Pathobiochemical aspects of alcoholic cardiomyopathy. The role of hydrogen sulfide in the mechanism of cardiocytoprotection (a review)
DOI:
https://doi.org/10.14739/2310-1210.2022.2.242826Keywords:
alcoholic cardiomyopathy, mechanisms, hydrogen sulfide, oxidative stress, inflammation, apoptosis, cardiocytoprotectionAbstract
Aim: systematization of knowledge about the pathobiochemical mechanisms of heart disease in alcoholic cardiomyopathy (ACMP) and the search for promising ways of cardiocytoprotection.
Alcohol abuse is an important medical and social problem, risk factor for metabolic disorders, malnutrition, cancers, dementia, neuropathy, and others. Consumption of large amounts of ethanol increases a risk of sudden cardiac death and cardiac arrhythmias. The term “alcoholic cardiomyopathy” describes a heart disease in people with a history of long-term alcohol use. ACMP is characterized by left ventricular dilatation, decreased wall thickness and (at the later stages) decreased left ventricular ejection fraction (less than 40 %).
Analysis of literature data about the mechanisms of alcohol-induced cardiotoxicity revealed trigger factors for myocardial damage. Negative effect of ethanol on the heart is realized through induction of oxidative-nitrosative stress, apoptosis, inflammation, fibrogenesis, hypoenergetic state and ion pump dysfunction, development of endothelial dysfunction, impaired ribosomal synthesis. In-depth study of biochemical mechanisms and identification of new molecular targets, integrated into the pathogenesis of ACMP, will optimize the pharmacotherapy for this pathology.
Hydrogen sulfide (H2S), is a metabolic factor involved in the regulation of cardiovascular activity. Use of exogenous H2S has potent cardioprotective properties in cardio-vascular diseases. Donors of H2S and H2S-releasing drugs (hybrid molecules – H2S-aspirin, H2S-NO) show a powerful cardioprotective role in various pathological conditions. Therefore, it is advisable to further study the role of H2S system in the pathogenesis of ACMP to develop new approaches to more effective treatment of this disease.
Conclusions. Modulation of the H2S level in the organism may be a predictor of the severity of myocardial damage, as well as a promising vector in pharmacotherapy, including alcoholic cardiomyopathy.
References
- Spies, C. D., Sander, M., Stangl, K., Fernandez-Sola, J., Preedy, V. R., Rubin, E., Andreasson, S., Hanna, E. Z., & Kox, W. J. (2001). Effects of alcohol on the heart. Current Opinion in Critical Care, 7(5), 337-343. https://doi.org/10.1097/00075198-200110000-00004
- Krenz, M., & Korthuis, R. J. (2012). Moderate ethanol ingestion and cardiovascular protection: from epidemiologic associations to cellular mechanisms. Journal Molecular and Cellular Cardiology, 52(1), 93-104. https://doi.org/10.1016/j.yjmcc.2011.10.011
- Walker, R. K., Cousins, V. M., Umoh, N. A., Jeffress, M. A., Taghipour, D., Al-Rubaiee, M., & Haddad, G. E. (2013). The Good, the Bad, and the Ugly with Alcohol Use and Abuse on the Heart. Alcoholism Clinical & Experimental Research, 37(8), 1253-1260. https://doi.org/10.1111/acer.12109
- Mostbauer, H. V. (2020). Ishemichna khvoroba sertsia ta alkohol: dvi storony odniiei medali [Ischemic heart disease and alcohol: two sides of the same coin]. Zdorovia Ukrainy, (6. Kardiolohiia. Revmatolohiia. Kardiokhirurhiia), 38-40. https://health-ua.com/multimedia/6/2/7/2/6/1609233517.pdf [in Ukrainian].
- Mostbauer, H. V. (2021). Ishemichna khvoroba sertsia ta alkohol: dvi storony odniiei medali [Ischemic heart disease and alcohol: two sides of the same coin]. Zdorovia Ukrainy, (1. Kardiolohiia. Revmatolohiia. Kardiokhirurhiia), 52-54. https://health-ua.com/multimedia/6/3/6/2/8/1615542952.pdf [in Ukrainian].
