Melatonin attenuates brain contusion-induced oxidative insult, inactivation of signal transducers and activators of transcription 1, and upregulation of suppressor of cytokine signaling-3 in rats

Journal of Pineal Research

Volumn 51, Issue 2, 2011, Pages 233-245

  Tsai, Ming Che ^a,b   Chen, Wei Ju ^c   Tsai, Ming Shi ^d   Ching, Cheng Hsin ^c   Chuang, Jih Ing ^c  

^a CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d Sinying Hospital   (Taiwan)

Author keywords

brain contusion; glutathione; inducible nitric oxide synthetase; interleukine 6; melatonin; signal transducers and activators of transcription 1; suppressor of cytokine signaling 1

Indexed keywords

DNA; GLUTATHIONE; GLUTATHIONE DISULFIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MELATONIN; MESSENGER RNA; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN INHIBITOR OF ACTIVATED STAT1; STAT1 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; BRAIN CONTUSION; BRAIN NERVE CELL; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; TRAUMATIC BRAIN INJURY; UPREGULATION;

ANIMALS; ANTIOXIDANTS; BRAIN INJURIES; INTERLEUKIN-6; MALE; MELATONIN; NERVE TISSUE PROTEINS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PROTEIN INHIBITORS OF ACTIVATED STAT; RATS; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 80051671405     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00885.x     Document Type: Article

References (57)

