Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 9049782, 11 pages
http://dx.doi.org/10.1155/2016/9049782
Review Article

Physiological Importance of Hydrogen Sulfide: Emerging Potent Neuroprotector and Neuromodulator

1Department of Biomedical Science, Graduate School, Kyung Hee University, No. 26, Kyungheedae-ro, Dongdaemun-gu, Seoul 02447, Republic of Korea
2Department of Anesthesiology and Pain Medicine, College of Medicine, Kosin University, No. 262, Gamcheon-ro, Seo-gu, Busan 49267, Republic of Korea
3Department of Anatomy and Neurobiology, College of Medicine, Kyung Hee University, No. 26, Kyungheedae-ro, Dongdaemun-gu, Seoul 02447, Republic of Korea
4Department of Anatomy and Cell Biology, College of Medicine, Dong-A University, No. 32, Daesingongwon-ro, Seo-gu, Busan 49201, Republic of Korea

Received 6 April 2016; Accepted 24 May 2016

Academic Editor: Yanxi Pei

Copyright © 2016 Sandesh Panthi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. K. Kashfi and K. R. Olson, “Biology and therapeutic potential of hydrogen sulfide and hydrogen sulfide-releasing chimeras,” Biochemical Pharmacology, vol. 85, no. 5, pp. 689–703, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. K. M. Holwerda, S. A. Karumanchi, and A. T. Lely, “Hydrogen sulfide: role in vascular physiology and pathology,” Current Opinion in Nephrology and Hypertension, vol. 24, no. 2, pp. 170–176, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Wang, “Hydrogen sulfide: the third gasotransmitter in biology and medicine,” Antioxidants & Redox Signaling, vol. 12, no. 9, pp. 1061–1064, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Furne, A. Saeed, and M. D. Levitt, “Whole tissue hydrogen sulfide concentrations are orders of magnitude lower than presently accepted values,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 295, no. 5, pp. R1479–R1485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Qu, S. W. Lee, J. S. Bian, C.-M. Low, and P. T.-H. Wong, “Hydrogen sulfide: neurochemistry and neurobiology,” Neurochemistry International, vol. 52, no. 1-2, pp. 155–165, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Cuevasanta, A. Denicola, B. Alvarez, and M. N. Möller, “Solubility and permeation of hydrogen sulfide in lipid membranes,” PLoS ONE, vol. 7, no. 4, Article ID e34562, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Kimura, “Production and physiological effects of hydrogen sulfide,” Antioxidants and Redox Signaling, vol. 20, no. 5, pp. 783–793, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Wang, “Physiological implications of hydrogen sulfide: a whiff exploration that blossomed,” Physiological Reviews, vol. 92, no. 2, pp. 791–896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Kimura, “Physiological role of hydrogen sulfide and polysulfide in the central nervous system,” Neurochemistry International, vol. 63, no. 5, pp. 492–497, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. X. Zhang and J.-S. Bian, “Hydrogen sulfide: a neuromodulator and neuroprotectant in the central nervous system,” ACS Chemical Neuroscience, vol. 5, no. 10, pp. 876–883, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Gheibi, N. Aboutaleb, M. Khaksari et al., “Hydrogen sulfide protects the brain against ischemic reperfusion injury in a transient model of focal cerebral ischemia,” Journal of Molecular Neuroscience, vol. 54, no. 2, pp. 264–270, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. B. S. Park, H.-W. Kim, I. J. Rhyu et al., “Hydrogen sulfide is essential for Schwann cell responses to peripheral nerve injury,” Journal of Neurochemistry, vol. 132, no. 2, pp. 230–242, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. Q.-H. Gong, X.-R. Shi, Z.-Y. Hong, L.-L. Pan, X.-H. Liu, and Y.-Z. Zhu, “A new hope for neurodegeneration: possible role of hydrogen sulfide,” Journal of Alzheimer's Disease, vol. 24, supplement 2, pp. 173–182, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. P. K. Moore and M. Whiteman, Chemistry, Biochemistry and Pharmacology of Hydrogen Sulfide, Springer, Berlin, Germany, 2015.
