Microglia are less pro-inflammatory than myeloid infiltrates in the hippocampus of mice exposed to status epilepticus

GLIA

Volumn 64, Issue 8, 2016, Pages 1350-1362

  Vinet, Jonathan ^a   Vainchtein, Ilia D ^b   Spano, Carlotta ^c   Giordano, Carmela ^a   Bordini, Domenico ^a   Curia, Giulia ^a   Dominici, Massimo ^c   Boddeke, Hendrikus W G M ^b   Eggen, Bart J L ^b   Biagini, Giuseppe ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

epileptogenesis; metalloproteinases; pilocarpine; pro inflammatory cytokines; temporal lobe epilepsy

Indexed keywords

CD40 ANTIGEN; GELATINASE B; INTERLEUKIN 1BETA; MACROPHAGE ELASTASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PILOCARPINE; PROTEIN AXL; RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPILEPTIC STATE; EPILEPTOGENESIS; FLUORESCENCE ACTIVATED CELL SORTING; HIPPOCAMPUS; INFLAMMATION; MALE; MICROGLIA; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; REAL TIME POLYMERASE CHAIN REACTION;

EID: 84975230627     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.23008     Document Type: Article

References (52)

1. Abraham J, Fox PD, Condello C, Bartolini A, Koh S. 2012. Minocycline attenuates microglia activation and blocks the long-term epileptogenic effects of early-life seizures. Neurobiol Dis 46:425–430.
2. Balosso S, Ravizza T, Perego C, Peschon J, Campbell IL, De Simoni MG, Vezzani A. 2005. Tumor necrosis factor-alpha inhibits seizures in mice via p75 receptors. Ann Neurol 57:804–812.
3. Benson MJ, Manzanero S, Borges K. 2015. Complex alterations in microglial M1/M2 markers during the development of epilepsy in two mouse models. Epilepsia 56:895–905.
4. Bernardino L, Xapelli S, Silva AP, Jakobsen B, Poulsen FR, Oliveira CR, Vezzani A, Malva JO, Zimmer J. 2005. Modulator effects of interleukin-1beta and tumor necrosis factor-alpha on AMPA-induced excitotoxicity in mouse organotypic hippocampal slice cultures. J Neurosci 25:6734–6744.
5. Bezzi P, Domercq M, Brambilla L, Galli R, Schols D, De Clercq E, Vescovi A, Bagetta G, Kollias G, Meldolesi J, Volterra A. 2001. CXCR4-activated astrocyte glutamate release via TNFalpha: amplification by microglia triggers neurotoxicity. Nat Neurosci 4:702–710.
6. Biagini G, Baldelli E, Longo D, Contri MB, Guerrini U, Sironi L, Gelosa P, Zini I, Ragsdale DS, Avoli M. 2008. Proepileptic influence of a focal vascular lesion affecting entorhinal cortex-CA3 connections after status epilepticus. J Neuropathol Exp Neurol 67:687–701.
7. Biswas A, Bruder D, Wolf SA, Jeron A, Mack M, Heimesaat MM, Dunay IR. 2015. Ly6C(high) monocytes control cerebral toxoplasmosis. J Immunol 194:3223–3235.
8. Bruton CJ. 1988. The neuropathology of temporal lobe epilepsy. New York, NY: Oxford University Press. 158p.
9. Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE, Fanek Z, Liu L, Chen Z, Rothstein JD, Ransohoff RM, Gygi SP, Antel JP, Weiner HL. 2014. Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci 17:131–143.
10. Chandler S, Cossins J, Lury J, Wells G. 1996. Macrophage metalloelastase degrades matrix and myelin proteins and processes a tumour necrosis factor-alpha fusion protein. Biochem Biophys Res Commun 228:421–429.
11. Choi J, Koh S. 2008. Role of brain inflammation in epileptogenesis. Yonsei Med J 49:1–18.
12. Curia G, Longo D, Biagini G, Jones RS, Avoli M. 2008. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172:143–157.
13. de Haas AH, Boddeke HW, Brouwer N, Biber K. 2007. Optimized isolation enables ex vivo analysis of microglia from various central nervous system regions. Glia 55:1374–1384.
14. De Simoni MG, Perego C, Ravizza T, Moneta D, Conti M, Marchesi F, De Luigi A, Garattini S, Vezzani A. 2000. Inflammatory cytokines and related genes are induced in the rat hippocampus by limbic status epilepticus. Eur J Neurosci 12:2623–2633.