1. Singh IN, Sullivan PG, Deng Y, et al., Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J Cereb Blood Flow Metab 2006; 26: 1407-1418. (Pubitemid 44629888)
2. Yi JH, Hazell AS,. Excitotoxic mechanisms and the role of astrocytic glutamate transporters in traumatic brain injury. Neurochem Int 2006; 48: 394-403. (Pubitemid 43327279)
3. Tyurin VA, Tyurina YY, Borisenko GG, et al., Oxidative stress following traumatic brain injury in rats: quantitation of biomarkers and detection of free radical intermediates. J Neurochem 2000; 75: 2178-2189.
4. Mustafa AG, Singh IN, Wang J, et al., Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals. J Neurochem 2010; 114: 271-280.
5. Ansari MA, Roberts KN, Scheff SW,. Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic Biol Med 2008; 45: 443-452.
6. Li L, Cheung SH, Evans EL, et al., Modulation of gene expression and tumor cell growth by redox modification of STAT3. Cancer Res 2010; 70: 8222-8232.
7. Kabe Y, Ando K, Hirao S, et al., Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus. Antioxid Redox Signal 2005; 7: 395-403. (Pubitemid 40279807)
8. Levy DE, Darnell JE Jr,. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 2002; 3: 651-662. (Pubitemid 34987786)
9. Kisseleva T, Bhattacharya S, Braunstein J, et al., Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 2002; 285: 1-24. (Pubitemid 34246317)
10. Dziennis S, Alkayed NJ,. Role of signal transducer and activator of transcription 3 in neuronal. Rev Neurosci 2008; 19: 341-361.
11. Stephanou A,. Role of STAT-1 and STAT-3 in ischaemia/reperfusion injury. J Cell Mol Med 2004; 8: 519-525. (Pubitemid 44145484)
12. Satriotomo I, Bowen KK, Vemuganti R,. JAK2 and STAT3 activation contributes to neuronal damage following transient focal cerebral ischemia. J Neurochem 2006; 98: 1353-1368. (Pubitemid 44200428)
13. Jung JE, Kim GS, Narasimhan P, et al., Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci 2009; 29: 7003-7014.
14. Sarafian TA, Montes C, Imura T, et al., Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS ONE 2010; 5: e9532.
15. Takagi Y, Harada J, Chiarugi A, et al., STAT1 is activated in neurons after ischemia and contributes to ischemic brain injury. J Cereb Blood Flow Metab 2002; 22: 1311-1318. (Pubitemid 35285088)
16. Wang J, Schreiber RD, Campbell IL,. STAT1 deficiency unexpectedly and markedly exacerbates the pathophysiological actions of IFN-alpha in the central nervous system. Proc Natl Acad Sci USA 2002; 99: 16209-16214. (Pubitemid 35462774)
17. Terui K, Haga S, Enosawa S, et al., Hypoxia/re-oxygenation-induced, redox-dependent activation of STAT1 (signal transducer and activator of transcription 1) confers resistance to apoptotic cell death via hsp70 induction. Biochem J 2004; 380: 203-209. (Pubitemid 38725745)
18. Larsen L, Ropke C,. Suppressors of cytokine signalling: SOCS. APMIS 2002; 110: 833-844. (Pubitemid 36177279)
19. Choi JS, Shin YJ, Cha JH, et al., Induction of suppressor of cytokine signaling-3 in astrocytes of the rat hippocampus following transient forebrain ischemia. Neurosci Lett 2008; 441: 323-327.
20. Raghavendra Rao VL, Dhodda VK, Song G, et al., Traumatic brain injury-induced acute gene expression changes in rat cerebral cortex identified by GeneChip analysis. J Neurosci Res 2003; 71: 208-219. (Pubitemid 36055465)
21. Shuai K,. Regulation of cytokine signaling pathways by PIAS proteins. Cell Res 2006; 16: 196-202. (Pubitemid 43247977)
22. Hung MW, Tipoe GL, Poon AM, et al., Protective effect of melatonin against hippocampal injury of rats with intermittent hypoxia. J Pineal Res 2008; 44: 214-221. (Pubitemid 351252925)
23. Chen ST, Chuang JI, Hong MH, et al., Melatonin attenuates MPP+-induced neurodegeneration and glutathione impairment in the nigrostriatal dopaminergic pathway. J Pineal Res 2002; 32: 262-269.
24. Hong Y, Palaksha KJ, Park K, et al., Melatonin plus exercise-based neurorehabilitative therapy for spinal cord injury. J Pineal Res 2010; 49: 201-209.
25. Tocharus J, Khonthun C, Chongthammakun S, et al., Melatonin attenuates methamphetamine-induced overexpression of pro-inflammatory cytokines in microglial cell lines. J Pineal Res 2010; 48: 347-352.
26. Das A, Mcdowell M, Pava MJ, et al., The inhibition of apoptosis by melatonin in VSC4.1 motoneurons exposed to oxidative stress, glutamate excitotoxicity, or TNF-alpha toxicity involves membrane melatonin receptors. J Pineal Res 2010; 48: 157-169.
27. Shekleton JA, Parcell DL, Redman JR, et al., Sleep disturbance and melatonin levels following traumatic brain injury. Neurology 2010; 74: 1732-1738.
28. Seifman MA, Adamides AA, Nguyen PN, et al., Endogenous melatonin increases in cerebrospinal fluid of patients after severe traumatic brain injury and correlates with oxidative stress and metabolic disarray. J Cereb Blood Flow Metab 2008; 28: 684-696. (Pubitemid 351432798)
29. Kerman M, Cirak B, Ozguner MF, et al., Does melatonin protect or treat brain damage from traumatic oxidative stress? Exp Brain Res 2005; 163: 406-410. (Pubitemid 41175264)
