Journal of Neuroinflammation | |
Inflammatory monocytes and the pathogenesis of viral encephalitis | |
Nicholas JC King3  Iain L Campbell2  Caryn van Vreden3  Celine Deffrasnes3  Daniel R Getts1  Rachael L Terry1  | |
[1] Department of Microbiology-Immunology, Feinberg School of Medicine, Chicago Avenue, Northwestern University, Chicago, 60611, USA;School of Molecular and Microbial Biosciences, Butlin Avenue, The University of Sydney, Sydney, 2006, Australia;Bosch Institute, The University of Sydney, Sydney, 2006, Australia | |
关键词: Integrins; LFA-1; VLA-4; CCR2; CCL2; Neurotrophic virus; Viral encephalitis; Ly6Chi inflammatory monocytes; | |
Others : 1160113 DOI : 10.1186/1742-2094-9-270 |
|
received in 2012-08-29, accepted in 2012-11-19, 发布年份 2012 | |
【 摘 要 】
Monocytes are a heterogeneous population of bone marrow-derived cells that are recruited to sites of infection and inflammation in many models of human diseases, including those of the central nervous system (CNS). Ly6Chi/CCR2hi inflammatory monocytes have been identified as the circulating precursors of brain macrophages, dendritic cells and arguably microglia in experimental autoimmune encephalomyelitis; Alzheimer’s disease; stroke; and more recently in CNS infection caused by Herpes simplex virus, murine hepatitis virus, Theiler’s murine encephalomyelitis virus, Japanese encephalitis virus and West Nile virus. The precise differentiation pathways and functions of inflammatory monocyte-derived populations in the inflamed CNS remains a contentious issue, especially in regard to the existence of monocyte-derived microglia. Furthermore, the contributions of monocyte-derived subsets to viral clearance and immunopathology are not well-defined. Thus, understanding the pathways through which inflammatory monocytes migrate to the brain and their functional capacity within the CNS is critical to inform future therapeutic strategies. This review discusses some of the key aspects of inflammatory monocyte trafficking to the brain and addresses the role of these cells in viral encephalitis.
【 授权许可】
2012 Terry et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150410094009161.pdf | 1167KB | download | |
Figure 1. | 102KB | Image | download |
【 图 表 】
Figure 1.
【 参考文献 】
- [1]Chaudhuri A, Kennedy P: Diagnosis and treatment of viral encephalitis. Postgrad Med J 2002, 78:575-583.
- [2]Whitley R, Gnann J: Viral encephalitis: familiar infections and emerging pathogens. Lancet 2002, 359:507-513.
- [3]Raschilas F, Wolff M, Delatour F, Chaffaut C, De Broucker T, Chevret S, Lebon P, Canton P, Rozenberg F: Outcome of and prognostic factors for herpes simplex encephalitis in adult patients: results of a multicenter study. Clin Infect Dis 2002, 35:254-260.
- [4]Lawrence DM, Major EO: HIV-1 and the brain: connections between HIV-1-associated dementia, neuropathology and neuroimmunology. Microbes Infect 2002, 4:301-308.
- [5]Domingues RB: Treatment of viral encephalitis. Cent Nerv Syst Agents Med Chem 2009, 9:56-62.
- [6]Utley TF, Ogden JA, Gibb A, McGrath N, Anderson NE: The long-term neuropsychological outcome of herpes simplex encephalitis in a series of unselected survivors. Neuropsychiatry Neuropsychol Behav Neurol 1997, 10:180-189.
- [7]McGrath N, Anderson NE, Croxson MC, Powell KF: Herpes simplex encephalitis treated with acyclovir: diagnosis and long term outcome. J Neurol Neurosurg Psychiatry 1997, 63:321-326.
- [8]McArthur JC: HIV dementia: an evolving disease. J Neuroimmunol 2004, 157:3-10.
- [9]Ito Y, Kimura H, Yabuta Y, Ando Y, Murakami T, Shiomi M, Morishima T: Exacerbation of herpes simplex encephalitis after successful treatment with acyclovir. Clin Infect Dis 2000, 30:185-187.
- [10]Gras G, Kaul M: Molecular mechanisms of neuroinvasion by monocytes-macrophages in HIV-1 infection. Retrovirology 2010, 7:30. BioMed Central Full Text
- [11]Getts DR, Terry RL, Getts MT, Muller M, Rana S, Shrestha B, Radford J, Van Rooijen N, Campbell IL, King NJ: Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med 2008, 205:2319-2337.
