Research progress on role of hydrogen sulfide in liver diseases_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

SONG Shuxian , ZHANG Yuqing , LI Yundong , LI Kuan , PA Chengzhou ,  GAO Hongqiang

Department of Hepatobiliary Pancreatic Surgery, The First People’s Hospital of Kunming / The Affiliated Calmette Hospital of Kunming Medical University, Kunming 650100, P. R. China;

Corresponding author：

GAO Hongqiang, Email: 13708466595@163.com

Keywords：

hydrogen sulfide; liver ischemia-reperfusion injury; liver cirrhosis; nonalcoholic fatty liver disease; hepatocellular carcinoma; liver transplantation

DOI：

10.7507/1007-9424.202409011

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the progress in research on the role of hydrogen sulfide (H₂S) in liver diseases. Method The relevant literature at home and abroad in recent years was searched and reviewed. Results The H₂S played an important role in the occurrence and development of the liver diseases through anti-oxidative stress, anti-inflammation, regulation of autophagy, endoplasmic reticulum stress, angiogenesis, cell death, and other mechanisms. However, the relevant mechanisms are still controversial. Future studies needed to deeply explore the specific role of H₂S in the different liver diseases, and how to accurately control its level in vivo and achieve targeted drug administration. Conclusions The concentration of H₂S in vivo can be regulated by supplementing exogenous H₂S, adjusting intestinal microbiota or inhibiting key enzymes of H₂S synthesis, which provides a new strategy for the treatment of liver diseases. However, the relevant mechanisms are still controversial, and future research needs to delve into the specific role of H₂S in different liver diseases, as well as how to precisely control its levels in vivo and achieve targeted drug delivery.

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2.	Younossi ZM, Kalligeros M, Henry L. Epidemiology of metabolic dysfunction-associated steatotic liver disease. Clin Mol Hepatol, 2024 Aug 19. doi: 10.3350/cmh.2024.0431. Online ahead of print.
3.	Wang R. Two’s company, three’s a crowd: can H₂S be the third endogenous gaseous transmitter?. FASEB J, 2002, 16(13): 1792-1798.
4.	Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov, 2015, 14(5): 329-345.
5.	Munteanu C, Turnea MA, Rotariu M. Hydrogen sulfide: An emerging regulator of oxidative stress and cellular homeostasis—A comprehensive one-year review. Antioxidants (Basel), 2023, 12(9): 1737. doi: 10.3390/antiox12091737.
6.	Pandey T, Pandey V. Hydrogen sulfide (H₂S) metabolism: Unraveling cellular regulation, disease implications, and therapeutic prospects for precision medicine. Nitric Oxide, 2024, 144: 20-28.
7.	Sun HJ, Wu ZY, Nie XW, et al. Implications of hydrogen sulfide in liver pathophysiology: Mechanistic insights and therapeutic potential. J Adv Res, 2020, 27: 127-135.
8.	Nguyen TTP, Nguyen PL, Park SH, et al. Hydrogen sulfide and liver health: Insights into liver diseases. Antioxid Redox Signal, 2024, 40(1-3): 122-144.
9.	徐文静. 肝脏内源性硫化氢代谢和功能. 生命的化学, 2020, 40(8): 1289-1297.
10.	Jeitner TM, Azcona JA, Ables GP, et al. Cystine rather than cysteine is the preferred substrate for β-elimination by cystathionine γ-lyase: implications for dietary methionine restriction. Geroscience, 2024, 46(4): 3617-3634.
11.	Kabil O, Vitvitsky V, Xie P, et al. The quantitative significance of the transsulfuration enzymes for H₂S production in murine tissues. Antioxid Redox Signal, 2011, 15(2): 363-372.
12.	Kabil O, Banerjee R. Enzymology of H₂S biogenesis, decay and signaling. Antioxid Redox Signal, 2014, 20(5): 770-782.
13.	Hao Y, Hao Z, Zeng X, et al. Gut microbiota and metabolites of cirrhotic portal hypertension: a novel target on the therapeutic regulation. J Gastroenterol, 2024, 59(9): 788-797.
