Hydrogen sulfide offers neuroprotection on traumatic brain injury in parallel with reduced apoptosis and autophagy in mice

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zhang, Mingyang ^a,b   Shan, Haiyan ^c   Chang, Pan ^a   Wang, Tao ^a   Dong, Wenwen ^a   Chen, Xiping ^a   Tao, Luyang ^a  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c SUZHOU MUNICIPAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; CASPASE 3; HYDROGEN SULFIDE; LC3II PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN P62; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN CORTEX; BRAIN EDEMA; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MORRIS WATER MAZE TEST; MOTOR PERFORMANCE; MOUSE; NEUROPROTECTION; NONHUMAN; PROTEIN CLEAVAGE; SPATIAL MEMORY; TRAUMATIC BRAIN INJURY;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; BRAIN EDEMA; BRAIN INJURIES; HYDROGEN SULFIDE; MAZE LEARNING; MICE; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; PROPIDIUM; TRANSCRIPTION FACTORS;

EID: 84899148921     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087241     Document Type: Article

References (46)

1. Jain KK (2008) Neuroprotection in traumatic brain injury. Drug discovery today 13: 1082-1089.
2. Zhang M, Shan H, Gu Z, Wang D, Wang T, et al. (2012) Increased expression of calcium/calmodulin-dependent protein kinase type II subunit delta after rat traumatic brain injury. J Mol Neurosci 46: 631-643.
3. Jennings JS, Gerber AM, Vallano ML (2008) Pharmacological strategies for neuroprotection in traumatic brain injury. Mini Rev Med Chem 8: 689-701.
4. Martelli A, Testai L, Breschi MC, Blandizzi C, Virdis A, et al. (2012) Hydrogen sulphide: novel opportunity for drug discovery. Med Res Rev 32: 1093-1130.
5. Abe K, Kimura H (1996) The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci 16: 1066-1071. (Pubitemid 26140863)
6. Kimura H (2010) Hydrogen sulfide: from brain to gut. Antioxid Redox Signal 12: 1111-1123.
7. Liu YH, Lu M, Hu LF, Wong PT, Webb GD, et al. (2012) Hydrogen sulfide in the mammalian cardiovascular system. Antioxid Redox Signal 17: 141-185.
8. Francis RC, Vaporidi K, Bloch KD, Ichinose F, Zapol WM (2011) Protective and Detrimental Effects of Sodium Sulfide and Hydrogen Sulfide in Murine Ventilator-induced Lung Injury. Anesthesiology 115: 1012-1021.
9. Enokido Y, Suzuki E, Iwasawa K, Namekata K, Okazawa H, et al. (2005) Cystathionine beta-synthase, a key enzyme for homocysteine metabolism, is preferentially expressed in the radial glia/astrocyte lineage of developing mouse CNS. Faseb J 19: 1854-1856. (Pubitemid 41598773)
10. Nagai Y, Tsugane M, Oka J, Kimura H (2004) Hydrogen sulfide induces calcium waves in astrocytes. Faseb J 18: 557-559.
11. Wong PT, Qu K, Chimon GN, Seah AB, Chang HM, et al. (2006) High plasma cyst(e)ine level may indicate poor clinical outcome in patients with acute stroke: possible involvement of hydrogen sulfide. J Neuropathol Exp Neurol 65: 109-115.
12. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT (2006) Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke 37: 889-893. (Pubitemid 43731927)
13. Slivka A, Mytilineou C, Cohen G (1987) Histochemical evaluation of glutathione in brain. Brain Res 409: 275-284. (Pubitemid 17077548)
14. Xuan A, Long D, Li J, Ji W, Zhang M, et al. (2012) Hydrogen sulfide attenuates spatial memory impairment and hippocampal neuroinflammation in beta-amyloid rat model of Alzheimer's disease. J Neuroinflammation 9: 202.
15. Zhang M, Shan H, Wang T, Liu W, Wang Y, et al. (2013) Dynamic change of hydrogen sulfide after traumatic brain injury and its effect in mice. Neurochem Res 38: 714-725.
16. Luo CL, Chen XP, Yang R, Sun YX, Li QQ, et al. (2010) Cathepsin B contributes to traumatic brain injury-induced cell death through a mitochondria-mediated apoptotic pathway. J Neurosci Res 88: 2847-2858.
17. Luo CL, Li BX, Li QQ, Chen XP, Sun YX, et al. (2011) Autophagy is involved in traumatic brain injury-induced cell death and contributes to functional outcome deficits in mice. Neuroscience 184: 54-63.
18. Shohami E, Novikov M, Mechoulam R (1993) A nonpsychotropic cannabinoid, HU-211, has cerebroprotective effects after closed head injury in the rat. J Neurotrauma 10: 109-119. (Pubitemid 23209478)
19. Bierbach B, Meier M, Kasper-Konig W, Heimann A, Alessandri B, et al. (2008) Emboli formation rather than inflammatory mediators are responsible for increased cerebral water content after conventional and assisted beating-heart myocardial revascularization in a porcine model. Stroke 39: 213-219.
20. Bermpohl D, You Z, Korsmeyer SJ, Moskowitz MA, Whalen MJ (2006) Traumatic brain injury in mice deficient in Bid: effects on histopathology and functional outcome. J Cereb Blood Flow Metab 26: 625-633.
