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Hydrogen Sulfide and Pathophysiology of the CNS

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Neurophysiology Aims and scope

The literature data and results of our research team concerning the physiological and pathological effects of hydrogen sulfide, a gas transmitter that has recently attracted significant and increasing attention of neurophysiologists, are analyzed. Hydrogen sulfide is a gaseous signaling molecule, the effects of which were discovered later than those of NO and CO; H2S was found to play great pathophysiological roles in various diseases. This compound is synthesized in the body by enzymatic and non-enzymatic pathways from cysteine, using the pyridoxal 5’-phosphate-dependent enzymes cystathionine β-synthase (CBS) or cystathionine γ-lyase (CSE); 3-mercaptopyruvate sulfurtransferase (3MST) plays a considerable role in H2S catabolism. Abnormal deviations in H2S metabolism are important factors involved in the development of a number of dangerous neurological pathologies, in particular of Parkinson’s disease (PD), Alzheimer’s disease (AD), Huntington’s disease (HD), and Down’s syndrome (DS). This compound was also demonstrated to be involved in various biological and pathophysiological processes in the brain resulting from traumatic brain injury (TBI), stroke, oxidative stress, and cerebral edema. In the case of traumatic injury in the trout brain, the activation of CBS expression in the radial glia phenotypes occurs in the aNSC.

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References

  1. X. Che, Y. Fang, X. Si, et al., “The role of gaseous molecules in traumatic brain injury: an updated review,” Front. Neurosci., 12, 392 (2018). doi: https://doi.org/10.3389/fnins.2018.00392.

    Article  PubMed  PubMed Central  Google Scholar 

  2. J. Zhou, P. F. Wu, F. Wang, and J. G. Chen, “Targeting gaseous molecules to protect against cerebral ischaemic injury: mechanisms and prospects,” Clin. Exp. Pharmacol. Physiol., 39, No. 6, 566–576 (2012). doi: https://doi.org/10.1111/j.1440-1681.2011.05654.x.

    Article  CAS  PubMed  Google Scholar 

  3. J. Deng, C. Lei, Y. Chen, et al., “Neuroprotective gases – fantasy or reality for clinical use?,” Prog. Neurobiol., 115, 210–245 (2014). doi: https://doi.org/10.1016/j.pneurobio.2014.01.001.

    Article  CAS  PubMed  Google Scholar 

  4. U. Förstermann and W. C. Sessa, “Nitric oxide synthases: regulation and function,” Eur. Heart J., 33, No. 7, 829–837 (2012). doi: https://doi.org/10.1093/eurheartj/ehr304.

    Article  CAS  PubMed  Google Scholar 

  5. E. Galea, D. L. Feinstein, and D. J. Reis, “Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures,” Proc. Natl. Acad. Sci. U.S.A., 89, No. 22, 10945–10949 (1992). doi: https://doi.org/10.1073/pnas.89.22.10945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. R. Olivenza, M. A. Moro, I. Lizasoain, et al., “Chronic stress induces the expression of inducible nitric oxide synthase in rat brain cortex,” J. Neurochem., 74, No. 2, 785–791 (2000). doi: https://doi.org/10.1046/j.1471-4159.2000.740785.x.

    Article  CAS  PubMed  Google Scholar 

  7. W. Cai, H. Liu, J. Zhao, et al., “Pericytes in brain injury and repair after ischemic stroke,” Transl. Stroke Res., 8, No. 2, 107–121 (2017). doi: https://doi.org/10.1007/s12975-016-0504-4.

    Article  CAS  PubMed  Google Scholar 

  8. H. Parfenova, and C. W. Leffler, “Cerebroprotective functions of HO-2,” Curr. Pharm. Des., 14, No. 5, 443–453 (2008). doi: https://doi.org/10.2174/138161208783597380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. H. Liu, Y. Wang, Y. Xiao, et al., “Hydrogen sulfide attenuates tissue plasminogen activator-induced cerebral hemorrhage following experimental stroke,” Transl. Stroke Res., 7, No. 3, 209–219 (2016). doi: https://doi.org/10.1007/s12975-016-0459-5.

