Neurotropic viral infections leading to epilepsy: Focus on Theiler's murine encephalomyelitis virus

Future Virology

Volumn 6, Issue 11, 2011, Pages 1339-1350

  Libbey, Jane E ^a   Fujinami, Robert S ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

animal model; epilepsy; inflammation; innate immune response; macrophages; microglia; picornavirus; seizures; Theiler's murine encephalomyelitis virus; viral encephalitis

Indexed keywords

COMPLEMENT COMPONENT C3; CYTOKINE; INTERLEUKIN 6;

EPILEPSY; EPILEPTOGENESIS; HUMAN; INNATE IMMUNITY; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEIZURE; VIRAL CLEARANCE; VIRUS ENCEPHALITIS; VIRUS PATHOGENESIS;

ANIMALIA; MUS; PICORNAVIRIDAE; THEILER'S ENCEPHALOMYELITIS VIRUS;

EID: 80755142775     PISSN: 17460794     EISSN: 17460808     Source Type: Journal    
DOI: 10.2217/fvl.11.107     Document Type: Review

References (81)

1. Getts DR, Balcar VJ, Matsumoto I, Müller M, King NJC. Viruses and the immune system: their roles in seizure cascade development. J. Neurochem. 104, 1167-1176 (2008). (Pubitemid 351297649)
2. Misra UK, Tan CT, Kalita J. Viral encephalitis and epilepsy. Epilepsia 49(Suppl. 6), 13-18 (2008).
3. Rzadkiewicz E, Lipowski D. Seizure attacks in viral encephalitis: influence on a course and outcome. Critical Care 15(Suppl. 1), S117 (2011).
4. Singhi P. Infectious causes of seizures and epilepsy in the developing world. Dev. Med. Child Neurol. 53, 600-609 (2011).
5. Yamashita N, Morishima T. HHV-6 and seizures. Herpes. 12, 46-49 (2005). (Pubitemid 41512783)
6. Choi J, Koh S. Role of brain inflammation in epileptogenesis. Yonsei Med. J. 49, 1-18 (2008). (Pubitemid 351513640)
7. Millichap JG, Millichap JJ. Role of viral infections in the etiology of febrile seizures. Pediatr. Neurol. 35, 165-172 (2006). (Pubitemid 44291533)
8. Donati D, Akhyani N, Fogdell-Hahn A et al. Detection of human herpesvirus-6 in mesial temporal lobe epilepsy surgical brain resections. Neurology 61, 1405-1411 (2003). (Pubitemid 37463379)
9. Niehusmann P, Mittelstaedt T, Bien CG et al. Presence of human herpes virus 6 DNA exclusively in temporal lobe epilepsy brain tissue of patients with history of encephalitis. Epilepsia 51, 2478-2483 (2010).
10. Elbers JM, Bitnun A, Richardson SE et al. A 12-year prospective study of childhood herpes simplex encephalitis: is there a broader spectrum of disease? Pediatrics 119, E399-E407 (2007). (Pubitemid 46397737)
11. Tan CT, Goh KJ, Wong KT et al. Relapsed and late-onset Nipah encephalitis. Ann. Neurol. 51, 703-708 (2002). (Pubitemid 34568848)
12. Satishchandra P, Sinha S. Seizures in HIV-seropositive individuals: NIMHANS experience and review. Epilepsia 49(Suppl 6), 33-41 (2008).
13. Gupta S, Shah DM, Shah I. Neurological disorders in HIV-infected children in India. Ann. Trop. Paediatr. 29, 177-181 (2009).
14. Eeg-Olofsson O. Virological and immunological aspects of seizure disorders. Brain Dev. 25, 9-13 (2003). (Pubitemid 36132197)
15. Chiu SS, Tse CY, Lau YL, Peiris M. Influenza A infection is an important cause of febrile seizures. Pediatrics 108, E63 (2001).
16. Hung JJ, Wen HY, Yen MH et al. Rotavirus gastroenteritis associated with afebrile convulsion in children: clinical analysis of 40 cases. Chang Gung. Med. J. 26, 654-659 (2003).
17. Chung B, Wong V. Relationship between five common viruses and febrile seizure in children. Arch. Dis. Child 92, 589-593 (2007). (Pubitemid 47012950)
18. Hosoya M, Sato M, Honzumi K et al. Association of nonpolio enteroviral infection in the central nervous system of children with febrile seizures. Pediatrics 107, E12 (2001).
19. Verboon-Maciolek MA, Krediet TG, Gerards LJ, Fleer A, van Loon TM. Clinical and epidemiologic characteristics of viral infections in a neonatal intensive care unit during a 12-year period. Pediatr. Infect. Dis. J. 24, 901-904 (2005). (Pubitemid 41475926)
20. Verboon-Maciolek MA, Krediet TG, Gerards LJ, de Vries LS, Groenendaal F, van Loon AM. Severe neonatal parechovirus infection and similarity with enterovirus infection. Pediatr. Infect. Dis. J. 27, 241-245 (2008).