- Reichart, D., Magnussen, C., Zeller, T., & Blankenberg, S. (2019). Dilated cardiomyopathy: from epidemiologic to genetic phenotypes: A translational review of current literature. Journal of Internal Medicine, 286(4), 362-372. https://doi.org/10.1111/joim.12944
- Piano, M. R., & Phillips, S. A. (2014). Alcoholic cardiomyopathy: Pathophysiologic insights. Cardiovascular Toxicology, 14(4), 291-308. https://doi.org/10.1007/s12012-014-9252-4
- Dorogoi, A. P. (2016). Alkoholna kardiomiopatiia i alkoholna khvoroba pechinky: problemy ta naslidky vzhyvannia alkoholiu [Alcohol cardiomyopathy and alcohol liver disease: problems and consequences of alcohol consumption]. Ukrainskyi kardiolohichnyi zhurnal, (Supl. 1), 22-31. [in Ukrainian].
- Mogos, M. F., Salemi, J. L., Phillips, S. A., & Piano, M. R. (2019). Contemporary Appraisal of Sex Differences in Prevalence, Correlates, and Outcomes of Alcoholic Cardiomyopathy. Alcohol and Alcoholism, 54(4), 386-395. https://doi.org/10.1093/alcalc/agz050
- Fernández-Solà, J., Estruch, R., Nicolás, J.-M., Paré, J.-C., Sacanella, E., Antúnez, E., & Urbano-Márquez, A. (1997). Comparison of Alcoholic Cardiomyopathy in Women Versus Menfn1. The American Journal of Cardiology, 80(4), 481-485. https://doi.org/10.1016/s0002-9149(97)00399-8
- Piano, M. R., Thur, L. A., Hwang, C. L., & Phillips, S. A. (2020). Effects of Alcohol on the Cardiovascular System in Women. Alcohol Research: Current Reviews, 40(2), Article 12. https://doi.org/10.35946/arcr.v40.2.12
- Fernández-Solà, J. (2020). The Effects of Ethanol on the Heart: Alcoholic Cardiomyopathy. Nutrients, 12(2), Article 572. https://doi.org/10.3390/nu12020572
- Ren, J., & Wold, L. E. (2008). Mechanisms of alcoholic heart disease. Therapeutic Advances in Cardiovascular Disease, 2(6), 497-506. https://doi.org/10.1177/1753944708095137
- Leibing, E., & Meyer, T. (2016). Enzymes and signal pathways in the pathogenesis of alcoholic cardiomyopathy. Herz, 41(6), 478-483. https://doi.org/10.1007/s00059-016-4459-8
- Fernández-Solà, J. (2015). Cardiovascular risks and benefits of moderate and heavy alcohol consumption. Nature Reviews Cardiology, 12(10), 576-587. https://doi.org/10.1038/nrcardio.2015.91
- Molina, P. E., Gardner, J. D., Souza-Smith, F. M., & Whitaker, A. M. (2014). Alcohol Abuse: Critical Pathophysiological Processes and Contribution to Disease Burden. Physiology, 29(3), 203-215. https://doi.org/10.1152/physiol.00055.2013
- Laurent, D., & Edwards, J. G. (2014). Alcoholic Cardiomyopathy: Multigenic Changes Underlie Cardiovascular Dysfunction. Journal of Cardiology & Clinical Research, 2(1), Article 1022.
- Belenichev, I. F., & Kucher, T. V. (2016). Vliyanie tiol'nykh antioksidantov na sostoyanie nitroziruyushchego stressa v golovnom mozge krys, podverzhennykh khronicheskoi alkogol'noi intoksikatsii [The influence of thiol antioxidants on the state of nitrosating stress in brain of rats with chronic ethanol intoxication]. Farmakolohiia ta likarska toksykolohiia, (2), 24-29. [in Russian].
