Hydrogen sulfide induces neuroprotection against experimental stroke in rats by down-regulation of AQP4 via activating PKC

Brain Research

Volumn 1622, Issue , 2015, Pages 292-299

  Wei, Xia ^a   Zhang, Bing ^a   Cheng, Long ^a   Chi, Meng ^a   Deng, Lin ^a   Pan, Hong ^a   Yao, Xuan ^a   Wang, Guonian ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Aquaporin 4; Brain edema; Hydrogen sulfide; Middle cerebral artery occlusion; Protein kinase C

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 5 METHOXY 1H INDOL 3 YL] 3 (1H INDOL 3 YL)MALEIMIDE; AQUAPORIN 4; HYDROGEN SULFIDE; NEUROPROTECTIVE AGENT; PROTEIN KINASE C; 2-(1-(3-DIMETHYLAMINOPROPYL)-5-METHOXYINDOL-3-YL)-3-(1H-INDOL-3-YL)MALEIMIDE; AQP4 PROTEIN, RAT; INDOLE DERIVATIVE; MALEIMIDE DERIVATIVE; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD GAS; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN TISSUE; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; EXPERIMENTAL STROKE; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN; CEREBRAL ARTERY DISEASE; DISEASE MODEL; DRUG EFFECTS; INHALATIONAL DRUG ADMINISTRATION; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT; STROKE;

ADMINISTRATION, INHALATION; ANIMALS; AQUAPORIN 4; BRAIN; BRAIN EDEMA; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HYDROGEN SULFIDE; INDOLES; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MALEIMIDES; NEUROPROTECTIVE AGENTS; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; STROKE;

EID: 84940909764     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2015.07.001     Document Type: Article

References (38)

