Mesial temporal lobe epilepsy with psychiatric comorbidities: A place for differential neuroinflammatory interplay

Journal of Neuroinflammation

Volumn 12, Issue 1, 2015, Pages

  Kandratavicius, Ludmyla ^a   Peixoto Santos, Jose Eduardo ^a   Monteiro, Mariana Raquel ^a   Scandiuzzi, Renata Caldo ^a   Carlotti, Carlos Gilberto ^a   Assirati, Joao Alberto ^a   Hallak, Jaime Eduardo ^a,b   Leite, Joao Pereira ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b National Science and Technology Institute INCT for Translational Medicine   (Brazil)

Author keywords

Aquaporin 4; Astrocytes; Major depression; Metallothionein; Microglia; Psychosis; Temporal lobe epilepsy

Indexed keywords

AQUAPORIN 4; BENZODIAZEPINE DERIVATIVE; CARBAMAZEPINE; FLUOXETINE; GLIAL FIBRILLARY ACIDIC PROTEIN; HALOPERIDOL; HLA ANTIGEN; HLA DR ANTIGEN; METALLOTHIONEIN; METALLOTHIONEIN I; METALLOTHIONEIN II; OXCARBAZEPINE; PHENOBARBITAL; PHENYTOIN; AQP4 PROTEIN, HUMAN; CYTOKINE;

ADULT; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE HILUS; ENTORHINAL CORTEX; FEMALE; GLIA; GLIOSIS; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERICTAL PSYCHOSIS; MAJOR DEPRESSION; MALE; MESIAL TEMPORAL LOBE EPILEPSY; MICROGLIA; PARASUBICULUM; PROSUBICULUM; PROTEIN EXPRESSION; PSYCHOSIS; SUBICULUM; ADOLESCENT; CHILD; COMORBIDITY; DEPRESSIVE DISORDER, MAJOR; EPILEPSY, TEMPORAL LOBE; METABOLISM; NONPARAMETRIC TEST; PATHOLOGY; PRESCHOOL CHILD; PSYCHOTIC DISORDERS; SEVERITY OF ILLNESS INDEX;

ADOLESCENT; AQUAPORIN 4; CHILD; CHILD, PRESCHOOL; COMORBIDITY; CYTOKINES; DEPRESSIVE DISORDER, MAJOR; EPILEPSY, TEMPORAL LOBE; FEMALE; GLIAL FIBRILLARY ACIDIC PROTEIN; HIPPOCAMPUS; HLA-DR ANTIGENS; HUMANS; MALE; PSYCHOTIC DISORDERS; SEVERITY OF ILLNESS INDEX; STATISTICS, NONPARAMETRIC;

EID: 84924104512     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-015-0266-z     Document Type: Article

References (68)

