane ameliorates spatial learning and memory deficit via attenuating endoplasmic reticulum stress induced neuron apoptosis in a rat model of hemorrhage shock and resuscitation. Brain Res. 1696: 49-55. https://doi.org/10.1016/j.brainres.2018.05.047
  12. Deyhimy DI, Fleming NW, Brodkin IG, Liu H. 2007. Anesthetic preconditioning combined with postconditioning offers no additional benefit over preconditioning or postconditioning alone. Anesth. Analg. 105: 316-324. https://doi.org/10.1213/01.ane.0000267524.71445.e7
  13. Yao Y-T, Li L-H, Chen L, Wang W-P, Li L-B, Gao C-Q. 2010. Sevoflurane postconditioning protects isolated rat hearts against ischemia-reperfusion injury: the role of radical oxygen species, extracellular signal-related kinases 1/2 and mitochondrial permeability transition pore. Mol. Biol. Rep. 37: 2439-2446. https://doi.org/10.1007/s11033-009-9755-4
  14. Tang Y, Wang QY. 2003. [Effects of sevoflurane-induced and anoxia-induced preconditioning on HSP70 expression in neonatal rat cardiomyocytes]. Hunan yi ke da xue xue bao 28: 129-132.
  15. Mizzen LA, Welch WJ. 1998. Characterization of the thermotolerant cell. I. Effects on protein synthesis activity and the regulation of heat-shock protein 70 expression. J. Cell Biol. 106:1105-1116. https://doi.org/10.1083/jcb.106.4.1105
  16. Zhou JJ, Pei JM, Wang GY, Wu S, Wang WP, Cho CH, et al. 2001. Inducible HSP70 mediates delayed cardioprotection via U-50488H pretreatment in rat ventricular myocytes. Am. J. Physiol. Heart Circ. Physiol. 281: H40-47. https://doi.org/10.1152/ajpheart.2001.281.1.H40
  17. Song YJ, Zhong CB, Wang XB. 2019. Heat shock protein 70: a promising therapeutic target for myocardial ischemia-reperfusion injury. J. Cell. Physiol. 234: 1190-1207. https://doi.org/10.1002/jcp.27110
  18. Yuan Y, Pan SS, Shen YJ. 2018. Cardioprotection of exercise preconditioning involving heat shock protein 70 and concurrent autophagy: a potential chaperone-assisted selective macroautophagy effect. J. Physiol. Sci. 68: 55-67. https://doi.org/10.1007/s12576-016-0507-7
  19. Liu J-C, H Ming, W Li, 2007. Cheng XS. Heat shock protein 70 gene transfection protects rat myocardium cell against anoxia-reoxygeneration injury. Chin. Med. J. 120: 578-583. https://doi.org/10.1097/00029330-200704010-00010
  20. Chen Z, Shen X, Shen F, Zhong W, Wu H, Liu S, et al. 2013. TAK1 activates AMPK-dependent cell death pathway in hydrogen peroxide-treated cardiomyocytes, inhibited by heat shock protein-70. Mol. Cell. Biochem. 377: 35-44. https://doi.org/10.1007/s11010-013-1568-z
  21. Mayer MP, Bukau B. 2005. Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62: 670. https://doi.org/10.1007/s00018-004-4464-6
  22. Wei J, Tong J, Yu L, Zhang J. 2016. EMF protects cardiomyocytes against hypoxia-induced injury via heat shock protein 70 activation. Chem. Biol. Interact. 248: 8-17. https://doi.org/10.1016/j.cbi.2016.02.003
  23. Kitahata H, Nozaki J, Kawahito S, Tomino T, Oshita S. 2008. Low-dose sevoflurane inhalation enhances late cardioprotection from the anti-ulcer drug geranylgeranylacetone. Anesth. Analg. 107: 755-761. https://doi.org/10.1213/ane.0b013e31817f0e61
  24. Gao S, Yang Z, Shi R, Xu D, Li H, Xia Z, et al. 2016. Diabetes blocks the cardioprotective effects of sevoflurane postconditioning by impairing Nrf2/Brg1/HO-1 signaling. Eur. J. Pharmacol. 779: 111-121. https://doi.org/10.1016/j.ejphar.2016.03.018
