Current Review on H2S Signaling
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Apr 16, 2015
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Abstract
Hydrogen Sulfide, a pungent gas traditionally thought to be toxic to the human body, is now emerging as one of the most important endogenously synthesized gaseous transmitters. Over the course of the past decade, we have witnessed better characterization of its synthetic pathways, discovered how it affects its targets at the molecular level by modifying cysteine residues, a process termed sulfhydration, as well as begun to identify the critical role it plays in the modulation of various cellular processes. In this article, we will review some of these findings.
Article Details
How to Cite
MUSTAFA, Asif K; GAZI, Sadia K.
Current Review on H2S Signaling.
Medical Research Archives, [S.l.], n. 2, apr. 2015.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/64>. Date accessed: 03 dec. 2024.
Keywords
Hydrogen Sulfide (H2S), Sulfhydration, Gasotransmitter, Vasorelaxation
Issue
Section
Review Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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Calvert, J.W., Elston, M., Nicholson, C.K., Gundewar, S., Jha, S., Elrod, J.W., Ramachandran, A. and Lefer, D.J. (2010). "Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice." Circulation 122(1): 11-19.
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Cohen, R.A. (2005). "The endothelium-derived hyperpolarizing factor puzzle: a mechanism without a mediator?" Circulation 111(6): 724-727.
El-Husseini, A.E., Schnell, E., Chetkovich, D.M., Nicoll, R.A. and Bredt, D.S. (2000). "PSD-95 involvement in maturation of excitatory synapses." Science 290(5495): 1364-1368.
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HDCRG (1993). "Huntington’s Disease Collaborative Research Group: A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group." Cell 72(6): 971-983.
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Kump, L.R., Pavlov, A. and Arthur, M.A. (2005). "Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia." Geology 33(5): 397–400.
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Mustafa, A.K., Gadalla, M.M., Sen, N., Kim, S., Mu, W., Gazi, S.K., Barrow, R.K., Yang, G., Wang, R. and Snyder, S.H. (2009a). "H2S signals through protein S-sulfhydration." Sci Signal 2(96): ra72.
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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., Amzel, L.M., Berkowitz, D.E. and Snyder, S.H. (2011). "Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels." Circ Res 109(11): 1259-1268.
Paul, B.D., Sbodio, J.I., Xu, R., Vandiver, M.S., Cha, J.Y., Snowman, A.M. and Snyder, S.H. (2014). "Cystathionine gamma-lyase deficiency mediates neurodegeneration in Huntington's disease." Nature 509(7498): 96-100.
Paul, B.D. and Snyder, S.H. (2012). "H(2)S signalling through protein sulfhydration and beyond." Nat Rev Mol Cell Biol 13(8): 499-507.
Polhemus, D.J. and Lefer, D.J. (2014). "Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease." Circ Res 114(4): 730-737.
Schneider, D.J. and Moore, J.W. (2006). "Patent ductus arteriosus." Circulation 114(17): 1873-1882.
Sen, N., Paul, B.D., Gadalla, M.M., Mustafa, A.K., Sen, T., Xu, R., Kim, S. and Snyder, S.H. (2012). "Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions." Mol Cell 45(1): 13-24.
Vandiver, M.S., Paul, B.D., Xu, R., Karuppagounder, S., Rao, F., Snowman, A.M., Ko, H.S., Lee, Y.I., Dawson, V.L., Dawson, T.M., Sen, N. and Snyder, S.H. (2013). "Sulfhydration mediates neuroprotective actions of parkin." Nat Commun 4: 1626.
Voet, D.H. and Voet, J.G. (1995). Biochemistry, John Wiley and Sons Inc.
Wang, Y., Zhao, X., Jin, H., Wei, H., Li, W., Bu, D., Tang, X., Ren, Y., Tang, C. and Du, J. (2009). "Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice." Arterioscler Thromb Vasc Biol 29(2): 173-179.
Watanabe, M., Osada, J., Aratani, Y., Kluckman, K., Reddick, R., Malinow, M.R. and Maeda, N. (1995). "Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia." Proc Natl Acad Sci U S A 92(5): 1585-1589.
Yang, G., Wu, L., Jiang, B., Yang, W., Qi, J., Cao, K., Meng, Q., Mustafa, A.K., Mu, W., Zhang, S., Snyder, S.H. and Wang, R. (2008). "H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase." Science 322(5901): 587-590.
Yang, G., Zhao, K., Ju, Y., Mani, S., Cao, Q., Puukila, S., Khaper, N., Wu, L. and Wang, R. (2013). "Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2." Antioxid Redox Signal 18(15): 1906-1919.