    Article  CAS  PubMed  Google Scholar 

  10. M. Ishigami, K. Hiraki, K. Umemura, et al., “A source of hydrogen sulfide and a mechanism of its release in the brain,” Antioxid. Redox Signal., 11, No. 2, 205–214 (2009). doi: https://doi.org/10.1089/ars.2008.2132.

    Article  CAS  PubMed  Google Scholar 

  11. N. Shibuya, M. Tanaka, M. Yoshida, et al., “3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain,” Antioxid. Redox Signal., 11, No. 4, 703–714 (2009). doi: https://doi.org/10.1089/ars.2008.2253.

  12. R. Wang, “Two’s company, three’s a crowd: can H2S be the third endogenous gaseous transmitter?,” FASEB J., 16, No. 13, 1792–1798 (2002). doi: https://doi.org/10.1096/fj.02-0211hyp.

    Article  CAS  PubMed  Google Scholar 

  13. E. Łowicka and J. Bełtowski, “Hydrogen sulfide (H2S) – the third gas of interest for pharmacologists,” Pharmacol. Rep., 59, No. 1, 4–24 (2007).

    PubMed  Google Scholar 

  14. R. Wang, “Shared signaling pathways among gasotransmitters,” Proc. Natl. Acad. Sci. U.S.A., 109, No. 23, 8801–8802 (2012). doi: https://doi.org/10.1073/pnas.1206646109.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Y. Liu, R. Yang, X. Liu, et al., “Hydrogen sulfide maintains mesenchymal stem cell function and bone homeostasis via regulation of Ca(2+) channel sulfhydration,” Cell Stem Cell, 15, No. 1, 66–78. (2014). doi: https://doi.org/10.1016/j.stem.2014.03.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. R. F. Furchgott and D. Jothianandan, “Endotheliumdependent and independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light,” Blood Vessels, 28, Nos. 1–3, 52–61 (1991).

    CAS  PubMed  Google Scholar 

  17. P. Mergenthaler, U. Dirnagl, and A. Meisel, “Pathophysiology of stroke: lessons from animal models,” Metab. Brain Dis., 19, Nos. 3–4, 151–167 (2004). doi: https://doi.org/10.1023/b:mebr.0000043966.46964.e6.

    Article  CAS  PubMed  Google Scholar 

  18. G. Cirino, V. Vellecco, and M. Bucci, “Nitric oxide and hydrogen sulfide: the gasotransmitter paradigm of the vascular system,” Br. J. Pharmacol., 174, No. 22, 4021–4031 (2017). doi: https://doi.org/10.1111/bph.13815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. S. Panthi, S. Manandhar, and K. Gautam, “Hydrogen sulfide, nitric oxide, and neurodegenerative disorders,” Transl. Neurodegener., 7, 3 (2018). doi: https://doi.org/10.1186/s40035-018-0108-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. S. Panthi, H.-J. Chung, J. Jung, and N. Y. Jeong, “Physiological importance of hydrogen sulfide: emerging potent neuroprotector and neuromodulator”, Oxid. Med. Cell. Longev., 2016, 9049782 (2016). doi: https://doi.org/10.1155/2016/9049782.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. C. Coletta, A. Papapetropoulos, K. Erdelyi, et al., “Hydrogen sulfide and nitric oxide are mutually dependent in the regulation of angiogenesis and endothelium-dependent vasorelaxation,” Proc. Natl. Acad. Sci. U.S.A., 109, No. 23, 9161–9166 (2012). doi: https://doi.org/10.1073/pnas.1202916109.

    Article  PubMed  PubMed Central  Google Scholar 

  22. S. Taoka and R. Banerjee, “Characterization of NO binding to human cystathionine β-synthase: Possible implications of the effects of CO and NO binding to the human enzyme,” J. Inorg. Biochem., 87, No. 4, 245–251 (2001). doi: https://doi.org/10.1016/s0162-0134(01)00335-x.