1. Mathern GW, Babb TL, Pretorius JK, Leite JP. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci. 1995;15:3990-4004.
2. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 1991;42:351-63.
3. Kandratavicius L, Rosa-Neto P, Monteiro MR, Guiot MC, Assirati Jr JA, Carlotti Jr CG, et al. Distinct increased metabotropic glutamate receptor type 5 (mGluR5) in temporal lobe epilepsy with and without hippocampal sclerosis. Hippocampus. 2013;23:1212-30.
4. Peixoto-Santos JE, Galvis-Alonso OY, Velasco TR, Kandratavicius L, Assirati JA, Carlotti CG, et al. Increased metallothionein I/II expression in patients with temporal lobe epilepsy. PLoS One. 2012;7:e44709.
5. Qin P, Xu H, Laursen TM, Vestergaard M, Mortensen PB. Risk for schizophrenia and schizophrenia-like psychosis among patients with epilepsy: population based cohort study. BMJ. 2005;331:23.
6. Kandratavicius L, Lopes-Aguiar C, Bueno-Junior LS, Romcy-Pereira RN, Hallak JE, Leite JP. Psychiatric comorbidities in temporal lobe epilepsy: possible relationships between psychotic disorders and involvement of limbic circuits. Rev Bras Psiquiatr. 2012;34:454-66.
7. Kandratavicius L, Ruggiero RN, Hallak JE, Garcia-Cairasco N, Leite JP. Pathophysiology of mood disorders in temporal lobe epilepsy. Rev Bras Psiquiatr. 2012;34 Suppl 2:S233-45.
8. Kandratavicius L, Hallak JE, Young LT, Assirati JA, Carlotti Jr CG, Leite JP. Differential aberrant sprouting in temporal lobe epilepsy with psychiatric co-morbidities. Psychiatry Res. 2012;195:144-50.
9. Kandratavicius L, Monteiro MR, Assirati Jr JA, Carlotti Jr CG, Hallak JE, Leite JP. Neurotrophins in mesial temporal lobe epilepsy with and without psychiatric comorbidities. J Neuropathol Exp Neurol. 2013;72:1029-42.
10. Kandratavicius L, Monteiro MR, Hallak JE, Carlotti Jr CG, Assirati Jr JA, Leite JP. Microtubule-associated proteins in mesial temporal lobe epilepsy with and without psychiatric comorbidities and their relation with granular cell layer dispersion. Biomed Res Int. 2013;2013:960126.
11. Najjar S, Pearlman DM, Alper K, Najjar A, Devinsky O. Neuroinflammation and psychiatric illness. J Neuroinflammation. 2013;10:43.
12. Ebadi M, Iversen PL, Hao R, Cerutis DR, Rojas P, Happe HK, et al. Expression and regulation of brain metallothionein. Neurochem Int. 1995;27:1-22.
13. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT. Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia. 2006;53:631-6.
14. Jukkola P, Guerrero T, Gray V, Gu C. Astrocytes differentially respond to inflammatory autoimmune insults and imbalances of neural activity. Acta Neuropathol Commun. 2013;1:70-89.
15. Choi KH, Elashoff M, Higgs BW, Song J, Kim S, Sabunciyan S, et al. Putative psychosis genes in the prefrontal cortex: combined analysis of gene expression microarrays. BMC Psychiatry. 2008;8:87.
16. Feresten AH, Barakauskas V, Ypsilanti A, Barr AM, Beasley CL. Increased expression of glial fibrillary acidic protein in prefrontal cortex in psychotic illness. Schizophr Res. 2013;150:252-7.
17. Radewicz K, Garey LJ, Gentleman SM, Reynolds R. Increase in HLA-DR immunoreactive microglia in frontal and temporal cortex of chronic schizophrenics. J Neuropathol Exp Neurol. 2000;59:137-50.
18. Rajkowska G, Stockmeier CA. Astrocyte pathology in major depressive disorder: insights from human postmortem brain tissue. Curr Drug Targets. 2013;14:1225-36.
19. Shelton RC, Claiborne J, Sidoryk-Wegrzynowicz M, Reddy R, Aschner M, Lewis DA, et al. Altered expression of genes involved in inflammation and apoptosis in frontal cortex in major depression. Mol Psychiatry. 2011;16:751-62.
20. Kandratavicius L, Hallak JE, Leite JP. What are the similarities and differences between schizophrenia and schizophrenia-like psychosis of epilepsy? A neuropathological approach to the understanding of schizophrenia spectrum and epilepsy. Epilepsy Behav. 2014;38C:143-7.
21. Gittins R, Harrison PJ. Neuronal density, size and shape in the human anterior cingulate cortex: a comparison of Nissl and NeuN staining. Brain Res Bull. 2004;63:155-60.
