Glutamate released by Japanese encephalitis virus-infected microglia involves TNF-α signaling and contributes to neuronal death

GLIA

Volumn 60, Issue 3, 2012, Pages 487-501

  Chen, Chun Jung ^a,b   Ou, Yen Chuan ^a   Chang, Cheng Yi ^c   Pan, Hung Chuan ^a   Liao, Su Lan ^a   Chen, Shih Yun ^a   Raung, Shue Ling ^a   Lai, Ching Yi ^a  

^a TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

^b TUNGHAI UNIVERSITY   (Taiwan)

^c FENG YUAN HOSPITAL   (Taiwan)

Author keywords

Excitotoxicity; Flavivirus; Neuroinflammation

Indexed keywords

2 AMINOADIPIC ACID; 6 DIAZO 5 OXONORLEUCINE; CARBENOXOLONE; CCAAT ENHANCER BINDING PROTEIN BETA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; GLUTAMINASE; PROTEIN KINASE C; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; JAPANESE ENCEPHALITIS; JAPANESE ENCEPHALITIS VIRUS; MICROGLIA; NERVE CELL; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SUPERNATANT; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELL COMMUNICATION; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA, CONDITIONED; CYTOKINES; DIZOCILPINE MALEATE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENCEPHALITIS VIRUS, JAPANESE; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; GENE EXPRESSION REGULATION, VIRAL; GLUTAMIC ACID; NEUROGLIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84856219367     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22282     Document Type: Article

References (38)

