Viral pre-challenge increases central nervous system inflammation after intracranial interleukin-1β injection

Journal of Neuroinflammation

Daniel C Anthony¹  Sandra J Campbell¹  Inês Sá-Pereira¹  Andrew E Davis¹  Yvonne Couch¹ 

[1] Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK

关键词: Rat;    Inflammation;    CNS injury;    Adenovirus;    Interleukin-1?;    Pre-challenge;   

Others  :  1150487
DOI  :  10.1186/s12974-014-0178-3

 received in 2014-08-04, accepted in 2014-10-01,  发布年份 2014

【 摘 要 】

Introduction

Systemic inflammation has been shown to significantly worsen the outcome of neurological disease. However, after acute injuries to the brain both pre- and post-conditioning with bacterial endotoxin has been shown to reduce leukocyte recruitment to the CNS. Here, we sought to determine whether viral pre-challenge would have an effect on the outcome of acute CNS inflammation that was distinct from endotoxin.

Methods

Animals received a single intracranial microinjection of IL-1? in the presence or absence of a viral pre-challenge 24 hours prior to surgery. Liver and brain tissue were analysed for chemokine expression by qRT-PCR and leukocyte and monocyte infiltration 12 hours, 3 days and 7 days after the IL-1? injection.

Results

Here, a single injection of adenovirus prior to IL-1? injection resulted in adhesion molecule expression, chemokine expression and the recruitment of neutrophils to the injured CNS in significantly higher numbers than in IL-1? injected animals. The distribution and persistence of leukocytes within the CNS was also greater after pre-challenge, with neutrophils being found in both the ipsilateral and contralateral hemispheres. Thus, despite the absence of virus within the CNS, the presence of virus within the periphery was sufficient to exacerbate CNS disease.

Conclusions

These data suggest that the effect of a peripheral inflammatory challenge on the outcome of CNS injury or disease is not generic and will be highly dependent on the nature of the pathogen.

