Journal of Shandong University (Health Sciences) ›› 2022, Vol. 60 ›› Issue (12): 7-12.doi: 10.6040/j.issn.1671-7554.0.2022.0736

• 基础医学 • Previous Articles    

Mechanism of hydrogen sulfide in improving atrial fibrillation induced by obstructive sleep apnea based on oxidative stress

ZHAO Yaqing1,2, XU Jingwen2, WANG Xiao2, HOU Yinglong2, GAO Mei1,2   

  1. 1. The Second Clinical College of Shandong University of Traditional Chinese Medicine, Jinan 250014, Shandong, China;
    2. Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University &
    Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan 250014, Shandong, China
  • Published:2022-12-01

PDF (PC)

311

Abstract: Objective To investigate the mechanism of exogenous donor of hydrogen sulfide, NaHS, in the treatment of atrial fibrillation(AF)in rats with obstructive sleep apnea(OSA)induced oxidative stress. Methods A total of 24 male SD rats were randomly divided into control, model and NaHS groups, with 8 rats in each group. All rats were intubated under anesthesia. The model and NaHS groups simulated OSA process by circulating air holding method. The electrophysiological process of the heart was recorded throughout the experiment. Blood and left atrial tissue were collected after the experiment. The content of malondialdehyde was determined with thiobarbituric acid method. The activity of superoxide dismutase was detected with xanthine oxidase method. The expressions of oxidative stress indexes NADPH oxidase 4(Nox4)and connexin 43(Cx43)were detected with Western blotting. Results Compared with the model group, the NaHS group had reduced induction rate and duration of AF(P<0.05). Compared with the control group, the model group had increased expression of Nox4 and malondialdehyde, decreased superoxide dismutase activity, and decreased expression of Cx43. After NaHS intervention, Nox4 expression was inhibited, malondialdehyde content was decreased, superoxide dismutase activity was increased, and Cx43 expression was increased(P<0.05). Conclusion Hydrogen sulfide can reduce the oxidative stress injury of AF induced by OSA, thus reducing the occurrence and duration of AF. The mechanism is closely related to the inhibiting of Nox4 activation, scavenging of oxygen free radicals, inhibiting of lipid peroxidation, and up-regulating of Cx43 expression.

Key words: Atrial fibrillation, Obstructive sleep apnea, Hydrogen sulfide, NADPH oxidase 4

CLC Number: 