  25. Yu J, Wu J, Xie P, Maimaitili Y, Wang J, Xia Z, et al. 2016. Sevoflurane postconditioning attenuates cardiomyocyte hypoxia/reoxygenation injury via restoring mitochondrial morphology. PeerJ 4: e2659. https://doi.org/10.7717/peerj.2659
  26. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  27. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R. 2001. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev. 15: 3088-3103. https://doi.org/10.1101/gad.944801
  28. Frangogiannis NG. 2015. Pathophysiology of myocardial infarction. Compr. Physiol. 5: 1841-1875. https://doi.org/10.1002/cphy.c150006
  29. Wang PF, Jiang LS, Bu J, Huang XJ, Song W, Du YP, et al. 2012. Cannabinoid-2 receptor activation protects against infarct and ischemia-reperfusion heart injury. J. Cardiovasc. Pharmacol. 59: 301-307. https://doi.org/10.1097/FJC.0b013e3182418997
  30. Sigaut S, Jannier V, Rouelle D, Gressens P, Mantz J, Dahmani S. 2009. The preconditioning effect of sevoflurane on the oxygen glucose-deprived hippocampal slice: the role of tyrosine kinases and duration of ischemia. Anesth. Analg. 108: 601-608. https://doi.org/10.1213/ane.0b013e31818e2018
  31. Wang J, Lei B, Popp S, Meng F, Cottrell JE, Kass IS. 2007. Sevoflurane immediate preconditioning alters hypoxic membrane potential changes in rat hippocampal slices and improves recovery of CA1 pyramidal cells after hypoxia and global cerebral ischemia. Neuroscience 145: 1097-1107. https://doi.org/10.1016/j.neuroscience.2006.12.047
  32. Julier K, da Silva R, Garcia C, Bestmann L, Frascarolo P, Zollinger A, et al. 2003. Preconditioning by sevoflurane decreases biochemical markers for myocardial and renal dysfunction in coronary artery bypass graft surgery: a double-blinded, placebo-controlled, multicenter study. Anesthesiology 98: 1315-1327. https://doi.org/10.1097/00000542-200306000-00004
  33. Peng S, Kalikiri P, Mychaskiw G, 2nd, Zhang D, Zhang Y, Liu GJ, et al. 2011. Sevoflurane postconditioning ameliorates oxygen-glucose deprivation-reperfusion injury in the rat hippocampus. CNS Neurosci. Ther. 17: 605-611. https://doi.org/10.1111/j.1755-5949.2010.00193.x
  34. Xu H, Mei XP, Xu LX. 2018. The effect of pre- and after-treatment of sevoflurane on central ischemia tolerance and the underlying mechanisms. J. Dent. Anesth. Pain Med. 18: 1-8. https://doi.org/10.17245/jdapm.2018.18.1.1
  35. Wang H, Shi H, Yu Q, Chen J, Zhang F, Gao Y. 2016. Sevoflurane preconditioning confers neuroprotection via anti-apoptosis effects. Acta Neurochir. Suppl. 121: 55-61. https://doi.org/10.1007/978-3-319-18497-5_10
  36. Zhang J, Wang C, Yu S, Luo Z, Chen Y, Liu Q, et al. 2014. Sevoflurane postconditioning protects rat hearts against ischemia-reperfusion injury via the activation of PI3K/AKT/mTOR signaling. Sci. Rep. 4: 7317. https://doi.org/10.1038/srep07317
  37. Drenger B, Ostrovsky IA, Barak M, Nechemia-Arbely Y, Ziv E, Axelrod JH. 2011. Diabetes blockade of sevoflurane postconditioning is not restored by insulin in the rat heart: phosphorylated signal transducer and activator of transcription 3- and phosphatidylinositol 3-kinase-mediated inhibition. Anesthesiology 114: 1364-1372. https://doi.org/10.1097/ALN.0b013e31820efafd
  38. Shi CX, Jin J, Wang XQ, Song T, Li GH, Li KZ, et al. 2020. Sevoflurane attenuates brain damage through inhibiting autophagy and apoptosis in cerebral ischemia-reperfusion rats. Mol. Med. Rep. 21: 123-130.