    Article  CAS  PubMed  Google Scholar 

  23. J. Bełtowskil and A. Jamroz-Wiśniewska, “Hydrogen sulfide and endothelium-dependent vasorelaxation,” Molecules, 19, No. 12, 21506–21528 (2014). doi: https://doi.org/10.3390/molecules191221183.

    Article  CAS  Google Scholar 

  24. H. Kimura, Y. Nagai, K. Umemura, and Y. Kimura, “Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation,” Antioxid. Redox Signal., 7, Nos. 5–6, 795–803 (2005). doi: https://doi.org/10.1089/ars.2005.7.795.

    Article  CAS  PubMed  Google Scholar 

  25. J. Zhang, Y. Ding, Z. Wang, et al., “Hydrogen sulfide therapy in brain diseases: from bench to bedside,” Med. Gas. Res., 7, No. 2, 113–119 (2017). doi: https://doi.org/10.4103/2045-9912.208517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. K. Qu, S. W. Lee, J. S. Bian, et al., “Hydrogen sulfide: neurochemistry and neurobiology,” Neurochem. Int., 52, Nos. 1–2, 155–165 (2008). doi: https://doi.org/10.1016/j.neuint.2007.05.016.

    Article  CAS  PubMed  Google Scholar 

  27. X. Chen, K. H. Jhee, and W. D. Kruger, “Production of the neuromodulator H2S by cystathionine beta-synthase via the condensation of cysteine and homocysteine,” J. Biol. Chem., 279, No. 50, 52082–52086 (2004). doi: https://doi.org/10.1074/jbc.C400481200.

    Article  CAS  PubMed  Google Scholar 

  28. Y. Mikami, N. Shibuya, Y. Kimura, et al., “Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide,” Biochem. J., 439, No. 3, 479–485 (2011). doi: https://doi.org/10.1042/BJ20110841.

    Article  CAS  PubMed  Google Scholar 

  29. S. Tang, D. Huang, N. An, et al., “A novel pathway for the production of H2S by DAO in rat jejunum,” Neurogastroenterol Motil., 28, No. 5, 687–692 (2016). doi: https://doi.org/10.1111/nmo.12765.

    Article  CAS  PubMed  Google Scholar 

  30. D. J. Polhemus and D. J. Lefer, “Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease,” Circ. Res., 114, No. 4, 730–737 (2014). doi: https://doi.org/10.1161/CIRCRESAHA.114.300505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. A. Hermann, G. F. Sitdikova, and T. M. Weiger, Gasotransmitters: Physiology and Pathophysiology, Springer, 163–201 (2012).

  32. B. H. Tan, P. T.-H. Wong, and J.-S. Bian, “Hydrogen sulfide: a novel signaling molecule in the central nervous system,” Neurochem. Int., 56, No. 1, 3–10 (2010). doi: https://doi.org/10.1016/j.neuint.2009.08.008.

    Article  CAS  PubMed  Google Scholar 

  33. K. Kida and F. Ichinose, “Hydrogen sulfide and neuroinflammation,” Handb. Exp. Pharmacol., 230, 181–189 (2015). doi: https://doi.org/10.1007/978-3-319-18144-8_9.

    Article  CAS  PubMed  Google Scholar 

  34. L. Xie, L.-F. Hu, X. Q. Teo, et al., “Therapeutic effect of hydrogen sulfide-releasing L-Dopa derivative ACS84 on 6-OHDA-induced Parkinson’s disease rat model,” PLoS One, 8, No. 4, e60200. (2013). doi: https://doi.org/10.1371/journal.pone.0060200.

  35. X. Cao, L. Cao, L. Ding, and J. Bian, “A new hope for a devastating disease: hydrogen sulfide in Parkinson’s disease,” Mol. Neurobiol., 55, No. 5, 3789–3799 (2017).

