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TIP Revista Especializada en Ciencias Químico-Biológicas

2016, Number 1

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TIP Rev Esp Cienc Quim Biol 2016; 19 (1)

Epilepsy and neuroinflammation

Herrera-Vázquez O, Toledo RA, Fleury A

Language: Spanish
References: 81
Page: 24-31
PDF size: 356.75 Kb.


ABSTRACT

Epilepsy is a neurological disorder affecting 50 million people worldwide. It is defined by the presence of spontaneous seizures result of synchronous discharges of neuronal population due to abnormal dynamics of neural networks. Different factors have been implicated in its pathogenesis, one of them being immune and inflammatory processes. In this paper we review the existing data on the role of inflammation / neuroinflammation in epilepsy.


REFERENCES

  1. Banerjee, P.N., Filippi, D. & Allen Hauser, W. The descriptive epidemiology of epilepsy-a review. Epilepsy Res. 85(1), 31-45 (2009).

  2. Kwan, P. et al. Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 51 (6), 1069-1077 (2010).

  3. Wiebe, S. & Jette, N. Pharmacoresistance and the role of surgery in difficult to treat epilepsy. Nat. Rev. Neurol. 8 (12), 669-677 (2012).

  4. Kwan, P. & Brodie, M.J. Early Identification of Refractory Epilepsy. N. Engl. J. Med. 342, 314-319 (2000).

  5. Al Sufiani, F. & Ang, L.C. Neuropathology of temporal lobe epilepsy. Epilepsy Res. Treat. Vol. 2012, article ID 624519 (2012).

  6. Vezzani, A. & Rüegg, S. The pivotal role of immunity and inflammatory processes in epilepsy is increasingly recognized: introduction. Epilepsia. 52 Suppl. 3, 1-4 (2011).

  7. Vezzani, A., Friedman, A. & Dingledine, R.J. The role of inflammation in epileptogenesis. Neuropharmacology 69,16-24 (2013).

  8. Marchi, N., Granata, T. & Janigro, D. Inflammatory pathways of seizure disorders. Trends Neurosci. 37 (2), 55-65 (2014).

  9. Wang, H., Liu, S., Tang, Z. & Liu, J. Some cross-talks between immune cells and epilepsy should not be forgotten. Neurol. Sci. 35 (12), 1843-1849 (2014).

  10. Rasmussen, T., Olszewski, J. & Lloydsmith, D. Focal seizures due to chronic localized encephalitis. Neurology 8 (6), 435-445 (1958).

  11. Watson, R. et al. Alpha7 acetylcholine receptor antibodies in two patients with Rasmussen encephalitis. Neurology 65 (11), 1802-1804 (2005).

  12. Álvarez-Barón, E., Bien, C.G., Schramm, J., Elger, C.E., Becker, A.J. & Schoch, S. Autoantibodies to Munc18, cerebral plasmacells and B-lymphocytes in Rasmussen encephalitis. Epilepsy Res. 80(1), 93-97 (2008).

  13. Granata, T., Cross, H., Theodore, W. & Avanzini, G. Immunemediated epilepsies. Epilepsia. 52 Suppl. 3, 5-11 (2011).

  14. Vincent, A., Bien, C.G., Irani, S.R. & Waters, P. Autoantibodies associated with diseases of the CNS: new developments and future challenges Lancet Neurol. 10 (8),759-772 (2011b).

  15. Quek, A.M. et al. Autoimmune epilepsy: clinical characteristics and response to immunotherapy. Arch. Neurol. 69 (5),582-593 (2012).

  16. Bien, C.G. et al. Immunopathology of autoantibody-associated encephalitides: clues for pathogenesis. Brain 135 (Pt 5), 1622- 1638 (2012).

  17. Varadkar, S. et al. Rasmussen´s encephalitis: clinical features, pathobiology, and treatment advances. Lancet Neurol. 13(2): 195-205 (2014)

  18. Carvalho, K.S., Walleigh, D.J. & Legido, A. Generalized epilepsies: immunologic and inflammatory mechanisms. Semin. Pediatr. Neurol. 21 (3), 214-220 (2014).

  19. Bien, C.G. & Bauer, J. Autoimmune epilepsies. Neurotherapeutics. 11 (2), 311-318 (2014).

  20. Vincent, A. & Crino, P.B. Systemic and neurologic autoimmune disorders associated with seizures or epilepsy. Epilepsia 52 Suppl. 3, 12-17 (2011a).