- [12]Christophi GP, Massa PT: Central neuroinvasion and demyelination by inflammatory macrophages after peripheral virus infection is controlled by SHP-1. Viral Immunol 2009, 22:371-387.
- [13]Templeton S, Kim T, O'Malley K, Perlman S: Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathol 2008, 18:40-51.
- [14]Marques CP, Cheeran MC, Palmquist JM, Hu S, Urban SL, Lokensgard JR: Prolonged microglial cell activation and lymphocyte infiltration following experimental herpes encephalitis. J Immunol 2008, 181:6417-6426.
- [15]Liang XH, Goldman JE, Jiang HH, Levine B: Resistance of interleukin-1beta-deficient mice to fatal Sindbis virus encephalitis. J Virol 1999, 73:2563-2567.
- [16]Sergerie Y, Rivest S, Boivin G: Tumor necrosis factor-alpha and interleukin-1 beta play a critical role in the resistance against lethal herpes simplex virus encephalitis. J Infect Dis 2007, 196:853-860.
- [17]Libbey JE, Kennett NJ, Wilcox KS, White HS, Fujinami RS: Interleukin-6, produced by resident cells of the central nervous system and infiltrating cells, contributes to the development of seizures following viral infection. J Virol 2011, 85:6913-6922.
- [18]Shaftel SS, Carlson TJ, Olschowka JA, Kyrkanides S, Matousek SB, O'Banion MK: Chronic interleukin-1beta expression in mouse brain leads to leukocyte infiltration and neutrophil-independent blood brain barrier permeability without overt neurodegeneration. J Neurosci 2007, 27:9301-9309.
- [19]Allan SM, Tyrrell PJ, Rothwell NJ: Interleukin-1 and neuronal injury. Nat Rev Immunol 2005, 5:629-640.
- [20]Spooren A, Kolmus K, Laureys G, Clinckers R, De Keyser J, Haegeman G, Gerlo S: Interleukin-6, a mental cytokine. Brain Res Rev 2011, 67:157-183.
- [21]Park KM, Bowers WJ: Tumor necrosis factor-alpha mediated signaling in neuronal homeostasis and dysfunction. Cell Signal 2010, 22:977-983.
- [22]McCoy MK, Tansey MG: TNF signaling inhibition in the CNS: implications for normal brain function and neurodegenerative disease. J Neuroinflammation 2008, 5:45. BioMed Central Full Text
- [23]Kapil P, Atkinson R, Ramakrishna C, Cua DJ, Bergmann CC, Stohlman SA: Interleukin-12 (IL-12), but not IL-23, deficiency ameliorates viral encephalitis without affecting viral control. J Virol 2009, 83:5978-5986.
- [24]Komatsu T, Barna M, Reiss CS: Interleukin-12 promotes recovery from viral encephalitis. Viral Immunol 1997, 10:35-47.
- [25]Camelo S, Lafage M, Lafon M: Absence of the p55 Kd TNF-alpha receptor promotes survival in rabies virus acute encephalitis. J Neurovirol 2000, 6:507-518.
- [26]Ubol S, Sukwattanapan C, Maneerat Y: Inducible nitric oxide synthase inhibition delays death of rabies virus-infected mice. J Med Microbiol 2001, 50:238-242.
- [27]Lobigs M, Mullbacher A, Wang Y, Pavy M, Lee E: Role of type I and type II interferon responses in recovery from infection with an encephalitic flavivirus. J Gen Virol 2003, 84:567-572.
- [28]Gomez RM, Yep A, Schattner M, Berria MI: Junin virus-induced astrocytosis is impaired by iNOS inhibition. J Med Virol 2003, 69:145-149.
- [29]Tucker PC, Griffin DE, Choi S, Bui N, Wesselingh S: Inhibition of nitric oxide synthesis increases mortality in Sindbis virus encephalitis. J Virol 1996, 70:3972-3977.
- [30]Getts DR, Terry RL, Getts MT, Muller MA, Radford J, Rana S, Ashhurst T, Deffrasnes C, Hofer M, Thomas S, Campbell IL, King NJ: Targeted blockade in lethal West Nile virus encephalitis shows a critical role for VLA-4-dependant recruitment of nitric oxide-producing macrophages. J Neuroinflammation 2012, 9:246. BioMed Central Full Text
- [31]Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM: Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 2007, 8:766-775.