【 授权许可】

   
2014 Couch et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Buljevac D, Flach HZ, Hop WC, Hijdra D, Laman JD, Savelkoul HF, van Der Meché FG, van Doorn PA, Hintzen RQ: Prospective study on the relationship between infections and multiple sclerosis exacerbations. Brain 2002, 125(Pt 5):952-960.
• [2]Westendorp WF, Nederkoorn PJ, Vermeij JD, Dijkgraaf MG, van de Beek D: Post-stroke infection: a systematic review and meta-analysis. BMC Neurol 2011, 11:110. BioMed Central Full Text
• [3]Koprich JB, Reske-Nielsen C, Mithal P, Isacson O: Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J Neuroinflammation 2008, 5:8. BioMed Central Full Text
• [4]McGeer PL, McGeer EG: Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat Disord 2004, 10(Suppl 1):S3-S7.
• [5]Kitazawa M, Cheng D, Tsukamoto MR, Koike MA, Wes PD, Vasilevko V, Cribbs DH, LaFerla FM: Blocking IL-1 signaling rescues cognition, attenuates tau pathology, and restores neuronal beta-catenin pathway function in an Alzheimer's disease model. J Immunol 2011, 187(12):6539-6549.
• [6]Combrinck MI, Perry VH, Cunningham C: Peripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease. Neuroscience 2002, 112(1):7-11.
• [7]McColl BW, Rothwell NJ, Allan SM: Systemic inflammatory stimulus potentiates the acute phase and CXC chemokine responses to experimental stroke and exacerbates brain damage via interleukin-1- and neutrophil-dependent mechanisms. J Neurosci 2007, 27(16):4403-4412.
• [8]McColl BW, Allan SM, Rothwell NJ: Systemic infection, inflammation and acute ischemic stroke. Neuroscience 2009, 158(3):1049-1061.
• [9]Campbell SJ, Meier U, Mardiguian S, Jiang Y, Littleton ET, Bristow A, Relton J, Connor TJ, Anthony DC: Sickness behaviour is induced by a peripheral CXC-chemokine also expressed in multiple sclerosis and EAE. Brain Behav Immun 2010, 24(5):738-746.
• [10]Arai H, Furuya T, Mizuno Y, Mochizuki H: Inflammation and infection in Parkinson's disease. Histol Histopathol 2006, 21(6):673-678.
• [11]Chamorro A, Amaro S, Vargas M, Obach V, Cervera A, Gómez-Choco M, Torres F, Planas AM: Catecholamines, infection, and death in acute ischemic stroke. J Neurol Sci 2007, 252(1):29-35.
• [12]Chamorro A, Urra X, Planas AM: Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke 2007, 38(3):1097-1103.
• [13]Simon RP, Niiro M, Gwinn R: Prior ischemic stress protects against experimental stroke. Neurosci Lett 1993, 163(2):135-137.
• [14]Towfighi J, Housman C, Mauger D, Vannucci RC: Effect of seizures on cerebral hypoxic-ischemic lesions in immature rats. Brain Res Dev Brain Res 1999, 113(1¿2):83-95.
• [15]Kapinya KJ, Löwl D, Fütterer C, Maurer M, Waschke KF, Isaev NK, Dirnagl U: Tolerance against ischemic neuronal injury can be induced by volatile anesthetics and is inducible NO synthase dependent. Stroke 2002, 33(7):1889-1898.
• [16]Bordet R, Deplanque D, Maboudou P, Puisieux F, Pu Q, Robin E, Martin A, Bastide M, Leys D, Lhermitte M, Dupuis B: Increase in endogenous brain superoxide dismutase as a potential mechanism of lipopolysaccharide-induced brain ischemic tolerance. J Cereb Blood Flow Metab 2000, 20(8):1190-1196.
• [17]Rosenzweig HL, Lessov NS, Henshall DC, Minami M, Simon RP, Stenzel-Poore MP: Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke 2004, 35(11):2576-2581.
• [18]Davis A, Campbell SJ, Wilainam P, Anthony DC: Post-conditioning with lipopolysaccharide reduces the inflammatory infiltrate to the injured brain and spinal cord: a potential neuroprotective treatment. Eur J Neurosci 2005, 22(10):2441-2450.
• [19]Edwards S, Zvartau M, Clarke H, Irving W, Blumhardt LD: Clinical relapses and disease activity on magnetic resonance imaging associated with viral upper respiratory tract infections in multiple sclerosis. J Neurol Neurosurg Psychiatry 1998, 64(6):736-741.
• [20]Panitch H: Influence of infection on exacerbations of multiple sclerosis. Ann Neurol 1994, 36(Suppl):S25-S28.
• [21]Andersen O, Lygner PE, Bergström T, Andersson M, Vahlne A: Viral infections trigger multiple sclerosis relapses: a prospective seroepidemiological study. J Neurol 1993, 240(7):417-422.
• [22]Kriesel JD, White A, Hayden FG, Spruance SL, Petajan J: Multiple sclerosis attacks are associated with picornavirus infections. Mult Scler 2004, 10(2):145-148.
• [23]Ordonez G, Pineda B, Garcia-Navarrete R, Sotelo J: Brief presence of varicella-zoster vral DNA in mononuclear cells during relapses of multiple sclerosis. Arch Neurol 2004, 61(4):529-532.
• [24]Rapp N, Gilroy J, Lerner A: Role of bacterial infection in exacerbation of multiple sclerosis. Am J Phys Med Rehabil 1995, 74(6):415-418.
• [25]Zhu J, Huang X, Yang Y: Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and -independent pathways. J Virol 2007, 81(7):3170-3180.
• [26]Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG: Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8(6):e1000412.
• [27]Couch Y, Martin CJ, Howarth C, Raley J, Khrapitchev AA, Stratford M, Sharp T, Sibson NR, Anthony DC: Systemic inflammation alters central 5-HT function as determined by pharmacological MRI. Neuroimage 2013, 75:177-186.