- Steiner, J. L., & Lang, C. H. (2017). Etiology of alcoholic cardiomyopathy: Mitochondria, oxidative stress and apoptosis. The International Journal of Biochemistry & Cell Biology, 89, 125-135. https://doi.org/10.1016/j.biocel.2017.06.009
- Fernández-Solà, J., & Planavila Porta, A. (2016). New Treatment Strategies for Alcohol-Induced Heart Damage. International Journal of Molecular Sciences, 17(10), Article 1651. https://doi.org/10.3390/ijms17101651
- Rajbanshi, S. L., & Pandanaboina, C. S. (2014). Alcohol stress on cardiac tissue - Ameliorative effects of Thespesia populnea leaf extract. Journal of Cardiology, 63(6), 449-459. https://doi.org/10.1016/j.jjcc.2013.10.015
- Vaideeswar, P., Chaudhari, C., Rane, S., Gondhalekar, J., & Dandekar, S. (2014). Cardiac pathology in chronic alcoholics: A preliminary study. Journal of Postgraduate Medicine, 60(4), 372-376. https://doi.org/10.4103/0022-3859.143958
- Li, X., Nie, Y., Lian, H., & Hu, S. (2018). Histopathologic features of alcoholic cardiomyopathy compared with idiopathic dilated cardiomyopathy. Medicine, 97(39), Article e12259. https://doi.org/10.1097/MD.0000000000012259
- Tertyshnyi, S. I., Shuliatnikova, T. V., & Zubko, M. D. (2020). Heart pathomorphological changes in the long-term alcohol consumption. Pathologia, 17(2), 149-155. https://doi.org/10.14739/2310-1237.2020.2.212734
- Belenichev, I. F., Chernii, V. I., Kolesnik, Yu. M., Pavlov, S. V., Andronova, I. A., Abramov, A. V., Ostrovaya, T. V., Bukhtiyarova, N. V., & Kucherenko, L. I. (2009). Ratsional'naya neiroprotektsiya [Rational neuroprotection]. Izdatel' Zaslavskii A. Yu. [in Russian].
- Belenichev, I. F., Gorbacheva, S. V., Demchenko, A. V., & Bukhtiyarova, N. V. (2014). The thiol-disulfide balance and the nitric oxide system in the brain tissue of rats subjected to experimental acute impairment of cerebral blood flow: The therapeutic effects of nootropic drugs. Neurochemical Journal, 8(1), 24-27. https://doi.org/10.1134/s181971241401005x
- Belenichev, I. F., Burlaka, B. S., Bukhtiyarova, N. V., Aliyeva, E. G., Suprun, E. V., Ishchenko, A. M., & Simbirtsev, A. S. (2021). Pharmacological Correction of Thiol-Disulphide Imbalance in the Rat Brain by Intranasal Form of Il-1b Antagonist in a Model of Chronic Cerebral Ischemia. Neurochemical Journal, 15(1), 30-36. https://doi.org/10.1134/s1819712421010153
- Belenichev, I. F., Chekman, I. S., Nagornaya, E. A., Gorbacheva, S. V., Gorchakova, N. A., Bukhtiyarova, N. V., Reznichenko, N. Yu., & Feroz Shakh. (2020). Tiol-disul'fidnaya sistema: rol' v endogennoi tsito- i organoprotektsii, puti farmakologicheskoi modulyatsii [Thiol-disulfide system: the role in endogenous cyto- and organ protection, pharmacological modulation pathways]. TOV Vidavnitstvo «Yuston». [in Russian].
- Day, E., & Rudd, J. (2019). Alcohol use disorders and the heart. Addiction, 114(9), 1670-1678. https://doi.org/10.1111/add.14703
- Mirijello, A., Tarli, C., Vassallo, G. A., Sestito, L., Antonelli, M., d'Angelo, C., Ferrulli, A., De Cosmo, S., Gasbarrini, A., & Addolorato, G. (2017). Alcoholic cardiomyopathy: What is known and what is not known. European Journal of Internal Medicine, 43, 1-5. https://doi.org/10.1016/j.ejim.2017.06.014
- Bielenichev, I. F., Stebliuk, V. S., & Kamyshnyi, A. M. (2017). Kharakter ekspressii mRNK iNOS i eNOS v miokarde krys s alkogol'noi kardiomiopatiei i na fone provodimoi terapii metabolitotropnymi kardioprotektorami [The mRNA expression character of inos and enos in the rats myocardium with alcoholic cardiomyopathy during metabolitotropic cardioprotectors therapy]. Visnyk problem biolohii i medytsyny, (2), 82-87. [in Ukrainian].