1. M. Amiry-Moghaddam, T. Otsuka, P.D. Hurn, R.J. Traystman, F.M. Haug, S.C. Froehner, M.E. Adams, J.D. Neely, P. Agre, O.P. Ottersen, and A. Bhardwaj An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain Proc. Natl. Acad. Sci. USA 100 2003 2106 2111
2. L. Belayev, O.F. Alonso, R. Busto, W. Zhao, and M.D. Ginsberg Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model Stroke 27 1996 1616 1622
3. P. Bhattacharya, A.K. Pandey, S. Paul, and R. Patnaik Melatonin renders neuroprotection by protein kinase C mediated aquaporin-4 inhibition in animal model of focal cerebral ischemia Life Sci. 100 2014 97 109
4. 2S induces a suspended animation-like state in mice Science 308 2005 518
5. V. Bouet, M. Boulouard, M. Toutain, J. Divoux, D. Bernaudin, M. Schumann-Bard, and P. Freret, T. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice Nat. Protoc. 4 2009 1560 1564
6. G. Fazzina, A.M. Amorini, C.R. Marmarou, S. Fukui, K. Okuno, J.G. Dunbar, R. Glisson, A. Marmarou, and A. Kleindienst The protein kinase C activator phorbol myristate acetate decreases brain edema by aquaporin 4 downregulation after middle cerebral artery occlusion in the rat J. Neurotrauma 27 2010 453 461
7. J.H. Garcia, S. Wagner, K.F. Liu, and X.J. Hu Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats. Statistical validation Stroke 26 1995 627 634 (discussion 635)
8. S. Gheibi, N. Aboutaleb, M. Khaksari, H. Kalalian-Moghaddam, A. Vakili, and Y. Asadi Hydrogen sulfide protects the brain against ischemic reperfusion injury in a transient model of focal cerebral ischemia J. Mol. Neurosci. 54 2014 264 270
9. Z. Han, M.B. Wax, and R.V. Patil Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation J. Biol. Chem. 273 1998 6001 6004
10. Y. Ikeda-Matsuo, A. Ota, T. Fukada, S. Uematsu, S. Akira, and Y. Sasaki Microsomal prostaglandin E synthase-1 is a critical factor of stroke-reperfusion injury Proc. Natl. Acad. Sci. USA 103 2006 11790 11795
11. 2S) protects against regional myocardial ischemia-reperfusion injury - Evidence for a role of K ATP channels Basic Res. Cardiol. 101 2006 53 60
12. C. Joseph, A.M. Buga, R. Vintilescu, A.T. Balseanu, M. Moldovan, H. Junker, L. Walker, M. Lotze, and A. Popa-Wagner Prolonged gaseous hypothermia prevents the upregulation of phagocytosis-specific protein annexin 1 and causes low-amplitude EEG activity in the aged rat brain after cerebral ischemia J. Cereb. Blood Flow Metab. 32 2012 1632 1642
13. Y. Kimura, and H. Kimura Hydrogen sulfide protects neurons from oxidative stress FASEB J. 18 2004 1165 1167
14. Y. Kimura, Y. Goto, and H. Kimura Hydrogen sulfide increases glutathione production and suppresses oxidative stress in mitochondria Antioxid. Redox Signal. 12 2010 1 13
15. T. Kovalenko, I. Osadchenko, A. Nikonenko, I. Lushnikova, K. Voronin, I. Nikonenko, D. Muller, and G. Skibo Ischemia-induced modifications in hippocampal CA1 stratum radiatum excitatory synapses Hippocampus 16 2006 814 825
16. B. Lapergue, B.Q. Dang, J.P. Desilles, G. Ortiz-Munoz, S. Delbosc, S. Loyau, L. Louedec, P.O. Couraud, M. Mazighi, J.B. Michel, O. Meilhac, and P. Amarenco High-density lipoprotein-based therapy reduces the hemorrhagic complications associated with tissue plasminogen activator treatment in experimental stroke Stroke 44 2013 699 707
17. J. Li, G. Zhang, S. Cai, and A.N. Redington Effect of inhaled hydrogen sulfide on metabolic responses in anesthetized, paralyzed, and mechanically ventilated piglets Pediatr. Crit. Care Med. 9 2008 110 112
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. J.C. Louis, E. Magal, A. Brixi, R. Steinberg, E. Yavin, and G. Vincendon Reduction of protein kinase C activity in the adult rat brain following transient forebrain ischemia Brain Res. 541 1991 171 174
20. 2S) - the third gas of interest for pharmacologists Pharmacol. Rep. 59 2007 4 24
21. G.T. Manley, M. Fujimura, T. Ma, N. Noshita, F. Filiz, A.W. Bollen, P. Chan, and A.S. Verkman Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke Nat. Med. 6 2000 159 163
22. G.T. Manley, D.K. Binder, D.K. Papadopoulos, and M.C. Verkman, A.S. New insights into water transport and edema in the central nervous system from phenotype analysis of aquaporin-4 null mice Neuroscience 129 2004 983 991
23. E. Marutani, S. Kosugi, K. Tokuda, A. Khatri, R. Nguyen, D.N. Atochin, K. Kida, K. Van, Leyen, K. Arai, and F. Ichinose A novel hydrogen sulfide-releasing N-methyl-d-aspartate receptor antagonist prevents ischemic neuronal death J. Biol. Chem. 287 2012 32124 32135
24. E.S. McCoy, B.R. Haas, and H. Sontheimer Water permeability through aquaporin-4 is regulated by protein kinase C and becomes rate-limiting for glioma invasion Neuroscience 168 2010 971 981
25. M.A. Moskowitz, E.H. Lo, and C. Iadecola The science of stroke: mechanisms in search of treatments Neuron 67 2010 181 198
26. T.T. Pan, K.L. Neo, L.F. Hu, Q.C. Yong, and J.S. Bian H2S preconditioning-induced PKC activation regulates intracellular calcium handling in rat cardiomyocytes Am. J. Physiol. Cell Physiol. 294 2008 C169 C177
27. M.C. Papadopoulos, S. Krishna, and A.S. Verkman Aquaporin water channels and brain edema Mt. Sinai. J. Med. 69 2002 242 248
28. M.F. Struve, J.N. Brisbois, R.A. James, M.W. Marshall, and D.C. Dorman Neurotoxicological effects associated with short-term exposure of Sprague-Dawley rats to hydrogen sulfide Neurotoxicology 22 2001 375 385
29. B.A. Sutherland, and A.M. Buchan Alteplase treatment does not increase brain injury after mechanical middle cerebral artery occlusion in the rat J. Cereb. Blood Flow Metab. 33 2013 e1 e7
30. Z. Tang, X. Sun, Q. Shi, X. Wang, Y. Xie, G. Huo, S. Zhou, and Z. Liao Beneficial effects of carbamylated erythropoietin against oxygen-glucose deprivation/reperfusion-induced astrocyte swelling: proposed molecular mechanisms of action Neurosci. Lett. 530 2012 23 28
31. G.P. Volpato, R. Searles, B. Yu, M. Scherrer-Crosbie, K.D. Bloch, F. Ichinose, and W.M. Zapol Inhaled hydrogen sulfide: a rapidly reversible inhibitor of cardiac and metabolic function in the mouse Anesthesiology 108 2008 659 668
32. J. Wang, C. Jiang, C. Liu, X. Li, N. Chen, and Y. Hao Neuroprotective effects of progesterone following stroke in aged rats Behav. Brain Res. 209 2010 119 122
33. Y. Wang, J. Jia, G. Ao, L. Hu, H. Liu, and Y. Xiao Hydrogen sulfide protects blood-brain barrier integrity following cerebral ischemia J. Neurochem. 129 2014 827 838
34. X. Wei, L. Duan, L. Bai, M. Tian, W. Li, and B. Zhang Effects of exogenous hydrogen sulfide on brain metabolism and early neurological function in rabbits after cardiac arrest Intensive Care Med. 38 2012 1877 1885
35. J. Yin, C. Tu, J. Zhao, D. Ou, G. Chen, Y. Liu, and X. Xiao 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 2013 188 196
36. Y. Yukutake, and M. Yasui Regulation of water permeability through aquaporin-4 Neuroscience 168 2010 885 891
37. Z. Zador, S. Stiver, V. Wang, and G.T. Manley Role of aquaporin-4 in cerebral edema and stroke Handb. Exp. Pharmacol. 190 2009 159 170
38. M. Zelenina, S. Zelenin, A.A. Bondar, H. Brismar, and A. Aperia Water permeability of aquaporin-4 is decreased by protein kinase C and dopamine Am. J. Physiol.: Ren. Physiol. 283 2002 F309 F318