Hydrogen sulfide attenuates hypoxia-induced neurotoxicity through inhibiting microglial activation

Pharmacological Research

Volumn 84, Issue , 2014, Pages 32-44

  Zhang, Qun ^a   Yuan, Lin ^a   Liu, Dexiang ^a   Wang, Jianmei ^a   Wang, Shuanglian ^a   Zhang, Qingrui ^a   Gong, Yanfen ^a   Liu, Hongda ^a   Hao, Aijun ^a   Wang, Zhen ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Hydrogen sulfide; Hypoxia; Microglial activation; Neurotoxicity; Nuclear factor B

Indexed keywords

HYDROGEN SULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; NITRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BRAIN CELL CULTURE; CELL ACTIVATION; CELL VIABILITY; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME PHOSPHORYLATION; GENE EXPRESSION REGULATION; HYPOXIA; IL 6 GENE; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; INOS GENE; MICROGLIA; MICROGLIAL CELL CULTURE; MOUSE; NEUROPROTECTION; NEUROTOXICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TNF ALPHA GENE; ANIMAL; ANOXIA; BAGG ALBINO MOUSE; CELL SURVIVAL; DRUG EFFECTS; MACROPHAGE ACTIVATION; METABOLISM; NERVE CELL;

ANIMALS; ANOXIA; CELL SURVIVAL; HYDROGEN SULFIDE; INTERLEUKIN-6; MACROPHAGE ACTIVATION; MICE; MICE, INBRED BALB C; MICROGLIA; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; NF-KAPPA B; NITRIC OXIDE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84901062338     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2014.04.009     Document Type: Article

References (47)