- Belenichev, I. F., Duyun, I. F., Kamyshnyi, O. M., Mazulin, O. V., Suprun, E. V., & Makyeyeva, L. V. (2020). Expression of mRNA iNOS and mRNA eNOS in the liver of rats with chronic alcohol intoxication and with the introduction of Achillea Micranthoides Klok herb extract. Et krytzka. Biological Markers in Fundamental and Clinical Medicine, 4(1), 6-10. https://doi.org/10.29256/v.04.01.2020.escbm02
- Marchi, K. C., Muniz, J. J., & Tirapelli, C. R. (2014). Hypertension and chronic ethanol consumption: What do we know after a century of study? World Journal of Cardiology, 6(5), 283-294. https://doi.org/10.4330/wjc.v6.i5.283
- Vary, T. C., Deiter, G., & Lantry, R. (2008). Chronic Alcohol Feeding Impairs mTOR(Ser2448) Phosphorylation in Rat Hearts. Alcoholism, Clinical & Experimental Research, 32(1), 43-51. https://doi.org/10.1111/j.1530-0277.2007.00544.x
- Fogle, R. L., Lynch, C. J., Palopoli, M., Deiter, G., Stanley, B. A., & Vary, T. C. (2010). Impact of Chronic Alcohol Ingestion on Cardiac Muscle Protein Expression. Alcoholism, Clinical & Experimental Research, 34(7), 1226-1234. https://doi.org/10.1111/j.1530-0277.2010.01200.x
- Lang, C. H., & Korzick, D. H. (2014). Chronic alcohol consumption disrupts myocardial protein balance and function in aged, but not adult, female F344 rats. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 306(1), R23-R33. https://doi.org/10.1152/ajpregu.00414.2013
- Guo, W., Kan, J. T., Cheng, Z. Y., Chen, J. F., Shen, Y. Q., Xu, J., Wu, D., & Zhu, Y. Z. (2012). Hydrogen Sulfide as an Endogenous Modulator in Mitochondria and Mitochondria Dysfunction. Oxidative Medicine and Cellular Longevity, 2012, Article 878052. https://doi.org/10.1155/2012/878052
- Kuo, M. M., Kim, D. H., Jandu, S., Bergman, Y., Tan, S., Wang, H., Pandey, D. R., Abraham, T. P., Shoukas, A. A., Berkowitz, D. E., & Santhanam, L. (2016). MPST but not CSE is the primary regulator of hydrogen sulfide production and function in the coronary artery. American Journal of Physiology-Heart and Circulatory Physiology, 310(1), H71-H79. https://doi.org/10.1152/ajpheart.00574.2014
- Luchkova, A. Yu., Hoshovska, Yu. V., Fedichkina, R. A., Strutynska, N. A., & Sagach, V. F. (2017). Pryhnichennia mitokhondrialnoho shliakhu syntezu sirkovodniu pohirshuie skorotlyvu funktsiiu sertsia ta pidvyshchuie chutlyvist mitokhondrialnoi pory do Sa2+ u sertsi shchuriv [Inhibition of mitochondrial H2S synthesis depresses heart function and increases sensitivity of mitochondril pore to calcium load]. Fiziolohichnyi zhurnal, 63(4), 3-9. https://doi.org/10.15407/fz63.04.003 [in Ukrainian].
- Murphy, B., Bhattacharya, R., & Mukherjee, P. (2019). Hydrogen sulfide signaling in mitochondria and disease. FASEB Journal, 33(12), 13098-13125. https://doi.org/10.1096/fj.201901304R
- Zaichko, N. V., Melnik, A. V., Yoltukhivskyy, M. M., Olhovskiy, A. S., & Palamarchuk, I. V. (2014). Hydrogen sulfide: metabolism, biological and medical role. Ukrainian Biochemical Journal, 86(5), 5-25. https://doi.org/10.15407/ubj86.05.005
- Kimura, H. (2014). Production and Physiological Effects of Hydrogen Sulfide. Antioxidants & Redox Signaling, 20(5), 783-793. https://doi.org/10.1089/ars.2013.5309
- Łowicka, E., & Bełtowski, J. (2007). Hydrogen sulfide (H2S) - the third gas of interest for pharmacologists. Pharmacological Reports, 59(1), 4-24. http://if-pan.krakow.pl/pjp/pdf/2007/1_4.pdf