• [28]Couch Y, Alvarez-Erviti L, Sibson NR, Wood MJ, Anthony DC: The acute inflammatory response to intranigral alpha-synuclein differs significantly from intranigral lipopolysaccharide and is exacerbated by peripheral inflammation. J Neuroinflammation 2011, 8:166. BioMed Central Full Text
• [29]Paxinos G, Watson CR, Emson PC: AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 1980, 3(2):129-149.
• [30]Wilcockson DC, Campbell SJ, Anthony DC, Perry VH: The systemic and local acute phase response following acute brain injury. J Cereb Blood Flow Metab 2002, 22(3):318-326.
• [31]Campbell SJ, Perry VH, Pitossi FJ, Butchart AG, Chertoff M, Waters S, Dempster R, Anthony DC: Central nervous system injury triggers hepatic CC and CXC chemokine expression that is associated with leukocyte mobilization and recruitment to both the central nervous system and the liver. Am J Pathol 2005, 166(5):1487-1497.
• [32]Campbell S, Deacon RM, Jiang Y, Ferrari C, Pitossi FJ, Anthony DC: Overexpression of IL-1 beta by adenoviral-mediated gene transfer in the rat brain causes a prolonged hepatic chemokine response, axonal injury and the suppression of spontaneous behaviour. Neurobiol Dis 2007, 27(2):151-163.
• [33]Campbell SJ, Anthony DC, Oakley F, Carlsen H, Elsharkawy AM, Blomhoff R, Mann DA: Hepatic nuclear factor kappa B regulates neutrophil recruitment to the injured brain. J Neuropathol Exp Neurol 2008, 67(3):223-230.
• [34]Guidotti JE, Mignon A, Haase G, Caillaud C, McDonell N, Kahn A, Poenaru L: Adenoviral gene therapy of the Tay-Sachs disease in hexosaminidase A-deficient knock-out mice. Hum Mol Genet 1999, 8(5):831-838.
• [35]Yarovinsky TO, Mohning MP, Bradford MA, Monick MM, Hunninghake GW: Increased sensitivity to staphylococcal enterotoxin B following adenoviral infection. Infect Immun 2005, 73(6):3375-3384.
• [36]Nociari M, Ocheretina O, Schoggins JW, Falck-Pedersen E: Sensing infection by adenovirus: Toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J Virol 2007, 81(8):4145-4157.
• [37]Bonville CA, Rosenberg HF, Domachowske JB: Macrophage inflammatory protein-1alpha and RANTES are present in nasal secretions during ongoing upper respiratory tract infection. Pediatr Allergy Immunol 1999, 10(1):39-44.
• [38]Tsai SC, Lin SJ, Lin CJ, Chou YC, Lin JH, Yeh TH, Chen MR, Huang LM, Lu MY, Huang YC, Chen HY, Tsai CH: Autocrine CCL3 and CCL4 induced by the oncoprotein LMP1 promote Epstein-Barr virus-triggered B cell proliferation. J Virol 2013, 87(16):9041-9052.
• [39]Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH: Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J Neurosci 2005, 25(40):9275-9284.
• [40]Field R, Campion S, Warren C, Murray C, Cunningham C: Systemic challenge with the TLR3 agonist poly I:C induces amplified IFNalpha/beta and IL-1beta responses in the diseased brain and exacerbates chronic neurodegeneration. Brain Behav Immun 2010, 24(6):996-1007.
• [41]Sibley WA, Bamford CR, Clark K: Clinical viral infections and multiple sclerosis. Lancet 1985, 1(8441):1313-1315.
• [42]Correale J, Fiol M, Gilmore W: The risk of relapses in multiple sclerosis during systemic infections. Neurology 2006, 67(4):652-659.
• [43]Olson JK, Miller SD: The innate immune response affects the development of the autoimmune response in Theiler's virus-induced demyelinating disease. J Immunol 2009, 182(9):5712-5722.
• [44]Krstic D, Madhusudan A, Doehner J, Vogel P, Notter T, Imhof C, Manalastas A, Hilfiker M, Pfister S, Schwerdel C, Riether C, Meyer U, Knuesel I: Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J Neuroinflammation 2012, 9:151. BioMed Central Full Text
• [45]McColl BW, Allan SM, Rothwell NJ: Systemic inflammation and stroke: aetiology, pathology and targets for therapy. Biochem Soc Trans 2007, 35(Pt 5):1163-1165.
• [46]Bernardes-Silva M, Anthony DC, Issekutz AC, Perry VH: Recruitment of neutrophils across the blood¿brain barrier: the role of E- and P-selectins. J Cereb Blood Flow Metab 2001, 21(9):1115-1124.
• [47]Campbell SJ, Hughes PM, Iredale JP, Wilcockson DC, Waters S, Docagne F, Perry VH, Anthony DC: CINC-1 is an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. Faseb J 2003, 17(9):1168-1170.
• [48]Babcock AA, Kuziel WA, Rivest S, Owens T: Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 2003, 23(21):7922-7930.
• [49]Tousi NS, Buck DJ, Curtis JT, Davis RL: Alpha-Synuclein potentiates interleukin-1beta-induced CXCL10 expression in human A172 astrocytoma cells. Neurosci Lett 2012, 507(2):133-136.
• [50]Muzio L, Cavasinni F, Marinaro C, Bergamaschi A, Bergami A, Porcheri C, Cerri F, Dina G, Quattrini A, Comi G, Furlan R, Martino G: Cxcl10 enhances blood cells migration in the sub-ventricular zone of mice affected by experimental autoimmune encephalomyelitis. Mol Cell Neurosci 2010, 43(3):268-280.
• [51]Ip PP, Liao F: Resistance to dengue virus infection in mice is potentiated by CXCL10 and is independent of CXCL10-mediated leukocyte recruitment. J Immunol 2010, 184(10):5705-5714.
• [52]Sahin H, Borkham-Kamphorst E, Do ONT, Berres ML, Kaldenbach M, Schmitz P, Weiskirchen R, Liedtke C, Streetz KL, Maedler K, Trautwein C, Wasmuth HE: Proapoptotic effects of the chemokine, CXCL 10 are mediated by the noncognate receptor TLR4 in hepatocytes. Hepatology 2013, 57(2):797-805.