15. Eriksson C, Zou LP, Ahlenius S, Winblad B, Schultzberg M. 2000. Inhibition of kainic acid induced expression of interleukin-1 beta and interleukin-1 receptor antagonist mRNA in the rat brain by NMDA receptor antagonists. Brain Res Mol Brain Res 85:103–113.
16. Fabene PF, Navarro Mora G, Martinello M, Rossi B, Merigo F, Ottoboni L, Bach S, Angiari S, Benati D, Chakir A, Zanetti L, Schio F, Osculati A, Marzola P, Nicolato E, Homeister JW, Xia L, Lowe JB, McEver RP, Osculati F, Sbarbati A, Butcher EC, Constantin G. 2008. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 14:1377–1383.
17. Gaikwad S, Patel D, Agrawal-Rajput R. 2016. CD40 negatively regulates ATP-TLR4-activated inflammasomes in microglia. Cell Mol Neurobiol. DOI 10.1007/s10571-016-0358-z.
18. Gorter JA, van Vliet EA, Aronica E, Breit T, Rauwerda H, Lopes da Silva FH, Wadman WJ. 2006. Potential new antiepileptogenic targets indicated by microarray analysis in a rat model for temporal lobe epilepsy. J Neurosci 26:11083–11110.
19. Gorter JA, van Vliet EA, Aronica E. 2015. Status epilepticus, blood-brain barrier disruption, inflammation, and epileptogenesis. Epilepsy Behav 49:13–16.
20. Gu Z, Cui J, Brown S, Fridman R, Mobashery S, Strongin AY, Lipton SA. 2005. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 25:6401–6408.
21. Gualtieri F, Curia G, Marinelli C, Biagini G. 2012. Increased perivascular laminin predicts damage to astrocytes in CA3 and piriform cortex following chemoconvulsive treatments. Neuroscience 218:278–94.
22. Hildebrandt M, Amann K, Schröder R, Pieper T, Kolodziejczyk D, Holthausen H, Buchfelder M, Stefan H, Blümcke I. 2008. White matter angiopathy is common in pediatric patients with intractable focal epilepsies. Epilepsia 49:804–815.
23. Hu S, Sheng WS, Ehrlich LC, Peterson PK, Chao CC. 2000. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation 7:153–159.
24. Lai AY, Swayze RD, El-Husseini A, Song C. 2006. Interleukin-1 beta modulates AMPA receptor expression and phosphorylation in hippocampal neurons. J Neuroimmunol 175:97–106.
25. Lambertsen KL, Clausen BH, Babcock AA, Gregersen R, Fenger C, Nielsen HH, Haugaard LS, Wirenfeldt M, Nielsen M, Dagnaes-Hansen F, Bluethmann H, Faergeman NJ, Meldgaard M, Deierborg T, Finsen B. 2009. Microglia protect neurons against ischemia by synthesis of tumor necrosis factor. J Neurosci 29:1319–1330.
26. Librizzi L, Noè F, Vezzani A, de Curtis M, Ravizza T. 2012. Seizure-induced brain-borne inflammation sustains seizure recurrence and blood-brain barrier damage. Ann Neurol 72:82–90.
27. Liu W, Tang Y, Feng J. 2011. Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci 89:141–146.
28. Lu MO, Zhang XM, Mix E, Quezada HC, Jin T, Zhu J, Adem A. 2008. TNF-alpha receptor 1 deficiency enhances kainic acid-induced hippocampal injury in mice. J Neurosci Res 86:1608–1614.
29. Lucchi C, Vinet J, Meletti S, Biagini G. 2015. Ischemic-hypoxic mechanisms leading to hippocampal dysfunction as a consequence of status epilepticus. Epilepsy Behav 49:47–54.
30. Masuch A, Shieh CH, van Rooijen N, van Calker D, Biber K. 2016. Mechanism of microglia neuroprotection: Involvement of P2X7, TNFα, and valproic acid. Glia 64:76–89.
31. Mathern GW, Wilson CL, Beck H. 2008. Hippocampal sclerosis. In: Engel J, Pedley TA, editors. Epilepsy: A comprehensive textbook, 2nd ed. Volume 1. Philadelphia: Lippincott Williams & Wilkins. pp 121–136.
32. Mirrione MM, Konomos DK, Gravanis I, Dewey SL, Aguzzi A, Heppner FL, Tsirka SE. 2010. Microglial ablation and lipopolysaccharide preconditioning affects pilocarpine-induced seizures in mice. Neurobiol Dis 39:85–97.