- Feliers, D., Lee, H. J., & Kasinath, B. S. (2016). Hydrogen Sulfide in Renal Physiology and Disease. Antioxidants & Redox Signaling, 25(13), 720-731. https://doi.org/10.1089/ars.2015.6596
- Wu, D., Hu, Q., & Zhu, D. (2018). An Update on Hydrogen Sulfide and Nitric Oxide Interactions in the Cardiovascular System. Oxidative Medicine and Cellular Longevity, 2018, Article 4579140. https://doi.org/10.1155/2018/4579140
- Calvert, J. W., Coetzee, W. A., & Lefer, D. J. (2010). Novel Insights Into Hydrogen Sulfide - Mediated Cytoprotection. Antioxidants & Redox Signaling, 12(10), 1203-1217. https://doi.org/10.1089/ars.2009.2882
- Papapetropoulos, A., Pyriochou, A., Altaany, Z., Yang, G., Marazioti, A., Zhou, Z., Jeschke, M. G., Branski, L. K., Herndon, D. N., Wang, R., & Szabó, C. (2009). Hydrogen sulfide is an endogenous stimulator of angiogenesis. PNAS, 106(51), 21972-21977. https://doi.org/10.1073/pnas.0908047106
- Palamarchuk, I. V., Strutynska, O. B., Melnyk, A. V., & Zaichko, N. V. (2020). Vplyv metforminu ta yoho poiednannia z natrii hidrohensulfidom na stan systemy H2S ta asotsiiovani biokhimichni porushennia v miokardi ta nyrkakh shchuriv za streptozototsyn-indukovanoho diabetu [Influence of metformin and its combination with sodium hydrogen sulphide on H2S system and associated biochemical disorders in myocardium and kidney of rats with streptozotocininduced diabetes]. Visnyk problem biolohii i medytsyny, (3), 133-137. https://doi.org/10.29254/2077-4214-2020-3-157-133-137 [in Ukrainian].
- Kang, S. C., Sohn, E. H., & Lee, S. R. (2020). Hydrogen Sulfide as a Potential Alternative for the Treatment of Myocardial Fibrosis. Oxidative Medicine and Cellular Longevity, 2020, Article 4105382. https://doi.org/10.1155/2020/4105382
- Li, N., Wang, M. J., Jin, S., Bai, Y. D., Hou, C. L., Ma, F. F., Li, X. H., & Zhu, Y. C. (2016). The H2S Donor NaHS Changes the Expression Pattern of H2S-Producing Enzymes after Myocardial Infarction. Oxidative Medicine and Cellular Longevity, 2016, Article 6492469. https://doi.org/10.1155/2016/6492469
- Melnyk, A. V., Zaichko, N. V., Khodakovskyi, O. A., & Khodakivska, O. V. (2018). Statevi osoblyvosti vplyvu sirkovodniu na perebih ishemii-reperfuzii v miokardi shchuriv [Sex characteristics of hydrogen sulfide influence on ischemiareperfsion in miocardium of rats]. Fiziolohichnyi zhurnal, 64(1), 40-46. https://doi.org/10.15407/fz64.01.040 [in Ukrainian].
- Wang, R., Szabo, C., Ichinose, F., Ahmed, A., Whiteman, M., & Papapetropoulos, A. (2015). The role of H2S bioavailability in endothelial dysfunction. Trends in Pharmacological Sciences, 36(9), 568-578. https://doi.org/10.1016/j.tips.2015.05.007
- Sanchez-Aranguren, L. C., Ahmad, S., Dias, I., Alzahrani, F. A., Rezai, H., Wang, K., & Ahmed, A. (2020). Bioenergetic effects of hydrogen sulfide suppress soluble Flt-1 and soluble endoglin in cystathionine gamma-lyase compromised endothelial cells. Scientific Reports, 10(1), Article 15810. https://doi.org/10.1038/s41598-020-72371-2
- Altaany, Z., Yang, G., & Wang, R. (2013). Crosstalk between hydrogen sulfide and nitric oxide in endothelial cells. Journal of Cellular and Molecular Medicine, 17(7), 879-888. https://doi.org/10.1111/jcmm.12077