  15. J. Y. Jung and N. Y. Jeong, “Hydrogen sulfide controls peripheral nerve degeneration and regeneration: a novel therapeutic strategy for peripheral demyelinating disorders or nerve degenerative diseases,” Neural Regeneration Research, vol. 9, no. 24, pp. 2119–2121, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Mikami, N. Shibuya, Y. Kimura, N. Nagahara, Y. Ogasawara, and H. Kimura, “Thioredoxin and dihydrolipoic acid are required for 3-mercaptopyruvate sulfurtransferase to produce hydrogen sulfide,” Biochemical Journal, vol. 439, no. 3, pp. 479–485, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Julian, J. L. Statile, S. E. Wohlgemuth, and A. J. Arp, “Enzymatic hydrogen sulfide production in marine invertebrate tissues,” Comparative Biochemistry and Physiology, Part A—Molecular and Integrative Physiology, vol. 133, no. 1, pp. 105–115, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Kamoun, “H2S, un nouveau neuromodulateur,” Médecine/Sciences, vol. 20, no. 6-7, pp. 697–700, 2004. View at Publisher · View at Google Scholar
  19. X. Chen, K.-H. Jhee, and W. D. Kruger, “Production of the neuromodulator H2S by cystathionine β-synthase via the condensation of cysteine and homocysteine,” The Journal of Biological Chemistry, vol. 279, no. 50, pp. 52082–52086, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. O. Kabil, V. Vitvitsky, P. Xie, and R. Banerjee, “The quantitative significance of the transsulfuration enzymes for H2S production in murine tissues,” Antioxidants & Redox Signaling, vol. 15, no. 2, pp. 363–372, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. L. L. Pan, X. H. Liu, Q. H. Gong, H. B. Yang, and Y. Z. Zhu, “Role of cystathionine γ-Lyase/hydrogen sulfide pathway in cardiovascular disease: a novel therapeutic strategy?” Antioxidants & Redox Signaling, vol. 17, no. 1, pp. 106–118, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. N. Shibuya, M. Tanaka, M. Yoshida et al., “3-Mercaptopyruvate sulfurtransferase produces hydrogen sulfide and bound sulfane sulfur in the brain,” Antioxidants and Redox Signaling, vol. 11, no. 4, pp. 703–714, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Ishigami, K. Hiraki, K. Umemura, Y. Ogasawara, K. Ishii, and H. Kimura, “A source of hydrogen sulfide and a mechanism of its release in the brain,” Antioxidants and Redox Signaling, vol. 11, no. 2, pp. 205–214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Tang, D. Huang, N. An, D. Chen, and D. Zhao, “A novel pathway for the production of H2S by DAO in rat jejunum,” Neurogastroenterology & Motility, vol. 28, no. 5, pp. 687–692, 2016. View at Publisher · View at Google Scholar
  25. N. Shibuya, S. Koike, M. Tanaka et al., “P33 A novel pathway for the production of hydrogen sulfide from d-cysteine in mammalian cells,” Nitric Oxide, vol. 39, supplement, article S26, 2014. View at Publisher · View at Google Scholar
  26. N. Shibuya, S. Koike, M. Tanaka et al., “A novel pathway for the production of hydrogen sulfide from D-cysteine in mammalian cells,” Nature Communications, vol. 4, article 1366, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. G. A. Aboalsamh, “Mitochondria-Targeted Hydrogen Sulphide Donors Protect Renal Cells From Hypoxia Re-Oxygenation Injury,” Electronic Thesis and Dissertation Repository, Paper 2912, 2015.