22. Stan AD, Ghose S, Gao XM, Roberts RC, Lewis-Amezcua K, Hatanpaa KJ, et al. Human postmortem tissue: what quality markers matter? Brain Res. 2006;1123:1-11.
23. Berg AT. Identification of pharmacoresistant epilepsy. Neurol Clin. 2009;27:1003-13.
24. Engel Jr J. Surgery for seizures. N Engl J Med. 1996;334:647-52.
25. Sachdev P. Schizophrenia-like psychosis and epilepsy: the status of the association. Am J Psychiatry. 1998;155:325-36.
26. Elliott B, Joyce E, Shorvon S. Delusions, illusions and hallucinations in epilepsy: 2. Complex phenomena and psychosis. Epilepsy Res. 2009;85:172-86.
27. Beard AW, Slater E. The schizophrenic-like psychoses of epilepsy. Proc R Soc Med. 1962;55:311-6.
28. LorentedeNo R. Studies on the structure of the cerebral cortex II: continuation of study of the ammonic system. J Psychol Neurol. 1934;46:113-77.
29. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, et al. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology. 1999;52:453-72.
30. Mathern GW, Pretorius JK, Kornblum HI, Mendoza D, Lozada A, Leite JP, et al. Human hippocampal AMPA and NMDA mRNA levels in temporal lobe epilepsy patients. Brain. 1997;120(Pt 11):1937-59.
31. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjornsen LP, Spencer DD, et al. Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci U S A. 2005;102:1193-8.
32. Arisi GM. Nervous and immune systems signals and connections: cytokines in hippocampus physiology and pathology. Epilepsy Behav. 2014;38C:43-7.
33. 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.
34. Pineda E, Shin D, Sankar R, Mazarati AM. Comorbidity between epilepsy and depression: experimental evidence for the involvement of serotonergic, glucocorticoid, and neuroinflammatory mechanisms. Epilepsia. 2010;51 Suppl 3:110-4.
35. Xie W, Cai L, Yu Y, Gao L, Xiao L, He Q, et al. Activation of brain indoleamine 2,3-dioxygenase contributes to epilepsy-associated depressive-like behavior in rats with chronic temporal lobe epilepsy. J Neuroinflammation. 2014;11:41.
36. Zamanian JL, Xu L, Foo LC, Nouri N, Zhou L, Giffard RG, et al. Genomic analysis of reactive astrogliosis. J Neurosci. 2012;32:6391-410.
37. Hostenbach S, Cambron M, D'Haeseleer M, Kooijman R, De Keyser J. Astrocyte loss and astrogliosis in neuroinflammatory disorders. Neurosci Lett. 2014;565:39-41.
38. Liu W, Tang Y, Feng J. Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci. 2011;89:141-6.
39. Muller MB, Lucassen PJ, Yassouridis A, Hoogendijk WJ, Holsboer F, Swaab DF. Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur J Neurosci. 2001;14:1603-12.
40. Steffek AE, McCullumsmith RE, Haroutunian V, Meador-Woodruff JH. Cortical expression of glial fibrillary acidic protein and glutamine synthetase is decreased in schizophrenia. Schizophr Res. 2008;103:71-82.
41. Webster MJ, Knable MB, Johnston-Wilson N, Nagata K, Inagaki M, Yolken RH. Immunohistochemical localization of phosphorylated glial fibrillary acidic protein in the prefrontal cortex and hippocampus from patients with schizophrenia, bipolar disorder, and depression. Brain Behav Immun. 2001;15:388-400.
42. Catts VS, Wong J, Fillman SG, Fung SJ, Weickert CS. Increased expression of astrocyte markers in schizophrenia: association with neuroinflammation. Aust N Z J Psychiatry. 2014;48:722-34.
43. Song X, Fan X, Song X, Zhang J, Zhang W, Li X, et al. Elevated levels of adiponectin and other cytokines in drug naive, first episode schizophrenia patients with normal weight. Schizophr Res. 2013;150:269-73.
44. Thom M, Kensche M, Maynard J, Liu J, Reeves C, Goc J, et al. Interictal psychosis following temporal lobe surgery: dentate gyrus pathology. Psychol Med. 2014;44:3037-49.
45. Busse S, Busse M, Schiltz K, Bielau H, Gos T, Brisch R, et al. Different distribution patterns of lymphocytes and microglia in the hippocampus of patients with residual versus paranoid schizophrenia: further evidence for disease course-related immune alterations? Brain Behav Immun. 2012;26:1273-9.
46. Rosenblat JD, Cha DS, Mansur RB, McIntyre RS. Inflamed moods: a review of the interactions between inflammation and mood disorders. Prog Neuropsychopharmacol Biol Psychiatry. 2014;53C:23-34.