- Benetti, L. R., Campos, D., Gurgueira, S. A., Vercesi, A. E., Guedes, C. E., Santos, K. L., Wallace, J. L., Teixeira, S. A., Florenzano, J., Costa, S. K., Muscará, M. N., & Ferreira, H. H. (2013). Hydrogen sulfide inhibits oxidative stress in lungs from allergic mice in vivo. European Journal of Pharmacology, 698(1-3), 463-469. https://doi.org/10.1016/j.ejphar.2012.11.025
- Bir, S. C., Kolluru, G. K., McCarthy, P., Shen, X., Pardue, S., Pattillo, C. B., & Kevil, C. G. (2012). Hydrogen Sulfide Stimulates Ischemic Vascular Remodeling Through Nitric Oxide Synthase and Nitrite Reduction Activity Regulating Hypoxia-Inducible Factor‐1α and Vascular Endothelial Growth Factor-Dependent Angiogenesis. Journal of the American Heart Association, 1(5), Article e004093. https://doi.org/10.1161/JAHA.112.004093
- Kolluru, G. K., Yuan, S., Shen, X., & Kevil, C. G. (2015). Chapter Fifteen - H2S Regulation of Nitric Oxide Metabolism. Methods in Enzymology, 554, 271-297. https://doi.org/10.1016/bs.mie.2014.11.040
- Cortese-Krott, M. M., Fernandez, B. O., Santos, J. L., Mergia, E., Grman, M., Nagy, P., Kelm, M., Butler, A., & Feelisch, M. (2014). Nitrosopersulfide (SSNOˉ) accounts for sustained NO bioactivity of S-nitrosothiols following reaction with sulfide. Redox Biology, 2, 234-244. https://doi.org/10.1016/j.redox.2013.12.031
- Wang, Y., Zhao, X., Jin, H., Wei, H., Li, W., Bu, D., Tang, X., Ren, Y., Tang, C., & Du, J. (2009). Role of Hydrogen Sulfide in the Development of Atherosclerotic Lesions in Apolipoprotein E Knockout Mice. Arteriosclerosis, Thrombosis, and Vascular Biology, 29(2), 173-179. https://doi.org/10.1161/ATVBAHA.108.179333
- Kar, S., Kambis, T. N., & Mishra, P. K. (2019). Hydrogen sulfide-mediated regulation of cell death signaling ameliorates adverse cardiac remodeling and diabetic cardiomyopathy. American Journal of Physiology - Heart and Circulatory Physiology, 316(6), H1237-H1252. https://doi.org/10.1152/ajpheart.00004.2019
- Gorini, F., Bustaffa, E., Chatzianagnostou, K., Bianchi, F., & Vassalle, C. (2020). Hydrogen sulfide and cardiovascular disease: Doubts, clues, and interpretation difficulties from studies in geothermal areas. Science of The Total Environment, 743, Article 140818. https://doi.org/10.1016/j.scitotenv.2020.140818
- Zheng, Y., Ji, X., Ji, K., & Wang, B. (2015). Hydrogen sulfide prodrugs - a review. Acta Pharmaceutica Sinica B, 5(5), 367-377. https://doi.org/10.1016/j.apsb.2015.06.004
- Corvino, A., Frecentese, F., Magli, E., Perissutti, E., Santagada, V., Scognamiglio, A., Caliendo, G., Fiorino, F., & Severino, B. (2021). Trends in H2S-Donors Chemistry and Their Effects in Cardiovascular Diseases. Antioxidants, 10(3), Article 429. https://doi.org/10.3390/antiox10030429
- Benavides, G. A., Squadrito, G. L., Mills, R. W., Patel, H. D., Isbell, T. S., Patel, R. P., Darley-Usmar, V. M., Doeller, J. E., & Kraus, D. W. (2007). Hydrogen sulfide mediates the vasoactivity of garlic. PNAS, 104(46), 17977-17982. https://doi.org/10.1073/pnas.0705710104
- Li, L., Whiteman, M., Guan, Y. Y., Neo, K. L., Cheng, Y., Lee, S. W., Zhao, Y., Baskar, R., Tan, C. H., & Moore, P. K. (2008). Characterization of a Novel, Water-Soluble Hydrogen Sulfide-Releasing Molecule (GYY4137): New Insights Into the Biology of Hydrogen Sulfide. Circulation, 117(18), 2351-2360. https://doi.org/10.1161/CIRCULATIONAHA.107.753467
- Rose, P., Dymock, B. W., & Moore, P. K. (2015). Chapter Nine - GYY4137, a Novel Water-Soluble, H2S-Releasing Molecule. Methods in Enzymology, 554, 143-167. https://doi.org/10.1016/bs.mie.2014.11.014