  28. H. Zhang, P. Wang, G. Chen, H.-Y. Cheung, and H. Sun, “A highly sensitive fluorescent probe for imaging hydrogen sulfide in living cells,” Tetrahedron Letters, vol. 54, no. 36, pp. 4826–4829, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Kimura, “Hydrogen sulfide: its production, release and functions,” Amino Acids, vol. 41, no. 1, pp. 113–121, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. M. S. Vandiver and S. H. Snyder, “Hydrogen sulfide: a gasotransmitter of clinical relevance,” Journal of Molecular Medicine, vol. 90, no. 3, pp. 255–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Abe and H. Kimura, “The possible role of hydrogen sulfide as an endogenous neuromodulator,” The Journal of Neuroscience, vol. 16, no. 3, pp. 1066–1071, 1996. View at Google Scholar · View at Scopus
  32. 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,” Journal of Inorganic Biochemistry, vol. 87, no. 4, pp. 245–251, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. W. Zhao, J. Zhang, Y. Lu, and R. Wang, “The vasorelaxant effect of H2S as a novel endogenous gaseous KATP channel opener,” The EMBO Journal, vol. 20, no. 21, pp. 6008–6016, 2001. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Bełtowski and A. Jamroz-Wiśnniewska, “Hydrogen sulfide and endothelium-dependent vasorelaxation,” Molecules, vol. 19, no. 12, pp. 21506–21528, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. 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,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 23, pp. 9161–9166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. Q.-C. Yong, J. L. Cheong, F. Hua et al., “Regulation of heart function by endogenous gaseous mediators-crosstalk between nitric oxide and hydrogen sulfide,” Antioxidants and Redox Signaling, vol. 14, no. 11, pp. 2081–2091, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. Z. Altaany, G. Yang, and R. Wang, “Crosstalk between hydrogen sulfide and nitric oxide in endothelial cells,” Journal of Cellular and Molecular Medicine, vol. 17, no. 7, pp. 879–888, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. D. J. Polhemus and D. J. Lefer, “Emergence of hydrogen sulfide as an endogenous gaseous signaling molecule in cardiovascular disease,” Circulation Research, vol. 114, no. 4, pp. 730–737, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. V. Telezhkin, S. P. Brazier, S. Cayzac, C. T. Müller, D. Riccardi, and P. J. Kemp, “Hydrogen sulfide inhibits human BKCa channels,” in Arterial Chemoreceptors, pp. 65–72, Springer, New York, NY, USA, 2009. View at Google Scholar
  40. M. Whiteman, N. S. Cheung, Y.-Z. Zhu et al., “Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain?” Biochemical and Biophysical Research Communications, vol. 326, no. 4, pp. 794–798, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Whiteman, J. S. Armstrong, S. H. Chu et al., “The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite ‘scavenger’?” Journal of Neurochemistry, vol. 90, no. 3, pp. 765–768, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Han, J. Qin, X. Chang, Z. Yang, D. Bu, and J. Du, “Modulating effect of hydrogen sulfide on gamma-aminobutyric acid B receptor in recurrent febrile seizures in rats,” Neuroscience Research, vol. 53, no. 2, pp. 216–219, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. R. C. Koehler, D. Gebremedhin, and D. R. Harder, “Role of astrocytes in cerebrovascular regulation,” Journal of Applied Physiology, vol. 100, no. 1, pp. 307–317, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Wojtera, B. Sikorska, T. Sobow, and P. P. Liberski, “Microglial cells in neurodegenerative disorders,” Folia Neuropathologica, vol. 43, no. 4, pp. 311–321, 2005. View at Google Scholar · View at Scopus
  45. Y. S. Kim and T. H. Joh, “Microglia, major player in the brain inflammation: their roles in the pathogenesis of Parkinson's disease,” Experimental and Molecular Medicine, vol. 38, no. 4, pp. 333–347, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. S. W. Lee, Y.-S. Hu, L.-F. Hu et al., “Hydrogen sulphide regulates calcium homeostasis in microglial cells,” Glia, vol. 54, no. 2, pp. 116–124, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. J.-F. Wang, Y. Li, J.-N. Song, and H.-G. Pang, “Role of hydrogen sulfide in secondary neuronal injury,” Neurochemistry International, vol. 64, no. 1, pp. 37–47, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Malik and A. V. Ferguson, “Hydrogen sulfide depolarizes neurons in the nucleus of the solitary tract of the rat,” Brain Research, vol. 1633, pp. 1–9, 2016. View at Publisher · View at Google Scholar
