Viral-induced spinal motor neuron death is non-cell-autonomous and involves glutamate excitotoxicity

Journal of Neuroscience

Volumn 24, Issue 34, 2004, Pages 7566-7575

  Darman, Jessica ^a,b   Backovic, Stephanie ^a,b   Dike, Sonny ^a   Maragakis, Nicholas J ^a   Krishnan, Chitra ^a   Rothstein, Jeffrey D ^a   Irani, David N ^a,b,c   Kerr, Douglas A ^a,b,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

Encephalomyelitis; Glutamate; Motor neuron; Paralysis; Spinal; Transport; Virus

Indexed keywords

AMPA RECEPTOR; CALCIUM; GLUTAMIC ACID; MINOCYCLINE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL DEATH; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; ION PERMEABILITY; MACROGLIA; MALE; MOUSE; NERVE CELL DEGENERATION; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PARALYSIS; POLIOMYELITIS; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; SINDBIS VIRUS; SPINAL CORD MOTONEURON; VIRUS INFECTION; WEST NILE FLAVIVIRUS;

ALPHAVIRUS INFECTIONS; ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; CELL DEATH; COCULTURE TECHNIQUES; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MINOCYCLINE; MOTOR NEURONS; NEUROPROTECTIVE AGENTS; PARALYSIS; RATS; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SINDBIS VIRUS; SPINAL CORD;

EID: 4444282209     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2002-04.2004     Document Type: Article

References (76)

1. Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1-14.
2. Belin MF, Didier-Bazes M, Akaoka H, Hardin-Pouzet H, Bernard A, Giraudon P (1997) Changes in astrocytic glutamate catabolism enzymes following neuronal degeneration or viral infection. Glia 21:154-161.
3. Biber K, Zuurman MW, Dijkstra IM, Boddeke HW (2002) Chemokines in the brain: neuroimmunology and beyond. Curr Opin Pharmacol 2:63-68.
4. Binder GK, Griffin DE (2001) Interferon-γ-mediated site-specific clearance of alphavirus from CNS neurons. Science 293:303-306.
5. Bridges RJ, Stanley MS, Anderson MW, Cotman CW, Chamberlin AR (1991) Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereomer. J Med Chem 34:717-725.
6. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW (2002) Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125:1297-1308.
7. 2+ overload and ROS generation in spinal motor neurons in vitro. J Neurosci 20:240-250.
8. Cheng EH, Levine B, Boise LH, Thompson CB, Hardwick JM (1996) Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379:554-556.
9. Chretien F, Vallat-Decouvelaere AV, Bossuet C, Rimaniol AC, Le Grand R, Le Pavec G, Creminon C, Dormont D, Gray F, Gras G (2002) Expression of excitatory amino acid transporter-2 (EAAT-2) and glutamine synthetase (GS) in brain macrophages and microglia of SIVmac251-infected macaques. Neuropathol Appl Neurobiol 28:410-417.
10. Dawson LA, Djali S, Gonzales C, Vinegra MA, Zaleska MM (2000) Characterization of transient focal ischemia-induced increases in extracellular glutamate and aspartate in spontaneously hypertensive rats. Brain Res Bull 53:767-776.
11. Dugan LL, Bruno VM, Amagasu SM, Giffard RG (1995) Glia modulate the response of murine cortical neurons to excitotoxicity: glia exacerbate AMPA neurotoxicity. J Neurosci 15:4545-4555.
12. Dunlop J, Beal MH, She Y, Howland DS (2003) Impaired spinal cord glutamate transport capacity and reduced sensitivity to riluzole in a transgenic superoxide dismutase mutant rat model of amyotrophic lateral sclerosis. J Neurosci 23:1688-1696.
13. Gegelashvili G, Robinson MB, Trotti D, Rauen T (2001) Regulation of glutamate transporters in health and disease. Prog Brain Res 132:267-286.
14. Ginsberg SD, Martin LJ, Rothstein JD (1995) Regional deafferentation down-regulates subtypes of glutamate transporter proteins. J Neurochem 65:2800-2803.
15. Ginsberg SD, Rothstein JD, Price DL, Martin LJ (1996) Fimbria-fornix transections selectively down-regulate subtypes of glutamate transporter and glutamate receptor proteins in septum and hippocampus. J Neurochem 67:1208-1216.
16. Ginsberg SD, Portera-Cailliau C, Martin LJ (1999) Fimbria-fornix transection and excitotoxicity produce similar neurodegeneration in the septum. Neuroscience 88:1059-1071.
17. Griffin DE, Levine B, Ubol S, Hardwick JM (1994) The effects of alphavirus infection on neurons. Ann Neurol [Suppl] 35:S23-S27.
18. Havert MB, Schofield B, Griffin DE, Irani DN (2000) Activation of divergent neuronal cell death pathways in different target cell populations during neuroadapted Sindbis virus infection of mice. J Virol 74:5352-5356.
19. Heath PR, Shaw PJ (2002) Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis. Muscle Nerve 26:438-458.
20. Hensley K, Fedynyshyn J, Ferrell S, Floyd RA, Gordon B, Grammas P, Hamdheydari L, Mhatre M, Mou S, Pye QN, Stewart C, West M, West S, Williamson KS (2003) Message and protein level elevation of tumor necrosis factor alpha (TNFα) and TNFα-modulating cytokines in spinal cords of the G93A-SOD1 mouse model for amyotrophic lateral sclerosis. Neurobiol Dis 14:74-80.
21. Hirata A, Nakamura R, Kwak S, Nagata N, Kamakura K (1997) AMPA receptor-mediated slow neuronal death in the rat spinal cord induced by long-term blockade of glutamate transporters with THA. Brain Res 771:37-44.
22. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, Erickson J, Kulik J, DeVito L, Psaltis G, DeGennaro LJ, Cleveland DW, Rothstein JD (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci USA 99:1604-1609.
23. Huang TL, O'Banion MK (1998) Interleukin-1β and tumor necrosis factor-α suppress dexamethasone induction of glutamine synthetase in primary mouse astrocytes. J Neurochem 71:1436-1442.
