Recent Development of the Molecular and Cellular Mechanisms of Hydrogen Sulfide Gasotransmitter
Abstract
:1. Introduction
2. The Direct Target of H2S
2.1. Targeting ROS/RNS and Forming Reactive Species Interactome (RSI)
2.2. Binding to HEME Proteins
2.3. Persulfidation
2.4. NO/CO Feedback Loop
3. H2S Regulates Different Cellular Processes and Functions
3.1. Cell Signaling Pathways
3.1.1. PI3K/Akt Signaling Pathway
3.1.2. NF-κB and MAPK Signaling Pathways
3.2. Tight Junctions
3.3. Autophagy
3.4. Apoptosis
3.5. Vesicle Trafficking: Exocytosis/Endocytosis/Pinocytosis
3.6. Epigenetics
3.7. NLRP3 Inflammasome
3.8. Ion Channels
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
References
- Wang, R. Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol. Rev. 2012, 92, 791–896. [Google Scholar] [CrossRef]
- Reiffenstein, R.J.; Hulbert, W.C.; Roth, S.H. Toxicology of hydrogen sulfide. Annu. Rev. Pharmacol. Toxicol. 1992, 32, 109–134. [Google Scholar] [CrossRef]
- Cirino, G.; Szabo, C.; Papapetropoulos, A. Physiological roles of hydrogen sulfide in mammalian cells, tissues and organs. Physiol. Rev. 2022, in press. [CrossRef]
- Wang, R. Two’s company, three’s a crowd: Can H2S be the third endogenous gaseous transmitter? FASEB J. 2002, 16, 1792–1798. [Google Scholar] [CrossRef]
- Abe, K.; Kimura, H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 1996, 16, 1066–1071. [Google Scholar] [CrossRef] [PubMed]
- Olson, K.R. Are Reactive Sulfur Species the New Reactive Oxygen Species? Antioxid. Redox Signal. 2020, 33, 1125–1142. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Bai, Z.; Zhu, L.; Liang, Y.; Fan, X.; Li, J.; Wen, H.; Shi, T.; Zhao, Q.; Wang, Z. Hydrogen sulfide donors: Therapeutic potential in anti-atherosclerosis. Eur. J. Med. Chem. 2020, 205, 112665. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Biggs, T.D.; Xian, M. Hydrogen sulfide (H2S) releasing agents: Chemistry and biological applications. Chem. Commun. 2014, 50, 11788–11805. [Google Scholar] [CrossRef] [PubMed]
- Powell, C.R.; Dillon, K.M.; Matson, J.B. A review of hydrogen sulfide (H2S) donors: Chemistry and potential therapeutic applications. Biochem. Pharmacol. 2018, 149, 110–123. [Google Scholar] [CrossRef]
- Song, Z.L.; Zhao, L.; Ma, T.; Osama, A.; Shen, T.; He, Y.; Fang, J. Progress and perspective on hydrogen sulfide donors and their biomedical applications. Med. Res. Rev. 2022, 42, 1930–1977. [Google Scholar] [CrossRef]
- Corvino, A.; Frecentese, F.; Magli, E.; Perissutti, E.; Santagada, V.; Scognamiglio, A.; Caliendo, G.; Fiorino, F.; Severino, B. Trends in H2S-Donors Chemistry and Their Effects in Cardiovascular Diseases. Antioxidants 2021, 10, 429. [Google Scholar] [CrossRef] [PubMed]
- 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. Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): New insights into the biology of hydrogen sulfide. Circulation 2008, 117, 2351–2360. [Google Scholar] [CrossRef] [PubMed]
- Lee, Z.W.; Zhou, J.; Chen, C.S.; Zhao, Y.; Tan, C.H.; Li, L.; Moore, P.K.; Deng, L.W. The slow-releasing hydrogen sulfide donor, GYY4137, exhibits novel anti-cancer effects in vitro and in vivo. PLoS ONE 2011, 6, e21077. [Google Scholar] [CrossRef] [PubMed]