  • R541.7
[1] Kornej J, Benjamin EJ, Magnani JW. Atrial fibrillation: global burdens and global opportunities [J]. Heart, 2021: 516-518. doi: 10.1136/heartjnl-2020-318480.
[2] Baman JR, Passman RS. Atrial Fibrillation [J]. JAMA, 2021, 325(21): 2218.
[3] Serpytis R, Navickaite A, Serpytiene E, et al. Impact of atrial fibrillation on cognitive function, psychological distress, quality of life, and impulsiveness [J]. Am J Med, 2018, 131(6): 701-703.
[4] Huang B, Liu H, Scherlag BJ, et al. Atrial fibrillation in obstructive sleep apnea: neural mechanisms and emerging therapies [J]. Trends Cardiovasc Med, 2021, 31(2): 127-132.
[5] Goudis CA, Ketikoglou DG. Obstructive sleep and atrial fibrillation: Pathophysiological mechanisms and therapeutic implications [J]. Int J Cardiol, 2017, 230: 293-300. doi: 10.1016/j.ijcard.2016.12.120.
[6] Avula U, Hernandez JJ, Yamazaki M, et al. Atrial infarction-induced spontaneous focal discharges and atrial fibrillation in sheep: role of dantrolene-sensitive aberrant ryanodine receptor calcium release [J]. Circ Arrhythm Electrophysiol, 2018, 11(3): e5659.
[7] Cai X, Yang C, Shao L, et al. Targeting NOX 4 by petunidin improves anoxia/reoxygenation-induced myocardium injury [J]. Eur J Pharmacol, 2020, 888: 173414. doi: 10.1016/j.ejphar.2020.173414.
[8] Pei J, Wang F, Pei S, et al. Hydrogen sulfide promotes cardiomyocyte proliferation and heart regeneration via ROS scavenging [J]. Oxid Med Cell Longev, 2020, 2020: 1412696. doi: 10.1155/2020/1412696.
[9] Nguyen K, Chau VQ, Mauro AG, et al. Hydrogen sulfide therapy suppresses cofilin-2 and attenuates ischemic heart failure in a mouse model of myocardial infarction [J]. J Cardiovasc Pharmacol Ther, 2020, 25(5): 472-483.
[10] Lv B, Chen S, Tang C, et al. Hydrogen sulfide and vascular regulation- An update [J]. J Adv Res, 2021, 27: 85-97. doi: 10.1016/j.jare.2020.05.007.
[11] Gao M, Zhang L, Scherlag BJ, et al. Low-level vagosympathetic trunk stimulation inhibits atrial fibrillation in a rabbit model of obstructive sleep apnea [J]. Heart Rhythm, 2015, 12(4): 818-824.
[12] Wiktorowicz A, Kleczynski P, Dziewierz A, et al. Impact of pre-procedural cerebrovascular events on clinical outcomes after transcatheter aortic valve implantation in patients with severe aortic stenosis [J]. Curr Pharm Des, 2018, 24(5): 641-646.
[13] Guilleminault C, Connolly SJ, Winkle RA. Cardiac arrhythmia and conduction disturbances during sleep in 400 patients with sleep apnea syndrome [J]. Am J Cardiol, 1983, 52(5): 490-494.
[14] Bazan V, Vicente I, Lozano L, et al. Previously undetected obstructive sleep apnea in patients with new-onset atrial fibrillation [J]. Am J Cardiol, 2021, 138: 46-52. doi: 10.1016/j.amjcard.2020.09.058.
[15] Linz B, Hohl M, Lang L, et al. Repeated exposure to transient obstructive sleep apnea-related conditions causes an atrial fibrillation substrate in a chronic rat model [J]. Heart Rhythm, 2021, 18(3): 455-464.
[16] Tietjens JR, Claman D, Kezirian EJ, et al. Obstructive sleep apnea in cardiovascular disease: a review of the literature and proposed multidisciplinary clinical management strategy [J]. J Am Heart Assoc, 2019, 8(1): e10440.
[17] Geng B, Chang L, Pan C, et al. Endogenous hydrogen sulfide regulation of myocardial injury induced by isoproterenol [J]. Biochem Biophys Res Commun, 2004, 318(3): 756-763.
[18] Zhang HX, Liu SJ, Tang XL, et al. H2S attenuates LPS-induced acute lung injury by reducing oxidative/nitrative stress and inflammation [J]. Cell Physiol Biochem, 2016, 40(6): 1603-1612.
[19] Li L, Li M, Li Y, et al. Exogenous H2S contributes to recovery of ischemic post-conditioning-induced cardioprotection by decrease of ROS level via down-regulation of NF-kappaB and JAK2-STAT3 pathways in the aging cardiomyocytes [J]. Cell Biosci, 2016, 6: 26. doi: 10.1186/s13578-016-0090-x.