Yang, W., Yang, G., Jia, X., Wu, L. and Wang, R. (2005). "Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms." J Physiol 569(Pt 2): 519-531.
Zanardo, R.C., Brancaleone, V., Distrutti, E., Fiorucci, S., Cirino, G. and Wallace, J.L. (2006). "Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation." FASEB J 20(12): 2118-2120.
Zhao, K., Li, S., Wu, L., Lai, C. and Yang, G. (2014). "Hydrogen sulfide represses androgen receptor transactivation by targeting at the second zinc finger module." J Biol Chem 289(30): 20824-20835.
Ashcroft, F.M. and Rorsman, P. (2013). "K(ATP) channels and islet hormone secretion: new insights and controversies." Nat Rev Endocrinol 9(11): 660-669.
Beard, R.S., Jr. and Bearden, S.E. (2011). "Vascular complications of cystathionine beta-synthase deficiency: future directions for homocysteine-to-hydrogen sulfide research." Am J Physiol Heart Circ Physiol 300(1): H13-26.
Beg, A.A. and Baltimore, D. (1996). "An essential role for NF-kappaB in preventing TNF-alpha-induced cell death." Science 274(5288): 782-784.
Beg, A.A., Sha, W.C., Bronson, R.T., Ghosh, S. and Baltimore, D. (1995). "Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-kappa B." Nature 376(6536): 167-170.
Calvert, J.W., Elston, M., Nicholson, C.K., Gundewar, S., Jha, S., Elrod, J.W., Ramachandran, A. and Lefer, D.J. (2010). "Genetic and pharmacologic hydrogen sulfide therapy attenuates ischemia-induced heart failure in mice." Circulation 122(1): 11-19.
Chung, K.K., Thomas, B., Li, X., Pletnikova, O., Troncoso, J.C., Marsh, L., Dawson, V.L. and Dawson, T.M. (2004). "S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function." Science 304(5675): 1328-1331.
Cohen, R.A. (2005). "The endothelium-derived hyperpolarizing factor puzzle: a mechanism without a mediator?" Circulation 111(6): 724-727.
El-Husseini, A.E., Schnell, E., Chetkovich, D.M., Nicoll, R.A. and Bredt, D.S. (2000). "PSD-95 involvement in maturation of excitatory synapses." Science 290(5495): 1364-1368.
Finkelstein, J.D., Kyle, W.E., Martin, J.L. and Pick, A.M. (1975). "Activation of cystathionine synthase by adenosylmethionine and adenosylethionine." Biochem Biophys Res Commun 66(1): 81-87.
Givvimani, S., Munjal, C., Gargoum, R., Sen, U., Tyagi, N., Vacek, J.C. and Tyagi, S.C. (2011). "Hydrogen sulfide mitigates transition from compensatory hypertrophy to heart failure." J Appl Physiol (1985) 110(4): 1093-1100.
Guo, C., Liang, F., Shah Masood, W. and Yan, X. (2014). "Hydrogen sulfide protected gastric epithelial cell from ischemia/reperfusion injury by Keap1 s-sulfhydration, MAPK dependent anti-apoptosis and NF-kappaB dependent anti-inflammation pathway." Eur J Pharmacol 725: 70-78.
HDCRG (1993). "Huntington’s Disease Collaborative Research Group: A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group." Cell 72(6): 971-983.
Jaffrey, S.R. and Snyder, S.H. (2001). "The biotin switch method for the detection of S-nitrosylated proteins." Sci STKE 2001(86): pl1.
Kabil, O., Weeks, C.L., Carballal, S., Gherasim, C., Alvarez, B., Spiro, T.G. and Banerjee, R. (2011). "Reversible heme-dependent regulation of human cystathionine beta-synthase by a flavoprotein oxidoreductase." Biochemistry 50(39): 8261-8263.
Krishnan, N., Fu, C., Pappin, D.J. and Tonks, N.K. (2011). "H2S-Induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response." Sci Signal 4(203): ra86.
Kump, L.R., Pavlov, A. and Arthur, M.A. (2005). "Massive release of hydrogen sulfide to the surface ocean and atmosphere during intervals of oceanic anoxia." Geology 33(5): 397–400.
Liu, Y., Yang, R., Liu, X., Zhou, Y., Qu, C., Kikuiri, T., Wang, S., Zandi, E., Du, J., Ambudkar, I.S. and Shi, S. (2014). "Hydrogen sulfide maintains mesenchymal stem cell function and bone homeostasis via regulation of Ca(2+) channel sulfhydration." Cell Stem Cell 15(1): 66-78.