  49. T. Li, H. Liu, H. Xue et al., “Neuroprotective effects of hydrogen sulfide against early brain injury and secondary cognitive deficits following subarachnoid hemorrhage,” Brain Pathology, 2016. View at Publisher · View at Google Scholar
  50. L.-F. Hu, M. Lu, C. X. Tiong, G. S. Dawe, G. Hu, and J.-S. Bian, “Neuroprotective effects of hydrogen sulfide on Parkinson's disease rat models,” Aging Cell, vol. 9, no. 2, pp. 135–146, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. A. D. Korczyn, “Vascular contribution to dementia in Parkinson's disease,” Neurodegenerative Diseases, vol. 7, no. 1–3, pp. 127–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. L.-F. Hu, M. Lu, P. T. Hon Wong, and J.-S. Bian, “Hydrogen sulfide: neurophysiology and neuropathology,” Antioxidants and Redox Signaling, vol. 15, no. 2, pp. 405–419, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. C. X. Tiong, M. Lu, and J.-S. Bian, “Protective effect of hydrogen sulphide against 6-OHDA-induced cell injury in SH-SY5Y cells involves PKC/PI3K/Akt pathway,” British Journal of Pharmacology, vol. 161, no. 2, pp. 467–480, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Hattoria, M. Wanga, H. Taka et al., “Toxic effects of dopamine metabolism in Parkinson's disease,” Parkinsonism and Related Disorders, vol. 15, no. 1, pp. S35–S38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Jankovic and M. Stacy, “Medical management of levodopa-associated motor complications in patients with Parkinson's disease,” CNS Drugs, vol. 21, no. 8, pp. 677–692, 2007. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Lu, L.-F. Hu, G. Hu, and J.-S. Bian, “Hydrogen sulfide protects astrocytes against H2O2-induced neural injury via enhancing glutamate uptake,” Free Radical Biology and Medicine, vol. 45, no. 12, pp. 1705–1713, 2008. View at Publisher · View at Google Scholar · View at Scopus
  57. X. Xue and J.-S. Bian, “Neuroprotective effects of hydrogen sulfide in Parkinson's disease animal models: methods and protocols,” Methods in Enzymology, vol. 554, pp. 169–186, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Wang, J. Zhu, Y. Pan et al., “Hydrogen sulfide functions as a neuromodulator to regulate striatal neurotransmission in a mouse model of Parkinson's disease,” Journal of Neuroscience Research, vol. 93, no. 3, pp. 487–494, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. O. Cakmak, “Coffee consumption, smoking, and Parkinson's disease? The beneficial role of hydrogen sulfide,” Movement Disorders, vol. 31, no. 3, p. 429, 2016. View at Publisher · View at Google Scholar
  60. H. Hampel, “Amyloid-β and cognition in aging and Alzheimer's disease: molecular and neurophysiological mechanisms,” Journal of Alzheimer's Disease, vol. 33, no. 1, pp. S79–S86, 2013. View at Publisher · View at Google Scholar · View at Scopus
  61. M. S. Parihar and T. Hemnani, “Alzheimer's disease pathogenesis and therapeutic interventions,” Journal of Clinical Neuroscience, vol. 11, no. 5, pp. 456–467, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. K. Iqbal and I. Grundke-Iqbal, “Opportunities and challenges in developing Alzheimer disease therapeutics,” Acta Neuropathologica, vol. 122, no. 5, pp. 543–549, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. L. D. Morrison, D. D. Smith, and S. J. Kish, “Brain S-adenosylmethionine levels are severely decreased in Alzheimer's disease,” Journal of Neurochemistry, vol. 67, no. 3, pp. 1328–1331, 1996. View at Google Scholar · View at Scopus
  64. X.-Q. Liu, X.-Q. Liu, P. Jiang, H. Huang, and Y. Yan, “Plasma levels of endogenous hydrogen sulfide and homocysteine in patients with Alzheimer's disease and vascular dementia and the significance thereof,” National Medical Journal of China, vol. 88, no. 32, pp. 2246–2249, 2008. View at Google Scholar · View at Scopus
