Hydrogen sulfide induced disruption of Na+ homeostasis in the cortex

Toxicological Sciences

Volumn 128, Issue 1, 2012, Pages 198-208

  Chao, Dongman ^a,b   He, Xiaozhou ^c   Yang, Yilin ^c   Balboni, Gianfranco ^d   Salvadori, Severo ^e   Kim, Dong H ^a   Xia, Ying ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c THE THIRD AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^d UNIVERSITY OF CAGLIARI   (Italy)

^e UNIVERSITY OF FERRARA   (Italy)

Author keywords

Cortex; Delta opioid receptor; Hydrogen sulfide; Ionotropic glutamate receptor; Na+ channel; Na+ homeostasis

Indexed keywords

6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; DELTA OPIATE RECEPTOR; DIZOCILPINE; HYDROGEN SULFIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; SODIUM CHANNEL BLOCKING AGENT; SODIUM ION; UFP 512; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DATA ANALYSIS; ELECTRODE; HOMEOSTASIS; HYPOXIA; ISCHEMIA; MALE; NERVE CELL LESION; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN FUNCTION; SODIUM TRANSPORT;

ANIMALS; CEREBRAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; HOMEOSTASIS; HYDROGEN SULFIDE; ION TRANSPORT; MALE; MICE; MICE, INBRED C57BL; RECEPTORS, GLUTAMATE; SODIUM;

EID: 84863426923     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs125     Document Type: Article

References (71)

