期刊论文详细信息
Journal of Neuroinflammation
Differential expression of major histocompatibility complex class I in developmental glioneuronal lesions
Eleonora Aronica1  Peter C van Rijen2  Wim GM Spliet2  Jasper J Anink3  Anand M Iyer3  Avanita S Prabowo3 
[1] Swammerdam Institute for Life Sciences, Center for Neuroscience, University of Amsterdam, Amsterdam, The Netherlands;Departments of Pathology and Neurosurgery /Rudolf Magnus Institute for Neuroscience, University Medical Center Utrecht, Utrecht, The Netherlands;Department of (Neuro)Pathology, Academic Medical Center, University of Amsterdam, Meibergdreef 9, Amsterdam, 1105 AZ, The Netherlands
关键词: Major histocompatibility complex (MHC) class I;    Microglia;    Neurons;    Cortical tubers;    Ganglioglioma;    Focal cortical dysplasia;   
Others  :  1160059
DOI  :  10.1186/1742-2094-10-12
 received in 2012-11-14, accepted in 2013-01-10,  发布年份 2013
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【 摘 要 】

Purpose

The expression of the major histocompatibility complex class I (MHC-I) in the brain has received considerable interest not only because of its fundamental role in the immune system, but also for its non-immune functions in the context of activity-dependent brain development and plasticity.

Methods

In the present study we evaluated the expression and cellular pattern of MHC-I in focal glioneuronal lesions associated with intractable epilepsy. MHC-I expression was studied in epilepsy surgery cases with focal cortical dysplasia (FCD I, n = 6; FCD IIa, n = 6 and FCD IIb, n = 15), tuberous sclerosis complex (TSC, cortical tubers; n = 6) or ganglioglioma (GG; n = 15) using immunocytochemistry. Evaluation of T lymphocytes with granzyme-B+ granules and albumin immunoreactivity was also performed.

Results

All lesions were characterized by MHC-I expression in blood vessels. Expression in both endothelial and microglial cells as well as in neurons (dysmorphic/dysplastic neurons) was observed in FCD II, TSC and GG cases. We observed perivascular and parenchymal T lymphocytes (CD8+, T-cytotoxic) with granzyme-B+ granules in FCD IIb and TSC specimens. Albumin extravasation, with uptake in astrocytes, was observed in FCD IIb and GG cases.

Conclusions

Our findings indicate a prominent upregulation of MHC-I as part of the immune response occurring in epileptogenic glioneuronal lesions. In particular, the induction of MHC-I in neuronal cells appears to be a feature of type II FCD, TSC and GG and may represent an important accompanying event of the immune response, associated with blood–brain barrier dysfunction, in these developmental lesions.