1. R. Wang Hydrogen sulfide: the third gasotransmitter in biology and medicine Antioxid Redox Signal 12 2010 1061 1064
2. K. Abeand, and H. Kimura The possible role of hydrogen sulfide as an endogenous neuromodulator J Neurosci 16 1996 1066 1071
3. Y. Kimura, and H. Kimura Hydrogen sulfide protects neurons from oxidative stress FASEB J 18 2004 1165 1167
4. K. Eto, M. Ogasawara, K. Umemura, Y. Nagai, and H. Kimura Hydrogen sulfide is produced in response to neuronal excitation J Neurosci 22 2002 3386 3391
5. S.W. Lee, Y.S. Hu, L.F. Hu, Q. Lu, G.S. Dawe, and P.K. Moore et al. Hydrogen sulphide regulates calcium homeostasis in microglial cells Glia 54 2006 116 124
6. Y. Nagai, M. Tsugane, J. Oka, and H. Kimura Hydrogen sulfide induces calcium waves in astrocytes FASEB J 18 2004 557 559
7. X.Q. Tang, L.L. Fan, Y.J. Li, X.T. Shen, Y.Y. Zhuan, and J.Q. He et al. Inhibition of hydrogen sulfide generation contributes to 1-methy-4- phenylpyridinium ion-induced neurotoxicity Neurotox Res 19 2010 403 411
8. X.Q. Tang, C.T. Yang, J. Chen, W.L. Yin, S.W. Tian, and B. Hu et al. Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells Clin Exp Pharmacol Physiol 35 2008 180 186
9. M. Whiteman, J.S. Armstrong, S.H. Chu, S. Jia-Ling, B.S. Wong, and N.S. Cheung et al. The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90 2004 765 768
10. M. Whiteman, N.S. Cheung, Y.Z. Zhu, S.H. Chu, J.L. Siau, and B.S. Wong et al. Hydrogen sulphide: a novel inhibitor of hypochlorous acid-mediated oxidative damage in the brain? Biochem Biophys Res Commun 326 2005 794 798
11. L.F. Hu, P.T. Wong, P.K. Moore, and J.S. Bian Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia J Neurochem 100 2007 1121 1128
12. L.F. Hu, M. Lu, Z.Y. Wu, P.T. Wong, and J.S. Bian Hydrogen sulfide inhibits rotenone-induced apoptosis via preservation of mitochondrial function Mol Pharmacol 75 2009 27 34
13. M. Lu, L.F. Hu, G. Hu, and J.S. Bian Hydrogen sulfide protects astrocytes against H(2)O(2)-induced neural injury via enhancing glutamate uptake Free Radic Biol Med 45 2008 1705 1713
14. H.W. Jung, Y.S. Chung, Y.S. Kim, and Y.K. Park Celastrol inhibits production of nitric oxide and proinflammatory cytokines through MAPK signal transduction and NF-kappaB in LPS-stimulated BV-2 microglial cells Exp Mol Med 39 2007 715 721
15. A. Lan, X. Liao, L. Mo, C. Yang, Z. Yang, and X. Wang et al. Hydrogen sulfide protects against chemical hypoxia-induced injury by inhibiting ROS-activated ERK1/2 and p38MAPK signaling pathways in PC12 cells PLoS One 6 2011 e25921
16. K. Kida, M. Yamada, K. Tokuda, E. Marutani, M. Kakinohana, and M. Kaneki et al. Inhaled hydrogen sulfide prevents neurodegeneration and movement disorder in a mouse model of Parkinson's disease Antioxid Redox Signal 15 2011 343 352
17. Y.Y. Liuand, and J.S. Bian Hydrogen sulfide protects amyloid-beta induced cell toxicity in microglia J Alzheimers Dis 22 2010 1189 1200
18. 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 Neurochem Res 36 2011 1840 1849
19. Z. Wang, J. Zhan, X. Wang, J. Gu, K. Xie, and Q. Zhang et al. Sodium hydrosulfide prevents hypoxia-induced behavioral impairment in neonatal mice Brain Res 1538 2013 126 134
20. Y. Deng, J. Lu, V. Sivakumar, E.A. Ling, and C. Kaur Amoeboid microglia in the periventricular white matter induce oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signaling pathway in hypoxic neonatal rats Brain Pathol (Zurich, Switzerland) 18 2008 387 400
21. Z. Wang, D. Liu, F. Wang, S. Liu, S. Zhao, and E.A. Ling et al. Saturated fatty acids activate microglia via Toll-like receptor 4/NF-kappaB signalling Br J Nutr 107 2012 229 241
22. Z. Wang, D. Liu, J. Wang, S. Liu, M. Gao, and E.A. Ling et al. Cytoprotective effects of melatonin on astroglial cells subjected to palmitic acid treatment in vitro J Pineal Res 52 2012 253 264
23. A. Ghoshal, S. Das, S. Ghosh, M.K. Mishra, V. Sharma, and P. Koli et al. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis Glia 55 2007 483 496
24. N.J. Robertson, T. Kato, A. Bainbridge, M. Chandrasekaran, O. Iwata, and A. Kapetanakis et al. Methyl-isobutyl amiloride reduces brain Lac/NAA, cell death and microglial activation in a perinatal asphyxia model J Neurochem 124 2013 645 657
25. G. Stolland, and S. Jander The role of microglia and macrophages in the pathophysiology of the CNS Prog Neurobiol 58 1999 233 247