47. Kanner AM. Can neurobiological pathogenic mechanisms of depression facilitate the development of seizure disorders? Lancet Neurol. 2012;11:1093-102.
48. 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;102:805-18.
49. Penkowa M, Florit S, Giralt M, Quintana A, Molinero A, Carrasco J, et al. Metallothionein reduces central nervous system inflammation, neurodegeneration, and cell death following kainic acid-induced epileptic seizures. J Neurosci Res. 2005;79:522-34.
50. Takeda A. Movement of zinc and its functional significance in the brain. Brain Res Brain Res Rev. 2000;34:137-48.
51. Najjar S, Pearlman DM, Devinsky O, Najjar A, Zagzag D. Neurovascular unit dysfunction with blood-brain barrier hyperpermeability contributes to major depressive disorder: a review of clinical and experimental evidence. J Neuroinflammation. 2013;10:142.
52. Szewczyk B, Kubera M, Nowak G. The role of zinc in neurodegenerative inflammatory pathways in depression. Prog Neuropsychopharmacol Biol Psychiatry. 2011;35:693-701.
53. Goldsmith SK, Joyce JN. Alterations in hippocampal mossy fiber pathway in schizophrenia and Alzheimer's disease. Biol Psychiatry. 1995;37:122-6.
54. Kolomeets NS, Orlovskaya DD, Uranova NA. Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse. 2007;61:615-21.
55. Joshi M, Akhtar M, Najmi AK, Khuroo AH, Goswami D. Effect of zinc in animal models of anxiety, depression and psychosis. Hum Exp Toxicol. 2012;31:1237-43.
56. Connor MA, Chavkin C. Ionic zinc may function as an endogenous ligand for the haloperidol-sensitive sigma 2 receptor in rat brain. Mol Pharmacol. 1992;42:471-9.
57. Carrasco J, Penkowa M, Hadberg H, Molinero A, Hidalgo J. Enhanced seizures and hippocampal neurodegeneration following kainic acid-induced seizures in metallothionein-I + II-deficient mice. Eur J Neurosci. 2000;12:2311-22.
58. Kandratavicius L, Hallak JE, Carlotti CG, Assirati JA, Leite JP. Neurotrophin receptors expression in mesial temporal lobe epilepsy with and without psychiatric comorbidities and their relation with seizure type and surgical outcome. Acta Neuropathol Commun. 2014;2:81-98.
59. Kandratavicius L, Hallak JE, Carlotti CG, Assirati JA, Leite JP. Hippocampal expression of heat shock proteins in mesial temporal lobe epilepsy with psychiatric comorbidities and their relation to seizure outcome. Epilepsia. 2014;55:1834-43.
60. Ohnishi M, Monda A, Takemoto R, Fujimoto Y, Sugitani M, Iwamura T, et al. High-mobility group box 1 up-regulates aquaporin 4 expression via microglia-astrocyte interaction. Neurochem Int. 2014;75:32-8.
61. Scharfman HE, Binder DK. Aquaporin-4 water channels and synaptic plasticity in the hippocampus. Neurochem Int. 2013;63:702-11.
62. Skucas VA, Mathews IB, Yang J, Cheng Q, Treister A, Duffy AM, et al. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J Neurosci. 2011;31:6392-7.
63. Zhang Z, Fan J, Ren Y, Zhou W, Yin G. The release of glutamate from cortical neurons regulated by BDNF via the TrkB/Src/PLC-gamma1 pathway. J Cell Biochem. 2013;114:144-51.
64. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, et al. Delayed K+ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci U S A. 2003;100:13615-20.
65. Krogias C, Hoepner R, Muller A, Schneider-Gold C, Schroder A, Gold R. Successful treatment of anti-Caspr2 syndrome by interleukin 6 receptor blockade through tocilizumab. JAMA Neurol. 2013;70:1056-9.
66. Chaudhry IB, Hallak J, Husain N, Minhas F, Stirling J, Richardson P, et al. Minocycline benefits negative symptoms in early schizophrenia: a randomised double-blind placebo-controlled clinical trial in patients on standard treatment. J Psychopharmacol. 2012;26:1185-93.
67. Muller N, Schwarz MJ, Dehning S, Douhe A, Cerovecki A, Goldstein-Muller B, et al. The cyclooxygenase-2 inhibitor celecoxib has therapeutic effects in major depression: results of a double-blind, randomized, placebo controlled, add-on pilot study to reboxetine. Mol Psychiatry. 2006;11:680-4.
68. Devinsky O, Vezzani A, Najjar S, De Lanerolle NC, Rogawski MA. Glia and epilepsy: excitability and inflammation. Trends Neurosci. 2013;36:174-84.