24. Ikematsu K, Tsuda R, Kondo T, Nakasono I (2002) The expression of excitatory amino acid transporter 2 in traumatic brain injury. Forensic Sci Int 130:83-89.
25. Jackson AC, Moench TR, Griffin DE, Johnson RT (1987) The pathogenesis of spinal cord involvement in the encephalomyelitis of mice caused by neuroadapted Sindbis virus infection. Lab Invest 56:418-423.
26. Jackson AC, Moench TR, Trapp BD, Griffin DE (1988) Basis of neurovirulence in Sindbis virus encephalomyelitis of mice. Lab Invest 58:503-509.
27. Jan JT, Griffin DE (1999) Induction of apoptosis by Sindbis virus occurs at cell entry and does not require virus replication. J Virol 73:10296-10302.
28. Kelley TW, Prayson RA, Isada CM (2003) Spinal cord disease in West Nile virus infection. N Engl J Med 348:564-566.
29. Kerr DA, Larsen T, Cook SH, Fannjiang YR, Choi E, Griffin DE, Hardwick JM, Irani DN (2002) BCL-2 and BAX protect adult mice from lethal Sindbis virus infection but do not protect spinal cord motor neurons or prevent paralysis. J Virol 76:10393-10400.
30. Kerr DA, Llado J, Shamblott MJ, Maragakis NJ, Irani DN, Crawford TO, Krishnan C, Dike S, Gearhart JD, Rothstein JD (2003) Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 23:5131-5140.
31. Krampfl K, Schlesinger F, Wolfes H, Dengler R, Bufler J (2001) Functional diversity of recombinant human AMPA-type glutamate receptors: possible implications for selective vulnerability of motor neurons. J Neurol Sci 191:19-23.
32. Kriz J, Gowing G, Julien JP (2003) Efficient three-drug cocktail for disease induced by mutant superoxide dismutase. Ann Neurol 53:429-436.
33. Leis AA, Stokic DS, Polk JL, Dostrow V, Winkelmann M (2002) A poliomyelitis-like syndrome from West Nile virus infection. N Engl J Med 347:1279-1280.
34. Levine B, Griffin DE (1993) Molecular analysis of neurovirulent strains of Sindbis virus that evolve during persistent infection of SCID mice. J Virol 67:6872-6875.
35. Levine B, Goldman JE, Jiang HH, Griffin DE, Hardwick JM (1996) Bcl-2 protects mice against fatal alphavirus encephalitis. Proc Natl Acad Sci USA 93:4810-4815.
36. Lewis DL, DeCamillis MA, Brunetti CR, Halder G, Kassner VA, Selegue JE, Higgs S, Carroll SB (1999) Ectopic gene expression and homeotic transformations in arthropods using recombinant Sindbis viruses. Curr Biol 9:1279-1287.
37. Lewis J, Wesselingh SL, Griffin DE, Hardwick JM (1996) Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol 70:1828-1835.
38. Liang XH, Goldman JE, Jiang HH, Levine B (1999) Resistance of interleukin-1β-deficient mice to fatal Sindbis virus encephalitis. J Virol 73:2563-2567.
39. Lin CL, Bristol LA, Jin L, Dykes-Hoberg M, Crawford T, Clawson L, Rothstein JD (1998) Aberrant RNA processing in a neurodegenerative disease: the cause for absent EAAT2, a glutamate transporter, in amyotrophic lateral sclerosis. Neuron 20:589-602.
40. Masliah E, Alford M, DeTeresa R, Mallory M, Hansen L (1996) Deficient glutamate transport is associated with neurodegeneration in Alzheimer's disease. Ann Neurol 40:759-766.
41. Mokhtarian F, Grob D, Griffin DE (1989) Role of the immune response in Sindbis virus-induced paralysis of SJL/J mice. J Immunol 143:633-637.
42. Namura S, Maeno H, Takami S, Jiang XF, Kamichi S, Wada K, Nagata I (2002) Inhibition of glial glutamate transporter GLT-1 augments brain edema after transient focal cerebral ischemia in mice. Neurosci Lett 324:117-120.
43. Nargi-Aizenman JL, Griffin DE (2001) Sindbis virus-induced neuronal death is both necrotic and apoptotic and is ameliorated by N-methyl-D-aspartate receptor antagonists. J Virol 75:7114-7121.
44. Nargi-Aizenman JL, Havert MB, Zhang M, Irani DN, Rothstein JD, Griffin DE (2004) Glutamate receptor antagonists protect from virus-induced neural degeneration. Ann Neurol 55:541-549.
45. Nava VE, Rosen A, Veliuona MA, Clem RJ, Levine B, Hardwick JM (1998) Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. J Virol 72:452-459.
46. Nedergaard M, Takano T, Hansen AJ (2002) Beyond the role of glutamate as a neurotransmitter. Nat Rev Neurosci 3:748-755.
47. Pitt D, Werner P, Raine CS (2000) Glutamate excitotoxicity in a model of multiple sclerosis. Nat Med 6:67-70.