- Alexander, B.E.; Coles, S.J.; Fox, B.C.; Khan, T.F.; Maliszewski, J.; Perry, A.; Pitak, M.B.; Whiteman, M.; Wood, M.E. Investigating the generation of hydrogen sulfide from the phosphonamidodithioate slow-release donor GYY4137. Medchemcomm 2015, 6, 1649–1655. [Google Scholar] [CrossRef]
- Ascenção, K.; Szabo, C. Emerging roles of cystathionine β-synthase in various forms of cancer. Redox Biol. 2022, 53, 102331. [Google Scholar] [CrossRef]
- Mishanina, T.V.; Libiad, M.; Banerjee, R. Biogenesis of reactive sulfur species for signaling by hydrogen sulfide oxidation pathways. Nat. Chem. Biol. 2015, 11, 457–464. [Google Scholar] [CrossRef]
- Olson, K.R. H2S and polysulfide metabolism: Conventional and unconventional pathways. Biochem. Pharmacol. 2018, 149, 77–90. [Google Scholar] [CrossRef]
- Sies, H.; Jones, D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 2020, 21, 363–383. [Google Scholar] [CrossRef]
- Adams, L.; Franco, M.C.; Estevez, A.G. Reactive nitrogen species in cellular signaling. Exp. Biol. Med. 2015, 240, 711–717. [Google Scholar] [CrossRef]
- Chen, T.; Tian, M.; Han, Y. Hydrogen sulfide: A multi-tasking signal molecule in the regulation of oxidative stress responses. J. Exp. Bot. 2020, 71, 2862–2869. [Google Scholar] [CrossRef]
- Xie, Z.Z.; Liu, Y.; Bian, J.S. Hydrogen Sulfide and Cellular Redox Homeostasis. Oxidative Med. Cell. Longev. 2016, 2016, 6043038. [Google Scholar] [CrossRef] [PubMed]
- Searcy, D.G.; Whitehead, J.P.; Maroney, M.J. Interaction of Cu, Zn superoxide dismutase with hydrogen sulfide. Arch. Biochem. Biophys. 1995, 318, 251–263. [Google Scholar] [CrossRef] [PubMed]
- Cortese-Krott, M.M.; Koning, A.; Kuhnle, G.G.C.; Nagy, P.; Bianco, C.L.; Pasch, A.; Wink, D.A.; Fukuto, J.M.; Jackson, A.A.; van Goor, H.; et al. The Reactive Species Interactome: Evolutionary Emergence, Biological Significance, and Opportunities for Redox Metabolomics and Personalized Medicine. Antioxid. Redox Signal. 2017, 27, 684–712. [Google Scholar] [CrossRef] [PubMed]
- Ríos-González, B.B.; Román-Morales, E.M.; Pietri, R.; López-Garriga, J. Hydrogen sulfide activation in hemeproteins: The sulfheme scenario. J. Inorg. Biochem. 2014, 133, 78–86. [Google Scholar] [CrossRef] [PubMed]
- Boubeta, F.M.; Bieza, S.A.; Bringas, M.; Palermo, J.C.; Boechi, L.; Estrin, D.A.; Bari, S.E. Hemeproteins as Targets for Sulfide Species. Antioxid. Redox Signal. 2020, 32, 247–257. [Google Scholar] [CrossRef] [PubMed]
- Pietri, R.; Román-Morales, E.; López-Garriga, J. Hydrogen sulfide and hemeproteins: Knowledge and mysteries. Antioxid. Redox Signal. 2011, 15, 393–404. [Google Scholar] [CrossRef] [PubMed]
- Collman, J.P.; Ghosh, S.; Dey, A.; Decréau, R.A. Using a functional enzyme model to understand the chemistry behind hydrogen sulfide induced hibernation. Proc. Natl. Acad. Sci. USA 2009, 106, 22090–22095. [Google Scholar] [CrossRef]
- Filipovic, M.R. Persulfidation (S-sulfhydration) and H2S. Handb. Exp. Pharmacol. 2015, 230, 29–59. [Google Scholar] [CrossRef]
- Filipovic, M.R.; Zivanovic, J.; Alvarez, B.; Banerjee, R. Chemical Biology of H2S Signaling through Persulfidation. Chem. Rev. 2018, 118, 1253–1337. [Google Scholar] [CrossRef]