14.	Li X, Jiang K, Ruan Y, et al. Hydrogen sulfide and its donors: Keys to unlock the chains of nonalcoholic fatty liver disease. Int J Mol Sci, 2022, 23(20): 12202. doi: 10.3390/ijms232012202.
15.	Sun X, Wu S, Mao C, et al. Therapeutic potential of hydrogen sulfide in ischemia and reperfusion injury. Biomolecules, 2024, 14(7): 740. doi: 10.3390/biom14070740.
16.	Lin X, Zhou Y, Ye L, et al. A bibliometric and visualized analysis of hepatic ischemia-reperfusion injury (HIRI) from 2002 to 2021. Heliyon, 2023, 9(11): e22644. doi: 10.1016/j.heliyon.2023.e22644.
17.	Yang F, Gao H, Niu Z, et al. Puerarin protects the fatty liver from ischemia-reperfusion injury by regulating the PI3K/AKT signaling pathway. Braz J Med Biol Res, 2024, 57: e13229. doi: 10.1590/1414-431X2024e13229.
18.	Dugbartey GJ. Cellular and molecular mechanisms of cell damage and cell death in ischemia-reperfusion injury in organ transplantation. Mol Biol Rep, 2024, 51(1): 473. doi: 10.1007/s11033-024-09261-7.
19.	Tang SP, Mao XL, Chen YH, et al. Reactive oxygen species induce fatty liver and ischemia-reperfusion injury by promoting inflammation and cell death. Front Immunol, 2022, 13: 870239. doi: 10.3389/fimmu.2022.870239.
20.	Press AT, Ungelenk L, Medyukhina A, et al. Sodium thiosulfate refuels the hepatic antioxidant pool reducing ischemia-reperfusion-induced liver injury. Free Radic Biol Med, 2023, 204: 151-160.
21.	Zhao S, Song T, Gu Y, et al. Hydrogen sulfide alleviates liver injury through the S-sulfhydrated-kelch-like ECH-associated protein 1/nuclear erythroid 2-related factor 2/low-density lipoprotein receptor-related protein 1 pathway. Hepatology, 2021, 73(1): 282-302.
22.	Bos EM, Snijder PM, Jekel H, et al. Beneficial effects of gaseous hydrogen sulfide in hepatic ischemia/reperfusion injury. Transpl Int, 2012, 25(8): 897-908.
23.	Ruan Z, Liang M, Deng X, et al. Exogenous hydrogen sulfide protects fatty liver against ischemia-reperfusion injury by regulating endoplasmic reticulum stress-induced autophagy in macrophage through mediating the class A scavenger receptor pathway in rats. Cell Biol Int, 2020, 44(1): 306-316.
24.	Cheng P, Wang F, Chen K, et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm, 2014, 2014: 935251. doi: 10.1155/2014/935251.
25.	Wu D, Wang H, Teng T, et al. Hydrogen sulfide and autophagy: A double edged sword. Pharmacol Res, 2018, 131: 120-127.
26.	Rinella ME, Lazarus JV, Ratziu V, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology, 2023, 78(6): 1966-1986.
27.	Peh MT, Anwar AB, Ng DS, et al. Effect of feeding a high fat diet on hydrogen sulfide (H₂S) metabolism in the mouse. Nitric Oxide, 2014, 41: 138-145.
28.	Xu W, Cui C, Cui C, et al. Hepatocellular cystathionine γ lyase/hydrogen sulfide attenuates nonalcoholic fatty liver disease by activating farnesoid X receptor. Hepatology, 2022, 76(6): 1794-1810.
29.	Li M, Xu C, Shi J, et al. Fatty acids promote fatty liver disease via the dysregulation of 3-mercaptopyruvate sulfurtransferase/hydrogen sulfide pathway. Gut, 2018, 67(12): 2169-2180.
30.	Sun L, Zhang S, Yu C, et al. Hydrogen sulfide reduces serum triglyceride by activating liver autophagy via the AMPK-mTOR pathway. Am J Physiol Endocrinol Metab, 2015, 309(11): E925-E935. doi: 10.1152/ajpendo.00294.2015.