Maron, B.A. and Loscalzo, J. (2009). "The treatment of hyperhomocysteinemia." Annu Rev Med 60: 39-54.
Mir, S., Sen, T. and Sen, N. (2014). "Cytokine-induced GAPDH sulfhydration affects PSD95 degradation and memory." Mol Cell 56(6): 786-795.
Mustafa, A.K., Gadalla, M.M., Sen, N., Kim, S., Mu, W., Gazi, S.K., Barrow, R.K., Yang, G., Wang, R. and Snyder, S.H. (2009a). "H2S signals through protein S-sulfhydration." Sci Signal 2(96): ra72.
Mustafa, A.K., Gadalla, M.M. and Snyder, S.H. (2009b). "Signaling by gasotransmitters." Sci Signal 2(68): re2.
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., Amzel, L.M., Berkowitz, D.E. and Snyder, S.H. (2011). "Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels." Circ Res 109(11): 1259-1268.
Paul, B.D., Sbodio, J.I., Xu, R., Vandiver, M.S., Cha, J.Y., Snowman, A.M. and Snyder, S.H. (2014). "Cystathionine gamma-lyase deficiency mediates neurodegeneration in Huntington's disease." Nature 509(7498): 96-100.
Paul, B.D. and Snyder, S.H. (2012). "H(2)S signalling through protein sulfhydration and beyond." Nat Rev Mol Cell Biol 13(8): 499-507.
Polhemus, D.J. and Lefer, D.J. (2014). "Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease." Circ Res 114(4): 730-737.
Schneider, D.J. and Moore, J.W. (2006). "Patent ductus arteriosus." Circulation 114(17): 1873-1882.
Sen, N., Paul, B.D., Gadalla, M.M., Mustafa, A.K., Sen, T., Xu, R., Kim, S. and Snyder, S.H. (2012). "Hydrogen sulfide-linked sulfhydration of NF-kappaB mediates its antiapoptotic actions." Mol Cell 45(1): 13-24.
Vandiver, M.S., Paul, B.D., Xu, R., Karuppagounder, S., Rao, F., Snowman, A.M., Ko, H.S., Lee, Y.I., Dawson, V.L., Dawson, T.M., Sen, N. and Snyder, S.H. (2013). "Sulfhydration mediates neuroprotective actions of parkin." Nat Commun 4: 1626.
Voet, D.H. and Voet, J.G. (1995). Biochemistry, John Wiley and Sons Inc.
Wang, Y., Zhao, X., Jin, H., Wei, H., Li, W., Bu, D., Tang, X., Ren, Y., Tang, C. and Du, J. (2009). "Role of hydrogen sulfide in the development of atherosclerotic lesions in apolipoprotein E knockout mice." Arterioscler Thromb Vasc Biol 29(2): 173-179.
Watanabe, M., Osada, J., Aratani, Y., Kluckman, K., Reddick, R., Malinow, M.R. and Maeda, N. (1995). "Mice deficient in cystathionine beta-synthase: animal models for mild and severe homocyst(e)inemia." Proc Natl Acad Sci U S A 92(5): 1585-1589.
Yang, G., Wu, L., Jiang, B., Yang, W., Qi, J., Cao, K., Meng, Q., Mustafa, A.K., Mu, W., Zhang, S., Snyder, S.H. and Wang, R. (2008). "H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase." Science 322(5901): 587-590.
Yang, G., Zhao, K., Ju, Y., Mani, S., Cao, Q., Puukila, S., Khaper, N., Wu, L. and Wang, R. (2013). "Hydrogen sulfide protects against cellular senescence via S-sulfhydration of Keap1 and activation of Nrf2." Antioxid Redox Signal 18(15): 1906-1919.
Yang, W., Yang, G., Jia, X., Wu, L. and Wang, R. (2005). "Activation of KATP channels by H2S in rat insulin-secreting cells and the underlying mechanisms." J Physiol 569(Pt 2): 519-531.
Zanardo, R.C., Brancaleone, V., Distrutti, E., Fiorucci, S., Cirino, G. and Wallace, J.L. (2006). "Hydrogen sulfide is an endogenous modulator of leukocyte-mediated inflammation." FASEB J 20(12): 2118-2120.
Zhao, K., Li, S., Wu, L., Lai, C. and Yang, G. (2014). "Hydrogen sulfide represses androgen receptor transactivation by targeting at the second zinc finger module." J Biol Chem 289(30): 20824-20835.