21. Mannix RC, Zhang J, Park J, Zhang X, Bilal K, et al. (2011) Age-dependent effect of apolipoprotein E4 on functional outcome after controlled cortical impact in mice. J Cereb Blood Flow Metab 31: 351-361.
22. Whalen MJ, Dalkara T, You Z, Qiu J, Bermpohl D, et al. (2008) Acute plasmalemma permeability and protracted clearance of injured cells after controlled cortical impact in mice. J Cereb Blood Flow Metab 28: 490-505. (Pubitemid 351304258)
23. Park J, Zhang J, Qiu J, Zhu X, Degterev A, et al. (2012) Combination therapy targeting Akt and mammalian target of rapamycin improves functional outcome after controlled cortical impact in mice. J Cereb Blood Flow Metab 32: 330-340.
24. Ichimura Y, Kumanomidou T, Sou YS, Mizushima T, Ezaki J, et al. (2008) Structural basis for sorting mechanism of p62 in selective autophagy. J Biol Chem 283: 22847-22857.
25. Clark RS, Bayir H, Chu CT, Alber SM, Kochanek PM, et al. (2008) Autophagy is increased in mice after traumatic brain injury and is detectable in human brain after trauma and critical illness. Autophagy 4: 88-90.
26. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G (2007) Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8: 741-752. (Pubitemid 47312826)
27. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, et al. (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122: 927-939. (Pubitemid 41345209)
28. Sadasivan S, Dunn WA Jr, Hayes RL, Wang KK (2008) Changes in autophagy proteins in a rat model of controlled cortical impact induced brain injury. Biochem Biophys Res Commun 373: 478-481.
29. Tan BH, Wong PT, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56: 3-10.
30. Donkin JJ, Vink R (2010) Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments. Curr Opin Neurol 23: 293-299.
31. Florian B, Vintilescu R, Balseanu AT, Buga AM, Grisk O, et al. (2008) Long-term hypothermia reduces infarct volume in aged rats after focal ischemia. Neurosci Lett 438: 180-185.
32. Yin J, Tu C, Zhao J, Ou D, Chen G, et al. (2013) Exogenous hydrogen sulfide protects against global cerebral ischemia/reperfusion injury via its antioxidative, anti-inflammatory and anti-apoptotic effects in rats. Brain Res 1491: 188-196.
33. Karlsson O, Roman E, Berg AL, Brittebo EB (2011) Early hippocampal cell death, and late learning and memory deficits in rats exposed to the environmental toxin BMAA (beta-N-methylamino-L-alanine) during the neonatal period. Behav Brain Res 219: 310-320.
34. Royo NC, Conte V, Saatman KE, Shimizu S, Belfield CM, et al. (2006) Hippocampal vulnerability following traumatic brain injury: a potential role for neurotrophin-4/5 in pyramidal cell neuroprotection. Eur J Neurosci 23: 1089-1102.
35. Pedersen MO, Larsen A, Stoltenberg M, Penkowa M (2009) Cell death in the injured brain: roles of metallothioneins. Prog Histochem Cytochem 44: 1-27.
36. Shaw K, MacKinnon MA, Raghupathi R, Saatman KE, McLntosh TK, et al. (2001) TUNEL-positive staining in white and grey matter after fatal head injury in man. Clinical neuropathology 20: 106-112. (Pubitemid 32476341)
37. Kajta M (2004) Apoptosis in the central nervous system: Mechanisms and protective strategies. Pol J Pharmacol 56: 689-700.
38. Raghupathi R (2004) Cell death mechanisms following traumatic brain injury. Brain Pathol 14: 215-222.
39. Zhang M, Shan H, Wang Y, Wang T, Liu W, et al. (2013) The expression changes of cystathionine-beta-synthase in brain cortex after traumatic brain injury. J Mol Neurosci 51: 57-67.
40. Smith CM, Chen Y, Sullivan ML, Kochanek PM, Clark RS (2011) Autophagy in acute brain injury: feast, famine, or folly? Neurobiol Dis 43: 52-59.
41. Zhang X, Chen Y, Jenkins LW, Kochanek PM, Clark RS (2005) Bench-to-bedside review: Apoptosis/programmed cell death triggered by traumatic brain injury. Crit Care 9: 66-75. (Pubitemid 40246773)
42. Lai Y, Hickey RW, Chen Y, Bayir H, Sullivan ML, et al. (2008) Autophagy is increased after traumatic brain injury in mice and is partially inhibited by the antioxidant gamma-glutamylcysteinyl ethyl ester. J Cereb Blood Flow Metab 28: 540-550. (Pubitemid 351304265)
43. Eto K, Asada T, Arima K, Makifuchi T, Kimura H (2002) Brain hydrogen sulfide is severely decreased in Alzheimer's disease. Biochem Biophys Res Commun 293: 1485-1488. (Pubitemid 34681045)
44. Kang R, Zeh HJ, Lotze MT, Tang D (2011) The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ 18: 571-580.
45. Decuypere JP, Parys JB, Bultynck G (2012) Regulation of the Autophagic Bcl-2/Beclin 1 Interaction. Cells 1: 284-312.
46. Oberstein A, Jeffrey PD, Shi Y (2007) Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 282: 13123-13132. (Pubitemid 47100641)