Thioredoxin-1: A potential target for prevention of heart-related reactive oxygen species injury_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

SUN Yiren ^1,2 , YANG Ziqi ² , WANG Xinran ³ ,  QIAN Yongjun ¹

1. Department of Cardiovascular Surgery, West China Hospital, Sichuan University, Chengdu, 610041, P. R. China;
2. West China School of Medicine, Sichuan University, Chengdu, 610041, P. R. China;
3. West China School of Stomatology, Sichuan University, Chengdu, 610041, P. R. China;

Corresponding author：

QIAN Yongjun, Email: qianyongjun@scu.edu.cn

Keywords：

Reactive oxygen species; oxidative stress; thioredoxin; antioxidant; review

DOI：

10.7507/1007-4848.202203025

Video：

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Reactive oxygen species (ROS) play an important role in the pathogenesis of various cardiovascular diseases, by leading to cell apoptosis and thus causing organic injuries. Anti-ROS therapy is highly anticipated, but currently, there is still no appropriate prevention method. Studies have shown that thioredoxin (Trx), being a kind of significant endogenous antioxidant system, has excellent antioxidant capacity. Promotion of Trx can reduce key biomolecules to eliminate ROS or regulate many signaling pathways, thus resisting ROS injuries, which may be a new anti-ROS strategy. Therefore, we reviewed the research progress of Trx in cardiac antioxidant therapy to discuss its potential and possibility to be a target for prevention of heart-related ROS injury.

Citation： SUN Yiren, YANG Ziqi, WANG Xinran, QIAN Yongjun. Thioredoxin-1: A potential target for prevention of heart-related reactive oxygen species injury. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(12): 1779-1783. doi: 10.7507/1007-4848.202203025 Copy