31.	Wu D, Zhong P, Wang Y, et al. Hydrogen sulfide attenuates high-fat diet-induced non-alcoholic fatty liver disease by inhibiting apoptosis and promoting autophagy via reactive oxygen species/phosphatidylinositol 3-kinase/AKT/mammalian target of rapamycin signaling pathway. Front Pharmacol, 2020, 11: 585860. doi: 10.3389/fphar.2020.585860.
32.	Grewal T, Buechler C. Emerging insights on the diverse roles of proprotein convertase subtilisin/kexin type 9 (PCSK9) in chronic liver diseases: Cholesterol metabolism and beyond. Int J Mol Sci, 2022, 23(3): 1070. doi: 10.3390/ijms23031070.
33.	Cui X, Yao M, Feng Y, et al. Exogenous hydrogen sulfide alleviates hepatic endoplasmic reticulum stress via SIRT1/FoxO1/PCSK9 pathway in NAFLD. FASEB J, 2023, 37(8): e23027. doi: 10.1096/fj.202201705RR.
34.	Ci L, Yang X, Gu X, et al. Cystathionine γ-lyase deficiency exacerbates CCl4-induced acute hepatitis and fibrosis in the mouse liver. Antioxid Redox Signal, 2017, 27(3): 133-149.
35.	Zhang F, Jin H, Wu L, et al. Diallyl trisulfide suppresses oxidative stress-induced activation of hepatic stellate cells through production of hydrogen sulfide. Oxid Med Cell Longev, 2017, 2017: 1406726. doi: 10.1155/2017/1406726.
36.	Damba T, Zhang M, Buist-Homan M, et al. Hydrogen sulfide stimulates activation of hepatic stellate cells through increased cellular bio-energetics. Nitric Oxide, 2019, 92: 26-33.
37.	杜少严, 尹硕, 郝文洋, 等. 硫化氢在肝脏疾病中的研究进展. 临床荟萃, 2019, 34(12): 1127-1130.
38.	Lu G, Zhang Y, Ren Y, et al. Diversity and comparison of intestinal desulfovibrio in patients with liver cirrhosis and healthy people. Microorganisms, 2023, 11(2): 276. doi: 10.3390/microorganisms11020276.
39.	郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
40.	Oza PP, Kashfi K. The triple crown: NO, CO, and H₂S in cancer cell biology. Pharmacol Ther, 2023, 249: 108502. doi: 10.1016/j.pharmthera.2023.108502.
41.	Lu S, Gao Y, Huang X, et al. GYY4137, a hydrogen sulfide (H₂S) donor, shows potent anti-hepatocellular carcinoma activity through blocking the STAT3 pathway. Int J Oncol, 2014, 44(4): 1259-1267.
42.	Pan Y, Ye S, Yuan D, et al. Hydrogen sulfide (H₂S)/cystathionine γ-lyase (CSE) pathway contributes to the proliferation of hepatoma cells. Mutat Res, 2014, 763-764: 10-18.
43.	Zhou YF, Song SS, Tian MX, et al. Cystathionine β-synthase mediated PRRX2/IL-6/STAT3 inactivation suppresses Tregs infiltration and induces apoptosis to inhibit HCC carcinogenesis. J Immunother Cancer, 2021, 9(8): e003031. doi: 10.1136/jitc-2021-003031.
44.	Li M, Song X, Jin Q, et al. 3-Mercaptopyruvate sulfurtransferase represses tumour progression and predicts prognosis in hepatocellular carcinoma. Liver Int, 2022, 42(5): 1173-1184.
45.	Wang SS, Chen YH, Chen N, et al. Hydrogen sulfide promotes autophagy of hepatocellular carcinoma cells through the PI3K/Akt/mTOR signaling pathway. Cell Death Dis, 2017, 8(3): e2688. doi: 10.1038/cddis.2017.18.
46.	Wu D, Li M, Tian W, et al. Hydrogen sulfide acts as a double-edged sword in human hepatocellular carcinoma cells through EGFR/ERK/MMP-2 and PTEN/AKT signaling pathways. Sci Rep, 2017, 7(1): 5134. doi: 10.1038/s41598-017-05457-z.
