Immunological perspectives of temporal lobe seizures

Journal of Neuroimmunology

Volumn 263, Issue 1-2, 2013, Pages 1-7

  Liimatainen, Suvi ^a   Kai, Lehtimäki ^a   Johanna, Palmio ^a   Tiina, Alapirtti ^a   Jukka, Peltola ^a  

^a TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

Adaptive immunity; Antibody; Cytokine; Innate immunity; Neurodegeneration; Neuromodulation

Indexed keywords

4 AMINOBUTYRIC ACID; CYCLOOXYGENASE 2; CYTOKINE; GANGLIOSIDE GM1 ANTIBODY; GLUTAMATE DECARBOXYLASE; GLUTEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERFERON; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 6; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA; VIRUS DNA; VOLTAGE GATED POTASSIUM CHANNEL;

ADAPTIVE IMMUNITY; ASTROCYTE; EPILEPTOGENESIS; GRANULOCYTE; HUMAN; HUMAN HERPESVIRUS 6; IMMUNOPATHOGENESIS; INNATE IMMUNITY; MACROPHAGE; MICROGLIA; NERVE CELL; NERVE DEGENERATION; NEUROIMMUNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TEMPORAL LOBE EPILEPSY;

ADAPTIVE IMMUNITY; ANTIBODY; CYTOKINE; INNATE IMMUNITY; NEURODEGENERATION; NEUROMODULATION;

ADAPTIVE IMMUNITY; ANIMALS; AUTOANTIBODIES; EPILEPSY, TEMPORAL LOBE; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; SEIZURES;

EID: 84884816505     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2013.08.001     Document Type: Review

References (93)