  39. Xu DZ, Lu Q, Kubicka R, Deitch EA. 1999. The effect of hypoxia/reoxygenation on the cellular function of intestinal epithelial cells. J. Trauma 46: 280-285. https://doi.org/10.1097/00005373-199902000-00014
  40. Almeida-Val VM, Oliveira AR, de Nazare Paula da Silva M, Ferreira-Nozawa MS, Araujo RM, Val AL, et al. 2011. Anoxia- and hypoxia-induced expression of LDH-A* in the Amazon Oscar, Astronotus crassipinis. Genet. Mol. Biol. 34: 315-322. https://doi.org/10.1590/S1415-47572011000200025
  41. Loh KP, Qi J, Tan BK, Liu XH, Wei BG, Zhu YZ. 2010. Leonurine protects middle cerebral artery occluded rats through antioxidant effect and regulation of mitochondrial function. Stroke 41: 2661-2668. https://doi.org/10.1161/STROKEAHA.110.589895
  42. Shi Y, Zhou X, Zhao S. 2001. Effects of ligustrazine on SOD, MDA, NO and apoptosis in rats by retina ischemia-reperfusion. Chin. Ophthal. Res. 19: 301-303.
  43. Dolka I, Krol M, Sapierzynski R. 2016. Evaluation of apoptosis-associated protein (Bcl-2, Bax, cleaved caspase-3 and p53) expression in canine mammary tumors: an immunohistochemical and prognostic study. Res. Vet. Sci. 105: 124-133. https://doi.org/10.1016/j.rvsc.2016.02.004
  44. Li J, Zhao J, Xu M, Li M, Wang B, Qu X, et al. 2020. Blocking GSDMD processing in innate immune cells but not in hepatocytes protects hepatic ischemia-reperfusion injury. Cell Death Dis. 11: 244. https://doi.org/10.1038/s41419-020-2437-9
  45. Posadas I, Terencio MC, Guillen I, Ferrandiz ML, Coloma J, Paya M, et al. 2000. Co-regulation between cyclo-oxygenase-2 and inducible nitric oxide synthase expression in the time-course of murine inflammation. Naunyn-Schmiedebergs Arch. Pharmacol. 361: 98-106. https://doi.org/10.1007/s002109900150
  46. Lange C, Huttner WB, Calegari F. 2009. Cdk4/Cyclin D1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5: 320-331. https://doi.org/10.1016/j.stem.2009.05.026
  47. Jiang JJ, Li C, Li H, Zhang L, Lin ZH, Fu BJ, et al. 2016. Sevoflurane postconditioning affects post-ischaemic myocardial mitochondrial ATP-sensitive potassium channel function and apoptosis in ageing rats. Clin. Exp. Pharmacol. Physiol. 43: 552-561. https://doi.org/10.1111/1440-1681.12565
  48. De Hert S, Vlasselaers D, Barbe R, Ory JP, Dekegel D, Donnadonni R, et al. 2009. A comparison of volatile and non volatile agents for cardioprotection during on-pump coronary surgery. Anaesthesia 64: 953-960. https://doi.org/10.1111/j.1365-2044.2009.06008.x
  49. Song N, Ma J, Meng XW, Liu H, Wang H, Song SY, et al. 2020. Heat shock protein 70 protects the heart from ischemia/reperfusion injury through inhibition of p38 MAPK signaling. Oxid. Med. Cell. Longev. 2020: 3908641.
  50. Zhao Y, Wang W, Qian L. 2007. Hsp70 may protect cardiomyocytes from stress-induced injury by inhibiting Fas-mediated apoptosis. Cell Stress Chaperones 12: 83-95. https://doi.org/10.1379/CSC-231R.1
  51. Wang X, Yuan B, Dong W, Yang B, Yang Y, Lin X, et al. 2014. Induction of heat-shock protein 70 expression by geranylgeranylacetone shows cytoprotective effects in cardiomyocytes of mice under humid heat stress. PLoS One 9: e93536. https://doi.org/10.1371/journal.pone.0093536
  52. Choudhury S, Bae S, Ke Q, Lee JY, Kim J, Kang PM. 2011. Mitochondria to nucleus translocation of AIF in mice lacking Hsp70 during ischemia/reperfusion. Basic Res. Cardiol. 106: 397-407. https://doi.org/10.1007/s00395-011-0164-1
  53. Mosser DD, Caron AW, Bourget L, Denis-Larose C, Massie B. 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17: 5317-5327. https://doi.org/10.1128/MCB.17.9.5317