【 授权许可】

   
2013 Prabowo et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Aronica E, Crino PB: Inflammation in epilepsy: clinical observations. Epilepsia 2011, 52(Suppl 3):26-32.
  • [2]Vezzani A, French J, Bartfai T, Baram TZ: The role of inflammation in epilepsy. Nature Reviews Neurology 2011, 7:31-40.
  • [3]Vezzani A, Auvin S, Ravizza T, Aronica E: Glia-neuronal interactions in ictogenesis and epileptogenesis: role of inflammatory mediators. In Jasper’s Basic Mechanisms of the Epilepsies. 4th edition. Edited by Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV. Bethesda, MD; 2012.
  • [4]Aronica E, Ravizza T, Zurolo E, Vezzani A: Astrocyte immune responses in epilepsy. Glia 2012, 60:1258-1268.
  • [5]Blumcke I, Thom M, Aronica E, Armstrong DD, Vinters HV, Palmini A, Jacques TS, Avanzini G, Barkovich AJ, Battaglia G, et al.: The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011, 52:158-174.
  • [6]Iyer A, Zurolo E, Spliet WGM, van Rijen PC, Baayen JC, Gorter JA, Aronica E: Evaluation of the innate and adaptive immunity in type I and type II focal cortical dysplasias. Epilepsia 2010, 51(9):1763-1773.
  • [7]Boulanger LM: MHC class I in activity-dependent structural and functional plasticity. Neuron Glia biology 2004, 1:283-289.
  • [8]Bien CG, Bauer J, Deckwerth TL, Wiendl H, Deckert M, Wiestler OD, Schramm J, Elger CE, Lassmann H: Destruction of neurons by cytotoxic T cells: a new pathogenic mechanism in Rasmussen’s encephalitis. Ann Neurol 2002, 51:311-318.
  • [9]Bauer J, Elger CE, Hans VH, Schramm J, Urbach H, Lassmann H, Bien CG: Astrocytes are a specific immunological target in Rasmussen’s encephalitis. Ann Neurol 2007, 62:67-80.
  • [10]Engel JJ: Outcome with respect to epileptic seizures. In Surgical Treatment of the Epilepsies. Edited by Engel JJ. New York: Raven Press; 1993:609-621.
  • [11]Gomez M, Sampson J, Whittemore V: The Tuberous Sclerosis Complex. Oxford: Oxford University Press; 1999.
  • [12]Louis DN, Ohgaki H, Wiestler OD, Cavanee WK: WHO Classification of Tumours of the Central Nervous System. Lyon: IARC; 2007.
  • [13]van Thiel PP, de Bie RM, Eftimov F, Tepaske R, Zaaijer HL, van Doornum GJ, Schutten M, Osterhaus AD, Majoie CB, Aronica E, et al.: Fatal human rabies due to Duvenhage virus from a bat in Kenya: failure of treatment with coma-induction, ketamine, and antiviral drugs. PLoS Neglected Tropical Diseases [electronic resource] 2009, 3:428.
  • [14]Ravizza T, Boer K, Redeker S, Spliet WG, van Rijen PC, Troost D, Vezzani A, Aronica E: The IL-1beta system in epilepsy-associated malformations of cortical development. Neurobiol Dis 2006, 24:128-143.
  • [15]Aronica E, Gorter JA, Redeker S, Ramkema M, Spliet WG, van Rijen PC, Leenstra S, Troost D: Distribution, characterization and clinical significance of microglia in glioneuronal tumours from patients with chronic intractable epilepsy. Neuropathol Appl Neurobiol 2005, 31:280-291.
  • [16]van der Loos CM: Multiple immunoenzyme staining: methods and visualizations for the observation with spectral imaging. J Histochem Cytochem 2008, 56:313-328.
  • [17]Boer K, Troost D, Timmermans W, Gorter JA, Spliet WG, Nellist M, Jansen F, Aronica E: Cellular localization of metabotropic glutamate receptors in cortical tubers and subependymal giant cell tumors of tuberous sclerosis complex. Neuroscience 2008, 156:203-215.
  • [18]Maldonado M, Baybis M, Newman D, Kolson DL, Chen W, McKhann G 2nd, Gutmann DH, Crino PB: Expression of ICAM-1, TNF-alpha, NF kappa B, and MAP kinase in tubers of the tuberous sclerosis complex. Neurobiol Dis 2003, 14:279-290.
  • [19]Aronica E, Gorter JA, Redeker S, van Vliet EA, Ramkema M, Scheffer GL, Scheper RJ, van der Valk P, Leenstra S, Baayen JC, et al.: Localization of breast cancer resistance protein (BCRP) in microvessel endothelium of human control and epileptic brain. Epilepsia 2005, 46:849-857.
  • [20]Airas L, Lindsberg PJ, Karjalainen-Lindsberg ML, Mononen I, Kotisaari K, Smith DJ, Jalkanen S: Vascular adhesion protein-1 in human ischaemic stroke. Neuropathol Appl Neurobiol 2008, 34:394-402.
  • [21]Mizuguchi M, Takashima S: Neuropathology of tuberous sclerosis. Brain Dev 2001, 23:508-515.
  • [22]DiMario FJ Jr: Brain abnormalities in tuberous sclerosis complex. J Child Neurol 2004, 19:650-657.
  • [23]Baybis M, Yu J, Lee A, Golden JA, Weiner H, McKhann G 2nd, Aronica E, Crino PB: mTOR cascade activation distinguishes tubers from focal cortical dysplasia. Ann Neurol 2004, 56:478-487.
  • [24]Schick V, Majores M, Engels G, Hartmann W, Elger CE, Schramm J, Schoch S, Becker AJ: Differential Pi3K-pathway activation in cortical tubers and focal cortical dysplasias with balloon cells. Brain Pathology 2007, 17:165-173.