30. Maldonado MD, Murillo-Cabezas F, Terron MP, et al., The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J Pineal Res 2007; 42: 1-11. (Pubitemid 44924321)
31. Beni SM, Kohen R, Reiter RJ, et al., Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-kappaB and AP-1. FASEB J 2004; 18: 149-151.
32. Anderson ME,. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol 1985; 113: 548-555. (Pubitemid 16195830)
33. Tsai MC, Chen WJ, Ching CH, et al., Resuscitation with hydroxyethyl starch solution prevents nuclear factor kappaB activation and oxidative stress after hemorrhagic shock and resuscitation in rats. Shock 2007; 27: 527-533.
34. Chuang JI, Chen TH,. Effect of melatonin on temporal changes of reactive oxygen species and glutathione after MPP(+) treatment in human astrocytoma U373MG cells. J Pineal Res 2004; 36: 117-125.
35. Li LM, Timofeev I, Czosnyka M, et al., Review article: the surgical approach to the management of increased intracranial pressure after traumatic brain injury. Anesth Analg 2010; 111: 736-748.
36. Madan E, Prasad S, Roy P, et al., Regulation of apoptosis by resveratrol through JAK/STAT and mitochondria mediated pathway in human epidermoid carcinoma A431 cells. Biochem Biophys Res Commun 2008; 377: 1232-1237.
37. Monroe RK, Halvorsen SW,. Environmental toxicants inhibit neuronal Jak tyrosine kinase by mitochondrial disruption. Neurotoxicology 2009; 30: 589-598.
38. Toklu HZ, Hakan T, Biber N, et al., The protective effect of alpha lipoic acid against traumatic brain injury in rats. Free Radic Res 2009; 43: 658-667.
39. Reed TT, Owen J, Pierce WM, et al., Proteomic identification of nitrated brain proteins in traumatic brain-injured rats treated postinjury with gamma-glutamylcysteine ethyl ester: insights into the role of elevation of glutathione as a potential therapeutic strategy for traumatic brain injury. J Neurosci Res 2009; 87: 408-417.
40. Xie Y, Kole S, Precht P, et al., S-glutathionylation impairs signal transducer and activator of transcription 3 activation and signaling. Endocrinology 2009; 150: 1122-1131.
41. Park SJ, Kim HY, Kim H, et al., Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes. Free Radic Biol Med 2009; 46: 1694-1702.
42. Monroe RK, Halvorsen SW,. Cadmium blocks receptor-mediated Jak/STAT signaling in neurons by oxidative stress. Free Radic Biol Med 2006; 41: 493-502. (Pubitemid 44037283)
43. Mccormick J, Barry SP, Sivarajah A, et al., Free radical scavenging inhibits STAT phosphorylation following in vivo ischemia/reperfusion injury. FASEB J 2006; 20: 2115-2117.
44. Osuka K, Watanabe Y, Usuda N, et al., Oxidative stress activates STAT1 in basilar arteries after subarachnoid hemorrhage. Brain Res 2010; 1332: 12-19.
45. Gorina R, Sanfeliu C, Galito A, et al., Exposure of glia to pro-oxidant agents revealed selective Stat1 activation by H2O2 and Jak2-independent antioxidant features of the Jak2 inhibitor AG490. Glia 2007; 55: 1313-1324. (Pubitemid 47328935)
46. Kim HS, Lee MS,. STAT1 as a key modulator of cell death. Cell Signal 2007; 19: 454-465. (Pubitemid 46107818)
47. Yadav A, Kalita A, Dhillon S, et al., JAK/STAT3 pathway is involved in survival of neurons in response to insulin-like growth factor and negatively regulated by suppressor of cytokine signaling-3. J Biol Chem 2005; 280: 31830-31840. (Pubitemid 41291933)
48. Smith PD, Sun F, Park KK, et al., SOCS3 deletion promotes optic nerve regeneration in vivo. Neuron 2009; 64: 617-623.
49. Emery B, Cate HS, Marriott M, et al., Suppressor of cytokine signaling 3 limits protection of leukemia inhibitory factor receptor signaling against central demyelination. Proc Natl Acad Sci USA 2006; 103: 7859-7864.
50. Spangenburg EE, Brown DA, Johnson MS, et al., Exercise increases SOCS-3 expression in rat skeletal muscle: potential relationship to IL-6 expression. J Physiol 2006; 572: 839-848.
51. Croker BA, Krebs DL, Zhang JG, et al., SOCS3 negatively regulates IL-6 signaling in vivo. Nat Immunol 2003; 4: 540-545. (Pubitemid 36701336)
52. Timmons SD,. Current trends in neurotrauma care. Crit Care Med 2010; 38: S431-S444.
53. Hergenroeder GW, Moore AN, Mccoy JP Jr, et al., Serum IL-6: a candidate biomarker for intracranial pressure elevation following isolated traumatic brain injury. J Neuroinflammation 2010; 7: 19.
54. Gahm C, Holmin S, Wiklund PN, et al., Neuroprotection by selective inhibition of inducible nitric oxide synthase after experimental brain contusion. J Neurotrauma 2006; 23: 1343-1354. (Pubitemid 46489620)
55. Negi G, Kumar A, Sharma SS,. Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades. J Pineal Res 2011; 50: 124-131.
56. Hoppe JB, Frozza RL, Horn AP, et al., Amyloid-beta neurotoxicity in organotypic culture is attenuated by melatonin: involvement of GSK-3beta, tau and neuroinflammation. J Pineal Res 2010; 48: 230-238.
57. Choi EY, Jin JY, Lee JY, et al., Melatonin inhibits Prevotella intermedia lipopolysaccharide-induced production of nitric oxide and interleukin-6 in murine macrophages by suppressing NF-kappaB and STAT1 activity. J Pineal Res 2011; 50: 197-206.