1.	Geest BD, Mishra M. Role of oxidative stress in heart failure: Insights from gene transfer studies. Biomedicines, 2021, 9(11): 1645.
2.	He L, He T, Farrar S, et al. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem, 2017, 44(2): 532-553.
3.	Andreadou I, Efentakis P, Frenis K, et al. Thiol-based redox-active proteins as cardioprotective therapeutic agents in cardiovascular diseases. Basic Res Cardiol, 2021, 116(1): 44.
4.	Li YY, Xiang Y, Song Z, et al. Intramyocardial injection of thioredoxin 2-expressing lentivirus alleviates myocardial ischemia-reperfusion injury in rats. Am J Transl Res, 2017, 9(10): 4428-4439.
5.	Chen C, Chen H, Zhou HJ, et al. Mechanistic role of thioredoxin 2 in heart failure. Adv Exp Med Biol, 2017, 982: 265-276.
6.	Kim MK, Zhao L, Jeong S, et al. Structural and biochemical characterization of thioredoxin-2 from deinococcus radiodurans. Antioxidants (Basel), 2021, 10(11): 1843.
7.	Wei B, Li F. Mechanisms of Trx2/ASK1-mediated mitochondrial injury in pemphigus vulgaris. Biomed Res Int, 2021, 2021: 2471518.
8.	Bian M, Fan R, Zhao S, et al. Targeting the thioredoxin system as a strategy for cancer therapy. J Med Chem, 2019, 62(16): 7309-7321.
9.	Wang BF, Yoshioka J. The emerging role of thioredoxin-interacting protein in myocardial ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther, 2017, 22(3): 219-229.
10.	Bechtel TJ, Eranthie W. From structure to redox: The diverse functional roles of disulfides and implications in disease. Proteomics, 2017, 17(6): 10.1002/pmic. 201600391.
11.	Benhar M. Oxidants, antioxidants and thiol redox switches in the control of regulated cell death pathways. Antioxidants (Basel), 2020, 9(4): 309.
12.	Nagarajan N, Oka S, Sadoshima J. Modulation of signaling mechanisms in the heart by thioredoxin 1. Free Radic Biol Med, 2017, 109: 125-131.
13.	Hwang-Bo H, Jeong JW, Han MH, et al. Auranofin, an inhibitor of thioredoxin reductase, induces apoptosis in hepatocellular carcinoma Hep3B cells by generation of reactive oxygen species. Gen Physiol Biophys, 2017, 36(2): 117-128.
14.	Branco V, Coppo L, Solá S, et al. Impaired cross-talk between the thioredoxin and glutathione systems is related to ASK-1 mediated apoptosis in neuronal cells exposed to mercury. Redox Biol, 2017, 13: 278-287.
15.	Yang J, Gong Y, Cai J, et al. Dysfunction of thioredoxin triggers inflammation through activation of autophagy in chicken cardiomyocytes. Biofactors, 2020, 46(4): 579-590.
16.	Neidhardt S, Garbade J, Emrich F, et al. Ischemic cardiomyopathy affects the thioredoxin system in the human myocardium. J Card Fail, 2019, 25(3): 204-212.
17.	Islam IM, Nagakannan P, Ogungbola O, et al. Thioredoxin system as a gatekeeper in caspase-6 activation and nuclear lamina integrity: Implications for Alzheimer's disease. Free Radic Biol Med, 2019,, 134: 567-580.
18.	Nishimura A, Tanaka T, Kato Y, et al. Cardiac robustness regulated by reactive sulfur species. J Clin Biochem Nutr, 2022, 70(1): 1-6.
19.	El Hadri K, Smith R, Duplus E, et al. Inflammation, oxidative stress, senescence in atherosclerosis: Thioredoxine-1 as an emerging therapeutic target. Int J Mol Sci, 2021, 23(1): 77.
20.	Liu X, Wang L, Cai J, et al. N-acetylcysteine alleviates H₂O₂-induced damage via regulating the redox status of intracellular antioxidants in H9c2 cells. Int J Mol Med, 2019, 43(1): 199-208.
21.	Ma M, Li R, Sun W, et al. Sevoflurane preconditioning inhibits cardiomyocyte injury induced by oxygen-glucose deprivation by modulating TXNIP. Int J Mol Med, 2020, 46(2): 889-897.
22.	Wu ZL, Davis JRJ, Zhu Y. Dexmedetomidine protects against myocardial ischemia/reperfusion injury by ameliorating oxidative stress and cell apoptosis through the Trx1-dependent Akt pathway. Biomed Res Int, 2020, 2020: 8979270.
23.	Liu F, Su H, Liu B, et al. STVNa Attenuates isoproterenol-induced cardiac hypertrophy response through the HDAC4 and Prdx2/ROS/Trx1 pathways. Int J Mol Sci, 2020, 21(2): 682.
24.	Matsuzaki S, Eyster C, Newhardt MF, et al. Insulin signaling alters antioxidant capacity in the diabetic heart. Redox Biol, 2021, 47: 102140.
25.	Wei H, Bu R, Yang Q, et al. Exendin-4 protects against hyperglycemia-induced cardiomyocyte pyroptosis via the AMPK-TXNIP pathway. J Diabetes Res, 2019, 2019: 8905917.
26.	Wang DS, Yan LY, Yang DZ, et al. Formononetin ameliorates myocardial ischemia/reperfusion injury in rats by suppressing the ROS-TXNIP-NLRP3 pathway. Biochem Biophys Res Commun, 2020, 525(3): 759-766.
27.	Li Y, Xu P, Wang Y, et al. Different intensity exercise preconditions affect cardiac function of exhausted rats through regulating TXNIP/TRX/NF-ĸB p65/NLRP3 inflammatory pathways. Evid Based Complement Alternat Med, 2020, 2020: 5809298.
28.	Tao L, Gao E, Bryan NS, et al. Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: Role of S-nitrosation. Proc Natl Acad Sci U S A, 2004, 101(31): 11471-11476.
29.	Ovalle F, Grimes T, Xu G, et al. Verapamil and beta cell function in adults with recent-onset type 1 diabetes. Nat Med, 2018, 24(8): 1108-1112.
30.	Zitta K, Meybohm P, Gruenewald M, et al. Profiling of cell stress protein expression in cardiac tissue of cardiosurgical patients undergoing remote ischemic preconditioning: Implications for thioredoxin in cardioprotection. J Transl Med, 2015, 13: 34.
31.	Gao C, Wang R, Li B, et al. TXNIP/Redd1 signalling and excessive autophagy: A novel mechanism of myocardial ischaemia/reperfusion injury in mice. Cardiovasc Res, 2020, 116(3): 645-657.
32.	Handy DE, Joseph J, Loscalzo J. Selenium, a micronutrient that modulates cardiovascular health via redox enzymology. Nutrients, 2021, 13(9): 3238.