- Gao, X.H.; Krokowski, D.; Guan, B.J.; Bederman, I.; Majumder, M.; Parisien, M.; Diatchenko, L.; Kabil, O.; Willard, B.; Banerjee, R.; et al. Quantitative H2S-mediated protein sulfhydration reveals metabolic reprogramming during the integrated stress response. eLife 2015, 4, e10067. [Google Scholar] [CrossRef]
- Mustafa, A.K.; Sikka, G.; Gazi, S.K.; Steppan, J.; Jung, S.M.; Bhunia, A.K.; Barodka, V.M.; Gazi, F.K.; Barrow, R.K.; Wang, R.; et al. Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 2011, 109, 1259–1268. [Google Scholar] [CrossRef] [PubMed]
- Krishnan, N.; Fu, C.; Pappin, D.J.; Tonks, N.K. H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response. Sci. Signal. 2011, 4, ra86. [Google Scholar] [CrossRef] [PubMed]
- Jiang, S.; Xu, W.; Chen, Z.; Cui, C.; Fan, X.; Cai, J.; Gong, Y.; Geng, B. Hydrogen sulphide reduces hyperhomocysteinaemia-induced endothelial ER stress by sulfhydrating protein disulphide isomerase to attenuate atherosclerosis. J. Cell. Mol. Med. 2021, 25, 3437–3448. [Google Scholar] [CrossRef] [PubMed]
- Andrew, P.J.; Mayer, B. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 1999, 43, 521–531. [Google Scholar] [CrossRef]
- Altaany, Z.; Ju, Y.; Yang, G.; Wang, R. The coordination of S-sulfhydration, S-nitrosylation, and phosphorylation of endothelial nitric oxide synthase by hydrogen sulfide. Sci. Signal. 2014, 7, ra87. [Google Scholar] [CrossRef]
- Zang, H.; Mathew, R.O.; Cui, T. The Dark Side of Nrf2 in the Heart. Front. Physiol. 2020, 11, 722. [Google Scholar] [CrossRef]
- Yang, G.; Zhao, K.; Ju, Y.; Mani, S.; Cao, Q.; Puukila, S.; Khaper, N.; Wu, L.; Wang, R. Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2. Antioxid. Redox Signal. 2013, 18, 1906–1919. [Google Scholar] [CrossRef]
- Xie, Z.Z.; Shi, M.M.; Xie, L.; Wu, Z.Y.; Li, G.; Hua, F.; Bian, J.S. Sulfhydration of p66Shc at cysteine59 mediates the antioxidant effect of hydrogen sulfide. Antioxid. Redox Signal. 2014, 21, 2531–2542. [Google Scholar] [CrossRef]
- Xie, L.; Gu, Y.; Wen, M.; Zhao, S.; Wang, W.; Ma, Y.; Meng, G.; Han, Y.; Wang, Y.; Liu, G.; et al. Hydrogen Sulfide Induces Keap1 S-sulfhydration and Suppresses Diabetes-Accelerated Atherosclerosis via Nrf2 Activation. Diabetes 2016, 65, 3171–3184. [Google Scholar] [CrossRef]
- Giuffrè, A.; Vicente, J.B. Hydrogen Sulfide Biochemistry and Interplay with Other Gaseous Mediators in Mammalian Physiology. Oxidative Med. Cell. Longev. 2018, 2018, 6290931. [Google Scholar] [CrossRef]
- Hennessy, B.T.; Smith, D.L.; Ram, P.T.; Lu, Y.; Mills, G.B. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat. Rev. Drug. Discov. 2005, 4, 988–1004. [Google Scholar] [CrossRef] [PubMed]
- Manning, B.D.; Toker, A. AKT/PKB Signaling: Navigating the Network. Cell 2017, 169, 381–405. [Google Scholar] [CrossRef] [PubMed]
- Qiu, Y.; Wu, Y.; Meng, M.; Luo, M.; Zhao, H.; Sun, H.; Gao, S. GYY4137 protects against myocardial ischemia/reperfusion injury via activation of the PHLPP-1/Akt/Nrf2 signaling pathway in diabetic mice. J. Surg. Res. 2018, 225, 29–39. [Google Scholar] [CrossRef] [PubMed]