47.	Yu M, Yu H, Wang H, et al. Tumor-associated macrophages activated in the tumor environment of hepatocellular carcinoma: Characterization and treatment (Review). Int J Oncol, 2024, 65(4): 100. doi: 10.3892/ijo.2024.5688.
48.	He Z, Zhu Y, Ma H, et al. Hydrogen sulfide regulates macrophage polarization and necroptosis to accelerate diabetic skin wound healing. Int Immunopharmacol, 2024, 132: 111990. doi: 10.1016/j.intimp.2024.111990.
49.	Ito T, Naini BV, Markovic D, et al. Ischemia-reperfusion injury and its relationship with early allograft dysfunction in liver transplant patients. Am J Transplant, 2021, 21(2): 614-625.
50.	Guo Z, Zhao Q, Jia Z, et al. A randomized-controlled trial of ischemia-free liver transplantation for end-stage liver disease. J Hepatol, 2023, 79(2): 394-402.
51.	Wang S, Lin X, Tang Y, et al. Ischemia-free liver transplantation improves the prognosis of recipients using functionally marginal liver grafts. Clin Mol Hepatol, 2024, 30(3): 421-435.
52.	McLean ST, Holkup S, Tchir A, et al. UW supplementation with AP39 improves liver viability following static cold storage. Res Sq, 2024 Jun 11: rs. 3. rs-4487319. doi: 10.21203/rs.3.rs-4487319/v1.
53.	Zhang MY, Dugbartey GJ, Juriasingani S, et al. Sodium thiosulfate-supplemented UW solution protects renal grafts against prolonged cold ischemia-reperfusion injury in a murine model of syngeneic kidney transplantation. Biomed Pharmacother, 2022, 145: 112435. doi: 10.1016/j.biopha.2021.112435.
54.	Balaban CL, Rodríguez JV, Tiribelli C, et al. The effect of a hydrogen sulfide releasing molecule (Na₂S) on the cold storage of livers from cardiac dead donor rats. A study in an ex vivo model. Cryobiology, 2015, 71(1): 24-32.
55.	Dugbartey GJ, Juriasingani S, Zhang MY, et al. H₂S donor molecules against cold ischemia-reperfusion injury in preclinical models of solid organ transplantation. Pharmacol Res, 2021, 172: 105842. doi: 10.1016/j.phrs.2021.105842.
56.	Zapolski T, Kornecki W, Jaroszyński A. The influence of balneotherapy using salty sulfide-hydrogen sulfide water on selected markers of the cardiovascular system: A prospective study. J Clin Med, 2024, 13(12): 3526. doi: 10.3390/jcm13123526.
57.	申欣欣, 张奕华, 黄张建. 硫化氢供体分子研究进展. 中国药科大学学报, 2019, 50(3): 265-273.
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1. Wu Z, Xia F, Wang W, et al. Worldwide burden of liver cancer across childhood and adolescence, 2000–2021: a systematic analysis of the Global Burden of Disease Study 2021. EClinicalMedicine, 2024, 75: 102765. doi: 10.1016/j.eclinm.2024.102765.
2. Younossi ZM, Kalligeros M, Henry L. Epidemiology of metabolic dysfunction-associated steatotic liver disease. Clin Mol Hepatol, 2024 Aug 19. doi: 10.3350/cmh.2024.0431. Online ahead of print.
3. Wang R. Two’s company, three’s a crowd: can H₂S be the third endogenous gaseous transmitter?. FASEB J, 2002, 16(13): 1792-1798.
4. Wallace JL, Wang R. Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter. Nat Rev Drug Discov, 2015, 14(5): 329-345.
5. Munteanu C, Turnea MA, Rotariu M. Hydrogen sulfide: An emerging regulator of oxidative stress and cellular homeostasis—A comprehensive one-year review. Antioxidants (Basel), 2023, 12(9): 1737. doi: 10.3390/antiox12091737.
6. Pandey T, Pandey V. Hydrogen sulfide (H₂S) metabolism: Unraveling cellular regulation, disease implications, and therapeutic prospects for precision medicine. Nitric Oxide, 2024, 144: 20-28.