21. Engel J Jr. ILAE classification of epilepsy syndromes. Epilepsy Res. 70(Suppl. 1), S5-S10 (2006).
22. Bender RA, Baram TZ. Epileptogenesis in the developing brain: what can we learn from animal models? Epilepsia 48(Suppl. 5), 2-6 (2007). (Pubitemid 47512194)
23. Giblin KA, Blumenfeld H. Is epilepsy a preventable disorder? New evidence from animal models. Neuroscientist 16, 253-275 (2010).
24. Pitkänen A, Kharatishvili I, Karhunen H et al. Epileptogenesis in experimental models. Epilepsia 48(Suppl 2), 13-20 (2007). (Pubitemid 46849999)
25. Hauser WA, Annegers JF, Rocca WA. Descriptive epidemiology of epilepsy: contributions of population-based studies from Rochester, Minnesota. Mayo Clin. Proc. 71, 576-586 (1996).
26. Mazarati AM, Thompson KW, Suchomelova L et al. Status epilepticus: Electrical stimulation models. In: Models of Seizures and Epilepsy. Pitkänen A, Schwartzkroin PA, Moshé SL (Eds.), Elsevier Academic Press, Burlington, MA, USA, 449-464 (2006).
27. Stringer JL. Models available for infection-induced seizures. In: Models of Seizures and Epilepsy. Pitkänen A, Schwartzkroin PA, Moshé SL (Eds.), Elsevier Academic Press, Burlington, MA, USA, 521-526 (2006).
28. Libbey JE, Kirkman NJ, Smith MCP et al. Seizures following picornavirus infection. Epilepsia 49, 1066-1074 (2008). (Pubitemid 351793997)
29. Kirkman NJ, Libbey JE, Wilcox KS, White HS, Fujinami RS. Innate but not adaptive immune responses contribute to behavioral seizures following viral infection. Epilepsia 51, 454-464 (2010).
30. Libbey JE, Kennett NJ, Wilcox KS, White HS, Fujinami RS. Interleukin-6, produced by resident cells of the central nervous system and infiltrating cells, contributes to the development of seizures following viral infection. J. Virol. 85, 6913-6922 (2011).
31. Libbey JE, Kirkman NJ, Wilcox KS, White HS, Fujinami RS. Role for complement in the development of seizures following acute viral infection. J. Virol. 84, 6452-6460 (2010).
32. Stewart KA, Wilcox KS, Fujinami RS, White HS. Theiler's virus infection chronically alters seizure susceptibility. Epilepsia 51, 1418-1428 (2010).
33. Stewart KA, Wilcox KS, Fujinami RS, White HS. Development of postinfection epilepsy after Theiler's virus infection of C57BL/6 mice. J. Neuropathol. Exp. Neurol. 69, 1210-1219 (2010).
34. Libbey JE, Kennett NJ, Wilcox KS, White HS, Fujinami RS. Lack of correlation of central nervous system inflammation and neuropathology with the development of seizures following acute virus infection. J. Virol. 85, 8149-8157 (2011).
35. Libbey JE, Kennett NJ, Wilcox KS, White HS, Fujinami RS. Once initiated, viral encephalitis-induced seizures are consistent no matter the treatment or lack of interleukin-6. J. Neurovirol. doi:10.1007/s13365-011-0050-5 (2011) (Epub ahead of print)
36. Theiler M. Spontaneous encephalomyelitis of mice, a new virus disease. J. Exp. Med. 65, 705-719 (1937).
37. Theiler M, Gard S. Encephalomyelitis of mice. I. Characteristics and pathogenesis of the virus. J. Exp. Med. 72, 49-67 (1940).
38. Libbey JE, Fujinami RS. Viral demyelinating disease in experimental animals. In: Multiple Sclerosis: Immunology, Pathology and Pathophysiology. Herndon RM (Ed.).Demos, NY, USA, 125-133 (2003).
39. Pena-Rossi C, Cash E, Aubert C, Coutinho A. Role of the humoral immune response in resistance to Theiler's virus infection. J. Virol. 65, 3895-3899 (1991).
40. Lindsley MD, Rodriguez M. Characterization of the inflammatory response in the central nervous system of mice susceptible or resistant to demyelination by Theiler's virus. J. Immunol. 142, 2677-2682 (1989). (Pubitemid 19114880)
41. Chamorro M, Aubert C, Brahic M. Demyelinating lesions due to Theiler's virus are associated with ongoing central nervous system infection. J. Virol. 52, 992-997 (1986). (Pubitemid 16143982)