- Yuan, S., Shen, X., & Kevil, C. G. (2017). Beyond a Gasotransmitter: Hydrogen Sulfide and Polysulfide in Cardiovascular Health and Immune Response. Antioxidants & Redox Signaling, 27(10), 634-653. https://doi.org/10.1089/ars.2017.7096
- Zhao, Y., Wang, H., & Xian, M. (2011). Cysteine-Activated Hydrogen Sulfide (H2S) Donors. Journal of the American Chemical Society, 133(1), 15-17. https://doi.org/10.1021/ja1085723
- Roger, T., Raynaud, F., Bouillaud, F., Ransy, C., Simonet, S., Crespo, C., Bourguignon, M. P., Villeneuve, N., Vilaine, J. P., Artaud, I., & Galardon, E. (2013). New Biologically Active Hydrogen Sulfide Donors. Chembiochem, 14(17), 2268-2271. https://doi.org/10.1002/cbic.201300552
- Martelli, A., Testai, L., Citi, V., Marino, A., Pugliesi, I., Barresi, E., Nesi, G., Rapposelli, S., Taliani, S., Da Settimo, F., Breschi, M. C., & Calderone, V. (2013). Arylthioamides as H2S Donors: L-Cysteine-Activated Releasing Properties and Vascular Effects in Vitro and in Vivo. ACS Medicinal Chemistry Letters, 4(10), 904-908. https://doi.org/10.1021/ml400239a
- Barresi, E., Nesi, G., Citi, V., Piragine, E., Piano, I., Taliani, S., Da Settimo, F., Rapposelli, S., Testai, L., Breschi, M. C., Gargini, C., Calderone, V., & Martelli, A. (2017). Iminothioethers as Hydrogen Sulfide Donors: From the Gasotransmitter Release to the Vascular Effects. Journal of Medicinal Chemistry, 60(17), 7512-7523. https://doi.org/10.1021/acs.jmedchem.7b00888
- Mitidieri, E., Tramontano, T., Gurgone, D., Citi, V., Calderone, V., Brancaleone, V., Katsouda, A., Nagahara, N., Papapetropoulos, A., Cirino, G., d'Emmanuele di Villa Bianca, R., & Sorrentino, R. (2018). Mercaptopyruvate acts as endogenous vasodilator independently of 3-mercaptopyruvate sulfurtransferase activity. Nitric Oxide, 75, 53-59. https://doi.org/10.1016/j.niox.2018.02.003
- Ercolano, G., De Cicco, P., Frecentese, F., Saccone, I., Corvino, A., Giordano, F., Magli, E., Fiorino, F., Severino, B., Calderone, V., Citi, V., Cirino, G., & Ianaro, A. (2019). Anti-metastatic Properties of Naproxen-HBTA in a Murine Model of Cutaneous Melanoma. Frontiers in Pharmacology, 10, Article 66. https://doi.org/10.3389/fphar.2019.00066
- Martelli, A., Testai, L., Citi, V., Marino, A., Bellagambi, F. G., Ghimenti, S., Breschi, M. C., & Calderone, V. (2014). Pharmacological characterization of the vascular effects of aryl isothiocyanates: Is hydrogen sulfide the real player? Vascular Pharmacology, 60(1), 32-41. https://doi.org/10.1016/j.vph.2013.11.003
- Citi, V., Corvino, A., Fiorino, F., Frecentese, F., Magli, E., Perissutti, E., Santagada, V., Brogi, S., Flori, L., Gorica, E., Testai, L., Martelli, A., Calderone, V., Caliendo, G., & Severino, B. (2020). Structure-activity relationships study of isothiocyanates for H2S releasing properties: 3-Pyridyl-isothiocyanate as a new promising cardioprotective agent. Journal of Advanced Research, 27, 41-53. https://doi.org/10.1016/j.jare.2020.02.017
- Zhao, Y., Steiger, A. K., & Pluth, M. D. (2019). Cyclic Sulfenyl Thiocarbamates Release Carbonyl Sulfide and Hydrogen Sulfide Independently in Thiol-Promoted Pathways. Journal of the American Chemical Society, 141(34), 13610-13618. https://doi.org/10.1021/jacs.9b06319
- Wu, D., Hu, Q., Ma, F., & Zhu, Y. Z. (2016). Vasorelaxant Effect of a New Hydrogen Sulfide-Nitric Oxide Conjugated Donor in Isolated Rat Aortic Rings through cGMP Pathway. Oxidative Medicine and Cellular Longevity, 2016, Article 7075682. https://doi.org/10.1155/2016/7075682
