Neuroprotective effects of hydrogen sulfide and the underlying signaling pathways

Reviews in the Neurosciences

Volumn 26, Issue 2, 2015, Pages 129-142

  Chen, Wen Lin ^a   Niu, Ying Ying ^a   Jiang, Wei Zheng ^a   Tang, Hui Lan ^a   Zhang, Chong ^a   Xia, Qi Ming ^a   Tang, Xiao Qing ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

Author keywords

central nervous system diseases; hydrogen sulfide; neuroprotective; signaling pathways

Indexed keywords

3 MERCAPTOPYRUVATE SULFUR TRANSFERASE; AMINOTRANSFERASE; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE AMINOTRANSFERASE; DEXTRO AMINO ACID OXIDASE; HYDROGEN SULFIDE; ION CHANNEL; SULFURTRANSFERASE; UNCLASSIFIED DRUG; NEUROPROTECTIVE AGENT;

ALZHEIMER DISEASE; ARTICLE; BRAIN ISCHEMIA; CATABOLISM; FEBRILE CONVULSION; HUMAN; MAJOR DEPRESSION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; ANIMAL; BRAIN; DRUG EFFECTS; METABOLISM; NERVOUS SYSTEM DISEASES; SIGNAL TRANSDUCTION;

ANIMALS; BRAIN; HUMANS; HYDROGEN SULFIDE; ION CHANNELS; NERVOUS SYSTEM DISEASES; NEUROPROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 84926314785     PISSN: 03341763     EISSN: 21910200     Source Type: Journal    
DOI: 10.1515/revneuro-2014-0051     Document Type: Article

References (115)

1. Abe, K. and Kimura, H. (1996). The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 16, 1066-1071.
2. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G.M., Cooper, N.R., Eikelenboom, P., Emmerling, M., Fiebich, B.L., et al. (2000). Inflammation and Alzheimer's disease. Neurobiol. Aging. 21, 383-421.
3. Andrikopoulos, P., Fraser, S.P., Patterson, L., Ahmad, Z., Burcu, H., Ottaviani, D., Diss, J.K., Box, C., Eccles, S.A., and Djamgoz, M.B. (2011). Angiogenic functions of voltage-gated Na+ channels in human endothelial cells: modulation of vascular endothelial growth factor (VEGF) signaling. J. Biol. Chem. 286, 16846-16860.
4. Ang, S.F., Moochhala, S.M., MacAry, P.A., and Bhatia, M. (2011a). Hydrogen sulfide and neurogenic inflammation in polymicrobial sepsis: involvement of substance P and ERK-NF-kappaB signaling. PLoS One 6, e24535.
5. Ang, S.F., Sio, S.W., Moochhala, S.M., MacAry, P.A., and Bhatia, M. (2011b). Hydrogen sulfide upregulates cyclooxygenase-2 and prostaglandin E metabolite in sepsis-evoked acute lung injury via transient receptor potential vanilloid type 1 channel activation. J. Immunol. 187, 4778-4787.
6. Braunstein, A.E., Goryachenkova, E.V., Tolosa, E.A., Willhardt, I.H., and Yefremova, L.L. (1971). Specificity and some other properties of liver serine sulphhydrase: evidence for its identity with cystathionine-synthase. Biochim. Biophys. Acta. 242, 247-260.
7. Cai, W.J., Wang, M.J., Moore, P.K., Jin, H.M., Yao, T., and Zhu, Y.C. (2007). The novel proangiogenic effect of hydrogen sulfide is dependent on Akt phosphorylation. Cardiovasc. Res. 76, 29-40.
8. Calvert, J.W., Jha, S., Gundewar, S., Elrod, J.W., Ramachandran, A., Pattillo, C.B., Kevil, C.G., and Lefer, D.J. (2009). Hydrogen sulfide mediates cardioprotection through Nrf2 signaling. Circ. Res. 105, 365-374.
9. Castren, E. and Rantamaki, T. (2010). The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev. Neurobiol. 70, 289-297.
10. Cavallini, D., Mondovi, B., de Marco, C., and Scioscia-Santoro, A. (1962). The mechanism of desulphhydration of cysteine. Enzymologia 24, 253-266.