1. Anderson CM, Swanson RA. 2000. Astrocyte glutamate transport: Review of properties, regulation, and physiological functions. Glia 32: 1-14.
2. Biswas SM, Kar S, Singh R, Chakraborty D, Vipat V, Raut CG, Mishra AC, Gore MM, Ghosh D. 2010. Immunomodulatory cytokines determine the outcome of Japanese encephalitis virus infection in mice. J Med Virol 82: 304-310.
3. Blakely PK, Kleinschmidt-DeMasters BK, Tyler KL, Irani DN. 2009. Disrupted glutamate transporter expression in the spinal cord with acute flaccid paralysis caused by West Nile virus infection. J Neuropathol Exp Neurol 68: 1061-1072.
4. Carmen J, Rothstein JD, Kerr DA. 2009. Tumor necrosis factor-α modulates glutamate transport in the CNS and is a critical determinant of outcome from viral encephalomyelitis. Brain Res 1263: 143-154.
5. Chambers TJ, Hahn CS, Galler R, Rice CM. 1990. Flavivirus genome organization, expression, and replication. Ann Rev Microbiol 44: 649-688.
6. Chen CJ, Chen JH, Chen SY, Liao SL, Raung SL. 2004. Up-regulaton of RANTES gene expression in neuroglia by Japanese encephalitis virus infection. J Virol 78: 12107-12119.
7. Chen CJ, Ou YC, Lin SY, Liao SL, Huang YS, Chiang AN. 2006. L-Glutamate activates RhoA GTPase leading to suppression of astrocyte stellation. Eur J Neurosci 23: 1977-1987.
8. Chen CJ, Ou YC, Lin SY, Raung SL, Liao SL, Lai CY, Chen SY, Chen JH. 2010. Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J Gen Virol 91: 1028-1037.
9. Choi DW. 1994. Glutamate receptors and the induction of excitotoxic neuronal death. Prog Brain Res 100: 47-51.
10. Chung-Bok MI, Vincent N, Jhala U, Watford M. 1997. Rat hepatic glutaminase: Identification of the full coding sequence and characterization of a functional promoter. Biochem J 324: 193-200.
11. German AC, Myint KS, Mai NT, Pomeroy I, Phu NH, Tzartos J, Winter P, Farrar J, Barrett A, Kipar A, Esiri MM, Solomon T. 2006. A preliminary neuropathological study of Japanese encephalitis in humans and a mouse model. Trans R Soc Trop Med Hyg 100: 1135-1145.
12. Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, Koli P, Sen E, Basu A. 2007. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55: 483-496.
13. Görg B, Morwinsky A, Keitel V, Qvartskhava N, Schrör K, Häussinger D. 2010. Ammonia triggers exocytotic release of L-glutamate from cultured rat astrocytes. Glia 58: 691-705.
14. Greenamyre JT, Porter RH. 1994. Anatomy and physiology of glutamate in the CNS. Neurology 44: S7-S13.
15. Greene MW, Ruhoff MS, Burrington CM, Garofalo RS, Oreña SJ. 2010. TNFα activation of PKCδ, mediated by NFκB and ER stress, cross-talks with the insulin signaling cascade. Cell Signal 22: 274-284.
16. He D, Natarajan V, Stern R, Gorshkova IA, Solway J, Spannhake EW, Zhao Y. 2008. Lysophosphatidic acid-induced transactivation of epidermal growth factor receptor regulates cyclo-oxygenase-2 expression and prostaglandin E(2) release via C/EBPbeta in human bronchial epithelial cells. Biochem J 412: 153-162.
17. Jiang ZG, Piggee C, Heyes MP, Murphy C, Quearry B, Bauer M, Zheng J, Gendelman HE, Markey SP. 2001. Glutamate is a mediator of neurotoxicity in secretion of activated HIV-1-infected macrophages. J Neuroimmunol 117: 97-107.
18. Kreutzberg GW. 1996. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
19. Kuo JS, Chen SF, Huang JH, Yang CS, Tsai PJ, Hsueh CM. 2001. The involvement of glutamate in recall of the conditioned NK cell response. J Neuroimmunol 118: 245-255.
20. Leonova J, Thorlin T, Åberg ND, Eriksson PS, Rönnbäck L, Hansson E. 2001. Endothelin-1 decreases glutamate uptake in primary cultured rat astrocytes. Am J Physiol Cell Physiol 281: C1495-C1503.
21. Liang J, Takeuchi H, Doi Y, Kawanokuchi J, Sonobe Y, Jin S, Yawata I, Li H, Yasuoka S, Mizuno T, Suzumura A. 2008. Excitatory amino acid transporter expression by astrocytes is neuroprotective against microglial excitotoxicity. Brain Res 1210: 11-19.
22. Liao SL, Chen CJ. 2001. Differential effects of cytokines and redox potential on glutamate uptake in rat cortical glial cultures. Neurosci Lett 299: 113-116.
23. Mishra MK, Basu A. 2008. Minocycline neuroprotects, reduces microglial activation, inhibits caspase 3 induction, and viral replication following Japanese encephalitis. J Neurochem 105: 1582-1595.
24. Nakajima K, Kohsaka S. 2001. Microglia: Activation and their significance in the central nervous system. J Biochem (Tokyo) 130: 169-175.
25. Persson M, Brantefjord M, Hansson E, Rönnbäck L. 2005. Lipopolysaccharide increases microglial GLT-1 expression and glutamate uptake capacity in vitro by a mechanism dependent on TNF-α. Glia 51: 111-120.
26. Prow NA, Irani DN. 2008. The inflammatory cytokine, interleukin-1 beta, mediates loss of astroglial glutamate transport and drives excitotoxic motor neuron injury in the spinal cord during acute vial encephalomyelitis. J Neurochem 105: 1276-1286.
27. Raung SL, Chen SY, Liao SL, Chen JH, Chen CJ. 2005. Tyrosine kinase inhibitors attenuate Japanese encephalitis virus-induced neurotoxicity. Biochem Biophys Res Commun 327: 399-406.
28. Ravi V, Parida S, Desai A, Chandramuki A, Gourie-Devi M, Grau GE. 1997. Correlation of tumor necrosis factor levels in the serum and cerebrospinal fluid with clinical outcome in Japanese encephalitis patients. J Med Virol 51: 132-136.
29. Saha RN, Ghosh A, Palencia CA, Fung YK, Dudek SM, Pahan K. 2009. TNF-α preconditioning protects neurons via neuron-specific up-regulation of CREB-binding protein. J Immunol 183: 2068-2078.
30. Sebastian L, Desai A, Madhusudana SN, Ravi V. 2009. Pentoxifylline inhibits replication of encephalitis virus: A comparative study with ribavirin. Int J Antimicr Agents 33: 168-173.
31. Shankar E, Krishnamurthy S, Paranandi R, Basu A. 2010. PKCepsilon induces Bcl-2 by activating CREB. Int J Oncol 36: 883-888.
32. Swarup V, Ghosh J, Das S, Basu A. 2008. Tumor necrosis factor receptor-associated death domain mediated neuronal death contributes to the glial activation and subsequent neuroinflammation in Japanese encephalitis. Neurochem Int 52: 1310-1321.
33. Szymocha R, Akaoka H, Dutuit M, Malcus C, Dider-Bazes M, Belin MF, Giraudon P. 2000. Human T-cell lymphotropic virus type 1-infected lymphocytes impair catabolism and uptake of glutamate by astrocytes via Tax-1 and tumor necrosis factor alpha. J Virol 74: 6433-6441.
34. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, Sonobe Y, Mizuno T, Suzumura A. 2006. Tumor necrosis factor-α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281: 21362-21368.
35. Thongtan T, Cheepsunthorn P, Chaiworakul V, Rattanarungsan C, Wikan N, Smith DR. 2010. Highly permissive infection of microglial cells by Japanese encephalitis virus: A possible role as a viral reservoir. Microbes Infect 12: 37-45.
36. Toivari E, Manninen T, Nahata AK, Jalonen TO, Linne ML. 2011. Effects of transmitters and amyloid-beta peptide on calcium signals in rat cortical astrocytes: Fura-2AM measurements and stochastic model stimulations. PLoS ONE 6: e17914.
37. Tolosa L, Caraballo-Miralles V, Olmos G, Lladó J. 2011. TNF-α potentiates glutamate-induced spinal cord motoneuron death via NF-κB. Mol Cell Neurosci 46: 176-186.
38. Wang Y, Singh R, Xiang Y, Greenbaum LE, Czaja MJ. 2010. Nuclear factor κB up-regulation of CCAAT/enhancer-binding protein β mediates hepatocyte resistance to tumor necrosis factor α toxicity. Hepatology 52: 2118-2126.