26. F. Liuand, and L.D. McCullough Inflammatory responses in hypoxic ischemic encephalopathy Acta Pharmacol Sin 34 2013 1121 1130
27. S. Grojean, H. Schroeder, G. Pourie, C. Charriaut-Marlangue, V. Koziel, and D. Desor et al. Histopathological alterations and functional brain deficits after transient hypoxia in the newborn rat pup: a long term follow-up Neurobiol Dis 14 2003 265 278
28. C. Kaurand, and E.A. Ling Periventricular white matter damage in the hypoxic neonatal brain: role of microglial cells Prog Neurobiol 87 2009 264 280
29. J.L. Daval, G. Pourie, S. Grojean, V. Lievre, C. Strazielle, and S. Blaise et al. Neonatal hypoxia triggers transient apoptosis followed by neurogenesis in the rat CA1 hippocampus Pediatr Res 55 2004 561 567
30. Z. Wang, D. Liu, J. Zhan, K. Xie, X. Wang, and X. Xian et al. Melatonin improves short and long-term neurobehavioral deficits and attenuates hippocampal impairments after hypoxia in neonatal mice Pharmacol Res 76 2013 84 97
31. 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 Neurochem Res 36 2011 1840 1849
32. P.Y. Cheung, M. Miedzyblocki, T.F. Lee, and D.L. Bigam Effects of post-resuscitation administration with sodium hydrosulfide on cardiac recovery in hypoxia-reoxygenated newborn piglets Eur J Pharmacol 718 2013 74 80
33. L. Xiao, A. Lan, L. Mo, W. Xu, N. Jiang, and F. Hu 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 2012 1126 1130
34. C. Kaur, G. Rathnasamy, and E.A. Ling Roles of activated microglia in hypoxia induced neuroinflammation in the developing brain and the retina J Neuroimmune Pharmacol 8 2012 66 78
35. J.E. Merrill, L.J. Ignarro, M.P. Sherman, J. Melinek, and T.E. Lane Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide J Immunol 151 1993 2132 2141
36. C. Kaur, V. Sivakumar, L.S. Ang, and A. Sundaresan Hypoxic damage to the periventricular white matter in neonatal brain: role of vascular endothelial growth factor, nitric oxide and excitotoxicity J Neurochem 98 2006 1200 1216
37. L.-F. Hu, P.T.H. Wong, P.K. Moore, and J.-S. Bian Hydrogen sulfide attenuates lipopolysaccharide-induced inflammation by inhibition of p38 mitogen-activated protein kinase in microglia J Neurochem 100 2007 1121 1128
38. Y. You, and C. Kaur Expression of induced nitric oxide synthase in amoeboid microglia in postnatal rats following an exposure to hypoxia Neurosci Lett 279 2000 101 104
39. X. Wang, C. Zhu, L. Qiu, H. Hagberg, M. Sandberg, and K. Blomgren Activation of ERK1/2 after neonatal rat cerebral hypoxia-ischaemia J Neurochem 86 2003 351 362
40. S.J. Choi, I.J. Shin, K.H. Je, E.K. Min, E.J. Kim, and H.S. Kim et al. Hypoxia antagonizes glucose deprivation on interleukin 6 expression in an Akt dependent, but HIF-1/2alpha independent manner PLoS One 8 2013 e58662
41. H. Zhang, S.M. Moochhala, and M. Bhatia Endogenous hydrogen sulfide regulates inflammatory response by activating the ERK pathway in polymicrobial sepsis J Immunol 181 2008 4320 4331
42. A. Xuan, D. Long, J. Li, W. Ji, M. Zhang, and L. Hong et al. Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-amyloid rat model of Alzheimer's disease J Neuroinflamm 9 2012 202
43. A. Schneider, A. Martin-Villalba, F. Weih, J. Vogel, T. Wirth, and M. Schwaninger NF-kappaB is activated and promotes cell death in focal cerebral ischemia Nat Med 5 1999 554 559
44. H. Fan, Y. Guo, X. Liang, Y. Yuan, X. Qi, and M. Wang et al. Hydrogen sulfide protects against amyloid beta-peptide induced neuronal injury via attenuating inflammatory responses in a rat model J Biomed Res 27 2013 296 304
45. Y. Nasuhara, I.M. Adcock, M. Catley, P.J. Barnes, and R. Newton Differential IkappaB kinase activation and IkappaBalpha degradation by interleukin-1beta and tumor necrosis factor-alpha in human U937 monocytic cells. Evidence for additional regulatory steps in kappaB-dependent transcription J Biol Chem 274 1999 19965 19972
46. V. Imbert, R.A. Rupec, A. Livolsi, H.L. Pahl, E.B. Traenckner, and C. Mueller-Dieckmann et al. Tyrosine phosphorylation of I kappa B-alpha activates NF-kappa B without proteolytic degradation of I kappa B-alpha Cell 86 1996 787 798
47. W. Vanden Berghe, S. Plaisance, E. Boone, K. De Bosscher, M.L. Schmitz, and W. Fiers et al. p38 and extracellular signal-regulated kinase mitogen-activated protein kinase pathways are required for nuclear factor-kappaB p65 transactivation mediated by tumor necrosis factor J Biol Chem 273 1998 3285 3290