1. Aarts, M., Liu, Y., Liu, L., Besshoh, S., Arundine, M., Gurd, J. W., Wang, Y.-T., and Salter, M. W. (2002). Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 298, 846-850.
2. Abe, K., and Kimura, H. (1996). The possible role of hydrogen sulfide as an endogenous neuromodulator. J. Neurosci. 16, 1066-1071.
3. Aizenman, E., Lipton, S. A., and Loring, R. H. (1989). Selective modulation of NMDA responses by reduction and oxidation. Neuron 2, 1257-1263.
4. Balboni, G., Salvadori, S., Guerrini, R., Negri, L., Giannini, E., Jinsmaa, Y., Bryant, S. D., and Lazarus, L. H. (2002). Potent δ-opioid receptor agonists containing the Dmt-Tic pharmacophore. J. Med. Chem. 45, 5556-5563.
5. Banasiak, K. J., Burenkova, O., and Haddad, G. G. (2004). Activation of voltage-sensitive sodium channels during oxygen deprivation leads to apoptotic neuronal death. Neuroscience 126, 31-44.
6. Blaustein, M. P., and Lederer, W. J. (1999). Sodium/calcium exchange: Its physiological implications. Physiol. Rev. 79, 763-854.
7. Bordji, K., Becerril-Ortega, J., and Buisson, A. (2011). Synapses, NMDA receptor activity and neuronal Ab production in Alzheimer's disease. Rev. Neurosci. 22, 285-294.
8. + homeostasis protects organotypic hippocampal slice cultures from hypoxic/hypoglycemic injury. Neuropharmacology 39, 1779-1787.
9. Brenneman, K. A., James, R. A., Gross, E. A., and Dorman, D. (2000). Olfactory neuron loss in adult male CD rats following subchronic inhalation exposure to hydrogen sulfide. Toxicol. Pathol. 28, 326-333.
10. Brierley, J. B., Prior, P. F., Calverley, J., and Brown, A. W. (1977). Cyanide intoxication in Macaca mulatta. J. Neurol. Sci. 31, 133-157.
11. Calabresi, P., Marfia, G. A., Centonze, D., Pisani, A., and Bernardi, G. (1999). Sodium influx plays a major role in the membrane depolarization induced by oxygen and glucose deprivation in rat striatal spiny neurons. Stroke 30, 171-179.
12. + leakage in the cortex. Cell. Mol. Life Sci. 66, 1105-1115.
13. 2+ influx in the cortex during acute hypoxia. J. Cell. Physiol. 212, 60-67.
14. + homeostasis during anoxia and oxygen-glucose deprivation. J. Cereb. Blood Flow Metab. 27, 356-368.
15. Chao, D., and Xia, Y. (2010). Ionic storm in hypoxic/ischemic stress: Can opioid receptors subside it? Prog. Neurobiol. 90, 439-470.
16. Chen, M. J., Peng, Z. F., Manikandan, J., Melendez, A. J., Tan, G. S., Chung, C. M., Li, Q. T., Tan, T. M., Deng, L. W., Whiteman, M., et al. (2011). Gene profiling reveals hydrogen sulphide recruits death signaling via the N-methyl-D-aspartate receptor identifying commonalities with excitotoxicity. J. Cell. Physiol. 226, 1308-1322.
17. Cheung, N. S., Peng, Z. F., Chen, M. J., Moore, P. K., and Whiteman, M. (2007). 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, 505-514.
18. Chohan, M. O., and Iqbal, K. (2006). From tau to toxicity: Emerging roles of NMDA receptor in Alzheimer's disease. J. Alzheimer's Dis. 10, 81-87.
19. Doraiswamy, P. M. (2003). Alzheimer's disease and the glutamate NMDA receptor. Psychopharmacol. Bull. 37, 41-49.
20. Elovaara, E., Tossavainen, A., and Savolainen, H. (1978). Effect of subclinical hydrogen sulfide intoxication on mouse brain protein metabolism. Exp. Neurol. 62, 93-98.
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. Farlow, M. R. (2004). NMDA receptor antagonists. A new therapeutic approach for Alzheimer's disease. Geriatrics 59, 22-27.
23. Friedman, J. E., and Haddad, G. G. (1994). Anoxia induces an increase in intracellular sodium in rat central neurons in vitro. Brain Res. 663, 329-334.
24. Gaitonde, U. B., and Sellar, R. J. (1987). Long term exposure to hydrogen sulphide producing subacute encephalopathy in a child. Br. Med. J. 294, 614.
25. Gong, Q. H., Shi, X. R., Hong, Z. Y., Pan, L. L., Liu, X. H., and Zhu, Y. Z. (2011). A new hope for neurodegeneration: Possible role of hydrogen sulfide. J. Alzheimer's Dis. 24(SUPPL. 2), 173-182.
26. Hannah, R. S., Hayden, L. J., and Roth, S. H. (1989). Hydrogen sulfide exposure alters the amino acid content in developing rat CNS. Neurosci. Lett. 99, 323-327.
27. Hannah, R. S., and Roth, S. H. (1991). Chronic exposure to low concentrations of hydrogen sulfide produces abnormal growth in developing cerebellar Purkinje cells. Neurosci. Lett. 122, 225-228.
28. Hasbani, M. J., Hyrc, K. L., Faddis, B. T., Romano, C., and Goldberg, M. P. (1998). Distinct role for sodium, chloride, and calcium in excitotoxic dendritic injury and recovery. Exp. Neurol. 154, 241-258.
29. Hirsch, A. R. (2002). Hydrogen sulfide exposure without loss of consciousness: Chronic effects in four cases. Toxicol. Ind. Health 18, 51-61.
30. Hooser, S. B., van Alstine, W., Kiupel, M., and Sojka, J. (2000). Acute pit gas (hydrogen sulfide) poisoning in confinement cattle. J. Vet. Diagn. Investig. 12, 272-275.
31. Hu, N. W., Ondrejcak, T., and Rowan, M. J. (2012). Glutamate receptors in preclinical research on Alzheimer's disease: Update on recent advances. Pharmacol. Biochem. Behav. 100, 855-862.
32. Integrated Risk Information System. (2003). Toxicological Review of Hydrogen Sulfide U.S. Environmental Protection Agency, Washington, DC. EPA/635/R-03/005. Available at: www.epa.gov/iris.
33. +. J. Neurochem. 71, 112-124.
34. Jarecki, B. W., Piekarz, A. D., Jackson, J. O., and Cummins, T. R. (2010). Human voltage-gated sodium channel mutations that cause inherited neuronal and muscle channelopathies increase resurgent sodium currents. J. Clin. Investig. 120, 369-378.