7. Sun HJ, Wu ZY, Nie XW, et al. Implications of hydrogen sulfide in liver pathophysiology: Mechanistic insights and therapeutic potential. J Adv Res, 2020, 27: 127-135.
8. Nguyen TTP, Nguyen PL, Park SH, et al. Hydrogen sulfide and liver health: Insights into liver diseases. Antioxid Redox Signal, 2024, 40(1-3): 122-144.
9. 徐文静. 肝脏内源性硫化氢代谢和功能. 生命的化学, 2020, 40(8): 1289-1297.
10. Jeitner TM, Azcona JA, Ables GP, et al. Cystine rather than cysteine is the preferred substrate for β-elimination by cystathionine γ-lyase: implications for dietary methionine restriction. Geroscience, 2024, 46(4): 3617-3634.
11. Kabil O, Vitvitsky V, Xie P, et al. The quantitative significance of the transsulfuration enzymes for H₂S production in murine tissues. Antioxid Redox Signal, 2011, 15(2): 363-372.
12. Kabil O, Banerjee R. Enzymology of H₂S biogenesis, decay and signaling. Antioxid Redox Signal, 2014, 20(5): 770-782.
13. Hao Y, Hao Z, Zeng X, et al. Gut microbiota and metabolites of cirrhotic portal hypertension: a novel target on the therapeutic regulation. J Gastroenterol, 2024, 59(9): 788-797.
14. Li X, Jiang K, Ruan Y, et al. Hydrogen sulfide and its donors: Keys to unlock the chains of nonalcoholic fatty liver disease. Int J Mol Sci, 2022, 23(20): 12202. doi: 10.3390/ijms232012202.
15. Sun X, Wu S, Mao C, et al. Therapeutic potential of hydrogen sulfide in ischemia and reperfusion injury. Biomolecules, 2024, 14(7): 740. doi: 10.3390/biom14070740.
16. Lin X, Zhou Y, Ye L, et al. A bibliometric and visualized analysis of hepatic ischemia-reperfusion injury (HIRI) from 2002 to 2021. Heliyon, 2023, 9(11): e22644. doi: 10.1016/j.heliyon.2023.e22644.
17. Yang F, Gao H, Niu Z, et al. Puerarin protects the fatty liver from ischemia-reperfusion injury by regulating the PI3K/AKT signaling pathway. Braz J Med Biol Res, 2024, 57: e13229. doi: 10.1590/1414-431X2024e13229.
18. Dugbartey GJ. Cellular and molecular mechanisms of cell damage and cell death in ischemia-reperfusion injury in organ transplantation. Mol Biol Rep, 2024, 51(1): 473. doi: 10.1007/s11033-024-09261-7.
19. Tang SP, Mao XL, Chen YH, et al. Reactive oxygen species induce fatty liver and ischemia-reperfusion injury by promoting inflammation and cell death. Front Immunol, 2022, 13: 870239. doi: 10.3389/fimmu.2022.870239.
20. Press AT, Ungelenk L, Medyukhina A, et al. Sodium thiosulfate refuels the hepatic antioxidant pool reducing ischemia-reperfusion-induced liver injury. Free Radic Biol Med, 2023, 204: 151-160.
21. Zhao S, Song T, Gu Y, et al. Hydrogen sulfide alleviates liver injury through the S-sulfhydrated-kelch-like ECH-associated protein 1/nuclear erythroid 2-related factor 2/low-density lipoprotein receptor-related protein 1 pathway. Hepatology, 2021, 73(1): 282-302.
22. Bos EM, Snijder PM, Jekel H, et al. Beneficial effects of gaseous hydrogen sulfide in hepatic ischemia/reperfusion injury. Transpl Int, 2012, 25(8): 897-908.
23. Ruan Z, Liang M, Deng X, et al. Exogenous hydrogen sulfide protects fatty liver against ischemia-reperfusion injury by regulating endoplasmic reticulum stress-induced autophagy in macrophage through mediating the class A scavenger receptor pathway in rats. Cell Biol Int, 2020, 44(1): 306-316.
24. Cheng P, Wang F, Chen K, et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm, 2014, 2014: 935251. doi: 10.1155/2014/935251.