11. Cazorla, M., Jouvenceau, A., Rose, C., Guilloux, J.-P., Pilon, C., Dranovsky, A., and Prémont, J. (2010). Cyclotraxin-B, the first highly potent and selective TrkB inhibitor, has anxiolytic properties in mice. PLoS One 5, e9777.
12. Chen, X., Jhee, K.H., and Kruger, W.D. (2004). Production of the neuromodulator H2S by cystathionine beta-synthase via the condensation of cysteine and homocysteine. J. Biol. Chem. 279, 52082-52086.
13. Chen, C.Q., Xin, H., and Zhu, Y.Z. (2007). Hydrogen sulfide: third gaseous transmitter, but with great pharmacological potential. Acta Pharmacol. Sin. 28, 1709-1716.
14. Chen, P.C., Vargas, M.R., Pani, A.K., Smeyne, R.J., Johnson, D.A., Kan, Y.W., and Johnson, J.A. (2009). Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte. Proc. Natl. Acad. Sci. USA 106, 2933-2938.
15. Chen, W.L., Xie, B., Zhang, C., Xu, K.L., Niu, Y.Y., Tang, X.Q., Zhang, P., Zou, W., Hu, B., and Tian, Y. (2013). Antidepressant-like and anxiolytic-like effects of hydrogen sulfide in behavioral models of depression and anxiety. Behav. Pharmacol. 24, 590-597.
16. Chiku, T., Padovani, D., Zhu, W., Singh, S., Vitvitsky, V., and Banerjee, R. (2009). H2S biogenesis by human cystathionine gamma-lyase leads to the novel sulfur metabolites lanthionine and homolanthionine and is responsive to the grade of hyperhomocysteinemia. J. Biol. Chem. 284, 11601-11612.
17. Dawe, G.S., Han, S.P., Bian, J.S., and Moore, P.K. (2008). Hydrogen sulphide in the hypothalamus causes an ATP-sensitive K+ channel-dependent decrease in blood pressure in freely moving rats. Neuroscience 152, 169-177.
18. Denollet, J., Maas, K., Knottnerus, A., Keyzer, J.J., and Pop, V.J. (2009). Anxiety predicted premature all-cause and cardiovascular death in a 10-year follow-up of middle-aged women. J. Clin. Epidemiol. 62, 452-456.
19. Eisch, A.J. and Petrik, D. (2012). Depression and hippocampal neurogenesis: a road to remission? Science 338, 72-75.
20. Enokido, Y., Suzuki, E., Iwasawa, K., Namekata, K., Okazawa, H., and Kimura, H. (2005). Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. FASEB J. 19, 1854-1856.
21. Eto, K., Asada, T., Arima, K., Makifuchi, T., and Kimura, H. (2002). Brain hydrogen sulfide is severely decreased in Alzheimer's disease. Biochem. Biophys. Res. Commun. 293, 1485-1488.
22. Fan, H., Guo, Y., Liang, X., Yuan, Y., Qi, X., Wang, M., Ma, J., and Zhou, H. (2013). Hydrogen sulfide protects against amyloid beta-peptide induced neuronal injury via attenuating inflammatory responses in a rat model. J. Biomed. Res. 27, 296-304.
23. Florian, B., Vintilescu, R., Balseanu, A.T., Buga, A.M., Grisk, O., Walker, L.C., Kessler, C., and Popa-Wagner, A. (2008). Long-term hypothermia reduces infarct volume in aged rats after focal ischemia. Neurosci. Lett. 438, 180-185.
24. Gadalla, M.M. and Snyder, S.H. (2010). Hydrogen sulfide as a gasotransmitter. J. Neurochem 113, 14-26.
25. Geng, B., Yang, J., Qi, Y., Zhao, J., Pang, Y., Du, J., and Tang, C. (2004). H2S generated by heart in rat and its effects on cardiac function. Biochem. Biophys. Res. Commun. 313, 362-368.
26. Goldberg-Stern, H., Aharoni, S., Afawi, Z., Bennett, O., Appenzeller, S., Pendziwiat, M., Kuhlenbäumer, G., Basel-Vanagaite, L., Shuper, A., Korczyn, A.D., et al. (2014). Broad phenotypic heterogeneity due to a novel SCN1A mutation in a family with genetic epilepsy with febrile seizures plus. J. Child Neurol. 29, 221-226.
27. Gordon, W.A. and Hibbard, M.R. (1997). Poststroke depression: an examination of the literature. Arch. Phys. Med. Rehabil. 78, 658-663.