- Karwi, Q.G.; Whiteman, M.; Wood, M.E.; Torregrossa, R.; Baxter, G.F. Pharmacological postconditioning against myocardial infarction with a slow-releasing hydrogen sulfide donor, GYY4137. Pharmacol. Res. 2016, 111, 442–451. [Google Scholar] [CrossRef]
- Xia, Y.Q.; Ning, J.Z.; Cheng, F.; Yu, W.M.; Rao, T.; Ruan, Y.; Yuan, R.; Du, Y. GYY4137 a H2S donor, attenuates ipsilateral epididymis injury in experimentally varicocele-induced rats via activation of the PI3K/Akt pathway. Iran J. Basic Med. Sci. 2019, 22, 729–735. [Google Scholar] [CrossRef]
- Lu, M.; Jiang, X.; Tong, L.; Zhang, F.; Ma, L.; Dong, X.; Sun, X. MicroRNA-21-Regulated Activation of the Akt Pathway Participates in the Protective Effects of H2S against Liver Ischemia-Reperfusion Injury. Biol. Pharm. Bull. 2018, 41, 229–238. [Google Scholar] [CrossRef]
- Tang, B.; Ma, L.; Yao, X.; Tan, G.; Han, P.; Yu, T.; Liu, B.; Sun, X. Hydrogen sulfide ameliorates acute lung injury induced by infrarenal aortic cross-clamping by inhibiting inflammation and angiopoietin 2 release. J. Vasc. Surg. 2017, 65, 501–508.e501. [Google Scholar] [CrossRef]
- Majumder, S.; Ren, L.; Pushpakumar, S.; Sen, U. Hydrogen sulphide mitigates homocysteine-induced apoptosis and matrix remodelling in mesangial cells through Akt/FOXO1 signalling cascade. Cell. Signal. 2019, 61, 66–77. [Google Scholar] [CrossRef]
- Slade, E.; Williams, L.; Gagnon, J. Hydrogen sulfide suppresses ghrelin secretion in vitro and delays postprandial ghrelin secretion while reducing appetite in mice. Physiol. Rep. 2018, 6, e13870. [Google Scholar] [CrossRef]
- Zheng, Y.; Lv, P.; Huang, J.; Ke, J.; Yan, J. GYY4137 exhibits anti-atherosclerosis effect in apolipoprotein E (-/-) mice via PI3K/Akt and TLR4 signalling. Clin. Exp. Pharmacol. Physiol. 2020, 47, 1231–1239. [Google Scholar] [CrossRef]
- Liu, T.; Zhang, L.; Joo, D.; Sun, S.-C. NF-κB signaling in inflammation. Signal Transduct. Target. Ther. 2017, 2, 17023. [Google Scholar] [CrossRef] [PubMed]
- Taniguchi, K.; Karin, M. NF-κB, inflammation, immunity and cancer: Coming of age. Nat. Rev. Immunol. 2018, 18, 309–324. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.J.; Leng, B.; Wu, Z.Y.; Bian, J.S. Polysulfide and Hydrogen Sulfide Ameliorate Cisplatin-Induced Nephrotoxicity and Renal Inflammation through Persulfidating STAT3 and IKKβ. Int. J. Mol. Sci. 2020, 21, 7805. [Google Scholar] [CrossRef] [PubMed]
- Zhuang, R.; Guo, L.; Du, J.; Wang, S.; Li, J.; Liu, Y. Exogenous hydrogen sulfide inhibits oral mucosal wound-induced macrophage activation via the NF-κB pathway. Oral Dis. 2018, 24, 793–801. [Google Scholar] [CrossRef]
- Plotnikov, A.; Zehorai, E.; Procaccia, S.; Seger, R. The MAPK cascades: Signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim. Biophys. Acta 2011, 1813, 1619–1633. [Google Scholar] [CrossRef]
- Alexander, S.P.H.; Mathie, A.; Peters, J.A. Ion Channels. Br. J. Pharmacol. 2011, 164 (Suppl. S1), S137–S174. [Google Scholar] [CrossRef]
- Cao, X.; Xiong, S.; Zhou, Y.; Wu, Z.; Ding, L.; Zhu, Y.; Wood, M.E.; Whiteman, M.; Moore, P.K.; Bian, J.S. Renal Protective Effect of Hydrogen Sulfide in Cisplatin-Induced Nephrotoxicity. Antioxid. Redox Signal. 2018, 29, 455–470. [Google Scholar] [CrossRef]