25. Wu D, Wang H, Teng T, et al. Hydrogen sulfide and autophagy: A double edged sword. Pharmacol Res, 2018, 131: 120-127.
26. Rinella ME, Lazarus JV, Ratziu V, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology, 2023, 78(6): 1966-1986.
27. Peh MT, Anwar AB, Ng DS, et al. Effect of feeding a high fat diet on hydrogen sulfide (H₂S) metabolism in the mouse. Nitric Oxide, 2014, 41: 138-145.
28. Xu W, Cui C, Cui C, et al. Hepatocellular cystathionine γ lyase/hydrogen sulfide attenuates nonalcoholic fatty liver disease by activating farnesoid X receptor. Hepatology, 2022, 76(6): 1794-1810.
29. Li M, Xu C, Shi J, et al. Fatty acids promote fatty liver disease via the dysregulation of 3-mercaptopyruvate sulfurtransferase/hydrogen sulfide pathway. Gut, 2018, 67(12): 2169-2180.
30. Sun L, Zhang S, Yu C, et al. Hydrogen sulfide reduces serum triglyceride by activating liver autophagy via the AMPK-mTOR pathway. Am J Physiol Endocrinol Metab, 2015, 309(11): E925-E935. doi: 10.1152/ajpendo.00294.2015.
31. Wu D, Zhong P, Wang Y, et al. Hydrogen sulfide attenuates high-fat diet-induced non-alcoholic fatty liver disease by inhibiting apoptosis and promoting autophagy via reactive oxygen species/phosphatidylinositol 3-kinase/AKT/mammalian target of rapamycin signaling pathway. Front Pharmacol, 2020, 11: 585860. doi: 10.3389/fphar.2020.585860.
32. Grewal T, Buechler C. Emerging insights on the diverse roles of proprotein convertase subtilisin/kexin type 9 (PCSK9) in chronic liver diseases: Cholesterol metabolism and beyond. Int J Mol Sci, 2022, 23(3): 1070. doi: 10.3390/ijms23031070.
33. Cui X, Yao M, Feng Y, et al. Exogenous hydrogen sulfide alleviates hepatic endoplasmic reticulum stress via SIRT1/FoxO1/PCSK9 pathway in NAFLD. FASEB J, 2023, 37(8): e23027. doi: 10.1096/fj.202201705RR.
34. Ci L, Yang X, Gu X, et al. Cystathionine γ-lyase deficiency exacerbates CCl4-induced acute hepatitis and fibrosis in the mouse liver. Antioxid Redox Signal, 2017, 27(3): 133-149.
35. Zhang F, Jin H, Wu L, et al. Diallyl trisulfide suppresses oxidative stress-induced activation of hepatic stellate cells through production of hydrogen sulfide. Oxid Med Cell Longev, 2017, 2017: 1406726. doi: 10.1155/2017/1406726.
36. Damba T, Zhang M, Buist-Homan M, et al. Hydrogen sulfide stimulates activation of hepatic stellate cells through increased cellular bio-energetics. Nitric Oxide, 2019, 92: 26-33.
37. 杜少严, 尹硕, 郝文洋, 等. 硫化氢在肝脏疾病中的研究进展. 临床荟萃, 2019, 34(12): 1127-1130.
38. Lu G, Zhang Y, Ren Y, et al. Diversity and comparison of intestinal desulfovibrio in patients with liver cirrhosis and healthy people. Microorganisms, 2023, 11(2): 276. doi: 10.3390/microorganisms11020276.
39. 郝运, 李川, 文天夫, 等. 全球及中国的肝癌流行病学特征: 基于《2022全球癌症统计报告》解读. 中国普外基础与临床杂志, 2024, 31(7): 781-789.
40. Oza PP, Kashfi K. The triple crown: NO, CO, and H₂S in cancer cell biology. Pharmacol Ther, 2023, 249: 108502. doi: 10.1016/j.pharmthera.2023.108502.
41. Lu S, Gao Y, Huang X, et al. GYY4137, a hydrogen sulfide (H₂S) donor, shows potent anti-hepatocellular carcinoma activity through blocking the STAT3 pathway. Int J Oncol, 2014, 44(4): 1259-1267.