[20] Pan TT, Feng ZN, Lee SW, et al. Endogenous hydrogen sulfide contributes to the cardioprotection by metabolic inhibition preconditioning in the rat ventricular myocytes [J]. J Mol Cell Cardiol, 2006, 40(1): 119-130.
[21] Watts M, Kolluru GK, Dherange P, et al. Decreased bioavailability of hydrogen sulfide links vascular endothelium and atrial remodeling in atrial fibrillation [J]. Redox Biol, 2021, 38: 101817. doi: 10.1016/j.redox.2020.101817.
[22] Xue X, Ling X, Xi W, et al. Exogenous hydrogen sulfide reduces atrial remodeling and atrial fibrillation induced by diabetes mellitus via activation of the PI3K/Akt/eNOS pathway [J]. Mol Med Rep, 2020, 22(3): 1759-1766.
[23] Imano H, Kato R, Tanikawa S, et al. Factor Xa inhibition by rivaroxaban attenuates cardiac remodeling due to intermittent hypoxia [J]. J Pharmacol Sci, 2018, 137(3): 274-282.
[24] Zhang Y, Murugesan P, Huang K, et al. NADPH oxidases and oxidase crosstalk in cardiovascular diseases: novel therapeutic targets [J]. Nat Rev Cardiol, 2020, 17(3): 170-194.
[25] Gray SP, Shah AM, Smyrnias I. NADPH oxidase 4 and its role in the cardiovascular system [J]. Vasc Biol, 2019, 1(1): 59-66.
[26] Wang Y, Zhong L, Liu X, et al. ZYZ-772 prevents cardiomyocyte injury by suppressing Nox4-Derived ROS production and apoptosis [J]. Molecules, 2017, 22(2): 331.
[27] Zhang Y, Qi Y, Li JJ, et al. Stretch-induced sarcoplasmic reticulum calcium leak is causatively associated with atrial fibrillation in pressure-overloaded hearts [J]. Cardiovasc Res, 2021, 117(4): 1091-1102.
[28] Lu G, Xu C, Tang K, et al. H2S inhibits angiotensin II-induced atrial Kv1.5 upregulation by attenuating Nox4-mediated ROS generation during atrial fibrillation [J]. Biochem Biophys Res Commun, 2017, 483(1): 534-540.
[29] 刘艳丽, 刘奔, 屈扬扬, 等. 氧化应激和钙/钙调蛋白依赖性蛋白激酶II参与β肾上腺素受体持久激动引起的大鼠心肌肥厚[J]. 生理学报, 2013, 65(1): 1-7. LIU Yanli, LIU Ben, QU Yangyang, et al. Oxidative stress and calcium / calmodulin dependent protein kinase II involvement β Myocardial hypertrophy induced by sustained adrenaline receptor activation in rats [J] Journal of physiology, 2013, 65(1): 1-7.
[30] Lu W, Kang J, Hu K, et al. The role of the Nox4-derived ROS-mediated RhoA/Rho kinase pathway in rat hypertension induced by chronic intermittent hypoxia [J]. Sleep Breath, 2017, 21(3): 667-677.
[31] Li J, Wang S, Bai J, et al. Novel Role for the immunoproteasome subunit PSMB10 in angiotensin II-Induced atrial fibrillation in mice [J]. Hypertension, 2018, 71(5): 866-876.
[32] Petersen F, Rodrigo R, Richter M, et al. The effects of polyunsaturated fatty acids and antioxidant vitamins on atrial oxidative stress, nitrotyrosine residues, and connexins following extracorporeal circulation in patients undergoing cardiac surgery [J]. Mol Cell Biochem, 2017, 433(1-2): 27-40.
[33] Linz B, Hohl M, Lang L, et al. Repeated exposure to transient obstructive sleep apnea-related conditions causes an atrial fibrillation substrate in a chronic rat model [J]. Heart Rhythm, 2021, 18(3): 455-464.
[1] HUANG Huining, DU Juanjuan, SUN Yi, HOU Yinglong, GAO Mei. Hydrogen sulfide alleviates acute obstructive sleep apnea-induced atrial fibrillation by regulating oxidative stress through glutaredoxin-1 [J]. Journal of Shandong University (Health Sciences), 2022, 60(1): 1-5.
[2] CAI Fanfan, JI Congshan, YANG Shifeng, GU Hui, YUAN Xianshun, LIU Hongwu, QIN Songnan, GAO Lin, WANG Ruopeng, WANG Ximing. Clinical application of third-generation double-source CT in coronary CT angiography for patients with atrial fibrillation [J]. Journal of Shandong University (Health Sciences), 2021, 59(2): 14-18.
