Herpes simplex virus type 1 inoculation enhances hippocampal excitability and seizure susceptibility in mice

European Journal of Neuroscience

Volumn 18, Issue 12, 2003, Pages 3294-3304

  Wu, Hung Ming ^a,b   Huang, Chiung Chun ^a   Chen, Shun Hua ^a   Liang, Ying Ching ^a   Tsai, Jing Jane ^a   Hsieh, Ching Liang ^c   Hsu, Kuei Sen ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b KUANG TIEN GENERAL HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Epilepsy; Herpes simplex virus type 1; Hippocampus; HSV encephalitis; Kainate

Indexed keywords

ACUTE DISEASE; AFTERHYPERPOLARIZATION; AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CELL SURVIVAL; CONTROLLED STUDY; CORNEA; CORTICAL SYNCHRONIZATION; DISEASE ASSOCIATION; EPILEPSY; EPILEPTOGENESIS; EXCITABILITY; HERPES SIMPLEX VIRUS 1; HIPPOCAMPUS; INOCULATION; LONG TERM EXPOSURE; MALE; MEMBRANE DEPOLARIZATION; MEMBRANE RESISTANCE; MEMBRANE STEADY POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEIZURE SUSCEPTIBILITY; VIRUS PATHOGENESIS;

ACTION POTENTIALS; ANIMALS; CAUSALITY; CELL MEMBRANE; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; ELECTRIC IMPEDANCE; ENCEPHALITIS, HERPES SIMPLEX; EPILEPSY; EPILEPSY, TEMPORAL LOBE; HERPESVIRUS 1, HUMAN; HIPPOCAMPUS; KAINIC ACID; MALE; MICE; MICE, INBRED BALB C; NEURAL PATHWAYS; ORGAN CULTURE TECHNIQUES; PYRAMIDAL CELLS; VIRAL PROTEINS;

EID: 0348049788     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2003.03075.x     Document Type: Article

References (62)