1. Geest BD, Mishra M. Role of oxidative stress in heart failure: Insights from gene transfer studies. Biomedicines, 2021, 9(11): 1645.
2. He L, He T, Farrar S, et al. Antioxidants maintain cellular redox homeostasis by elimination of reactive oxygen species. Cell Physiol Biochem, 2017, 44(2): 532-553.
3. Andreadou I, Efentakis P, Frenis K, et al. Thiol-based redox-active proteins as cardioprotective therapeutic agents in cardiovascular diseases. Basic Res Cardiol, 2021, 116(1): 44.
4. Li YY, Xiang Y, Song Z, et al. Intramyocardial injection of thioredoxin 2-expressing lentivirus alleviates myocardial ischemia-reperfusion injury in rats. Am J Transl Res, 2017, 9(10): 4428-4439.
5. Chen C, Chen H, Zhou HJ, et al. Mechanistic role of thioredoxin 2 in heart failure. Adv Exp Med Biol, 2017, 982: 265-276.
6. Kim MK, Zhao L, Jeong S, et al. Structural and biochemical characterization of thioredoxin-2 from deinococcus radiodurans. Antioxidants (Basel), 2021, 10(11): 1843.
7. Wei B, Li F. Mechanisms of Trx2/ASK1-mediated mitochondrial injury in pemphigus vulgaris. Biomed Res Int, 2021, 2021: 2471518.
8. Bian M, Fan R, Zhao S, et al. Targeting the thioredoxin system as a strategy for cancer therapy. J Med Chem, 2019, 62(16): 7309-7321.
9. Wang BF, Yoshioka J. The emerging role of thioredoxin-interacting protein in myocardial ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther, 2017, 22(3): 219-229.
10. Bechtel TJ, Eranthie W. From structure to redox: The diverse functional roles of disulfides and implications in disease. Proteomics, 2017, 17(6): 10.1002/pmic. 201600391.
11. Benhar M. Oxidants, antioxidants and thiol redox switches in the control of regulated cell death pathways. Antioxidants (Basel), 2020, 9(4): 309.
12. Nagarajan N, Oka S, Sadoshima J. Modulation of signaling mechanisms in the heart by thioredoxin 1. Free Radic Biol Med, 2017, 109: 125-131.
13. Hwang-Bo H, Jeong JW, Han MH, et al. Auranofin, an inhibitor of thioredoxin reductase, induces apoptosis in hepatocellular carcinoma Hep3B cells by generation of reactive oxygen species. Gen Physiol Biophys, 2017, 36(2): 117-128.
14. Branco V, Coppo L, Solá S, et al. Impaired cross-talk between the thioredoxin and glutathione systems is related to ASK-1 mediated apoptosis in neuronal cells exposed to mercury. Redox Biol, 2017, 13: 278-287.
15. Yang J, Gong Y, Cai J, et al. Dysfunction of thioredoxin triggers inflammation through activation of autophagy in chicken cardiomyocytes. Biofactors, 2020, 46(4): 579-590.
16. Neidhardt S, Garbade J, Emrich F, et al. Ischemic cardiomyopathy affects the thioredoxin system in the human myocardium. J Card Fail, 2019, 25(3): 204-212.
17. Islam IM, Nagakannan P, Ogungbola O, et al. Thioredoxin system as a gatekeeper in caspase-6 activation and nuclear lamina integrity: Implications for Alzheimer's disease. Free Radic Biol Med, 2019,, 134: 567-580.