  21. Ravizza, T. & Vezzani, A. Status epilepticus induces time-dependent neuronal and astrocytic expression of Interleukin-1 receptor type I in the rat limbic system. Neuroscience 137 (1), 301–308 (2006).

  22. Aronica, E. & Gorter, J.A. Gene Expression Profile in Temporal Lobe Epilepsy. The Neuroscientist: a Review Journal Bringing Neurobiology, Neurology and Psychiatry 13 (2): 100–108 (2007).

  23. 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. Neurobiology of Disease 29 (1), 142–160 (2008).

  24. Choi, J. et al. Cellular injury and neuroinflammation in children with chronic intractable epilepsy. J. Neuroinflammation 6: 38, (2009).

  25. Boer, K. et al. Gene expression analysis of tuberous sclerosis complex cortical tubers reveals increased expression of adhesion and inflammatory factors. Brain Pathol. 20 (4), 704-719 (2010).

  26. Lyer, A. et al. Evaluation of the innate and adaptive immunity in type I and type II focal cortical dysplasias. Epilepsia 51 (9),1763- 1773 (2010a).

  27. Lyer, A.M. et al. Tissue plasminogen activator and urokinase plasminogen activator in human epileptogenic pathologies. Neuroscience 167 (3), 929-945 (2010b).

  28. Zattoni, M. et al. Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J. Neurosci. 31 (11), 4037-4050 (2011).

  29. Pernhorst, K. et al. TLR4, ATF-3 and IL8 inflammation mediator expression correlates with seizure frequency in human epileptic brain tissue. Seizure 22 (8), 675-678 (2013).

  30. Banati, R.B. Visualising Microglial Activation in Vivo. Glia 40 (2), 206–217 (2002).

  31. Kumar, A., Chugani, H.T., Luat, A., Asano, E. & Sood, S. Epilepsy surgery in a case of encephalitis: use of 11C-PK11195 positron emission tomography. Pediatr. Neurol. 38 (6), 439-442 (2008).

  32. Butler, T. et al. Imaging inflammation in a patient with epilepsy due to focal cortical dysplasia. J. Neuroimaging 23(1), 129-131 (2013).

  33. Rogers, S.W. et al. Autoantibodies to glutamate receptor GluR3 in Rasmussen´s encephalitis. Science. 265 (5172):648-651 (1994).

  34. Hirsch, E. et al. Landau–Kleffner syndrome is not an eponymic badge of ignorance. Epilepsy research 70, 239-247 (2006).

  35. Chattopadhyay, S. et al. An autoantibody inhibitory to glutamic acid decarboxylase in the neurodegenerative disorder Batten disease. Hum. Mol. Genet. 11 (12), 1421-1431 (2002).

  36. De Simoni, M.G. et al. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur. J. Neurosci. 12 (7), 2623-2633 (2000).

  37. Devinsky, O., Vezzani, A., Najjar, S., De Lanerolle, N.C. & Rogawski, M.A. Glia and epilepsy: excitability and inflammation. Trends Neurosci. 36 (3),174-184 (2013).

  38. Maroso, M., Balosso, S., Ravizza, T., Liu, J., Bianchi, M.E. & Vezzani A. Interleukin-1 type 1 receptor/Toll-like receptor signalling in epilepsy: the importance of IL-1beta and high-mobility group box 1. J. Intern. Med. 270 (4), 319-326 (2011a).

  39. Maroso, M. et al. Interleukin-1β biosynthesis inhibition reduces acute seizures and drug resistant chronic epileptic activity in mice. Neurotherapeutics 8 (2), 304-315 (2011).

  40. Ravizza, T. et al. The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol. Dis. 24 (1), 128-143 (2006).

  41. Vezzani, A. et al. Powerful anticonvulsant action of IL-1 receptor antagonist on intracerebral injection and astrocytic overexpression in mice. Proc. Natl. Acad. Sci. U S A 97 (21), 11534-11539 (2000).

  42. Vezzani, A., Balosso, S., Maroso, M., Zardoni, D., Noé, F. & Ravizza, T. ICE/caspase 1 inhibitors and IL-1beta receptor antagonists as potential therapeutics in epilepsy. Curr. Opin. Investig. Drugs 11 (1), 43-50 (2010).

  43. Gorter, J.A., van Vliet, E.A. & Aronica, E. Status epilepticus, blood-brain barrier disruption, inflammation, and epileptogenesis. Epilepsy Behav. 49,13-16 (2015).