1. Annegers, J.F., Hauser, W.A., Beghi, E., Nicolosi, A. & Kurland, L.T. (1988) The risk of unprovoked seizures after encephalitis and meningitis. Neurology, 38, 1407-1410.
2. Baichwal, V.R. & Sugden, B. (1988) Latency comes of age for herpesviruses. Cell, 52, 787-789.
3. Baringer, J.R. & Pisani, P. (1994) Herpes simplex virus genomes in human nervous system tissue analyzed by polymerase chain reaction. Ann. Neurol., 36, 823-829.
4. Beers, D.R., Henkel, J.S., Schaefer, D.C., Rose, J.W. & Stroop, W.G. (1993) Neuropathology of herpes simplex virus encephalitis in a rat seizure model. J. Neuropathol. Exp. Neurol., 52, 241-252.
5. Bernard, C. & Wheal, H.V. (1995) Plasticity of AMPA and NMDA receptor-mediated epileptiform activity in a chronic model of temporal lobe epilepsy. Epilepsy Res., 21, 95-107.
6. Boerman, R.H., Peters, A.C., Bloem, B.R., Raap, A.K. & van der Ploeg, M. (1992) Spread of herpes simplex virus to the cerebrospinal fluid and the meninges in experimental mouse encephalitis. Acta Neuropathol., 83, 300-307.
7. Bragin, A., Wilson, C.L. & Engel, J. Jr (2000) Chronic epileptogenesis requires development of a network of pathologically interconnected neuron clusters: a hypothesis. Epilepsia, 41, S144-S152.
8. Chen, S.H., Kramer, M.F., Schaffer, P.A. & Coen, D.M. (1997) A viral function represses accumulation of transcripts from productive-cycle genes in mouse ganglia latently infected with herpes simplex virus. J. Virol., 71, 5878-5884.
9. Coen, D.M., Fleming, H.E. Jr, Leslie, L.K. & Retondo, M.J. (1985) Sensitivity of arabinosyladenine-resistant mutants of herpes simplex virus to other antiviral drugs and mapping of drug hypersensitivity mutations to the DNA polymerase locus. J. Virol., 53, 477-488.
10. Coen, D.M., Kosz-Vnenchak, M., Jacobson, J.G., Leib, D.A., Bogard, C.L., Schaffer, P.A., Tyler, K.L. & Knipe, D.M. (1989) Thymidine kinase-negative herpes simplex virus mutants establish latency in mouse trigeminal ganglia but do not reactivate. Proc. Natl. Acad. Sci. USA, 86, 4736-4740.
11. Cole, A.E. & Nicoll, R.A. (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science, 221, 1299-1301.
12. Colino, A. & Halliwell, J.V. (1987) Differential modulation of three separate K-conductances in hippocampal CA1 neurons by serotonin. Nature, 328, 73-77.
13. Cornford, M.E. & McCormick, G.F. (1997) Adult-onset temporal lobe epilepsy associated with smoldering herpes simplex 2 infection. Neurology, 48, 425-430.
14. Cornish, S.M. & Wheal, H.V. (1989) Long-term loss of paired pulse inhibition in the kainic acid-lesioned hippocampus of the rat. Neuroscience, 28, 563-571.
15. Davies, C.H., Davies, S.N. & Collingridge, G.L. ( 1990) Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J. Physiol. (Lond.), 424, 513-531.
16. Davis, L.E. & Johnson, R.T. (1979) An explanation for the localization of herpes simplex encephalitis? Ann. Neurol., 5, 2-5.
17. De Graff, A.S. ( 1974) Epidemiological aspects of epilepsy in Northern Norway. Epilepsia, 15, 291-299.
18. Dube, C., Chen, K., Eghbal-Ahmadi, M., Brunson, K., Soltesz, I. & Baram, T.Z. (2000) Prolonged febrile seizures in the immature rat model enhance hippocampal excitability long term. Ann. Neurol., 47, 336-344.
19. Esiri, M.M. (1982) Herpes simplex encephalitis: immunohistological study of the distribution of viral antigen within the brain. J. Neurol. Sci., 54, 209-226.
20. Fodor, P.A., Levin, M.J., Weinberg, A., Sandberg, E., Sylman, J. & Tyler, K.L. (1998) Atypical herpes simplex virus encephalitis diagnosed by PCR amplification of viral DNA from CSF. Neurology, 51, 554-559.
21. Gannicliffe, A., Saldanha, J.A., Itzhaki, R.F. & Sutton, R.N. (1985) Herpes simplex viral DNA in temporal lobe epilepsy. Lancet, 1, 214-215.
22. Griffith, J.F., Kibrick, S., Dodge, P.R. & Richardson, E.P. (1967) Experimental herpes simplex encephalitis. Electroencephalographic, clinical, virologic, and pathologic observations in the rabbit. Electroencephalogr. Clin. Neurophysiol., 23, 263-269.
23. Haas, H.L. & Konnerth, A. (1983) Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature, 302, 432-434.
24. Hablitz, J.J. & Johnston, D. ( 1981 ) Endogenous nature of spontaneous bursting in hippocampal pyramidal neurons. Cell Mol. Neurobiol., 1, 325-334.
25. Habu, S., Akamatsu, K., Tamaoki, N. & Okumura, K. (1984) In vivo significance of NK cell on resistance against virus (HSV-1) infections in mice. J. Immunol., 133, 2743-2747.
26. Haglund, M.M. & Schwartzkroin, P.A. (1990) Role of Na-K pump potassium regulation and IPSPs in seizures and spreading depression in immature rabbit hippocampal slices. J. Neurophysiol., 63, 25-239.
27. Haglund, M.M., Stahl, W.L., Kunkel, D.D. & Schwartzkroin, P.A. (1985) Developmental and regional differences in the localization of Na,K-ATPase activity in the rabbit hippocampus. Brain Res., 343, 98-203.
28. Hauser, W.A. & Kurland, L.T. (1975) The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia, 16, 1-66.
29. Hsieh, C.L., Tang, N.Y., Chiang, S.Y., Hsieh, C.T. & Lin, J.G. (1999) Anticonvulsive and free radical scavenging actions of two herbs, Uncaria rhynchophylla (MIQ) Jack and Gastrodia elata Bl., in kainic acid-treated rats. Life Sci., 65, 2071-2082.
30. Huang, C.C. & Hsu, K.S. (1999) Protein tyrosine kinase is required for the induction of long-term potentiation in the rat hippocampus. J. Physiol. (Lond.), 520, 783-796.
31. Jensen, M.S., Azouz, R. & Yaari, Y. (1994) Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium. J. Neurophysiol., 71, 831-839.