1. Aarli J.A. Epilepsy and the immune system. Arch. Neurol. 2000, 57:1689-1692.
2. Akin D., Ravizza T., Maroso M., Carcak N., Eryigit T., Vanzulli I., Aker R.G., Vezzani A., Onat F.Y. IL-1β is induced in reactive astrocytes in the somatosensory cortex of rats with genetic absence epilepsy at the onset of spike-and-wave discharges, and contributes to their occurrence. Neurobiol. Dis. 2011, 44:259-269.
3. Alapirtti T., Rinta S., Hulkkonen J., Mäkinen R., Keränen T., Peltola J. Interleukin-6, interleukin-1 receptor antagonist and interleukin-1beta production in patients with focal epilepsy: A video-EEG study. J. Neurol. Sci. 2009, 280:94-97.
4. Aronica E., Crino P.B. Inflammation in epilepsy: clinical observations. Epilepsia 2011, 52(Suppl. 3):26-32.
5. Balosso S., Ravizza T., Perego C., Peschon J., Campbell I.L., De Simoni M.G., Vezzani A. Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors. Ann. Neurol. 2005, 57:804-812.
6. Bartfai T., Sanchez-Alavez M., Andell-Jonsson S., Schultzberg M., Vezzani A., Danielsson E., Conti B. Interleukin-1 system in CNS stress: seizures, fever, and neurotrauma. Ann. N. Y. Acad. Sci. 2007, 1113:173-177.
7. Bartolomei F., Boucraut J., Barrié M., Kok J., Dravet C., Viallat D., Bernard D., Gastaut J.L. Cryptogenic partial epilepsies with anti-GM1 antibodies: a new form of immune-mediated epilepsy?. Epilepsia 1996, 37:922-926.
8. Bauer S., Cepok S., Todorova-Rudolph A., Nowak M., Köller M., Lorenz R., Oertel W.H., Rosenow F., Hemmer B., Hamer H.M. Etiology and site of temporal lobe epilepsy influence postiktal cytokine release. Epilepsy Res. 2009, 86:82-88.
9. Bauer J., Vezzani A., Bien C.G. Epileptic encephalitis: the role of the innate and adaptive immune system. Brain Pathol. 2012, 22:412-421.
10. Bien C.G., Scheffer I.E. Autoantibodies and epilepsy. Epilepsia 2011, 52(Suppl. 3):18-22.
11. Bien C.G., Urbach H., Schramm J., Soeder B.M., Becker A.J., Voltz R., Vincent A., Elger C.E. Limbic encephalitis as a precipitating event in adult-onset temporal lobe epilepsy. Neurology 2007, 69:1236-1244.
12. Bien C.G., Vincent A., Barnett M.H., Becker A.J., Blümcke I., Graus F., Jellinger K.A., Reuss D.E., Ribalta T., Schlegel J., Sutton I., Lassmann H., Bauer J. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 2012, 135:1622-1638.
13. Callenbach P.M., Jol-Van Der Zijde C.M., Geerts A.T., Arts W.F., Van Donselaar C.A., Peters A.C., Stroink H., Brouwer O.F., Van Tol M.J., Dutch Study of Epilepsy in Childhood Immunoglobulins in children with epilepsy: the Dutch Study of Epilepsy in Childhood. Clin. Exp. Immunol. 2003, 132:144-151.
14. Cavazos J.E., Golarai G., Sutula T.P. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J. Neurosci. 1991, 11:2795-2803.
15. Cavazos J.E., Das I., Sutula T.P. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J. Neurosci. 1994, 14:3106-3121.
16. Chen C., Bazan N.G. Endogenous PGE2 regulates membrane excitability and synaptic transmission in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2005, 93:929-941.
17. Crespel A., Coubes P., Rousset M.C., Brana C., Rougier A., Rondouin G., Bockaert J., Baldy-Moulinier M., Lerner-Natoli M. Inflammatory reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res. 2002, 18:159-169.
18. Dalmau J., Gleichman A.J., Hughes E.G., Rossi J.E., Peng X., Lai M., Dessain S.K., Rosenfeld M.R., Balice-Gordon R., Lynch D.R. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol. 2008, 7:1091-1098.
19. De Simoni M.G., Perego C., Ravizza T., Moneta D., Conti M., Marchesi F., De Luigi A., Garattini S., Vezzani A. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur. J. Neurosci. 2000, 12:2623-2633.
20. Dinkel K., Meinck H.M., Jury K.M., Karges W., Richter W. Inhibition of gamma-aminobutyric acid synthesis by glutamic acid decarboxylase autoantibodies in stiff-man syndrome. Ann. Neurol. 1998, 44:194-201.