  44. VanVliet, E.A., Aronica, E. & Gorter, J.A. Blood-brain barrier dysfunction, seizures and epilepsy. Semin. Cell. Dev. Biol. 38, 26-34 (2015).

  45. Bell, M.D. & Perry, V.H. Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammagen or during acute neuronal degeneration. J. Neurocytol. 24 (9), 695- 710 (1995).

  46. Librizzi, L., Regondi, M.C., Pastori, C., Frigerio, S., Frassoni, C. & de Curtis, M. Expression of adhesion factors induced by epileptiform activity in the endothelium of the isolated guinea pig brain in vitro. Epilepsia 48 (4), 743-751 (2007).

  47. Fabene, P.F. et al. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat. Med. 14 (12), 1377-1383 (2008).

  48. Aronica, E. & Crino, P.B. Inflammation in epilepsy: clinical observations. Epilepsia 52 Suppl. 3, 26-32 (2011).

  49. Balter-Seri, J., Yuhas, Y., Weizman, A., Nofech-Mozes, Y., Kaminsky, E. & Ashkenazi, S. Role of nitric oxide in the enhancement of pentylenetetrazole-induced seizures caused by Shigella dysenteriae. Infect. Immun. 67 (12), 6364-6368 (1999).

  50. Sayyah, M., Javad-Pour, M. & Ghazi-Khansari, M. The bacterial endotoxin lipopolysaccharide enhances seizure susceptibility in mice: involvement of proinflammatory factors: nitric oxide and prostaglandins. Neuroscience. 122 (4), 1073-1080 (2003).

  51. Yuhas, Y., Weizman, A., Vanichkin, A. & Ashkenazi, S. Involvement of prostaglandins in an animal model of Shigella-related seizures. J. Neuroimmunol. 168 (1-2), 34-39 (2005). http://www.who.int/mediacentre/factsheets/fs999/es/

  52. Ho, Y.H., Lin, Y.T., Wu, C.W., Chao, Y.M., Chang, A.Y. & Chan, J.Y. Peripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J. Biomed. Sci. 24, 22-46 (2015).

  53. Riazi, K., Galic, M.A., Kuzmiski, J.B., Ho, W., Sharkey, K.A. & Pittman, Q.J. Microglial activation and TNF alpha production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci U S A 105 (44), 17151-17156 (2008).

  54. Nowak, M. et al. Interictal alterations of cytokines and leukocytes in patients with active epilepsy. Brain Behav. Immun. 25 (3), 423- 428 (2011).

  55. Shiihara, T., Miyashita, M., Yoshizumi, M., Watanabe, M., Yamada, Y. & Kato, M. Peripheral lymphocyte subset and serum cytokine profiles of patients with West syndrome. Brain Dev. 32 (9), 695- 702 (2010).

  56. Li, C., Ma, W.N. & Wang, H. Changes of regulatory T cells in the peripheral blood of children with epilepsy. Zhongguo Dang Dai ErKeZaZhi 13 (11), 889-892 (2011).

  57. Stępień, K., Tomaszewski, M., Tomaszewska, J. & Czuczwar, S. The multidrug transporter P-glycoprotein in pharmacoresistance to antiepileptic drugs. Pharmacological Reports 64(5), 1011-1019 (2012).

  58. Moazzami, K., Emamzadeh-Fard, S. & Shabani, M. Anticonvulsive effect of atorvastatin on pentylenetetrazole-induced seizures in mice: the role of nitric oxide pathway. Fundam. Clin. Pharmacol. 27, 387-392 (2013).

  59. Santiago-Rodríguez, E., Alonso-Vanegas, M., Cárdenas-Morales, L., Harmony, T., Bernardino, M. & Fernández-Bouzas, A. Effects of two different cycles of vagus nerve stimulation on interictal epileptiform discharges. Seizure J. Br. Epilepsy Assoc. 15, 615–620 (2006).

  60. Aalbers, M., Vles, J., Klinkenberg, S., Hoogland, G., Majoie, M. & Rijkers, K. Animal models for vagus nerve stimulation in epilepsy. Exp. Neurol. 230, 167–175 (2011).

  61. Kaya, M. et al. Vagus nerve stimulation inhibits seizure activity and protects blood-brain barrier integrity in kindled rats with cortical dysplasia. Life Sci. 92, 289–297 (2013).