    PubMed  Google Scholar 

  36. A. Xuan, D. Long, J. Li, et al., “Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in β-amyloid rat model of Alzheimer’s disease,” J. Neuroinflammation, 9, 202 (2012). doi: https://doi.org/10.1186/1742-2094-9-202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. K. Eto, T. Asada, K. Arima, et al., “Brain hydrogen sulfide is severely decreased in Alzheimer’s disease,” Biochem. Biophys. Res. Commun., 293, No. 5, 1485–1488 (2002). doi: https://doi.org/10.1016/S0006-291X(02)00422-9.

    Article  CAS  PubMed  Google Scholar 

  38. L.-M. Zhang, C.-X. Jiang, and D.-W. Liu, “Hydrogen sulfide attenuates neuronal injury induced by vascular dementia via inhibiting apoptosis in rats,” Neurochem. Res., 34, No. 11, 1984–1992 (2009). doi: https://doi.org/10.1007/s11064-009-0006-9.

    Article  CAS  PubMed  Google Scholar 

  39. D. Giuliani, A. Ottani, D. Zaffe, et al., “Hydrogen sulfide slows down progression of experimental Alzheimer’s disease by targeting multiple pathophysiological mechanisms,” Neurobiol. Learn. Mem., 104, 82–91 (2013). doi: https://doi.org/10.1016/j.nlm.2013.05.006.

    Article  CAS  PubMed  Google Scholar 

  40. B. D. Paul, J. I. Sbodio, R. Xu, et al., “Cystathionine γ-lyase deficiency mediates neurodegeneration in Huntington’s disease,” Nature, 509, No. 7498, 96–100 (2014). doi: https://doi.org/10.1038/nature13136.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. H. Kimura, N. Shibuya, and Y. Kimura, “Hydrogen sulfide is a signaling molecule and a cytoprotectant,” Antioxid. Redox Signal., 17, No. 1, 45–57 (2012). doi: https://doi.org/10.1089/ars.2011.4345.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. S. W. Lee, Y.-S. Hu, L.-F. Hu, et al., “Hydrogen sulphide regulates calcium homeostasis in microglial cells,” Glia, 54, No. 2, 116–124 (2006). doi: https://doi.org/10.1002/glia.20362.

  43. J. F. Wang, Y. Li, J. N. Song, and H. G. Pang, “Role of hydrogen sulfide in secondary neuronal injury,” Neurochem. Int., 64, 37–47 (2014). doi: https://doi.org/10.1016/j.neuint.2013.11.002.

    Article  CAS  PubMed  Google Scholar 

  44. A. G. Mustafa and O. A. Alshboul, “Pathophysiology of traumatic brain injury,” Neurosciences (Riyadh), 18, No. 3, 222–234 (2013).

    Google Scholar 

  45. S. A. Karimi, N. Hosseinmardi, M. Janahmadi, et al., “The protective effect of hydrogen sulfide (H2S) on traumatic brain injury (TBI) induced memory deficits in rats,” Brain Res. Bull., 134, 177–182 (2017). doi: https://doi.org/10.1016/j.brainresbull.2017.07.014.

    Article  CAS  PubMed  Google Scholar 

  46. M. Zhang, H. Shan, T. Wang, et al., “Dynamic change of hydrogen sulfide after traumatic brain injury and its effect in mice,” Neurochem. Res., 38, No. 4, 714–725 (2013). doi: https://doi.org/10.1007/s11064-013-0969-4.

    Article  CAS  PubMed  Google Scholar 

  47. Q.-J. Chu, L. He, W. Zhang, et al., “Hydrogen sulfide attenuates surgical trauma-induced inflammatory response and cognitive deficits in mice,” J. Surg. Res., 183, No. 1, 330–336 (2013).