21. Eriksson C., Van Dam A.M., Lucassen P.J., Bol J.G., Winblad B., Schultzberg M. Immunohistochemical localization of interleukin-1beta, interleukin-1 receptor antagonist and interleukin-1beta converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 1999, 93:915-930.
22. Eriksson K., Peltola J., Keränen T., Haapala A.M., Koivikko M. High prevalence of antiphospholipid antibodies in children; a controlled study of 50 patients. Epilepsy Res. 2001, 46:129-137.
23. Errichiello L., Perruolo G., Pascarella A., Formisano P., Minetti C., Striano S., Zara F., Striano P. Autoantibodies to glutamic acid decarboxylase (GAD) in focal and generalized epilepsy: A study on 233 patients. J. Neuroimmunol. 2009, 211:120-123.
24. Fotheringham J., Donati D., Akhyani N., Fogdell-Hahn A., Vortmeyer A., Heiss J.D., Williams E., Weinstein S., Bruce D.A., Gaillard W.D., Sato S., Theodore W.H., Jacobson S. Association of human herpesvirus-6B with mesial temporal lobe epilepsy. PloS Med. 2007, 4:e180.
25. Friedman A., Dingledine R. Molecular cascades that mediate the influence of inflammation on epilepsy. Epilepsia 2011, 52(Suppl. 3):33-39.
26. Getts D.R., Balcar V.J., Matsumoto I., Müller M., King N.J. Viruses and the immune system: their roles in seizure cascade development. J. Neurochem. 2008, 104:1167-1176.
27. Granata T., Cross H., Theodore W., Avanzini G. Immune-mediated epilepsies. Epilepsia 2011, 52(Suppl. 3):5-11.
28. Graus F., Saiz A., Lai M., Bruna J., López F., Sabater L., Blanco Y., Rey M.J., Ribalta T., Dalmau J. Neuronal surface antigen antibodies in limbic encephalitis: clinical-immunologic associations. Neurology 2008, 71:930-936.
29. Hughes E.G., Peng X., Gleichman A.J., Lai M., Zhou L., Tsou R., Parsons T.D., Lynch D.R., Dalmau J., Balice-Gordon R.J. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J. Neurosci. 2010, 30:5866-5875.
30. Irani S.R., Buckley C., Vincent A., Cockerell O.C., Rudge P., Johnson M.R., Smith S. Immunotherapy-responsive seizure-like episodes with potassium channel antibodies. Neurology 2008, 71:1647-1648.
31. Irani S.R., Alexander S., Waters P., Kleopa K.A., Pettingill P., Zuliani L., Peles E., Buckley C., Lang B., Vincent A. Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan's syndrome and acquired neuromyotonia. Brain 2010, 133:2734-2748.
32. Irani S.R., Bera K., Waters P., Zuliani L., Maxwell S., Zandi M.S., Friese M.A., Galea I., Kullmann D.M., Beeson D., Lang B., Bien C.G., Vincent A. N-methyl-D-aspartate antibody encephalitis: temporal progression of clinical and paraclinical observations in a predominantly non-paraneoplastic disorder of both sexes. Brain 2010, 133:1655-1667.
33. Irani S.R., Bien C.G., Lang B. Autoimmune epilepsies. Curr. Opin. Neurol. 2011, 24:146-153.
34. Irani S.R., Michell A.W., Lang B., Pettingill P., Waters P., Johnson M.R., Schott J.M., Armstrong R.J., Zagami S., Bleasel A., Somerville E.R., Smith S.M., Vincent A. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann. Neurol. 2011, 69:892-900.
35. Ishida K., Mitoma H., Song S.Y., Uchihara T., Inaba A., Eguchi S., Kobayashi T., Mizusawa H. Selective suppression of cerebellar GABAergic transmission by an autoantibody to glutamic acid decarboxylase. Ann. Neurol. 1999, 46:263-267.
36. Kalueff A.V., Lehtimaki K.A., Ylinen A., Honkaniemi J., Peltola J. Intranasal administration of human IL-6 increases the severity of chemically induced seizures in rats. Neurosci. Lett. 2004, 365:106-110.
37. Kälviäinen R., Salmenperä T. Do recurrent seizures cause neuronal damage? A series of studies with MRI volumetry in adults with partial epilepsy. Prog. Brain Res. 2002, 135:279-295.
38. Kotloski R., Lynch M., Lauersdorf S., Sutula T. Repeated brief seizures induce progressive hippocampal neuron loss and memory deficit. Prog. Brain Res. 2002, 135:95-110.