- Pichette, J.; Fynn-Sackey, N.; Gagnon, J. Hydrogen Sulfide and Sulfate Prebiotic Stimulates the Secretion of GLP-1 and Improves Glycemia in Male Mice. Endocrinology 2017, 158, 3416–3425. [Google Scholar] [CrossRef]
- Peng, Z.; Kellenberger, S. Hydrogen Sulfide Upregulates Acid-sensing Ion Channels via the MAPK-Erk1/2 Signaling Pathway. Function 2021, 2, zqab007. [Google Scholar] [CrossRef]
- Zihni, C.; Mills, C.; Matter, K.; Balda, M.S. Tight junctions: From simple barriers to multifunctional molecular gates. Nat. Rev. Mol. Cell Biol. 2016, 17, 564–580. [Google Scholar] [CrossRef]
- Chen, S.; Bu, D.; Ma, Y.; Zhu, J.; Sun, L.; Zuo, S.; Ma, J.; Li, T.; Chen, Z.; Zheng, Y.; et al. GYY4137 ameliorates intestinal barrier injury in a mouse model of endotoxemia. Biochem. Pharmacol. 2016, 118, 59–67. [Google Scholar] [CrossRef] [PubMed]
- Cui, W.; Chen, J.; Yu, F.; Liu, W.; He, M. GYY4137 protected the integrity of the blood-brain barrier via activation of the Nrf2/ARE pathway in mice with sepsis. FASEB J. 2021, 35, e21710. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Tang, J.; Wang, P.; Zhu, J.; Liu, Y. GYY4137 Attenuates Sodium Deoxycholate-Induced Intestinal Barrier Injury Both In Vitro and In Vivo. Biomed. Res. Int. 2019, 2019, 5752323. [Google Scholar] [CrossRef] [PubMed]
- Zhao, H.; Yan, R.; Zhou, X.; Ji, F.; Zhang, B. Hydrogen sulfide improves colonic barrier integrity in DSS-induced inflammation in Caco-2 cells and mice. Int. Immunopharmacol. 2016, 39, 121–127. [Google Scholar] [CrossRef] [PubMed]
- Dikic, I.; Elazar, Z. Mechanism and medical implications of mammalian autophagy. Nat. Rev. Mol. Cell Biol. 2018, 19, 349–364. [Google Scholar] [CrossRef]
- Zhu, L.; Duan, W.; Wu, G.; Zhang, D.; Wang, L.; Chen, D.; Chen, Z.; Yang, B. Protective effect of hydrogen sulfide on endothelial cells through Sirt1-FoxO1-mediated autophagy. Ann. Transl. Med. 2020, 8, 1586. [Google Scholar] [CrossRef]
- Ni, K.; Hua, Y. Hydrogen sulfide exacerbated periodontal inflammation and induced autophagy in experimental periodontitis. Int. Immunopharmacol. 2021, 93, 107399. [Google Scholar] [CrossRef]
- Yang, F.; Zhang, L.; Gao, Z.; Sun, X.; Yu, M.; Dong, S.; Wu, J.; Zhao, Y.; Xu, C.; Zhang, W.; et al. Exogenous H2S Protects Against Diabetic Cardiomyopathy by Activating Autophagy via the AMPK/mTOR Pathway. Cell. Physiol. Biochem. 2017, 43, 1168–1187. [Google Scholar] [CrossRef]
- Carneiro, B.A.; El-Deiry, W.S. Targeting apoptosis in cancer therapy. Nat. Rev. Clin. Oncol. 2020, 17, 395–417. [Google Scholar] [CrossRef]
- Li, J.; Yuan, Y.Q.; Zhang, L.; Zhang, H.; Zhang, S.W.; Zhang, Y.; Xuan, X.X.; Wang, M.J.; Zhang, J.Y. Exogenous hydrogen sulfide protects against high glucose-induced apoptosis and oxidative stress by inhibiting the STAT3/HIF-1α pathway in H9c2 cardiomyocytes. Exp. Ther. Med. 2019, 18, 3948–3958. [Google Scholar] [CrossRef] [Green Version]
- Garcia, N.A.; Moncayo-Arlandi, J.; Vazquez, A.; Genovés, P.; Calvo, C.J.; Millet, J.; Martí, N.; Aguado, C.; Knecht, E.; Valiente-Alandi, I.; et al. Hydrogen Sulfide Improves Cardiomyocyte Function in a Cardiac Arrest Model. Ann. Transpl. 2017, 22, 285–295. [Google Scholar] [CrossRef] [PubMed]