    Article  CAS  Google Scholar 

  48. S. W. Scheff, M. A. Ansari, and K. N. Roberts, “Neuroprotective effect of Pycnogenol(R) following traumatic brain injury,” Exp. Neurol., 239, 183–191 (2013). doi: https://doi.org/10.1016/j.expneurol.2012.09.019.

    Article  CAS  PubMed  Google Scholar 

  49. R. Wang, “Physiological implication of hydrogen sulfide: a whiff exploration that blossomed,” Physiol. Rev., 92, No. 2, 791–896 (2012).

    Article  CAS  Google Scholar 

  50. X. Jiang, Y. Huang, W. Lin, et al., “Protective effects of hydrogen sulfide in a rat model of traumatic brain injury via activation of mitochondrial adenosine triphosphate-sensitive potassium channels and reduction of oxidative stress,” J. Surg. Res. 184, No. 2, e27–e35 (2013). doi: https://doi.org/10.1016/j.jss.2013.03.067.

    Article  CAS  PubMed  Google Scholar 

  51. M. Zhang, H. Shan, P. Chang, et al., “Hydrogen sulfide offers neuroprotection on traumatic brain injury in parallel with reduced apoptosis and autophagy in mice,” PLoS One, 9, No. 1, e87241 (2014). doi: https://doi.org/10.1371/journal.pone.0087241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. K. Qu, C. P. Chen, B. Halliwell, et al., “Hydrogen sulfide is a mediator of cerebral ischemic damage,” Stroke, 37, No. 3, 889–893 (2006). doi: https://doi.org/10.1161/01.STR.0000204184.34946.41.

    Article  CAS  PubMed  Google Scholar 

  53. C. W. Leffler, H. Parfenova, S. Basuroy, et al., “Hydrogen sulfide and cerebral microvascular tone in newborn pigs,” Am. J. Physiol. Heart. Circ. Physiol., 300, No. 2, H440–H447 (2011). doi: https://doi.org/10.1152/ajpheart.00722.2010.

    Article  CAS  PubMed  Google Scholar 

  54. G. H. Liang, A. Adebiyi, M. D. Leo, et al., “Hydrogen sulfide dilates cerebral arterioles by activating smooth muscle cell plasma membrane KATP channels,” Am. J. Physiol. Heart Circ. Physiol., 300, No. 6, H2088–H2095 (2011). doi: https://doi.org/10.1152/ajpheart.01290.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. T. Kalogeris, C. P Baines, M. Krenz, and R. J. Korthuis, “Cell biology of ischemia/reperfusion injury,” Int. Rev. Cell Mol. Biol., 298, 229–317 (2012). doi: https://doi.org/10.1016/B978-0-12-394309-5.00006-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. K. Abe and H. Kimura, “The possible role of hydrogen sulfide as an endogenous neuromodulator,” J. Neurosci., 16, No. 3, 1066–1071 (1996). doi: https://doi.org/10.1523/JNEUROSCI.16-03-01066.1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Y. Nagai, M. Tsugane, J.-I. Oka, and H. Kimura, “Hydrogen sulfide induces calcium waves in astrocytes,” FASEB J., 18, No. 3, 557–559 (2004). doi: https://doi.org/10.1096/fj.03-1052fje.

    Article  CAS  PubMed  Google Scholar 

  58. M. Lee, C. Schwab, S. Yu, E. McGeer, and P. L. Mc-Geer, “Astrocytes produce the anti-inflammatory and neuroprotective agent hydrogen sulfide,” Neurobiol. Aging, 30, No. 10, 1523–1534 (2009). doi: https://doi.org/10.1016/j.neurobiolaging.2009.06.001.

    Article  CAS  PubMed  Google Scholar 

  59. P. Nagy and C. Winterbourn, “Rapid reaction of hydrogen sulfide with the neutrophil oxidant hypochlorous acid to generate polysulfides,” Chem. Res. Toxicol., 23, No. 10, 1541–1543 (2010). doi: https://doi.org/10.1021/tx100266a.