39. Lai M., Hughes E.G., Peng X., Zhou L., Gleichman A.J., Shu H., Matà S., Kremens D., Vitaliani R., Geschwind M.D., Bataller L., Kalb R.G., Davis R., Graus F., Lynch D.R., Balice-Gordon R., Dalmau J. AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann. Neurol. 2009, 65:424-434.
40. Lai M., Huijbers M.G., Lancaster E., Graus F., Bataller L., Balice-Gordon R., Cowell J.K., Dalmau J. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol. 2010, 9:776-785.
41. Lalic T., Pettingill P., Vincent A., Capogna M. Human limbic encephalitis serum enhances hippocampal mossy fiber-CA3 pyramidal cell synaptic transmission. Epilepsia 2011, 52:121-131.
42. Lancaster E., Lai M., Peng X., Hughes E., Constantinescu R., Raizer J., Friedman D., Skeen M.B., Grisold W., Kimura A., Ohta K., Iizuka T., Guzman M., Graus F., Moss S.J., Balice-Gordon R., Dalmau J. Antibodies to the GABA(B) receptor in limbic encephalitis with seizures: case series and characterisation of the antigen. Lancet Neurol. 2010, 9:67-76.
43. Lehtimäki K.A., Peltola J., Koskikallio E., Keränen T., Honkaniemi J. Expression of cytokines and cytokine receptors in the rat brain after kainic acid-induced seizures. Mol. Brain Res. 2003, 110:253-260.
44. Lehtimäki K.A., Keränen T., Huhtala H., Hurme M., Ollikainen J., Honkaniemi J., Palmio J., Peltola J. Regulation of IL-6 system in cerebrospinal fluid and serum compartments by seizures: the effect of seizure type and duration. J. Neuroimmunol. 2004, 152:121-125.
45. Lehtimäki K.A., Keränen T., Palmio J., Mäkinen R., Hurme M., Honkaniemi J., Peltola J. Increased plasma levels of cytokines after seizures in localization-related epilepsy. Acta Neurol. Scand. 2007, 116:226-230.
46. Leung A.K., Robson W.L. Febrile seizures. J. Pediatr. Health Care 2007, 21:250-255.
47. Liimatainen S., Fallah M., Kharazmi E., Peltola M., Peltola J. Interleukin-6 levels are increased in temporal lobe epilepsy but not in extra-temporal lobe epilepsy. J. Neurol. 2009, 256:796-802.
48. Liimatainen S., Peltola M., Fallah M., Kharazmi E., Haapala A.M., Peltola J. The high prevalence of antiphospholipid antibodies in refractory focal epilepsy is related to recurrent seizures. Eur. J. Neurol. 2009, 16:134-141.
49. Liimatainen S., Peltola M., Sabater L., Fallah M., Kharazmi E., Haapala A.M., Dastidar P., Knip M., Saiz A., Peltola J. Clinical significance of glutamic acid decarboxylase antibodies in patients with epilepsy. Epilepsia 2010, 51:760-767.
50. Liimatainen S., Fallah M., Kharazmi E., Haapala A.-M., Isojärvi J., Peltola J. High concentration of immunoglobulin A is associated with temporal lobe epilepsy. Epilepsy Res. 2013, 103:54-61.
51. Mackworth-Young C.G., Hughes G.R. Epilepsy: an early symptom of systemic lupus erythematosus. J. Neurol. Neurosurg. Psychiatry 1985, 48:185.
52. Majoie H.J., Rijkers K., Berfelo M.W., Hulsman J.A., Myint A., Schwarz M., Vles J.S. Vagus nerve stimulation in refractory epilepsy: effects on pro- and anti-inflammatory cytokines in peripheral blood. Neuroimmunomodulation 2011, 18:52-56.
53. Malter M.P., Helmstaedter C., Urbach H., Vincent A., Bien C.G. Antibodies to glutamic acid decarboxylase define a form of limbic encephalitis. Ann. Neurol. 2010, 67:470-478.
54. Marcheselli V.L., Bazan N.G. Sustained induction of prostaglandin endoperoxide synthase-2 by seizures in hippocampus. Inhibition by a platelet-activating factor antagonist. J. Biol. Chem. 1996, 271:24794-2479.
55. Mathern G.W., Adelson P.D., Cahan L.D., Leite J.P. Hippocampal neuron damage in human epilepsy: Meyer's hypothesis revisited. Prog. Brain Res. 2002, 135:237-251.
56. McKnight K., Jiang Y., Hart Y., Cavey A., Wroe S., Blank M., Shoenfeld Y., Vincent A., Palace J., Lang B. Serum antibodies in epilepsy and seizure-associated disorders. Neurology 2005, 13:1730-1736.
57. Mitoma H., Song S.Y., Ishida K., Yamakuni T., Kobayashi T., Mizusawa H. Presynaptic impairment of cerebellar inhibitory synapses by an autoantibody to glutamate decarboxylase. J. Neurol. Sci. 2000, 175:40-44.