28. Gouret, C.J., Porsolt, R., Wettstein, J.G., Puech, A., Soulard, C., Pascaud, X., and Junien, J.L. (1990). Biochemical and pharmacological evaluation of the novel antidepressant and serotonin uptake inhibitor 2-(3,4-dichlorobenzyl)-2-dimethylamino-1-propanol hydrochloride. Arzneimittelforschung 40, 633-640.
29. Guo, W., Kan, J.T., Cheng, Z.Y., Chen, J.F., Shen, Y.Q., Xu, J., Wu, D., and Zhu, Y.Z. (2012). Hydrogen sulfide as an endogenous modulator in mitochondria and mitochondria dysfunction. Oxid. Med. Cell Longev. 2012, 878052.
30. Han, Y., Qin, J., Chang, X., Yang, Z., Bu, D., and Du, J. (2005a). Modulating effect of hydrogen sulfide on gamma-aminobutyric acid B receptor in recurrent febrile seizures in rats. Neurosci. Res. 53, 216-219.
31. Han, Y., Qin, J., Chang, X., Yang, Z., Tang, X., and Du, J. (2005b). Hydrogen sulfide may improve the hippocampal damage induced by recurrent febrile seizures in rats. Biochem. Biophys. Res. Commun. 327, 431-436.
32. Han, Y., Qin, J., Chang, X., Yang, Z., and Du, J. (2006). Hydrogen sulfide and carbon monoxide are in synergy with each other in the pathogenesis of recurrent febrile seizures. Cell. Mol. Neurobiol. 26, 101-107.
33. Hanson, N.D., Owens, M.J., and Nemeroff, C.B. (2011). Depression, antidepressants, and neurogenesis: a critical reappraisal. Neuropsychopharmacology 36, 2589-2602.
34. Hirsch, E.C. and Hunot, S. (2009). Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol. 8, 382-397.
35. Hirsch, E., Graybiel, A.M., and Agid, Y.A. (1988). Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334, 345-348.
36. Hoozemans, J.J., Veerhuis, R., Van Haastert, E.S., Rozemuller, J.M., Baas, F., Eikelenboom, P., and Scheper, W. (2005). The unfolded protein response is activated in Alzheimer's disease. Acta. Neuropathol. 110, 165-172.
37. Hoozemans, J.J., van Haastert, E.S., Nijholt, D.A., Rozemuller, A.J., Eikelenboom, P., and Scheper, W. (2009). The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus. Am. J. Pathol. 174, 1241-1251.
38. Hosoki, R., Matsuki, N., and Kimura, H. (1997). The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide. Biochem. Biophys. Res. Commun. 237, 527-531.
39. Hsu, C.C., Lin, R.L., Lee, L.Y., and Lin, Y.S. (2013). Hydrogen sulfide induces hypersensitivity of rat capsaicin-sensitive lung vagal neurons: role of TRPA1 receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305, R769-779.
40. Hu, L.F., Lu, M., Tiong, C.X., Dawe, G.S., Hu, G., and Bian, J.S. (2010). Neuroprotective effects of hydrogen sulfide on Parkinson's disease rat models. Aging Cell 9, 135-146.
41. Ichinohe, A., Kanaumi, T., Takashima, S., Enokido, Y., Nagai, Y., and Kimura, H. (2005). Cystathionine beta-synthase is enriched in the brains of Down's patients. Biochem. Biophys. Res. Commun. 338, 1547-1550.
42. Ishigami, M., Hiraki, K., Umemura, K., Ogasawara, Y., Ishii, K., and Kimura, H. (2009). A source of hydrogen sulfide and a mechanism of its release in the brain. Antioxid. Redox Signal. 11, 205-214.
43. Ishii, I., Akahoshi, N., Yamada, H., Nakano, S., Izumi, T., and Suematsu, M. (2010). Cystathionine gamma-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury. J. Biol. Chem. 285, 26358-26368.
44. Jang, H., Oh, M.Y., Kim, Y.J., Choi, I.Y., Yang, H.S., Ryu, W.S., Lee, S.H., and Yoon, B.W. (2014). Hydrogen sulfide treatment induces angiogenesis after cerebral ischemia. J. Neurosci. Res. 92, 1520-1528.