[3] HUANG Bosong, CONG Hongliang. Anticoagulant therapy of non-valvular atrial fibrillation in 1,430 middle-aged patients with moderate-risk thromboembolism [J]. Journal of Shandong University (Health Sciences), 2021, 59(10): 49-67.
[4] LIU Donglu, WANG Ximin, LI Zhan, DU Juanjuan, LI Jianhua, MA Shenzhou, HOU Yinglong. LncRNA056298 mediates the occurrence of neural remodeling recurrence in radiofrequency ablation dogs by affecting the expression of growth associated protein 43 [J]. Journal of Shandong University (Health Sciences), 2020, 58(5): 27-37.
[5] GUO Jing, ZHANG Yu, YANG Yujuan, SUN Yuemei, LIU Liping, SONG Xicheng. Establishment of airway management protocol based on ERAS for OSAHS children [J]. Journal of Shandong University (Health Sciences), 2019, 57(9): 54-58.
[6] LI Jianhua, LI Zhan, JIA Xiaomeng, DU Juanjuan, MA Shenzhou, LIU Donglu, ZHANG Yong, ZHANG Yujiao, HOU Yinglong. Roles and mechanisms of TCONS_00016478 in atrial energy metabolic remodeling by regulating PGC-1α/ PPARγ pathway in rabbit models of atrial fibrillation [J]. Journal of Shandong University (Health Sciences), 2019, 57(4): 1-8.
[7] CHEN Linlin, YI Shaolei, WANG Weizong, LI Zhan, ZHANG Yong, ZHANG Yujiao,REN Manyi, XIE Xinxing, LIU Tongbao, HOU Yinglong. Risk factors of recurrent atrial fibrillation after radiofrequency catheter ablation [J]. Journal of Shandong University (Health Sciences), 2019, 57(3): 49-57.
[8] ZHANG Xiuling, ZHANG Lei, LIU Dan, LIANG Jiangjiu. Association of ApoE gene polymorphism and risk of atrial fibrillation among Han people in Shandong Province [J]. Journal of Shandong University (Health Sciences), 2018, 56(3): 79-84.
[9] WEI Jinqiu, ZHANG Yujiao, LI Zhan, WANG Ximin, CHEN Linlin, DU Juanjuan, ZHANG Yong, XIE Xinxing, HOU Yinglong. Effects of GCH1 on atrial autonomic nerve remodeling by regulating tetrahydrobiopterin in A-TP canines [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2017, 55(5): 8-12.
[10] ZHANG Hongxia, XU Yonghong, CHEN Li, GONG Huicheng. Detection of peripheral thrombomodulin and myeloperoxidase and their significance in adults with obstructive sleep apnea hypopnea syndrome [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(12): 67-71.
[11] ZHAO Huichen, CHAI Jiachao, ZHANG Liang, YUAN Mingzhen, PENG Li, LIU Yuantao. Changes of hydrogen sulfide concentrations and synthetase expressions in the corpus cavernosum of diabetic rats [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2016, 54(10): 25-28.
[12] ZHANG Kai, LIANG Fei, HAN Bo, MA Xiaochun, ZHU Xiaolong, ZHANG Jun, ZHANG Tao, ZOU Chengwei. Radiofrequency modified maze Ⅲ plus ganglionic plexus ablation vs radiofrequency modified maze Ⅲ alone in the treatment of atrial fibrillation with rheumatic mitral lesion [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2015, 53(5): 66-70.
[13] LI Man, ZHONG Jingquan, YUE Xin, ZHU Qing, ZHENG Zhaotong, RONG Bing, YI Shaolei, XIE Fei, ZHANG Yun. Effect of different circumferential pulmonary vein ablation endpoints on prognosis of atrial fibrillation patients:bidirectional block between pulmonary veins and left atrium [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2015, 53(3): 62-68.
[14] ZHANG Fenglei, ZHENG Man, ZHANG Qi, GU Lei, XU Xinsheng. Clinical study on the association between metabolic syndrome and P wave dispersion [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2015, 53(2): 52-55.
[15] ZHANG Lingli, ZHOU Ying, LI Xiaohe, LI Hui, ZHONG Ming, ZHANG Wei. Myocardial MMPs and TIMPs mRNA expressions in Chinese population with atrial fibrillation: a Meta-analysis [J]. JOURNAL OF SHANDONG UNIVERSITY (HEALTH SCIENCES), 2015, 53(1): 47-53.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
Copyright 2018 © Editorial office of Journal of Shandong University (Health Sciences)
Supported by Beijing Magtech Co.Ltd