- Rossoni, G., Manfredi, B., Tazzari, V., Sparatore, A., Trivulzio, S., Del Soldato, P., & Berti, F. (2010). Activity of a new hydrogen sulfide-releasing aspirin (ACS14) on pathological cardiovascular alterations induced by glutathione depletion in rats. European Journal of Pharmacology, 648(1-3), 139-145. https://doi.org/10.1016/j.ejphar.2010.08.039
- Karwi, Q. G., Bornbaum, J., Boengler, K., Torregrossa, R., Whiteman, M., Wood, M. E., Schulz, R., & Baxter, G. F. (2017). AP39, a mitochondria-targeting hydrogen sulfide (H2S) donor, protects against myocardial reperfusion injury independently of salvage kinase signalling. British Journal of Pharmacology, 174(4), 287-301. https://doi.org/10.1111/bph.13688
- Polhemus, D. J., Li, Z., Pattillo, C. B., Gojon, G., Sr, Gojon, G., Jr, Giordano, T., & Krum, H. (2015). A Novel Hydrogen Sulfide Prodrug, SG1002, Promotes Hydrogen Sulfide and Nitric Oxide Bioavailability in Heart Failure Patients. Cardiovascular Therapeutics, 33(4), 216-226. https://doi.org/10.1111/1755-5922.12128
- Liang, B., Xiao, T., Long, J., Liu, M., Li, Z., Liu, S., & Yang, J. (2017). Hydrogen sulfide alleviates myocardial fibrosis in mice with alcoholic cardiomyopathy by downregulating autophagy. International Journal of Molecular Medicine, 40(6), 1781-1791. https://doi.org/10.3892/ijmm.2017.3191
- Wiliński, B., Wiliński, J., Somogyi, E., Góralska, M., & Piotrowska, J. (2010). Ramipril Affects Hydrogen Sulfide Generation in Mouse Liver and Kidney. Folia Biologica, 58(3-4), 177-180. https://doi.org/10.3409/fb58_3-4.177-180
- Xu, Y., Du, H. P., Li, J., Xu, R., Wang, Y. L., You, S. J., Liu, H., Wang, F., Cao, Y. J., Liu, C. F., & Hu, L. F. (2014). Statins upregulate cystathionine γ-lyase transcription and H2S generation via activating Akt signaling in macrophage. Pharmacological Research, 87, 18-25. https://doi.org/10.1016/j.phrs.2014.06.006
- Wiliński, B., Wiliński, J., Somogyi, E., Piotrowska, J., & Góralska, M. (2011). Digoxin increases hydrogen sulfide concentrations in brain, heart and kidney tissues in mice. Pharmacological Reports, 63(5), 1243-1247. https://doi.org/10.1016/s1734-1140(11)70645-4
- Ma, X., Jiang, Z., Wang, Z., & Zhang, Z. (2020). Administration of metformin alleviates atherosclerosis by promoting H2S production via regulating CSE expression. Journal of Cellular Physiology, 235(3), 2102-2112. https://doi.org/10.1002/jcp.29112
- Zhang, J., Zhang, Q., Wang, Y., Li, J., Bai, Z., Zhao, Q., Wang, Z., He, D., Zhang, J., & Chen, Y. (2019). Toxicities and beneficial protection of H2S donors based on nonsteroidal anti-inflammatory drugs. MedChemComm, 10(5), 742-756. https://doi.org/10.1039/c8md00611c
- Bielenichev, I. F., Vizir, V. A., Mamchur, V. Yo., & Kuriata, O. V. (2019). Mesto tiotriazolina v galeree sovremennykh metabolitotropnykh lekarstvennykh sredstv [Place of tiotriazoline in the gallery of modern metabolitotropic medicines]. Zaporozhye medical journal, 21(1), 118-128. https://doi.org/10.14739/2310-1210.2019.1.155856 [in Russian].
- Mazur, I. A., Chekman, I. S., Belenichev, I. F., Voloshin, N. A., Gorchakova, N. A., & Kucherenko, L. I. (2007). Metabolitotropnye preparaty [Metabolitotropic drugs]. Zaporozhye. [in Russian].
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