42. Lipton HL, Dal Canto MC. Susceptibility of inbred mice to chronic central nervous system infection by Theiler's murine encephalomyelitis virus. Infect. Immun. 26, 369-374 (1979). (Pubitemid 10245652)
43. Lipton HL, Dal Canto MC. Chronic neurologic disease in Theiler's virus infection of SJL/J mice. J. Neurol. Sci. 30, 201-207 (1976).
44. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294 (1972).
45. Schauwecker PE, Steward O. Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl Acad. Sci. USA 94, 4103-4108 (1997). (Pubitemid 27180506)
46. Schauwecker PE. Differences in ionotropic glutamate receptor subunit expression are not responsible for strain-dependent susceptibility to excitotoxin-induced injury. Brain Res. Mol. Brain Res. 112, 70-81 (2003). (Pubitemid 36369248)
47. Mohajeri MH, Madani R, Saini K, Lipp H-P, Nitsch RM, Wolfer DP. The impact of genetic background on neurodegeneration and behavior in seizured mice. Genes Brain Behav. 3, 228-239 (2004). (Pubitemid 39005678)
48. Bernardino L, Ferreira R, Cristóvão AJ, Sales F, Malva JO. Inflammation and neurogenesis in temporal lobe epilepsy. Curr. Drug Targets CNS Neurol. Disord. 4, 349-360 (2005). (Pubitemid 41086755)
49. Tsunoda I, McCright IJ, Kuang L-Q, Zurbriggen A, Fujinami RS. Hydrocephalus in mice infected with a Theiler's murine encephalomyelitis virus variant. J. Neuropathol. Exp. Neurol. 56, 1302-1313 (1997). (Pubitemid 28006576)
50. Wada Y, McCright IJ, Whitby FG, Tsunoda I, Fujinami RS. Replacement of loop II of VP1 of the DA strain with loop II of the GDVII strain of Theiler's murine encephalomyelitis virus alters neurovirulence, viral persistence, and demyelination. J. Virol. 72, 7557-7562 (1998). (Pubitemid 28377888)
51. Tsunoda I, Wada Y, Libbey JE, Cannon TS, Whitby FG, Fujinami RS. Prolonged gray matter disease without demyelination caused by Theiler's murine encephalomyelitis virus with a mutation in VP2 puff B. J. Virol. 75, 7494-7505 (2001). (Pubitemid 32738008)
52. Morgan TE, Nichols NR, Pasinetti GM, Finch CE. TGF-b1 mRNA increases in macrophage/microglial cells of the hippocampus in response to deafferentation and kainic acid-induced neurodegeneration. Exp. Neurol. 120, 291-301 (1993). (Pubitemid 23165023)
53. Kim H-C, Bing G, Kim S-J et al. Kainate treatment alters TGF-beta3 gene expression in the rat hippocampus. Brain Res. Mol. Brain Res. 108, 60-70 (2002). (Pubitemid 35447964)
54. Buenz EJ, Sauer BM, Lafrance-Corey RG et al. Apoptosis of hippocampal pyramidal neurons is virus independent in a mouse model of acute neurovirulent picornavirus infection. Am. J. Pathol. 175, 668-684 (2009).
55. Chakraborty S, Nazmi A, Dutta K, Basu A. Neurons under viral attack: victims or warriors? Neurochem. Int 56, 727-735 (2010).
56. Vezzani A, Granata T. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46, 1724-1743 (2005). (Pubitemid 44921957)
57. Vezzani A, Ravizza T, Balosso S, Aronica E. Glia as a source of cytokines: Implications for neuronal excitability and survival. Epilepsia 49 (Suppl. 2), 24-32 (2008). (Pubitemid 351143763)
58. Vezzani A, Balosso S, Ravizza T. The role of cytokines in the pathophysiology of epilepsy. Brain Behav. Immun. 22, 797-803 (2008).
59. Theil DJ, Tsunoda I, Libbey JE, Derfuss TJ, Fujinami RS. Alterations in cytokine but not chemokine mRNA expression during three distinct Theiler's virus infections. J. Neuroimmunol. 104, 22-30 (2000). (Pubitemid 30100534)
60. Alexander JJ, Anderson AJ, Barnum SR, Stevens B, Tenner AJ. The complement cascade: Yin-Yang in neuroinflammation- neuro-protection and -degeneration. J. Neurochem. 107, 1169-1187 (2008).
61. Zhang X, Kimura Y, Fang C et al. Regulation of Toll-like receptor-mediated inflammatory response by complement in vivo. Blood 110, 228-236 (2007). (Pubitemid 47026839)
62. Hosokawa M, Klegeris A, Maguire J, McGeer PL. Expression of complement messenger RNAs and proteins by human oligodendroglial cells. Glia 42, 417-423 (2003). (Pubitemid 36702282)
63. Yu JX, Bradt BM, Cooper NR. Constitutive expression of proinflammatory complement components by subsets of neurons in the central nervous system. J. Neuroimmunol. 123, 91-101 (2002). (Pubitemid 34195611)