58. Niehusmann P., Dalmau J., Rudlowski C., Vincent A., Elger C.E., Rossi J.E., Bien C.G. Diagnostic value of N-methyl-D-aspartate receptor antibodies in women with new-onset epilepsy. Arch. Neurol. 2009, 66:458-464.
59. Özkara Ç., Vigevano F. Immuno- and antiinflammatory therapies in epileptic disorders. Epilepsia 2011, 52(Suppl. 3):45-51.
60. Palace J., Lang B. Epilepsy: an autoimmune disease?. J. Neurol. Neurosurg. Psychiatry 2000, 69:711-714.
61. Palmio J., Keränen T., Alapirtti T., Hulkkonen J., Mäkinen R., Holm P., Suhonen J., Peltola J. Elevated serum neuron-specific enolase in patients with temporal lobe epilepsy: a video-EEG study. Epilepsy Res. 2008, 81:155-160.
62. Peltola J., Hurme M., Miettinen A., Keränen T. Elevated levels of interleukin-6 may occur in cerebrospinal fluid from patients with recent epileptic seizures. Epilepsy Res. 1998, 31:129-133.
63. Peltola J., Haapala A., Isojärvi J.I., Auvinen A., Palmio J., Latvala K., Kulmala P., Laine S., Vaarala O., Keränen T. Antiphospholipid and antinuclear antibodies in patients with epilepsy or new-onset seizure disorders. Am. J. Med. 2000, 109:712-717.
64. Peltola J., Kulmala J., Isojärvi J., Saiz A., Latvala K., Palmio J., Savola K., Knip M., Keränen T., Graus F. Autoantibodies to glutamic acid decarboxylase in patients with therapy-resistant epilepsy. Neurology 2000, 12:46-50.
65. Peltola J., Palmio J., Korhonen L., Suhonen J., Miettinen A., Hurme M., Lindholm D., Keränen T. Interleukin-6 and interleukin-1 receptor antagonist in cerebrospinal fluid from patients with recent tonic-clonic seizures. Epilepsy Res. 2000, 41:205-211.
66. Peltola M., Kaukinen K., Dastidar P., Haimila K., Partanen J., Haapala A.M., Mäki M., Keränen T., Peltola J. Hippocampal sclerosis in refractory temporal lobe epilepsy is associated with gluten sensitivity. J. Neurol. Neurosurg. Psychiatry 2009, 80:626-630.
67. Penkowa M., Molinero A., Carrasco J., Hidalgo J. Interleukin-6 deficiency reduces the brain inflammatory response and increases oxidative stress and neurodegeneration after kainic acid-induced seizures. Neuroscience 2001, 102:805-818.
68. Pitkänen A., Sutula T. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 2002, 1:173-181.
69. Probert L., Akassoglou K., Kassiotis G., Pasparakis M., Alexopoulou L., Kollias G. TNF-alpha transgenic and knockout models of CNS inflammation and degeneration. J. Neuroimmunol. 1997, 72:137-141.
70. Quek A.M., Britton J.W., McKeon A., So E., Lennon V.A., Shin C., Klein C.J., Watson R.E., Kotsenas A.L., Lagerlund T.D., Cascino G.D., Worrell G.A., Wirrell E.C., Nickels K.C., Aksamit A.J., Noe K.H., Pittock S.J. Autoimmune epilepsy: clinical characteristics and response to immunotherapy. Arch. Neurol. 2012, 69:582-593.
71. Ranua J., Luoma K., Peltola J., Haapala A.M., Raitanen J., Auvinen A., Isojärvi J. Anticardiolipin and antinuclear antibodies in adult patients with epilepsy - a population based cross-sectional study. Epilepsy Res. 2004, 58:13-18.
72. Ravizza T., Rizzi M., Perego C., Richichi C., Velísková J., Moshé S.L., De Simoni M.G., Vezzani A. Inflammatory response and glia activation in developing rat hippocampus after status epilepticus. Epilepsia 2005, 46:113-117.
73. Ravizza T., Boer K., Redeker S., Spliet W.G., van Rijen P.C., Troost D., Vezzani A., Aronica E. The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol. Dis. 2006, 24:128-143.
74. Ravizza T., Gagliardi B., Noé F., Boer K., Aronica E., Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: Evidence from experimental models and human temporal lobe epilepsy. Neurobiol. Dis. 2008, 29:142-160.
75. Rizzi M., Perego C., Aliprandi M., Richichi C., Ravizza T., Colella D., Velískǒvá J., Moshé S.L., De Simoni M.G., Vezzani A. Glia activation and cytokine increase in rat hippocampus by kainic acid-induced status epilepticus during postnatal development. Neurobiol. Dis. 2003, 14:494-503.