  65. X.-Q. Tang, X.-T. Shen, Y.-E. Huang et al., “Hydrogen sulfide antagonizes homocysteine-induced neurotoxicity in PC12 cells,” Neuroscience Research, vol. 68, no. 3, pp. 241–249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Zhang, Z.-H. Tang, Z. Ren et al., “Hydrogen sulfide, the next potent preventive and therapeutic agent in aging and age-associated disease,” Molecular and Cellular Biology, vol. 33, no. 6, pp. 1104–1113, 2013. View at Publisher · View at Google Scholar · View at Scopus
  67. Y.-Y. Liu and J.-S. Bian, “Hydrogen sulfide protects amyloid-β induced cell toxicity in microglia,” Journal of Alzheimer's Disease, vol. 22, no. 4, pp. 1189–1200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. S. M. Schreier, M. K. Muellner, H. Steinkellner et al., “Hydrogen sulfide scavenges the cytotoxic lipid oxidation product 4-HNE,” Neurotoxicity Research, vol. 17, no. 3, pp. 249–256, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. Y.-D. Wen, H. Wang, S.-H. Kho et al., “Hydrogen sulfide protects HUVECs against hydrogen peroxide induced mitochondrial dysfunction and oxidative stress,” PLoS ONE, vol. 8, no. 2, article e53147, 2013. View at Publisher · View at Google Scholar · View at Scopus
  70. D. Giuliani, A. Ottani, D. Zaffe et al., “Hydrogen sulfide slows down progression of experimental Alzheimer's disease by targeting multiple pathophysiological mechanisms,” Neurobiology of Learning and Memory, vol. 104, pp. 82–91, 2013. View at Publisher · View at Google Scholar · View at Scopus
  71. H.-J. Wei, X. Li, and X.-Q. Tang, “Therapeutic benefits of H2S in Alzheimer's disease,” Journal of Clinical Neuroscience, vol. 21, no. 10, pp. 1665–1669, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. R. Obeid, A. McCaddon, and W. Herrmann, “The role of hyperhomocysteinemia and B-vitamin deficiency in neurological and psychiatric diseases,” Clinical Chemistry and Laboratory Medicine, vol. 45, no. 12, pp. 1590–1606, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. M. van den Berg, M. S. van der Knaap, G. H. J. Boers, C. D. A. Stehouwer, J. A. Rauwerda, and J. Valk, “Hyperhomocysteinaemia; with reference to its neuroradiological aspects,” Neuroradiology, vol. 37, no. 5, pp. 403–411, 1995. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Eto, T. Asada, K. Arima, T. Makifuchi, and H. Kimura, “Brain hydrogen sulfide is severely decreased in Alzheimer's disease,” Biochemical and Biophysical Research Communications, vol. 293, no. 5, pp. 1485–1488, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. U. Sen, P. Basu, O. A. Abe et al., “Hydrogen sulfide ameliorates hyperhomocysteinemia-associated chronic renal failure,” American Journal of Physiology—Renal Physiology, vol. 297, no. 2, pp. F410–F419, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. S.-K. Yan, T. Chang, H. Wang, L. Wu, R. Wang, and Q. H. Meng, “Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells,” Biochemical and Biophysical Research Communications, vol. 351, no. 2, pp. 485–491, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. H. Lee, E.-J. Lee, Y. S. Song, and E. Kim, “Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/γ-secretase,” Philosophical Transactions of the Royal Society of London B: Biological Sciences, vol. 369, no. 1633, Article ID 20130158, 2014. View at Publisher · View at Google Scholar · View at Scopus
  78. P. K. Kamat, P. Kyles, A. Kalani, and N. Tyagi, “Hydrogen sulfide ameliorates homocysteine-induced Alzheimer’s disease-like pathology, blood–brain barrier disruption, and synaptic disorder,” Molecular Neurobiology, vol. 53, no. 4, pp. 2451–2467, 2016. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Xu, C. Liu, Z. Li, and T. Zhang, “Effects of hydrogen sulfide on modulation of theta–gamma coupling in hippocampus in vascular dementia rats,” Brain Topography, vol. 28, no. 6, pp. 879–894, 2015. View at Publisher · View at Google Scholar · View at Scopus