45. Johansen, D., Ytrehus, K., and Baxter, G.F. (2006). Exogenous hydrogen sulfide (H2S) protects against regional myocardial ischemia-reperfusion injury - evidence for a role of K ATP channels. Basic Res. Cardiol. 101, 53-60.
46. Kawabata, A., Ishiki, T., Nagasawa, K., Yoshida, S., Maeda, Y., Takahashi, T., Sekiguchi, F., Wada, T., Ichida, S., and Nishikawa, H. (2007). Hydrogen sulfide as a novel nociceptive messenger. Pain 132, 74-81.
47. Kida, K., Yamada, M., Tokuda, K., Marutani, E., Kakinohana, M., Kaneki, M., and Ichinose, F. (2011). Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson's disease. Antioxid. Redox Signal. 15, 343-352.
48. Kimura, H. (2010). Hydrogen sulfide: from brain to gut. Antioxid. Redox Signal. 12, 1111-1123.
49. Kimura, H. (2012). [Hydrogen sulfide: production, release, and functions]. Nihon Yakurigaku Zasshi. 139, 6-8.
50. Kimura, H. (2014). Signaling molecules: hydrogen sulfide and polysulfide. Antioxid. Redox Signal. Available at: http://www.ncbi.nlm.nih.gov/pubmed/?term=Signaling+molecules%3A+hydrogen+sulfide+and+polysulfide.+Antioxid.
51. Kimura, Y., Dargusch, R., Schubert, D., and Kimura, H. (2006). Hydrogen sulfide protects HT22 neuronal cells from oxidative stress. Antioxid. Redox Signal. 8, 661-670.
52. Kimura, Y., Goto, Y., and Kimura, H. (2010). Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria. Antioxid. Redox Signal. 12, 1-13.
53. Kimura, H., Shibuya, N., and Kimura, Y. (2012). Hydrogen sulfide is a signaling molecule and a cytoprotectant. Antioxid. Redox Signal. 17, 45-57.
54. Lee, M., Schwab, C., Yu, S., McGeer, E., and McGeer, P.L. (2009). Astrocytes produce the antiinflammatory and neuroprotective agent hydrogen sulfide. Neurobiol. Aging 30, 1523-1534.
55. Lee, M., Tazzari, V., Giustarini, D., Rossi, R., Sparatore, A., Del Soldato, P., McGeer, E., and McGeer, P.L. (2010). Effects of hydrogen sulfide-releasing L-DOPA derivatives on glial activation: potential for treating Parkinson disease. J. Biol. Chem. 285, 17318-17328.
56. Lee, Z.W., Low, Y.L., Huang, S., Wang, T., and Deng, L.W. (2014). The cystathionine gamma-lyase/hydrogen sulfide system maintains cellular glutathione status. Biochem. J. 460, 425-435.
57. Li, Z., Wang, Y., Xie, Y., Yang, Z., and Zhang, T. (2011). Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia. Neurochem. Res. 36, 1840-1849.
58. Li, G.F., Luo, H.K., Li, L.F., Zhang, Q.Z., Xie, L.J., Jiang, H., Li, L.P., Hao, N., Wang, W.W., and Zhang, J.X. (2012). Dual effects of hydrogen sulphide on focal cerebral ischaemic injury via modulation of oxidative stress-induced apoptosis. Clin. Exp. Pharmacol. Physiol. 39, 765-771.
59. Lipscombe, D., Helton, T.D., and Xu, W. (2004). l-type calcium channels: the low down. J. Neurophysiol. 92, 2633-2641.
60. Lowicka, E. and Beltowski, J. (2007). Hydrogen sulfide (H2S) - the third gas of interest for pharmacologists. Pharmacol. Rep. 59, 4-24.
61. Lu, M., Zhao, F.F., Tang, J.J., Su, C.J., Fan, Y., Ding, J.H., Bian, J.S., and Hu, G. (2012). The neuroprotection of hydrogen sulfide against MPTP-induced dopaminergic neuron degeneration involves uncoupling protein 2 rather than ATP-sensitive potassium channels. Antioxid. Redox Signal. 17, 849-859.
62. Maeda, Y., Aoki, Y., Sekiguchi, F., Matsunami, M., Takahashi, T., Nishikawa, H., and Kawabata, A. (2009). Hyperalgesia induced by spinal and peripheral hydrogen sulfide: evidence for involvement of Cav3.2 T-type calcium channels. Pain 142, 127-132.