- Bai, X.; Batallé, G.; Balboni, G.; Pol, O. Hydrogen Sulfide Increases the Analgesic Effects of µ- and δ-Opioid Receptors during Neuropathic Pain: Pathways Implicated. Antioxidants 2022, 11, 1321. [Google Scholar] [CrossRef] [PubMed]
- Jiang, T.; Yang, W.; Zhang, H.; Song, Z.; Liu, T.; Lv, X. Hydrogen Sulfide Ameliorates Lung Ischemia-Reperfusion Injury Through SIRT1 Signaling Pathway in Type 2 Diabetic Rats. Front. Physiol. 2020, 11, 596. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Shi, C.; Liu, Z.; Han, B.; Guo, L.; Zhu, L.; Ye, T. Hydrogen sulfide is a novel regulator implicated in glucocorticoids-inhibited bone formation. Aging 2019, 11, 7537–7552. [Google Scholar] [CrossRef] [PubMed]
- Ye, P.; Gu, Y.; Zhu, Y.R.; Chao, Y.L.; Kong, X.Q.; Luo, J.; Ren, X.M.; Zuo, G.F.; Zhang, D.M.; Chen, S.L. Exogenous hydrogen sulfide attenuates the development of diabetic cardiomyopathy via the FoxO1 pathway. J. Cell Physiol. 2018, 233, 9786–9798. [Google Scholar] [CrossRef]
- Wang, C.; Du, J.; Du, S.; Liu, Y.; Li, D.; Zhu, X.; Ni, X. Endogenous H2S resists mitochondria-mediated apoptosis in the adrenal glands via ATP5A1 S-sulfhydration in male mice. Mol. Cell Endocrinol. 2018, 474, 65–73. [Google Scholar] [CrossRef]
- Wu, J.; Yang, F.; Zhang, X.; Chen, G.; Zou, J.; Yin, L.; Yang, D. Hydrogen sulfide inhibits endoplasmic reticulum stress through the GRP78/mTOR pathway in rat chondrocytes subjected to oxidative stress. Int. J. Mol. Med. 2021, 47, 4867. [Google Scholar] [CrossRef]
- Liang, K.; Wei, L.; Chen, L. Exocytosis, Endocytosis, and Their Coupling in Excitable Cells. Front. Mol. Neurosci. 2017, 10, 109. [Google Scholar] [CrossRef]
- Trexler, A.J.; Taraska, J.W. Regulation of insulin exocytosis by calcium-dependent protein kinase C in beta cells. Cell Calcium 2017, 67, 1–10. [Google Scholar] [CrossRef]
- de Pascual, R.; Baraibar, A.M.; Méndez-López, I.; Pérez-Ciria, M.; Polo-Vaquero, I.; Gandía, L.; Ohia, S.E.; García, A.G.; de Diego, A.M.G. Hydrogen sulphide facilitates exocytosis by regulating the handling of intracellular calcium by chromaffin cells. Pflug. Arch. 2018, 470, 1255–1270. [Google Scholar] [CrossRef]
- Pearse, B.M. Clathrin: A unique protein associated with intracellular transfer of membrane by coated vesicles. Proc. Natl. Acad. Sci. USA 1976, 73, 1255–1259. [Google Scholar] [CrossRef] [PubMed]
- Allen, J.A.; Halverson-Tamboli, R.A.; Rasenick, M.M. Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 2007, 8, 128–140. [Google Scholar] [CrossRef] [PubMed]
- Canton, J. Macropinocytosis: New Insights Into Its Underappreciated Role in Innate Immune Cell Surveillance. Front. Immunol. 2018, 9, 2286. [Google Scholar] [CrossRef] [PubMed]
- Ge, S.N.; Zhao, M.M.; Wu, D.D.; Chen, Y.; Wang, Y.; Zhu, J.H.; Cai, W.J.; Zhu, Y.Z.; Zhu, Y.C. Hydrogen sulfide targets EGFR Cys797/Cys798 residues to induce Na(+)/K(+)-ATPase endocytosis and inhibition in renal tubular epithelial cells and increase sodium excretion in chronic salt-loaded rats. Antioxid. Redox Signal. 2014, 21, 2061–2082. [Google Scholar] [CrossRef] [PubMed]