  80. K. Qu, C. P. L. H. Chen, B. Halliwell, P. K. Moore, and P. T.-H. Wong, “Hydrogen sulfide is a mediator of cerebral ischemic damage,” Stroke, vol. 37, no. 3, pp. 889–893, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. I. Ishii, N. Akahoshi, H. Yamada, S. Nakano, T. Izumi, and M. Suematsu, “Cystathionine γ-lyase-deficient mice require dietary cysteine to protect against acute lethal myopathy and oxidative injury,” Journal of Biological Chemistry, vol. 285, no. 34, pp. 26358–26368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. Z. Li, Y. Wang, Y. Xie, Z. Yang, and T. Zhang, “Protective effects of exogenous hydrogen sulfide on neurons of hippocampus in a rat model of brain ischemia,” Neurochemical Research, vol. 36, no. 10, pp. 1840–1849, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. X. Wen, D. Qi, Y. Sun et al., “H2S attenuates cognitive deficits through Akt1/JNK3 signaling pathway in ischemic stroke,” Behavioural Brain Research, vol. 269, pp. 6–14, 2014. View at Publisher · View at Google Scholar · View at Scopus
  84. Z.-L. Chen, W.-M. Yu, and S. Strickland, “Peripheral regeneration,” Annual Review of Neuroscience, vol. 30, no. 1, pp. 209–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Bhatheja and J. Field, “Schwann cells: origins and role in axonal maintenance and regeneration,” The Journal of Biochemistry and Cell Biology, vol. 38, no. 12, pp. 1995–1999, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. W. W. Campbell, “Evaluation and management of peripheral nerve injury,” Clinical Neurophysiology, vol. 119, no. 9, pp. 1951–1965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. D. Levy, P. Kubes, and D. W. Zochodne, “Delayed peripheral nerve degeneration, regeneration, and pain in mice lacking inducible nitric oxide synthase,” Journal of Neuropathology & Experimental Neurology, vol. 60, no. 5, pp. 411–421, 2001. View at Publisher · View at Google Scholar · View at Scopus
  88. S. Rangaraju, D. Hankins, I. Madorsky et al., “Molecular architecture of myelinated peripheral nerves is supported by calorie restriction with aging,” Aging Cell, vol. 8, no. 2, pp. 178–191, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. H. Rösch, R. Schweigreiter, T. Bonhoeffer, Y.-A. Barde, and M. Korte, “The neurotrophin receptor p75NTR modulates long-term depression and regulates the expression of AMPA receptor subunits in the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 20, pp. 7362–7367, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. G. Dechant and Y.-A. Barde, “The neurotrophin receptor p75NTR: novel functions and implications for diseases of the nervous system,” Nature Neuroscience, vol. 5, no. 11, pp. 1131–1136, 2002. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Scheib and A. Höke, “Advances in peripheral nerve regeneration,” Nature Reviews Neurology, vol. 9, no. 12, pp. 668–676, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. X. Fontana, M. Hristova, C. Da Costa et al., “C-Jun in Schwann cells promotes axonal regeneration and motoneuron survival via paracrine signaling,” Journal of Cell Biology, vol. 198, no. 1, pp. 127–141, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. H. K. Lee, Y. K. Shin, J. Jung, S.-Y. Seo, S.-Y. Baek, and H. T. Park, “Proteasome inhibition suppresses schwann cell dedifferentiation in vitro and in vivo,” Glia, vol. 57, no. 16, pp. 1825–1834, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. J. Jung, W. Cai, S. Y. Jang et al., “Transient lysosomal activation is essential for p75 nerve growth factor receptor expression in myelinated Schwann cells during Wallerian degeneration,” Anatomy & Cell Biology, vol. 44, no. 1, pp. 41–49, 2011. View at Publisher · View at Google Scholar
  95. G. Yang, W. Yang, L. Wu, and R. Wang, “H2S, endoplasmic reticulum stress, and apoptosis of insulin-secreting beta cells,” Journal of Biological Chemistry, vol. 282, no. 22, pp. 16567–16576, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. R. Wang, “Signaling pathways for the vascular effects of hydrogen sulfide,” Current Opinion in Nephrology and Hypertension, vol. 20, no. 2, pp. 107–112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. H. Kimura, N. Shibuya, and Y. Kimura, “Hydrogen sulfide is a signaling molecule and a cytoprotectant,” Antioxidants & Redox Signaling, vol. 17, no. 1, pp. 45–57, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. N. Krishnan, C. Fu, D. J. Pappin, and N. K. Tonks, “H2S-induced sulfhydration of the phosphatase PTP1B and its role in the endoplasmic reticulum stress response,” Science Signaling, vol. 4, no. 203, article ra86, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. R. D. Di Villa Bianca, R. Sorrentino, P. Maffia et al., “Hydrogen sulfide as a mediator of human corpus cavernosum smooth-muscle relaxation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 11, pp. 4513–4518, 2009. View at Publisher · View at Google Scholar · View at Scopus