63. Malekova, L., Krizanova, O., and Ondrias, K. (2009). H(2)S and HS(-) donor NaHS inhibits intracellular chloride channels. Gen. Physiol. Biophys. 28, 190-194.
64. Martinos, M.M., Yoong, M., Patil, S., Chin, R.F., Neville, B.G., Scott, R.C., and de Haan, M. (2012). Recognition memory is impaired in children after prolonged febrile seizures. Brain 135, 3153-3164.
65. Meister, A., Fraser, P.E., and Tice, S.V. (1954). Enzymatic desulfuration of beta-mercaptopyruvate to pyruvate. J. Biol. Chem. 206, 561-575.
66. Mikami, Y., Shibuya, N., Kimura, Y., Nagahara, N., Ogasawara, Y., and Kimura, H. (2011a). Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide. Biochem. J. 439, 479-485.
67. Mikami, Y., Shibuya, N., Kimura, Y., Nagahara, N., Yamada, M., and Kimura, H. (2011b). Hydrogen sulfide protects the retina from light-induced degeneration by the modulation of Ca2+ influx. J. Biol. Chem. 286, 39379-39386.
68. Miller, C. (2006). ClC chloride channels viewed through a transporter lens. Nature 440, 484-489.
69. 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. (2011). Hydrogen sulfide as endothelium-derived hyperpolarizing factor sulfhydrates potassium channels. Circ. Res. 109, 1259-1268.
70. Nagahara, N., Ito, T., Kitamura, H., and Nishino, T. (1998). Tissue and subcellular distribution of mercaptopyruvate sulfurtransferase in the rat: confocal laser fluorescence and immunoelectron microscopic studies combined with biochemical analysis. Histochem. Cell Biol. 110, 243-250.
71. Nagasawa, K., Tarui, T., Yoshida, S., Sekiguchi, F., Matsunami, M., Ohi, A., Fukami, K., Ichida, S., Nishikawa, H., and Kawabata, A. (2009). Hydrogen sulfide evokes neurite outgrowth and expression of high-voltage-activated Ca2+ currents in NG108-15 cells: involvement of T-type Ca2+ channels. J. Neurochem. 108, 676-684.
72. Nilius, B. and Droogmans, G. (2003). Amazing chloride channels: an overview. Acta. Physiol. Scand. 177, 119-147.
73. Osborne, N.N., Ji, D., Majid, A.S., Del Soldata, P., and Sparatore, A. (2012). Glutamate oxidative injury to RGC-5 cells in culture is necrostatin sensitive and blunted by a hydrogen sulfide (H2S)-releasing derivative of aspirin (ACS14). Neurochem. Int. 60, 365-378.
74. Peers, C., Bauer, C.C., Boyle, J.P., Scragg, J.L., and Dallas, M.L. (2012). Modulation of ion channels by hydrogen sulfide. Antioxid. Redox Signal. 17, 95-105.
75. Puljak, L. and Kilic, G. (2006). Emerging roles of chloride channels in human diseases. Biochim. Biophys. Acta. 1762, 404-413.
76. Qu, K., Chen, C.P., Halliwell, B., Moore, P.K., and Wong, P.T. (2006). Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 37, 889-893.
77. Ren, C., Du, A., Li, D., Sui, J., Mayhan, W.G., and Zhao, H. (2010). Dynamic change of hydrogen sulfide during global cerebral ischemia-reperfusion and its effect in rats. Brain Res. 1345, 197-205.
78. Schechter, L.E., Ring, R.H., Beyer, C.E., Hughes, Z.A., Khawaja, X., Malberg, J.E., and Rosenzweig-Lipson, S. (2005). Innovative approaches for the development of antidepressant drugs: current and future strategies. NeuroRx 2, 590-611.
79. Schicho, R., Krueger, D., Zeller, F., Von Weyhern, C.W., Frieling, T., Kimura, H., Ishii, I., De Giorgio, R., Campi, B., and Schemann, M. (2006). Hydrogen sulfide is a novel prosecretory neuromodulator in the guinea-pig and human colon. Gastroenterology 131, 1542-1552.
80. Shao, J.L., Wan, X.H., Chen, Y., Bi, C., Chen, H.M., Zhong, Y., Heng, X.H., and Qian, J.Q. (2011). H2S protects hippocampal neurons from anoxia-reoxygenation through cAMP-mediated PI3K/Akt/p70S6K cell-survival signaling pathways. J. Mol. Neurosci. 43, 453-460.