64. Gasque P, Fontaine M, Morgan BP. Complement expression in human brain. Biosynthesis of terminal pathway components and regulators in human glial cells and cell lines. J. Immunol. 154, 4726-4733 (1995).
65. Gasque P, Dean YD, McGreal EP, VanBeek J, Morgan BP. Complement components of the innate immune system in health and disease in the CNS. Immunopharmacology 49, 171-186 (2000).
66. Depboylu C, Schäfer MKH, Schwaeble WJ et al. Increase of C1q biosynthesis in brain microglia and macrophages during lentivirus infection in the rhesus macaque is sensitive to antiretroviral treatment with 6-chloro-2′ 3′- dideoxyguanosine. Neurobiol. Dis. 20, 12-26 (2005). (Pubitemid 41219199)
67. Dietzschold B, Schwaeble W, Schäfer MKH et al. Expression of C1q, a subcomponent of the rat complement system, is dramatically enhanced in brains of rats with either Borna disease or experimental allergic encephalomyelitis. J. Neurol. Sci. 130, 11-16 (1995).
68. Nathanson N, Ahmed R. Immune responses to viral infection. In: Viral Pathogenesis and Immunity (2nd Edition).Nathanson N, Ahmed R, Biron CA et al. (Eds).Academic Press/Elsevier, Amsterdam, Boston, MA, USA, 72-87 (2007).
69. Nathanson N, Biron CA. Innate immunity. In: Viral Pathogenesis and Immunity (2nd Edition).Nathanson N, Ahmed R, Biron CA et al. (Eds).Academic Press/Elsevier, Amsterdam, Boston, MA, USA, 59-71 (2007).
70. Libbey JE, Fujinami RS. Adaptive immune response to viral infections in the central nervous system. In: Handbook of Clinical Neurology. Third Series: Neurovirology. Tselis A (Ed.).Elsevier, NY, USA (2011) (In Press).
71. de Araujo EG, da Silva GM, dos Santos AA. Neuronal cell survival. The role of interleukins. Ann. NY Acad. Sci. 1153, 57-64 (2009).
72. Tuttolomondo A, Di Raimondo D, di Sciacca R, Pinto A, Licata G. Inflammatory cytokines in acute ischemic stroke. Curr. Pharm. Des. 14, 3574-3589 (2008).
73. Bye N, Habgood MD, Callaway JK et al. Transient neuroprotection by minocycline following traumatic brain injury is associated with attenuated microglial activation but no changes in cell apoptosis or neutrophil infiltration. Exp. Neurol. 204, 220-233 (2007). (Pubitemid 46330272)
74. Campbell JH, Burdo TH, Autissier P et al. The tetracycline antibiotic minocycline prevents the activation of CD14/CD16 monocytes in blood and accumulation in the brain, as well as the development of SIV encephalitis in rhesus macaques. J. NeuroVirol. 15(Suppl. 1), 14 (2009).
75. Mishra MK, Basu A. Minocycline neuroprotects, reduces microglial activation, inhibits caspase 3 induction, and viral replication following Japanese encephalitis. J. Neurochem. 105, 1582-1595 (2008). (Pubitemid 351678483)
76. Dutta K, Kumawat KL, Nazmi A, Mishra MK, Basu A. Minocycline differentially modulates viral infection and persistence in an experimental model of Japanese encephalitis. J. Neuroimmune. Pharmacol. 5, 553-565 (2010).
77. Campbell IL, Abraham CR, Masliah E et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc. Natl Acad. Sci. USA 90, 10061-10065 (1993). (Pubitemid 23328251)
78. Samland H, Huitron-Resendiz S, Masliah E, Criado J, Henriksen SJ, Campbell IL. Profound increase in sensitivity to glutamatergic- but not cholinergic agonist-induced seizures in transgenic mice with astrocyte production of IL-6. J. Neurosci. Res. 73, 176-187 (2003). (Pubitemid 36835418)
79. Steffensen SC, Campbell IL, Henriksen SJ. Site-specific hippocampal pathophysiology due to cerebral overexpression of interleukin-6 in transgenic mice. Brain Res. 652, 149-153 (1994). (Pubitemid 24222909)
80. Campbell IL, Hofer MJ, Pagenstecher A. Transgenic models for cytokine-induced neurological disease. Biochim. Biophys. Acta 1802, 903-917 (2010).
81. McCright IJ, Tsunoda I, Whitby FG, Fujinami RS. Theiler's viruses with mutations in loop I of VP1 lead to altered tropism and pathogenesis. J. Virol. 73, 2814-2824 (1999). (Pubitemid 29135668)