    Article  CAS  PubMed  Google Scholar 

  60. Y. Kimura, Y. Mikami, K. Osumi, et al., “Polysulfides are possible H2S-derived signaling molecules in rat brain,” FASEB J., 27, No. 6, 2451–2457 (2013). doi: https://doi.org/10.1096/fj.12-226415.

    Article  CAS  PubMed  Google Scholar 

  61. H. Kimura, ‘Physiological role of hydrogen sulfide and polysulfide in the central nervous system,” Neurochem. Int., 63, No. 5, 492–497 (2013). doi: https://doi.org/10.1016/j.neuint.2013.09.003.

    Article  CAS  PubMed  Google Scholar 

  62. P. Gopalakrishnan, B. Shrestha, A. M. Kaskas, et al., “Hydrogen sulfide: therapeutic or injurious in ischemic stroke?,” Pathophysiology, 26, No. 1, 1–10 (2019). doi: https://doi.org/10.1016/j.pathophys.2018.10.005.

    Article  CAS  PubMed  Google Scholar 

  63. Y. Kimura, R. Dargusch, D. Schubert, and H. Kimura, “Hydrogen sulfide protects HT22 neuronal cells from oxidative stress,” Antioxid. Redox Signal., 8, Nos. 3–4, 661–670 (2006). doi: https://doi.org/10.1089/ars.2006.8.661.

    Article  CAS  PubMed  Google Scholar 

  64. L. Xiao, A. Lan, L. Mo, et al., “Hydrogen sulfide protects PC12 cells against reactive oxygen species and extracellular signal-regulated kinase 1/2-mediated downregulation of glutamate transporter-1 expression induced by chemical hypoxia,” Int. J. Mol. Med., 30, No. 5, 1126–1132 (2012). doi: https://doi.org/10.3892/ijmm.2012.1090.

    Article  CAS  PubMed  Google Scholar 

  65. N. S. Cheung, Z. F. Peng, M. J. Chen, et al., “Hydrogen sulfide induced neuronal death occurs via glutamate receptor and is associated with calpain activation and lysosomal rupture in mouse primary cortical neurons,” Neuropharmacology, 53, No. 4, 505–514 (2007). doi: https://doi.org/10.1016/j.neuropharm.2007.06.014.

  66. J. Wu, J. D. Holstein, G. Upadhyay, et al., “Purinergic receptor-stimulated IP3-mediated Ca2+ release enhances neuroprotection by increasing astrocyte mitochondrial metabolism during aging,” J. Neurosci., 27, No. 24, 6510–6520 (2007). doi: https://doi.org/10.1523/JNEUROSCI.1256-07.2007.

  67. M. Fu, W. Zhang, L. Wu, et al., “Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production,” Proc. Natl. Acad. Sci. U.S.A., 109, No. 8, 2943–2948 (2012). doi: https://doi.org/10.1073/pnas.1115634109.

  68. Y. Luo, X. Yang, S. Zhao, et al., “Hydrogen sulfide prevents OGD/R-induced apoptosis via improving mitochondrial dysfunction and suppressing an ROSmediated caspase-3 pathway in cortical neurons,” Neurochem. Int., 63, No. 8, 826–831 (2013). doi: https://doi.org/10.1016/j.neuint.2013.06.004.

  69. X. Wei, B. Zhang, L. Cheng, et al., “Hydrogen sulfide induces neuroprotection against experimental stroke in rats by down-regulation of AQP4 via activating PKC,” Brain Res., 1622, 292–299 (2015). doi: https://doi.org/10.1016/j.brainres.2015.07.001.

    Article  CAS  PubMed  Google Scholar 

  70. Z. Jiang, C. Li, M. L. Manuel, et al., “Role of hydrogen sulfide in early blood-brain barrier disruption following transient focal cerebral ischemia,” PLoS One, 10, No. 2, e0117982 (2015). doi: https://doi.org/10.1371/journal.pone.0117982.