- Dal-Secco, D.; Cunha, T.M.; Freitas, A.; Alves-Filho, J.C.; Souto, F.O.; Fukada, S.Y.; Grespan, R.; Alencar, N.M.; Neto, A.F.; Rossi, M.A.; et al. Hydrogen sulfide augments neutrophil migration through enhancement of adhesion molecule expression and prevention of CXCR2 internalization: Role of ATP-sensitive potassium channels. J. Immunol. 2008, 181, 4287–4298. [Google Scholar] [CrossRef] [PubMed]
- Cavalli, G.; Heard, E. Advances in epigenetics link genetics to the environment and disease. Nature 2019, 571, 489–499. [Google Scholar] [CrossRef]
- Zhang, T.; Kraus, W.L. SIRT1-dependent regulation of chromatin and transcription: Linking NAD(+) metabolism and signaling to the control of cellular functions. Biochim. Biophys. Acta 2010, 1804, 1666–1675. [Google Scholar] [CrossRef]
- Du, C.; Lin, X.; Xu, W.; Zheng, F.; Cai, J.; Yang, J.; Cui, Q.; Tang, C.; Cai, J.; Xu, G.; et al. Sulfhydrated Sirtuin-1 Increasing Its Deacetylation Activity Is an Essential Epigenetics Mechanism of Anti-Atherogenesis by Hydrogen Sulfide. Antioxid. Redox Signal. 2019, 30, 184–197. [Google Scholar] [CrossRef]
- Bartel, D.P. Metazoan MicroRNAs. Cell 2018, 173, 20–51. [Google Scholar] [CrossRef]
- Weber, G.J.; Pushpakumar, S.B.; Sen, U. Hydrogen sulfide alleviates hypertensive kidney dysfunction through an epigenetic mechanism. Am. J. Physiol. Heart Circ. Physiol. 2017, 312, H874–H885. [Google Scholar] [CrossRef] [Green Version]
- John, A.; Kundu, S.; Pushpakumar, S.; Fordham, M.; Weber, G.; Mukhopadhyay, M.; Sen, U. GYY4137, a Hydrogen Sulfide Donor Modulates miR194-Dependent Collagen Realignment in Diabetic Kidney. Sci. Rep. 2017, 7, 10924. [Google Scholar] [CrossRef]
- Nandi, S.S.; Mishra, P.K. H2S and homocysteine control a novel feedback regulation of cystathionine beta synthase and cystathionine gamma lyase in cardiomyocytes. Sci. Rep. 2017, 7, 3639. [Google Scholar] [CrossRef] [PubMed]
- Malik, A.; Kanneganti, T.D. Inflammasome activation and assembly at a glance. J. Cell Sci. 2017, 130, 3955–3963. [Google Scholar] [CrossRef]
- Swanson, K.V.; Deng, M.; Ting, J.P. The NLRP3 inflammasome: Molecular activation and regulation to therapeutics. Nat. Rev. Immunol. 2019, 19, 477–489. [Google Scholar] [CrossRef] [PubMed]
- Castelblanco, M.; Lugrin, J.; Ehirchiou, D.; Nasi, S.; Ishii, I.; So, A.; Martinon, F.; Busso, N. Hydrogen sulfide inhibits NLRP3 inflammasome activation and reduces cytokine production both in vitro and in a mouse model of inflammation. J. Biol. Chem. 2018, 293, 2546–2557. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Q.; Pan, L.; Ji, Y. H2S protects against diabetes-accelerated atherosclerosis by preventing the activation of NLRP3 inflammasome. J. Biomed. Res. 2019, 34, 94–102. [Google Scholar] [CrossRef]
- Li, J.; Ma, J.; Li, M.; Tao, J.; Chen, J.; Yao, C.; Yao, S. GYY4137 alleviates sepsis-induced acute lung injury in mice by inhibiting the PDGFRβ/Akt/NF-κB/NLRP3 pathway. Life Sci. 2021, 271, 119192. [Google Scholar] [CrossRef]
- Zhou, T.; Qian, H.; Zheng, N.; Lu, Q.; Han, Y. GYY4137 ameliorates sepsis-induced cardiomyopathy via NLRP3 pathway. Biochim. Biophys. Acta Mol. Basis Dis. 2022, 1868, 166497. [Google Scholar] [CrossRef]