42. Pan Y, Ye S, Yuan D, et al. Hydrogen sulfide (H₂S)/cystathionine γ-lyase (CSE) pathway contributes to the proliferation of hepatoma cells. Mutat Res, 2014, 763-764: 10-18.
43. Zhou YF, Song SS, Tian MX, et al. Cystathionine β-synthase mediated PRRX2/IL-6/STAT3 inactivation suppresses Tregs infiltration and induces apoptosis to inhibit HCC carcinogenesis. J Immunother Cancer, 2021, 9(8): e003031. doi: 10.1136/jitc-2021-003031.
44. Li M, Song X, Jin Q, et al. 3-Mercaptopyruvate sulfurtransferase represses tumour progression and predicts prognosis in hepatocellular carcinoma. Liver Int, 2022, 42(5): 1173-1184.
45. Wang SS, Chen YH, Chen N, et al. Hydrogen sulfide promotes autophagy of hepatocellular carcinoma cells through the PI3K/Akt/mTOR signaling pathway. Cell Death Dis, 2017, 8(3): e2688. doi: 10.1038/cddis.2017.18.
46. Wu D, Li M, Tian W, et al. Hydrogen sulfide acts as a double-edged sword in human hepatocellular carcinoma cells through EGFR/ERK/MMP-2 and PTEN/AKT signaling pathways. Sci Rep, 2017, 7(1): 5134. doi: 10.1038/s41598-017-05457-z.
47. Yu M, Yu H, Wang H, et al. Tumor-associated macrophages activated in the tumor environment of hepatocellular carcinoma: Characterization and treatment (Review). Int J Oncol, 2024, 65(4): 100. doi: 10.3892/ijo.2024.5688.
48. He Z, Zhu Y, Ma H, et al. Hydrogen sulfide regulates macrophage polarization and necroptosis to accelerate diabetic skin wound healing. Int Immunopharmacol, 2024, 132: 111990. doi: 10.1016/j.intimp.2024.111990.
49. Ito T, Naini BV, Markovic D, et al. Ischemia-reperfusion injury and its relationship with early allograft dysfunction in liver transplant patients. Am J Transplant, 2021, 21(2): 614-625.
50. Guo Z, Zhao Q, Jia Z, et al. A randomized-controlled trial of ischemia-free liver transplantation for end-stage liver disease. J Hepatol, 2023, 79(2): 394-402.
51. Wang S, Lin X, Tang Y, et al. Ischemia-free liver transplantation improves the prognosis of recipients using functionally marginal liver grafts. Clin Mol Hepatol, 2024, 30(3): 421-435.
52. McLean ST, Holkup S, Tchir A, et al. UW supplementation with AP39 improves liver viability following static cold storage. Res Sq, 2024 Jun 11: rs. 3. rs-4487319. doi: 10.21203/rs.3.rs-4487319/v1.
53. Zhang MY, Dugbartey GJ, Juriasingani S, et al. Sodium thiosulfate-supplemented UW solution protects renal grafts against prolonged cold ischemia-reperfusion injury in a murine model of syngeneic kidney transplantation. Biomed Pharmacother, 2022, 145: 112435. doi: 10.1016/j.biopha.2021.112435.
54. Balaban CL, Rodríguez JV, Tiribelli C, et al. The effect of a hydrogen sulfide releasing molecule (Na₂S) on the cold storage of livers from cardiac dead donor rats. A study in an ex vivo model. Cryobiology, 2015, 71(1): 24-32.
55. Dugbartey GJ, Juriasingani S, Zhang MY, et al. H₂S donor molecules against cold ischemia-reperfusion injury in preclinical models of solid organ transplantation. Pharmacol Res, 2021, 172: 105842. doi: 10.1016/j.phrs.2021.105842.
56. Zapolski T, Kornecki W, Jaroszyński A. The influence of balneotherapy using salty sulfide-hydrogen sulfide water on selected markers of the cardiovascular system: A prospective study. J Clin Med, 2024, 13(12): 3526. doi: 10.3390/jcm13123526.
57. 申欣欣, 张奕华, 黄张建. 硫化氢供体分子研究进展. 中国药科大学学报, 2019, 50(3): 265-273.
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