  • [25]Boer K, Troost D, Timmerman W, Spliet WGM, van Rijen PC, Aronica E: Pi3K-mTOR signaling and AMOG expression in epilepsy-associated glioneuronal tumors. Brain Pathology 2010, 20:234-244.
  • [26]Boer K, Jansen F, Nellist M, Redeker S, van den Ouweland AM, Spliet WG, van Nieuwenhuizen O, Troost D, Crino PB, Aronica E: Inflammatory processes in cortical tubers and subependymal giant cell tumors of tuberous sclerosis complex. Epilepsy Res 2008, 78:7-21.
  • [27]Aronica E, Boer K, Becker A, Redeker S, Spliet WG, van Rijen PC, Wittink F, Breit T, Wadman WJ, Lopes da Silva FH, et al.: Gene expression profile analysis of epilepsy-associated gangliogliomas. Neuroscience 2008, 151:272-292.
  • [28]Maehlen J, Schroder HD, Klareskog L, Olsson T, Kristensson K: Axotomy induces MHC class I antigen expression on rat nerve cells. Neurosci Lett 1988, 92:8-13.
  • [29]Pereira RA, Tscharke DC, Simmons A: Upregulation of class I major histocompatibility complex gene expression in primary sensory neurons, satellite cells, and Schwann cells of mice in response to acute but not latent herpes simplex virus infection in vivo. J Exp Med 1994, 180:841-850.
  • [30]Neumann H, Cavalie A, Jenne DE, Wekerle H: Induction of MHC class I genes in neurons. Science 1995, 269:549-552.
  • [31]Neumann H, Schmidt H, Cavalie A, Jenne D, Wekerle H: Major histocompatibility complex (MHC) class I gene expression in single neurons of the central nervous system: differential regulation by interferon (IFN)-gamma and tumor necrosis factor (TNF)-alpha. J Exp Med 1997, 185:305-316.
  • [32]Kimura T, Griffin DE: The role of CD8(+) T cells and major histocompatibility complex class I expression in the central nervous system of mice infected with neurovirulent Sindbis virus. J Virol 2000, 74:6117-6125.
  • [33]Foster JA, Quan N, Stern EL, Kristensson K, Herkenham M: Induced neuronal expression of class I major histocompatibility complex mRNA in acute and chronic inflammation models. J Neuroimmunol 2002, 131:83-91.
  • [34]Neumann H: Control of glial immune function by neurons. Glia 2001, 36:191-199.
  • [35]Neumann H: The immunological microenvironment in the CNS: implications on neuronal cell death and survival. J Neural Transm Suppl 2000, 59:59-68.
  • [36]Boer K, Crino PB, Gorter JA, Nellist M, Jansen FE, Spliet WG, van Rijen PC, Wittink F, Breit T, Troost D, et al.: Gene expression analysis of tuberous sclerosis complex cortical tubers reveals increased expression of adhesion and inflammatory factors. Brain Pathol 2010, 20:704-719.
  • [37]Oeckinghaus A, Hayden MS, Ghosh S: Crosstalk in NF-kappaB signaling pathways. Nat Immunol 2011, 12:695-708.
  • [38]Kesson AM, Cheng Y, King NJ: Regulation of immune recognition molecules by flavivirus, West Nile. Viral immunology 2002, 15:273-283.
  • [39]Forloni M, Albini S, Limongi MZ, Cifaldi L, Boldrini R, Nicotra MR, Giannini G, Natali PG, Giacomini P, Fruci D: NF-kappaB, and not MYCN, regulates MHC class I and endoplasmic reticulum aminopeptidases in human neuroblastoma cells. Cancer Res 2010, 70:916-924.
  • [40]Schild H, Rotzschke O, Kalbacher H, Rammensee HG: Limit of T cell tolerance to self proteins by peptide presentation. Science 1990, 247:1587-1589.
  • [41]Caron E, Vincent K, Fortier MH, Laverdure JP, Bramoulle A, Hardy MP, Voisin G, Roux PP, Lemieux S, Thibault P, Perreault C: The MHC I immunopeptidome conveys to the cell surface an integrative view of cellular regulation. Mol Syst Biol 2011, 7:533.
  • [42]Chen J, Tsai V, Parker WE, Aronica E, Baybis M, Crino PB: Detection of human papillomavirus in human focal cortical dysplasia type IIB. Ann Neurology 2012, 72:881-892.
  • [43]Christinck ER, Luscher MA, Barber BH, Williams DB: Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature 1991, 352:67-70.
  • [44]Choi J, Nordli DR Jr, Alden TD, DiPatri A Jr, Laux L, Kelley K, Rosenow J, Schuele SU, Rajaram V, Koh S: Cellular injury and neuroinflammation in children with chronic intractable epilepsy. J Neuroinflammation 2009, 6:38. BioMed Central Full Text
  • [45]Gobin SJ, Montagne L, Van Zutphen M, Van Der Valk P, Van Den Elsen PJ, De Groot CJ: Upregulation of transcription factors controlling MHC expression in multiple sclerosis lesions. Glia 2001, 36:68-77.
  • [46]Prabowo AS, Anink JJ, Lammens M, Nellist M, van den Ouweland AM, Adle-Biassette H, Sarnat HB, Flores-Sarnat L, Crino PB, Aronica E: Fetal brain lesions in tuberous sclerosis complex: TORC1 activation and inflammation. Brain Pathology 2012, 23:45-59.
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