- Pipatpolkai, T.; Usher, S.; Stansfeld, P.J.; Ashcroft, F.M. New insights into KATP channel gene mutations and neonatal diabetes mellitus. Nat. Rev. Endocrinol. 2020, 16, 378–393. [Google Scholar] [CrossRef]
- Zamponi, G.W. Targeting voltage-gated calcium channels in neurological and psychiatric diseases. Nat. Rev. Drug Discov. 2016, 15, 19–34. [Google Scholar] [CrossRef]
- Dallas, M.L.; Al-Owais, M.M.; Hettiarachchi, N.T.; Vandiver, M.S.; Jarosz-Griffiths, H.H.; Scragg, J.L.; Boyle, J.P.; Steele, D.; Peers, C. Hydrogen sulfide regulates hippocampal neuron excitability via S-sulfhydration of Kv2.1. Sci. Rep. 2021, 11, 8194. [Google Scholar] [CrossRef] [PubMed]
- Yu, L.; Park, B.M.; Ahn, Y.J.; Lee, G.J.; Kim, S.H. Hydrogen sulfide donor, NaHS, stimulates ANP secretion via the K(ATP) channel and the NOS/sGC pathway in rat atria. Peptides 2019, 111, 89–97. [Google Scholar] [CrossRef] [PubMed]
- Qabazard, B.; Masocha, W.; Khajah, M.; Phillips, O.A. H2S donor GYY4137 ameliorates paclitaxel-induced neuropathic pain in mice. Biomed. Pharmacother. 2020, 127, 110210. [Google Scholar] [CrossRef] [PubMed]
- Gallego-Martin, T.; Prieto-Lloret, J.; Aaronson, P.I.; Rocher, A.; Obeso, A. Hydroxycobalamin Reveals the Involvement of Hydrogen Sulfide in the Hypoxic Responses of Rat Carotid Body Chemoreceptor Cells. Antioxidants 2019, 8, 62. [Google Scholar] [CrossRef]
- Paul, B.D.; Snyder, S.H. Modes of physiologic H2S signaling in the brain and peripheral tissues. Antioxid. Redox Signal. 2015, 22, 411–423. [Google Scholar] [CrossRef]
- Sulfagenix Australia Pty Ltd. Assessing the Safety and Ability of SG1002 to Overcome Deficits in Hydrogen Sulfide in Heart Failure Patients. ClinicalTrials.gov Identifier: NCT01989208. Available online: https://clinicaltrials.gov/ct2/show/study/NCT01989208 (accessed on 5 May 2020).
- Zhao, W.; Zhang, J.; Lu, Y.; Wang, R. The vasorelaxant effect of H2S as a novel endogenous gaseous K(ATP) channel opener. EMBO J. 2001, 20, 6008–6016. [Google Scholar] [CrossRef] [Green Version]
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Liu, J.; Mesfin, F.M.; Hunter, C.E.; Olson, K.R.; Shelley, W.C.; Brokaw, J.P.; Manohar, K.; Markel, T.A. Recent Development of the Molecular and Cellular Mechanisms of Hydrogen Sulfide Gasotransmitter. Antioxidants 2022, 11, 1788. https://doi.org/10.3390/antiox11091788
Liu J, Mesfin FM, Hunter CE, Olson KR, Shelley WC, Brokaw JP, Manohar K, Markel TA. Recent Development of the Molecular and Cellular Mechanisms of Hydrogen Sulfide Gasotransmitter. Antioxidants. 2022; 11(9):1788. https://doi.org/10.3390/antiox11091788
Chicago/Turabian StyleLiu, Jianyun, Fikir M. Mesfin, Chelsea E. Hunter, Kenneth R. Olson, W. Christopher Shelley, John P. Brokaw, Krishna Manohar, and Troy A. Markel. 2022. "Recent Development of the Molecular and Cellular Mechanisms of Hydrogen Sulfide Gasotransmitter" Antioxidants 11, no. 9: 1788. https://doi.org/10.3390/antiox11091788
APA StyleLiu, J., Mesfin, F. M., Hunter, C. E., Olson, K. R., Shelley, W. C., Brokaw, J. P., Manohar, K., & Markel, T. A. (2022). Recent Development of the Molecular and Cellular Mechanisms of Hydrogen Sulfide Gasotransmitter. Antioxidants, 11(9), 1788. https://doi.org/10.3390/antiox11091788