35. Kamoun, P. (2004). Endogenous production of hydrogen sulfide in mammals. Amino Acids 26, 243-254.
36. + channel regulation. Cell. Mol. Life Sci. 66, 3505-3516.
37. 2+] elevations in cultured hippocampal CA1 neurons during anoxic depolarization. J. Neurochem. 100, 915-923.
38. Kilburn, K. H. (2003). Effects of hydrogen sulfide on neurobehavioral function. South. Med. J. 96, 639-646.
39. Kimura, H. (2000). Hydrogen sulfide induces cyclic AMP and modulates the NMDA receptor. Biochem. Biophys. Res. Commun. 276, 129-133.
40. Kombian, S. B., Reiffenstein, R. J., and Colmers, W. F. (1993). The actions of hydrogen sulfide on dorsal raphe serotonergic neurons in vitro. J. Neurophysiol. 70, 81-96.
41. Krnjević, K. (2008). Electrophysiology of cerebral ischemia. Neuropharmacology 55, 319-333.
42. Kwiatkoski, M., Soriano, R. N., Francescato, H. D. C., Batalhao, M. E., Coimbra, T. M., Carnio, E. C., and Branco, L. G. S. (2012). Hydrogen sulfide as a cryogenic mediator of hypoxia-induced anapyrexia. Neuroscience 201, 146-156.
43. Lee, J. M., Zipfel, G. J., and Choi, D. W. (1999). The changing landscape of ischemic brain injury mechanism. Nature 399, A7-A14.
44. Leonard, A. S., and Hell, J. W. (1997). Cyclic AMP-dependent protein kinase and protein kinase C phosphorylate N-methyl-D aspartate receptors at different sites. J. Biol. Chem. 272, 12107-12115.
45. Malinow, R. (Forthcoming.) New developments on the role of NMDA receptors in Alzheimer's disease. Curr. Opin. Neurobiol.
46. Mayer, M. L., and Westbrook, G. L. (1987). The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28, 197-276.
47. Meo, I. D., Fagiolari, G., Prelle, A., Viscorni, C., Zeviani, M., and Tiranti, V. (2011). Chronic exposure to sulfide causes accelerated degradation of cytochrome c oxidase in ethymalonic encephalopathy. Antioxid. Redox Signal. 15, 353-362.
48. 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. (2009). H2S signals through protein S-sulfhydration. Sci. Signal. 2, ra72.
49. Nagai, Y., Tsugane, M., Oka, J., and Kimura, H. (2004). Hydrogen sulfide induces calcium waves in astrocytes. FASEB J. 18, 557-559.
50. Pamenter, M. E., and Buck, L. T. (2008). δ-opioid receptor antagonism induces NMDA receptor-dependent excitotoxicity in anoxic turtle cortex. J. Exp. Biol. 211, 3512-3517.
51. Parameshwaran, K., Dhanasekaran, M., and Suppiramaniam, V. (2008). Amyloid beta peptides and glutamatergic synaptic dysregulation. Exp. Neurol. 210, 7-13.
52. Partlo, L. A., Sainsbury, R. S., and Roth, S. H. (2001). Effects of repeated hydrogen sulphide (H2S) exposure on learning and memory in the adult rat. Neurotoxicology 22, 177-189.
53. Petrat, F., Li, T., Dehne, N., de Groot, H., and Rauen, U. (2006). Sodium as the major mediator of NO-induced cell death in cultured hepatocytes. Life Sci. 79, 1606-1615.
54. Probert, A.W., Borosky, S., Marcoux, F.W., andTaylor, P. (1997). Sodiumchannel modulators prevent oxygen and glucose deprivation injury and glutamate release in rat neocortical cultures. Neuropharmacology 36, 1031-1038.
55. Qu, K., Chen, C. P. L. H., Halliwell, B., Moore, P. K., and Wong, P. T. H. (2006). Hydrogen sulfide is a mediator of cerebral ischemia damage. Stroke 37, 889-893.
56. Raley-Susman, K. M., Kass, I. S., Cottrell, J. E., Newman, R. B., Chambers, G., and Wang, J. (2001). Sodium influx blockade and hypoxic damage to CA1 pyramidal neurons in rat hippocampal slices. J. Neurophysiol. 86, 2715-2726.
57. Reisberg, B., Doody, R., Stöffler, A., Schmitt, F., Ferris, S., and Möbius, H. J. (2003). Memantine in moderate-to-severe Alzheimer's disease. N. Engl. J. Med. 348, 1333-1341.
58. 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.
59. 2+ release in rat cerebellar type-1 astrocytes. J. Neurochem. 100, 1188-1202.
60. + exchange to acid extrusion during anoxia in adult rat hippocampal CA1 neurons. J. Neurochem. 88, 594-603.
61. + influx triggers bleb formation on inner hair cells. Am. J. Physiol. Cell Physiol. 288, C1332-C1341.
62. Smith, R. P., and Gosselin, R. E. (1966). On the mechanism of sulfide inactivation by methemoglobin. Toxicol. Appl. Pharmacol. 8, 159-172.
63. Solnyshkova, T. G. (2003). Demyelination of nerve fibers in the central nervous system caused by chronic exposure to natural hydrogen sulfidecontaining gas. Bull. Exp. Biol. Med. 136, 328-332.
64. Solnyshkova, T. G., Shakhlamov, V. A., and Volodina, E. P. (2004). Cerebral cortex ultrastructure during exposure to hydrogen sulfide gas. Neurosci. Behav. Physiol. 34, 343-345.
65. Stene, R. J., Slosberg, B., and Beachman, B. E. (1976). Hydrogen sulfide intoxication. Ann. Intern. Med. 85, 756-758.
66. + channel, Nav1.5. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1105-G1114.
67. Sullivan, J. M., Traynelis, S. F., Chen, H. S., Escobar, W., Heinemann, S. F., and Lipton, S. A. (1994). Identification of two cysteine residues that are required for redox modulation of the NMDA subtype of glutamate receptor. Neuron 13, 929-936.
68. Szabó, C. (2007). Hydrogen sulphide and its therapeutic potential. Nat. Rev. Drug Discov. 6, 917-935.
69. Tan, B. H., Wong, P. T. H., and Bian, J. S. (2010). Hydrogen sulfide: A novel signaling molecule in the central nervous system. Neurochem. Int. 56, 3-10.
70. Tang, G., Wu, L., and Wang, R. (2010). Interaction of hydrogen sulfide with ion channels. Clin. Exp. Pharmacol. Physiol. 37, 753-763.
71. Wang, R. (2002). Two's company, three's a crowd: Can H2S be the third endogenous gaseous transmitter? FASEB J. 16, 1792-1798.