  62. Borovikova, L.V. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405, 458–462 (2000).

  63. Yamakawa, K. et al. Electrical Vagus Nerve Stimulation Attenuates Systemic Inflammation and Improves Survival in a Rat Heatstroke Model. PLoS One 8 (2), e56728 (2013).

  64. Kunz, T. & Oliw, E.H. The selective cyclooxygenase 2 inhibitor rofecoxib reduces kainate-induced cell death in the rat hippocampus. Eur. J. Neurosci. 13 (3), 569-575 (2001).

  65. Kovács, Z., Dobolyi, A., Juhász, G. & Kékesi, K.A. Lipopolysaccharide induced increase in seizure activity in two animal models of absence epilepsy WAG/Rijand GAERS rats and Long Evans rats. Brain Res. Bull. 104, 7-18 (2014).

  66. Jiang, J., Yang, M.S., Quan, Y., Gueorguieva, P., Ganesh, T. & Dingledine, R. Therapeutic window for cyclooxygenase-2 related anti-inflammatory therapy after status epilepticus. Neurobiol. Dis. 76, 126-136 (2015).

  67. Citraro, R., Leo, A., Marra, R., De Sarro, G. & Russo, E. Antiepileptogenic effects of the selective COX-2 inhibitor etoricoxib, on the development of spontaneous absence seizures in WAG/Rij rats. Brain Res. Bull. 113, 1-7 (2015).

  68. Dhir, A., Naidu, P. & Kulkarni S. Effect pf cyclooxygenase (COX-2) inhibitors in various animal models (bicullone, picrotoxin, maximal electroschock convulsions) of epilepsy with possible mechanism of action. Indian J. Exp. Biol. 44(4): 286-291.

  69. Wang, N. et al. Minocycline inhibits brain inflammation and attenuates spontaneous recurrent seizures following pilocarpineinduced status epilepticus. Neuroscience 287, 144-156 (2015).

  70. Gouveia, T.L. et al. Lovastatin decreases the synthesis of inflammatory mediators during epileptoge-nesis in the hippocampus ofrats submitted to pilocarpine-induced epilepsy. Epilepsy Behav. 36, 68-73 (2014).

  71. Melvin, J.J. & Huntley Hardison, H. Immunomodulatory treatments in epilepsy. Semin. Pediatr. Neurol. 21 (3), 232-237 (2014).

  72. Özkara, Ç. & Vigevano, F. Immuno- and antiinflammatory therapies in epileptic disorders. Epilepsia. 52 Suppl. 3, 45-51 (2011).

  73. Van Rijckevorsel-Harmant, K., Delire, M., Schmitz-Moorman, W. & Wieser, H.G. Treatment of refractory epilepsy with intravenous immunoglobulins. Results of the first double-blind/dosefinding clinical study. Int. J. Clin. Lab. Res. 24 (3), 162-166 (1994).

  74. Grosso, S., Farnetani, M., Mostardini, R., Cordelli, D., Berardi, R. & Balestri, P. A comparative study of hydrocortisone versus deflazacort in drug-resistant epilepsy of childhood. Epilepsy Res. 81 (1), 80-85 (2008).

  75. Buzatu, M., Bulteau, C., Altuzarra, C., Dulac, O. & Van Bogaert, P. Corticosteroids as treatment of epileptic syndromes with continuous spike-waves during slow-wave sleep. Epilepsia 50 Suppl. 7, 68-72 (2009).

  76. Mikati, M.A., Kurdi, R., El-Khoury, Z., Rahi, A. & Raad, W. Intravenous immunoglobulin therapy in intractable childhood epilepsy: open-label study and review of the literature. Epilepsy Behav. 17 (1), 90-94 (2010).

  77. D’Ambrosio, R., Eastman, C., Fattore, C. & Perucca, E. Novel Frontiers in Epilepsy Treatments: Preventing Epileptogenesis by Targeting Inflammation. Expert. Rev. Neurother. 13 (6), 615–625 (2013).

  78. Hancock, E.C., Osborne, J.P. & Edwards, S.W. Treatment of infantile spasms. Cochrane Database Syst. Rev. 5 (6), CD001770 (2013).

  79. Rüegg, S. & Panzer, J. Inmunoterapia para la epilepsia farmacoresistente Neurology 82, 1572-1573 (2014).

  80. Rojas, A. et al. Cyclooxygenase-2 in epilepsy. Epilepsia 55(1), 17-25 (2013).

  81. Hegde, M. & Lowenstein, D.H. The search for circulating epilepsy biomarkers. Biomark Med. 8 (3), 413-427 (2014).




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