18. Nishimura A, Tanaka T, Kato Y, et al. Cardiac robustness regulated by reactive sulfur species. J Clin Biochem Nutr, 2022, 70(1): 1-6.
19. El Hadri K, Smith R, Duplus E, et al. Inflammation, oxidative stress, senescence in atherosclerosis: Thioredoxine-1 as an emerging therapeutic target. Int J Mol Sci, 2021, 23(1): 77.
20. Liu X, Wang L, Cai J, et al. N-acetylcysteine alleviates H₂O₂-induced damage via regulating the redox status of intracellular antioxidants in H9c2 cells. Int J Mol Med, 2019, 43(1): 199-208.
21. Ma M, Li R, Sun W, et al. Sevoflurane preconditioning inhibits cardiomyocyte injury induced by oxygen-glucose deprivation by modulating TXNIP. Int J Mol Med, 2020, 46(2): 889-897.
22. Wu ZL, Davis JRJ, Zhu Y. Dexmedetomidine protects against myocardial ischemia/reperfusion injury by ameliorating oxidative stress and cell apoptosis through the Trx1-dependent Akt pathway. Biomed Res Int, 2020, 2020: 8979270.
23. Liu F, Su H, Liu B, et al. STVNa Attenuates isoproterenol-induced cardiac hypertrophy response through the HDAC4 and Prdx2/ROS/Trx1 pathways. Int J Mol Sci, 2020, 21(2): 682.
24. Matsuzaki S, Eyster C, Newhardt MF, et al. Insulin signaling alters antioxidant capacity in the diabetic heart. Redox Biol, 2021, 47: 102140.
25. Wei H, Bu R, Yang Q, et al. Exendin-4 protects against hyperglycemia-induced cardiomyocyte pyroptosis via the AMPK-TXNIP pathway. J Diabetes Res, 2019, 2019: 8905917.
26. Wang DS, Yan LY, Yang DZ, et al. Formononetin ameliorates myocardial ischemia/reperfusion injury in rats by suppressing the ROS-TXNIP-NLRP3 pathway. Biochem Biophys Res Commun, 2020, 525(3): 759-766.
27. Li Y, Xu P, Wang Y, et al. Different intensity exercise preconditions affect cardiac function of exhausted rats through regulating TXNIP/TRX/NF-ĸB p65/NLRP3 inflammatory pathways. Evid Based Complement Alternat Med, 2020, 2020: 5809298.
28. Tao L, Gao E, Bryan NS, et al. Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: Role of S-nitrosation. Proc Natl Acad Sci U S A, 2004, 101(31): 11471-11476.
29. Ovalle F, Grimes T, Xu G, et al. Verapamil and beta cell function in adults with recent-onset type 1 diabetes. Nat Med, 2018, 24(8): 1108-1112.
30. Zitta K, Meybohm P, Gruenewald M, et al. Profiling of cell stress protein expression in cardiac tissue of cardiosurgical patients undergoing remote ischemic preconditioning: Implications for thioredoxin in cardioprotection. J Transl Med, 2015, 13: 34.
31. Gao C, Wang R, Li B, et al. TXNIP/Redd1 signalling and excessive autophagy: A novel mechanism of myocardial ischaemia/reperfusion injury in mice. Cardiovasc Res, 2020, 116(3): 645-657.
32. Handy DE, Joseph J, Loscalzo J. Selenium, a micronutrient that modulates cardiovascular health via redox enzymology. Nutrients, 2021, 13(9): 3238.

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