  100. N. Barbera, A. Montana, F. Indorato, N. Arbouche, and G. Romano, “Domino effect: an unusual case of six fatal hydrogen sulfide poisonings in quick succession,” Forensic Science International, vol. 260, pp. e7–e10, 2016. View at Publisher · View at Google Scholar
  101. K. R. Olson and N. L. Whitfield, “Hydrogen sulfide and oxygen sensing in the cardiovascular system,” Antioxidants & Redox Signaling, vol. 12, no. 10, pp. 1219–1234, 2010. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Chang, A. Untereiner, J. Liu, and L. Wu, “Interaction of methylglyoxal and hydrogen sulfide in rat vascular smooth muscle cells,” Antioxidants and Redox Signaling, vol. 12, no. 9, pp. 1093–1100, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. H. Kimura, “Hydrogen sulfide: from brain to gut,” Antioxidants and Redox Signaling, vol. 12, no. 9, pp. 1111–1123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. W.-L. Yin, J.-Q. He, B. Hu, Z.-S. Jiang, and X.-Q. Tang, “Hydrogen sulfide inhibits MPP+-induced apoptosis in PC12 cells,” Life Sciences, vol. 85, no. 7-8, pp. 269–275, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. L.-F. Hu, M. Lu, Z.-Y. Wu, P. T.-H. Wong, and J.-S. Bian, “Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function,” Molecular Pharmacology, vol. 75, no. 1, pp. 27–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. Y. Geng, E. Li, Q. Mu et al., “Hydrogen sulfide inhalation decreases early blood-brain barrier permeability and brain edema induced by cardiac arrest and resuscitation,” Journal of Perinatology, vol. 35, no. 3, pp. 494–500, 2015. View at Publisher · View at Google Scholar · View at Scopus
  107. K. Kida, E. Marutani, R. K. Nguyen, and F. Ichinose, “Inhaled hydrogen sulfide prevents neuropathic pain after peripheral nerve injury in mice,” Nitric Oxide—Biology and Chemistry, vol. 46, pp. 87–92, 2015. View at Publisher · View at Google Scholar · View at Scopus
  108. W.-L. Chen, Y.-Y. Niu, W.-Z. Jiang et al., “Neuroprotective effects of hydrogen sulfide and the underlying signaling pathways,” Reviews in the Neurosciences, vol. 26, no. 2, pp. 129–142, 2015. View at Publisher · View at Google Scholar · View at Scopus
  109. J. L. Wallace and R. Wang, “Hydrogen sulfide-based therapeutics: exploiting a unique but ubiquitous gasotransmitter,” Nature Reviews Drug Discovery, vol. 14, no. 5, pp. 329–345, 2015. View at Publisher · View at Google Scholar · View at Scopus
  110. S. Fiorucci, S. Orlandi, A. Mencarelli et al., “Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis,” British Journal of Pharmacology, vol. 150, no. 8, pp. 996–1002, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. J. L. Wallace, “Hydrogen sulfide-releasing anti-inflammatory drugs,” Trends in Pharmacological Sciences, vol. 28, no. 10, pp. 501–505, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. Y.-P. Yu, X.-L. Chi, and L.-J. Liu, “A hypothesis: hydrogen sulfide might be neuroprotective against subarachnoid hemorrhage induced brain injury,” The Scientific World Journal, vol. 2014, Article ID 432318, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. Y. Cui, X. Duan, H. Li et al., “Hydrogen sulfide ameliorates early brain injury following subarachnoid hemorrhage in rats,” Molecular Neurobiology, 2015. View at Publisher · View at Google Scholar · View at Scopus
  114. E. Cadenas and L. Packer, Hydrogen Sulfide in Redox Biology, Academic Press, Elsevier, 2015.
  115. E. Lim, O. Mbowe, A. S. Lee, and J. Davis, “Effect of environmental exposure to hydrogen sulfide on central nervous system and respiratory function: a systematic review of human studies,” International Journal of Occupational and Environmental Health, vol. 22, no. 1, pp. 80–90, 2016. View at Publisher · View at Google Scholar
  116. 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, vol. 9, no. 1, Article ID e87241, 2014. View at Publisher · View at Google Scholar · View at Scopus