48. Ransohoff RM, Tani M (1998) Do chemokines mediate leukocyte recruitment in post-traumatic CNS inflammation? Trends Neurosci 21:154-159.
49. Rao VL, Dogan A, Todd KG, Bowen KK, Kim BT, Rothstein JD, Dempsey RJ (2001a) Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J Neurosci 21:1876-1883.
50. Rao VL, Bowen KK, Dempsey RJ (2001b) Transient focal cerebral ischemia down-regulates glutamate transporters GLT-1 and EAAC1 expression in rat brain. Neurochem Res 26:497-502.
51. Robinson MB, Djali S, Buchhalter JR (1993) Inhibition of glutamate uptake with L-trans-pyrrolidine-2,4-dicarboxylate potentiates glutamate toxicity in primary hippocampal cultures. J Neurochem 61:2099-2103.
52. Rosenberg PA, Aizenman E (1989) Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci Lett 103:162-168.
53. Rosenberg PA, Amin S, Leitner M (1992) Glutamate uptake disguises neurotoxic potency of glutamate agonists in cerebral cortex in dissociated cell culture. J Neurosci 12:56-61.
54. Rothstein JD, Martin LJ, Kuncl RW (1992) Decreased glutamate transport by the brain and spinal cord in amyotrophic lateral sclerosis. N Engl J Med 326:1464-1468.
55. Rothstein JD, Jin L, Dykes-Hoberg M, Kuncl RW (1993) Chronic inhibition of glutamate uptake produces a model of slow neurotoxicity. Proc Natl Acad Sci USA 90:6591-6595.
56. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, Kuncl RW (1994) Localization of neuronal and glial glutamate transporters. Neuron 13:713-725.
57. Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38:73-84.
58. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686.
59. + T-cells. J Immunol 162:1624-1632.
60. Sepkuty JP, Cohen AS, Eccles C, Rafiq A, Behar K, Ganel R, Coulter DA, Rothstein JD (2002) A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. J Neurosci 22:6372-6379.
61. Su ZZ, Leszczyniecka M, Kang DC, Sarkar D, Chao W, Volsky DJ, Fisher PB (2003) Insights into glutamate transport regulation in human astrocytes: cloning of the promoter for excitatory amino acid transporter 2 (EAAT2). Proc Natl Acad Sci USA 100:1955-1960.
62. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702.
63. Thach DC, Kimura T, Griffin DE (2000) Differences between C57BL/6 and BALB/cBy mice in mortality and virus replication after intranasal infection with neuroadapted Sindbis virus. J Virol 74:6156-6161.
64. Tikka TM, Koistinaho JE (2001) Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J Immunol 166:7527-7533.
65. Tikka TM, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580-2588.
66. Vandenbergbe W, Vanden Bosch L, Robberecht W (1998) Glial cells potentiate kainate-induced neuronal death in a motoneuron-enriched spinal coculture system. Brain Res 807:1-10.
67. Van den Bosch L, Robberecht W (2000) Different receptors mediate motor neuron death induced by short and long exposures to excitotoxicity. Brain Res Bull 53:383-388.
68. 2+ influx and not via calpain inhibition. Neuropharmacology 42:706-713.
69. Van den Bosch L, Schwaller B, Vleminckx V, Meijers B, Stork S, Ruehlicke T, Van Houtte E, Klaassen H, Celio MR, Missiaen L, Robberecht W, Berchtold MW (2002b) Protective effect of parvalbumin on excitotoxic motor neuron death. Exp Neurol 174:150-161.
70. Van den Bosch L, Tilkin P, Lemmens G, Robberecht W (2002c) Minocycline delays disease onset and mortality in a transgenic model of ALS. NeuroReport 13:1067-1070.
71. Ventura R, Harris KM (1999) Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19:6897-6906.
72. Warita H, Manabe Y, Murakami T, Shiote M, Shiro Y, Hayashi T, Nagano I, Shoji M, Abe K (2002) Tardive decrease of astrocytic glutamate transporter protein in transgenic mice with ALS-linked mutant SOD1. Neurol Res 24:577-581.
73. Wesselingh SL, Levine B, Fox RJ, Choi S, Griffin DE (1994) Intracerebral cytokine mRNA expression during fatal and nonfatal alphavirus encephalitis suggests a predominant type 2 T-cell response. J Immunol 152:1289-1297.
74. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J (1998) Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 95:15769-15774.
75. Zhang W, Narayanan M, Friedlander RM (2003) Additive neuroprotective effects of minocycline with creatine in a mouse model of ALS. Ann Neurol 53:267-270.
76. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-78.