  71. N. Ballatori, S. M. Krance, S. Notenboom, et al., “Glutathione dysregulation and the etiology and progression of human diseases,” Biol. Chem., 390, 3, 191–214 (2009). doi: https://doi.org/10.1515/BC.2009.033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Y. Hu, R. Li, H. Yang, et al., “Sirtuin 6 is essential for sodium sulfide-mediated cytoprotective effect in ischemia/reperfusion-stimulated brain endothelial cells,” J. Stroke Cerebrovasc. Dis., 24, No. 3, 601–609 (2015). doi: https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.10.006.

  73. Q. Yu, Z. Lu, L. Tao, et al., “ROS-dependent neuroprotective effects of NaHS in ischemia brain injury involves the PARP/AIF pathway,” Cell. Physiol. Biochem., 36, No. 4, 1539–1551 (2015). doi: https://doi.org/10.1159/000430317.

  74. A. K. Samhan-Arias, M. A. Garcia-Bereguiain, and C. Gutierrez-Merino, “Hydrogen sulfide is a reversible inhibitor of the NADH oxidase activity of synaptic plasma membranes,” Biochem. Biophys. Res. Commun., 388, No. 4, 718–722 (2009). doi: https://doi.org/10.1016/j.bbrc.2009.08.076.

    Article  CAS  PubMed  Google Scholar 

  75. M. Whiteman, J. S. Armstrong, S. H. Chu, et al., “The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite ’scavenger’?,” J. Neurochem., 90, No. 3, 765–768 (2004). doi: https://doi.org/10.1111/j.1471-4159.2004.02617.x.

    Article  CAS  PubMed  Google Scholar 

  76. S. J. Chan, C. Chai, T. W. Lim, et al., “Cystathionine β-synthase inhibition is a potential therapeutic approach to treatment of ischemic injury,” ASN Neuro., 7, No. 2, 1759091415578711 (2015). doi: https://doi.org/10.1177/1759091415578711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. K. N. Islam, D. J. Polhemus, E. Donnarumma, et al., “Hydrogen sulfide levels and nuclear factor-erythroid 2-related factor 2 (NRF2) activity are attenuated in the setting of critical limb ischemia (CLI),” J. Am. Heart Assoc., 4 No. 5, e001986 (2015). doi: https://doi.org/10.1161/JAHA.115.001986.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. R. J. Bridges, N. R. Natale, and S. A. Patel, “System xc cystine/glutamate antiporter: an update on molecular pharmacology and roles within the CNS,” Br. J. Pharmacol., 165, No. 1, 20–34 (2012). doi: https://doi.org/10.1111/j.1476-5381.2011.01480.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. B. Adolf, P. Chapouton, C. S. Lam, et al., “Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon,” Dev. Biol., 29, No. 1, 278–293 (2006). doi: https://doi.org/10.1016/j.ydbio.2006.03.023.

    Article  CAS  Google Scholar 

  80. Y. Ito, H. Tanaka, H. Okamoto, and T. Ohshima, “Characterization of neural stem cells and their progeny in the adult zebrafish optic tectum,” Dev. Biol., 342, No. 1, 26–38 (2010). doi: https://doi.org/10.1016/j.ydbio.2010.03.008.

    Article  CAS  PubMed  Google Scholar 

  81. E. Than-Trong and L. Bally-Cuif, “Radial glia and neural progenitors in the adult zebrafish central nervous system,” Glia, 63, No. 8, 1406–1428 (2015). doi: https://doi.org/10.1002/glia.22856.

    Article  PubMed  Google Scholar 

  82. G. K. H. Zupanc and R. F. Sîrbulescu, “Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish,” Eur. J. Neurosci., 34, 917–929 (2011). doi: https://doi.org/10.1111/j.1460-9568.2011.07854.x.