33. Mizoguchi H, Nakade J, Tachibana M, Ibi D, Someya E, Koike H, Kamei H, Nabeshima T, Itohara S, Takuma K, Sawada M, Sato J, Yamada K. 2011. Matrix metalloproteinase-9 contributes to kindled seizure development in pentylenetetrazole-treated mice by converting pro-BDNF to mature BDNF in the hippocampus. J Neurosci 31:12963–12971.
34. Mizoguchi H, Yamada K. 2013. Roles of matrix metalloproteinases and their targets in epileptogenesis and seizures. Clin Psychopharmacol Neurosci 11:45–52.
35. Penkowa M, Molinero A, Carrasco J, Hidalgo J. 2001. Interleukin-6 deficiency reduces the brain inflammatory response and increases oxidative stress and neurodegeneration after kainic acid-induced seizures. Neuroscience 102:805–818.
36. Pitkänen A, Sutula TP. 2002. Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 1:173–181.
37. Plata-Salamán CR, Ilyin SE, Turrin NP, Gayle D, Flynn MC, Romanovitch AE, Kelly ME, Bureau Y, Anisman H, McIntyre DC. 2000. Kindling modulates the IL-1beta system, TNF-alpha, TGF-beta1, and neuropeptide mRNAs in specific brain regions. Brain Res Mol Brain Res 75:248–258.
38. Ravizza T, Vezzani A. 2006. Status epilepticus induces time-dependent neuronal and astrocytic expression of interleukin-1 receptor type I in the rat limbic system. Neuroscience 137:301–308.
39. Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A. 2008. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29:142–160.
40. Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ. 2008. Microglial activation and TNFalpha production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci USA 105:17151–17156.
41. Suenaga N, Ichiyama T, Kubota M, Isumi H, Tohyama J, Furukawa S. 2008. Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures. J Neurol Sci 266:126–130.
42. Turrin NP, Rivest S. 2004. Innate immune reaction in response to seizures: implications for the neuropathology associated with epilepsy. Neurobiol Dis 16:321–334.
43. Vainchtein ID, Vinet J, Brouwer N, Brendecke S, Biagini G, Biber K, Boddeke HW, Eggen BJ. 2014. In acute experimental autoimmune encephalomyelitis, infiltrating macrophages are immune activated, whereas microglia remain immune suppressed. Glia 62:1724–1735.
44. Vezzani A, Conti M, De Luigi A, Ravizza T, Moneta D, Marchesi F, De Simoni MG. 1999. Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures. J Neurosci 19:5054–5065.
45. Vezzani A, French J, Bartfai T, Baram TZ. 2011. The role of inflammation in epilepsy. Nat Rev Neurol 7:31–40.
46. Vezzani A, Granata T. 2005. Brain inflammation in epilepsy: experimental and clinical evidence. Epilepsia 46:1724–1743.
47. Viviani B, Bartesaghi S, Gardoni F, Vezzani A, Behrens MM, Bartfai T, Binaglia M, Corsini E, Di Luca M, Galli CL, Marinovich M. 2003. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J Neurosci 23:8692–8700.
48. Weiss N, Miller F, Cazaubon S, Couraud PO. 2009. The blood-brain barrier in brain homeostasis and neurological diseases. Biochim Biophys Acta 1788:842–857.
49. Xu D, Miller SD, Koh S. 2013. Immune mechanisms in epileptogenesis. Front Cell Neurosci 7:195.
50. Ye ZC, Sontheimer H. 1996. Cytokine modulation of glial glutamate uptake: a possible involvement of nitric oxide. Neuroreport 7:2181–2185.
51. Zattoni M, Mura ML, Deprez F, Schwendener RA, Engelhardt B, Frei K, Fritschy JM. 2011. Brain infiltration of leukocytes contributes to the pathophysiology of temporal lobe epilepsy. J Neurosci 31:4037–4050.
52. Zheng H, Zhu W, Zhao H, Wang X, Wang W, Li Z. 2010. Kainic acid-activated microglia mediate increased excitability of rat hippocampal neurons in vitro and in vivo: crucial role of interleukin-1beta. Neuroimmunomodulation 17:31–38.