32. Johnson, R.T. (1964) The pathogenesis of herpes virus encephalitis. II. A cellular basis for the development of resistance with age. J. Exp. Med., 120, 359-374.
33. Klapper, P.E., Cleator, G.M. & Longson, M. (1984) Mild forms of herpes encephalitis. J. Neuro. Neurosurg. Psychiatry, 47, 1247-1250.
34. Lai, C.W. & Gragasin, M.E. (1988) Electroencephalography in herpes simplex encephalitis. J. Clin. Neurophysiol., 5, 87-103.
35. Lausch, R.N., Kleinschradt, W.R., Monteiro, C., Kayes, S.G. & Oakes, J.E. (1985) Resolution of HSV corneal infection in the absence of delayed-type hypersensitivity. Invest. Ophthalmol. Vis. Sci., 26. 1509-1515.
36. Leib, D.A., Coen, D.M., Bogard, C.L., Hicks, K.A., Yager, D.R., Knipe, D.M., Tyler, K.L. & Schaffer, P.A. (1989) Immediate-early regulatory gene mutants define different stages in the establishment and reactivation of herpes simplex virus latency. J. Virol., 63, 759-768.
37. Madison, D.V., Lancaster, B. & Nicoll, R.A. (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J. Neurosci., 7, 733-741.
38. Madison, D.V. & Nicoll, R.A. (1982) Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature, 299, 636-638.
39. Madison, D.V. & Nicoll, R.A. (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurons in vitro. J. Physiol. (Lond.), 354, 319-331.
40. Marks, D.A., Kim, J., Spencer, D.D. & Spencer, S.S. (1992) Characteristics of intractable seizures following meningitis and encephalitis. Neurology, 42, 1513-1518.
41. Mathern, G.W., Babb, T.L., Leite, J.P, Pretorius, K., Yeoman, K.M. & Kuhlman, P.A. (1996) The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res., 26, 151-161.
42. Mayer, M.L. (1986) Selective block of inward but not outward rectification in rat sensory neurones infected with herpes simplex virus. J. Physiol. (Lond.), 375, 327-338.
43. Pena, Y.M., el-Mallakh, R.S., Shanley, J.D. & Podurgiel, B.J. (1987) Periodic sharp complexes in herpes simplex virus encephalitis: survival in an elderly man. Clin. Electroencephalogr., 18, 1-9.
44. Racine, R.J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32, 281-294.
45. Reiner, P.B. & Kamondi, A. (1994) Mechanisms of antihistamine- induced sedation in the human brain: H1 receptor activation reduces a background leakage potassium current. Neuroscience, 59, 79-588.
46. Rocca, W.A., Sharbrough, F.W., Hauser, W.A., Annegers, J.F. & Schoenberg, B.S. (1987) Risk factors of complex partial seizures: a population-based case-control study. Ann. Neurol., 21, 22-31.
47. Ross, C.A. (1972) Herpes simplex and temporal lobe epilepsy. BMJ, 3, 112.
48. Rowley, A.H., Whitley, R.J., Lakeman, F.D. & Wolinsky, S.M. (1990) Rapid detection of herpes simplex virus DNA in CSF of patients with herpes simplex encephalitis. Lancet, 335, 440-444.
49. 2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol. (Lond.), 532, 205-216.
50. Sanders, V.J., Felisan, S.L., Waddell, A.E., Conrad, A.J., Schmid, P., Swartz, B.E., Kaufman, M., Walsh, G.O., De Salles, A.A.F. & Tourtellotte, W.W. (1997) Presence of herpes simplex DNA in surgical tissue from human epileptic seizure foci detected by polymerase chain reaction: preliminary study. Arch. Neurol., 54, 954-960.
51. Schlitt, M., Bucher, A.P., Stroop, W.G., Pindak, F., Bastian, F.O., Jennings, R.A., Lakeman, A.D. & Whitley, R.J. (1988) Neurovirulence in an experimental focal herpes encephalitis: relationship to observed seizures. Brain Res., 440, 293-298.
52. Schmutzhard, E. (2001) Viral infections of the CNS with special emphasis on herpes simplex infections. J. Neurol., 248, 469-477.
53. Storm, J.F. (1990) Potassium currents in hippocampal pyramidal cells. Prog. Brain. Res., 83, 61-187.
54. Stroop, W.G. & Schaefer, D.C. (1986) Production of encephalitis restricted to the temporal lobes by experimental reactivation of herpes simplex virus. J. Infect. Dis., 153, 721-731.
55. Stroop, W.G. & Schaefer, D.C. (1989) Neurovirulence of two clonally related herpes simplex virus type 1 strains in a rabbit seizure model. J. Neuropathol. Exp. Neurol., 48, 171-183.
56. Su, Y.H., Oakes, J.E. & Lausch, R.N. (1990) Ocular avirulence of a herpes simplex virus type 1 strain is associated with heightened sensitivity to alpha/ beta interferon. J. Virol., 64, 2187-2192.
57. Tumpey, T.M., Chen, S.H., Oakes, J.E. & Lausch, R.N. (1996) Neutrophil-mediated suppression of virus replication after herpes simplex virus type 1 infection of the murine cornea. J. Virol., 70, 898-904.
58. Whitley, R.J., Lakeman, A.D., Nahmias, A. & Roizman, S. (1982) DNA restriction-enzyme analysis of herpes simplex virus isolates obtained from patients with encephalitis. N. Engl. J. Med., 307, 1060-1062.
59. Whitley, R.J., Soong, S.J., Dolin, R., Galasso, G.J., Ch'ien, L.T. & Alford, CA. (1977) Adenine arabinoside therapy of biopsy-proved herpes simplex encephalitis. National Institute of Allergy and Infectious Diseases collaborative antiviral study. N. Engl. J. Med., 297, 289-294.
60. Williamson, A., Spencer, D.D. & Shepherd, G.M. (1993) Comparison between the membrane and synaptic properties of human and rodent dentate granule cells. Brain Res., 622, 194-202.
61. Wu, H.M., Huang, C.C., Li, L.H., Tsai, J.J. & Hsu, K.S. (2000) The Chinese herbal medicine Chai-Hu-Long-Ku-Mu-Li-Tan (TW-001) exerts anticonvulsant effects against different experimental models of seizure in rats. Jpn. J. Pharmacol., 82, 247-260.
62. Zawatzky, R., Gresser, I., DeMaeyer, E. & Kirchner, H. (1982) The role of interferon in the resistance of C57BL/6 mice to various doses of herpes simplex virus type 1. J. Infect. Dis., 146, 405-410.