76. Rogers S.W., Andrews P.I., Gahring L.C., Whisenand T., Cauley K., Crain B., Hughes T.E., Heinemann S.F., McNamara J.O. Autoantibodies to glutamate receptor GluR3 in Rasmussen's encephalitis. Science 1994, 265:648-651.
77. Salmenperä T., Kälviäinen R., Partanen K., Pitkänen A. Hippocampal and amygdaloid damage in partial epilepsy: a cross-sectional MRI study of 241 patients. Epilepsy Res. 2001, 46:69-82.
78. Sheng J.G., Boop F.A., Mrak R.E., Griffin W.S. Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1 alpha immunoreactivity. J. Neurochem. 1994, 63:1872-1879.
79. Somera-Molina K.C., Nair S., Van Eldik L.J., Watterson D.M., Wainwright M.S. Enhanced microglial activation and proinflammatory cytokine upregulation are linked to increased susceptibility to seizures and neurologic injury in a 'two-hit' seizure model. Brain Res. 2009, 1282:162-172.
80. Somera-Molina K.C., Robin B., Somera C.A., Anderson C., Stine C., Koh S., Behanna H.A., Van Eldik L.J., Watterson D.M., Wainwright M.S. Glial activation links early-life seizures and longterm neurologic dysfunction: evidence using a small molecule inhibitor of proinflammatory cytokine upregulation. Epilepsia 2007, 48:1785-1800.
81. Takenoshita H., Shizuka-Ikeda M., Mitoma H., Song S., Harigaya Y., Igeta Y., Yaguchi M., Ishida K., Shoji M., Tanaka M., Mizusawa H., Okamoto K. Presynaptic inhibition of cerebellar GABAergic transmission by glutamate decarboxylase autoantibodies in progressive cerebellar ataxia. J. Neurol. Neurosurg. Psychiatry 2001, 70:386-389.
82. Tan K.M., Lennon V.A., Klein C.J., Boeve B.F., Pittock S.J. Clinical spectrum of voltage-gated potassium channel autoimmunity. Neurology 2008, 70:1883-1890.
83. Thieben M.J., Lennon V.A., Boeve B.F., Aksamit A.J., Keegan M., Vernino S. Potentially reversible autoimmune limbic encephalitis with neuronal potassium channel antibody. Neurology 2004, 62:1177-1182.
84. Van Paesschen W., Connelly A., King M.D., Jackson G.D., Duncan J.S. The spectrum of hippocampal sclerosis: a quantitative magnetic resonance imaging study. Ann. Neurol. 1997, 41:41-51.
85. Vezzani A., Conti M., De Luigi A., Ravizza T., Moneta D., Marchesi F., De Simoni M.G. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J. Neurosci. 1999, 19:5054-5065.
86. Vezzani A., Moneta D., Conti M., Richichi C., Ravizza T., De Luigi A., De Simoni M.G., Sperk G., Andell-Jonsson S., Lundkvist J., Iverfeldt K., Bartfai T. Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11534-11539.
87. Vezzani A., Balosso S., Ravizza T. The role of cytokines in the pathophysiology of epilepsy. Brain Behav. Immun. 2008, 22:797-803.
88. Vezzani A., Ravizza T., Balosso S., Aronica E. Glia as a source of cytokines: implications for neuronal excitability and survival. Epilepsia 2008, 49(Suppl. 2):24-32.
89. Vezzani A., French J., Bartfai T., Baram T.Z. The role of inflammation in epilepsy. Nat. Rev. Neurol. 2011, 7:31-40.
90. Vianello M., Keir G., Giometto B., Betterle C., Tavolato B., Thompson E.J. Antigenic differences between neurological and diabetic patients with anti-glutamic acid decarboxylase antibodies. Eur. J. Neurol. 2005, 12:294-299.
91. Villani F., Bien C.G., Avanzini G.G. Immunoglobulin and immunomodulatory therapy. Epilepsy, A Comprehensive Textbook 2007, 1741-1746. Lippincott, Williams and Wilkins, Philadelphia. J. Engel, T.A. Pedley (Eds.).
92. Vincent A., Buckley C., Schott J.M., Baker I., Dewar B.K., Detert N., Clover L., Parkinson A., Bien C.G., Omer S., Lang B., Rossor M.N., Palace J. Potassium channel antibody-associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain 2004, 127:701-712.
93. Zandi M.S., Irani S.R., Follows G., Moody A.M., Molyneux P., Vincent A. Limbic encephalitis associated with antibodies to the NMDA receptor in Hodgkin lymphoma. Neurology 2009, 73:2039-2040.