    Article  PubMed  Google Scholar 

  83. E. V. Pushchina, A. A. Varaksin, D. K. Obukhov, and I. M. Prudnikov, “GFAP expression in the optic nerve and increased Н2S generation in the integration centers of the rainbow trout (Oncorhynchus mykiss) brain after unilateral eye injury,” Neural. Regen. Res., 15, No. 10, 1867–1886 (2020). doi:https://doi.org/10.4103/1673-5374.280320.

    Article  PubMed  PubMed Central  Google Scholar 

  84. E. V. Pushchina, A. A. Varaksin, and D. K. Obukhov, “Cystathionine β-synthase in the brain of the trout Oncorhynchus mykiss after unilateral eye damage and in conditions of in vitro cultivation,” Russ. J. Dev. Biol., 50, 39–58 (2019).

    Article  Google Scholar 

  85. E. V. Pushchina, A. A. Varaksin, and D. K. Obukhov, “Cystathionine β-synthase in the CNS of masu salmon Oncorhynchus masou (Salmonidae) and carp Cyprinus carpio (Cyprinidae),” Neurochem. J., 5, 24–34 (2011).

  86. E. V. Pushchina and A. A. Varaksin, “Hydrogen sulfide, parvalbumin-, and GABA-producing system in the masu salmon brain,” Neurophysiology, 43, 109–122 (2011).

    Google Scholar 

  87. B. Cuoghi and L. Mola, “Macroglial cells of the teleost central nervous system: a survey of the main types,” Cell Tissue Res., 338, No. 3, 319–332 (2009).

    Article  Google Scholar 

  88. E. V. Pushchina, S. Shukla, A. A. Varaksin, and D. K. Obukhov, “Cell proliferation and apoptosis in optic nerve and brain integration centers of adult trout Oncorhynchus mykiss after optic nerve injury,” Neural. Regen. Res., 11, No. 4, 578–590 (2016). doi: https://doi.org/10.4103/1673-5374.180742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. M. Arochena, R. Anadón, and S. M. Díaz-Regueira, “Development of vimentin and glial fibrillary acidic protein immunoreactivities in the brain of gray mullet (Chelon labrosus), an advanced teleost,” J. Comp. Neurol., 469, No. 3, 413–436 (2004).

    Article  CAS  Google Scholar 

  90. A. Alunni, S. Vaccari, S. Torcia, et al., “Characterization of glial fibrillary acidic protein and astroglial architecture in the brain of a continuously growing fish, the rainbow trout,” Eur. J. Histochem., 49, No. 2, 51–60 (2005).

    Google Scholar 

  91. M. Kálmán, “Astroglial architecture of the carp (Cyprinus carpio) brain as revealed by immunohistochemical staining against glial fibrillary acidic protein (GFAP),” Anat. Embryol. (Berl.), 198, No. 5, 409–433 (1998).

    Article  Google Scholar 

  92. J. Ganz, S. Kaslin, D. Hochmann, et al., “Heterogeneity and independence of adult neural progenitors in the zebrafish telencephalon,” Glia, 58, No. 11, 1345–1363 (2010). doi: https://doi.org/10.1002/glia.21012.

    Article  PubMed  Google Scholar 

  93. M. März, N. Chapouton, C. Diotel, et al., “Heterogeneity in progenitor cell subtypes in the ventricular zone of the zebrafish adult telencephalon,” Glia, 58, No. 7, 870–888 (2010). doi: https://doi.org/10.1002/glia.20971.

    Article  PubMed  Google Scholar 

  94. E. V. Pushchina, A. A. Varaksin, and D. K. Obukhov, “Reparative neurogenesis in the brain and changes in the optic nerve of adult trout Oncorhynchus mykiss after mechanical damage of the eye,” Russ. J. Dev. Biol., 47, 11–32 (2016).

    Article  Google Scholar 

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Pushchina, E.V., Marinina, K.S. & Myasoyedov, S.D. Hydrogen Sulfide and Pathophysiology of the CNS. Neurophysiology 52, 308–321 (2020). https://doi.org/10.1007/s11062-021-09887-4

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