81. Shibuya, N. and Kimura, H. (2013). Production of hydrogen sulfide from D-cysteine and its therapeutic potential. Front. Endocrinol. (Lausanne). 4, 87.
82. Shibuya, N., Mikami, Y., Kimura, Y., Nagahara, N., and Kimura, H. (2009a). Vascular endothelium expresses 3-mercaptopyruvate sulfurtransferase and produces hydrogen sulfide. J. Biochem. 146, 623-626.
83. Shibuya, N., Tanaka, M., Yoshida, M., Ogasawara, Y., Togawa, T., Ishii, K., and Kimura, H. (2009b). 3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain. Antioxid. Redox Signal. 11, 703-714.
84. Shibuya, N., Koike, S., Tanaka, M., Ishigami-Yuasa, M., Kimura, Y., Ogasawara, Y., Fukui, K., Nagahara, N., and Kimura, H. (2013). A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells. Nat. Commun. 4, 1366.
85. Shinnar, S. and Glauser, T.A. (2002). Febrile seizures. J. Child Neurol. 17 Suppl 1, S44-52.
86. Spencer, K.A., Tompkins, C.A., and Schulz, R. (1997). Assessment of depression in patients with brain pathology: the case of stroke. Psychol. Bull. 122, 132-152.
87. Strege, P.R., Bernard, C.E., Kraichely, R.E., Mazzone, A., Sha, L., Beyder, A., Gibbons, S.J., Linden, D.R., Kendrick, M.L., Sarr, M.G., et al. (2011). Hydrogen sulfide is a partially redox-independent activator of the human jejunum Na+ channel, Nav1.5. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1105-1114.
88. Stutzbach, L.D., Xie, S.X., Naj, A.C., Albin, R., Gilman S; PSP Genetics Study Group, Lee, V.M., Trojanowski, J.Q., Devlin, B., and Schellenberg, G.D. (2013). The unfolded protein response is activated in disease-affected brain regions in progressive supranuclear palsy and Alzheimer's disease. Acta. Neuropathol. Commun. 1, 31.
89. Sun, Y.G., Cao, Y.X., Wang, W.W., Ma, S.F., Yao, T., and Zhu, Y.C. (2008). Hydrogen sulphide is an inhibitor of L-type calcium channels and mechanical contraction in rat cardiomyocytes. Cardiovasc. Res. 79, 632-641.
90. Sutherland, B.A., Harrison, J.C., Nair, S.M., and Sammut, I.A. (2013). Inhalation gases or gaseous mediators as neuroprotectants for cerebral ischaemia. Curr. Drug Targets 14, 56-73.
91. Szabo, C. (2007). Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 6, 917-935.
92. Taliaz, D., Stall, N., Dar, D.E., and Zangen, A. (2010). Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol. Psychiatry 15, 80-92.
93. Tang, X.Q., Yang, C.T., Chen, J., Yin, W.L., Tian, S.W., Hu, B., Feng, J.Q., and Li, Y.J. (2008). Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells. Clin. Exp. Pharmacol. Physiol. 35, 180-186.
94. Tang, G., Wu, L., and Wang, R. (2010a). Interaction of hydrogen sulfide with ion channels. Clin. Exp. Pharmacol. Physiol. 37, 753-763.
95. Tang, X.Q., Shen, X.T., Huang, Y.E., Ren, Y.K., Chen, R.Q., Hu, B., He, J.Q., Yin, W.L., Xu, J.H., and Jiang, Z.S. (2010b). Hydrogen sulfide antagonizes homocysteine-induced neurotoxicity in PC12 cells. Neurosci. Res. 68, 241-249.
96. Tang, X.Q., Fan, L.L., Li, Y.J., Shen, X.T., Zhuan, Y.Y., He, J.Q., Xu, J.H., Hu, B., and Li, Y.J. (2011). Inhibition of hydrogen sulfide generation contributes to 1-methy-4-phenylpyridinium ion-induced neurotoxicity. Neurotox. Res. 19, 403-411.
97. Tang, X.Q., Zhuang, Y.Y., Fan, L.L., Fang, H.R., Zhou, C.F., Zhang, P., and Hu, B. (2012). Involvement of K(ATP)/PI (3)K/AKT/Bcl-2 pathway in hydrogen sulfide-induced neuroprotection against the toxicity of 1-methy-4-phenylpyridinium ion. J. Mol. Neurosci. 46, 442-449.
98. Tay, A.S., Hu, L.F., Lu, M., Wong, P.T., and Bian, J.S. (2010). Hydrogen sulfide protects neurons against hypoxic injury via stimulation of ATP-sensitive potassium channel/protein kinase C/extracellular signal-regulated kinase/heat shock protein 90 pathway. Neuroscience 167, 277-286.
99. Telezhkin, V., Brazier, S.P., Cayzac, S.H., Wilkinson, W.J., Riccardi, D., and Kemp, P.J. (2010). Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels. Respir. Physiol. Neurobiol. 172, 169-178.
100. Ubuka, T., Umemura, S., Yuasa, S., Kinuta, M., and Watanabe, K. (1978). Purification and characterization of mitochondrial cysteine aminotransferase from rat liver. Physiol. Chem. Phys. 10, 483-500.
101. 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., et al. (2013). Sulfhydration mediates neuroprotective actions of parkin. Nat. Commun. 4, 1626.
102. Wang, R. (2009). Hydrogen sulfide: a new EDRF. Kidney Int. 76, 700-704.
103. Wang, R. (2010). Hydrogen sulfide: the third gasotransmitter in biology and medicine. Antioxid. Redox Signal. 12, 1061-1064.
104. Wang, R. (2012). Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol. Rev. 92, 791-896.
105. Wei, H.J., Xu, J.H., Li, M.H., Tang, J.P., Zou, W., Zhang, P., Wang, L., Wang, C.Y., and Tang, X.Q. (2014). Hydrogen sulfide inhibits homocysteine-induced endoplasmic reticulum stress and neuronal apoptosis in rat hippocampus via upregulation of the BDNF-TrkB pathway. Acta. Pharmacol. Sin. 35, 707-715.
106. Wen, X., Qi, D., Sun, Y., Huang, X., Zhang, F., Wu, J., Fu, Y., Ma, K., Du, Y., Dong, H., et al. (2014). H(2)S attenuates cognitive deficits through Akt1/JNK3 signaling pathway in ischemic stroke. Behav. Brain Res. 269, 6-14.
107. Whitfield, N.L., Kreimier, E.L., Verdial, F.C., Skovgaard, N., and Olson, K.R. (2008). Reappraisal of H2S/sulfide concentration in vertebrate blood and its potential significance in ischemic preconditioning and vascular signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R1930-1937.
108. Wisniewski, K.E., Wisniewski, H.M., and Wen, G.Y. (1985). Occurrence of neuropathological changes and dementia of Alzheimer's disease in Down's syndrome. Ann. Neurol. 17, 278-282.
109. Xu, M., Wu, Y.M., Li, Q., Liu, S., Li, Q., and He, R.R. (2011). Electrophysiological effects of hydrogen sulfide on human atrial fibers. Chin. Med. J. (Engl) 124, 3455-3459.
110. Yang, G.D. and Wang, R. (2007). H(2)S and cellular proliferation and apoptosis. Sheng Li Xue Bao 59, 133-140.
111. Yang, G., Wu, L., Jiang, B., Yang, W., Qi, J., Cao, K., Meng, Q., Mustafa, A.K., Mu, W., Zhang, S., et al. (2008). H2S as a physiologic vasorelaxant: hypertension in mice with deletion of cystathionine gamma-lyase. Science 322, 587-590.
112. Yin, W.L., He, J.Q., Hu, B., Jiang, Z.S., and Tang, X.Q. (2009). Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells. Life Sci. 85, 269-275.
113. Yin, J., Tu, C., Zhao, J., Ou, D., Chen, G., Liu, Y., and Xiao, X. (2013). Exogenous hydrogen sulfide protects against global cerebral ischemia/reperfusion injury via its anti-oxidative, anti-inflammatory and anti-apoptotic effects in rats. Brain Res. 1491, 188-196.
114. 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, 2118-2120.
115. Zhao, H., Chan, S.J., Ng, Y.-K., and Wong, P.T.-H. (2013). Brain 3-mercaptopyruvate sulfurtransferase (3MST): cellular localization and downregulation after acute stroke. PLoS One 8, e67322.