- [32]Wang P, Dai J, Bai F, Kong KF, Wong SJ, Montgomery RR, Madri JA, Fikrig E: Matrix metalloproteinase 9 facilitates West Nile virus entry into the brain. J Virol 2008, 82:8978-8985.
- [33]Yong VW: Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 2005, 6:931-944.
- [34]Yong VW, Power C, Forsyth P, Edwards DR: Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci 2001, 2:502-511.
- [35]Greene IP, Lee EY, Prow N, Ngwang B, Griffin DE: Protection from fatal viral encephalomyelitis: AMPA receptor antagonists have a direct effect on the inflammatory response to infection. Proc Natl Acad Sci USA 2008, 105:3575-3580.
- [36]Nargi-Aizenman JL, Havert MB, Zhang M, Irani DN, Rothstein JD, Griffin DE: Glutamate receptor antagonists protect from virus-induced neural degeneration. Ann Neurol 2004, 55:541-549.
- [37]Brison E, Jacomy H, Desforges M, Talbot PJ: Glutamate excitotoxicity is involved in the induction of paralysis in mice after infection by a human coronavirus with a single point mutation in its spike protein. J Virol 2011, 85:12464-12473.
- [38]Hendriks JJ, Teunissen CE, de Vries HE, Dijkstra CD: Macrophages and neurodegeneration. Brain Res Brain Res Rev 2005, 48:185-195.
- [39]Akashi K, Traver D, Miyamoto T, Weissman IL: A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000, 404:193-197.
- [40]Spangrude GJ, Heimfeld S, Weissman IL: Purification and characterization of mouse hematopoietic stem cells. Science 1988, 241:58-62.
- [41]Kondo M, Weissman IL, Akashi K: Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997, 91:661-672.
- [42]Morrison SJ, Weissman IL: The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1994, 1:661-673.
- [43]Reddy MA, Yang BS, Yue X, Barnett CJ, Ross IL, Sweet MJ, Hume DA, Ostrowski MC: Opposing actions of c-ets/PU.1 and c-myb protooncogene products in regulating the macrophage-specific promoters of the human and mouse colony-stimulating factor-1 receptor (c-fms) genes. J Exp Med 1994, 180:2309-2319.
- [44]Krysinska H, Hoogenkamp M, Ingram R, Wilson N, Tagoh H, Laslo P, Singh H, Bonifer C: A two-step, PU.1-dependent mechanism for developmentally regulated chromatin remodeling and transcription of the c-fms gene. Mol Cell Biol 2007, 27:878-887.
- [45]DeKoter RP, Walsh JC, Singh H: PU.1 regulates both cytokine-dependent proliferation and differentiation of granulocyte/macrophage progenitors. EMBO J 1998, 17:4456-4468.
- [46]Tagoh H, Himes R, Clarke D, Leenen PJ, Riggs AD, Hume D, Bonifer C: Transcription factor complex formation and chromatin fine structure alterations at the murine c-fms (CSF-1 receptor) locus during maturation of myeloid precursor cells. Genes Dev 2002, 16:1721-1737.
- [47]Fogg DK, Sibon C, Miled C, Jung S, Aucouturier P, Littman DR, Cumano A, Geissmann F: A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
- [48]Auffray C, Fogg D, Narni-Mancinelli E, Senechal B, Trouillet C, Saederup N, Leemput J, Bigot K, Campisi L, Abitbol M, Molina T, Charo I, Hume DA, Cumano A, Lauvau G, Geissmann F: CX3CR1+ CD115+ CD135+ common macrophage/DC precursors and the role of CX3CR1 in their response to inflammation. J Exp Med 2009, 206:595-606.
- [49]Fogg D, Sibon C, Miled C, Jung S, Aucouturier P, Littman D, Cumano A, Geissmann F: A clonogenic bone marrow progenitor specific for macrophages and dendritic cells. Science 2006, 311:83-87.
- [50]Auffray C, Sieweke MH, Geissmann F: Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu Rev Immunol 2009, 27:669-692.
- [51]Geissmann F, Jung S, Littman D: Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
- [52]Strauss-Ayali A, Conrad SM, Mosser D: Monocyte subpopulations and their differentiation patterns during infection. JLB 2007, 82:244-252.
- [53]Bao Y, Kim E, Bhosle S, Mehta H, Cho S: A role for spleen monocytes in post-ischemic brain inflammation and injury. J Neuroinflammation 2010, 7:92. BioMed Central Full Text
- [54]Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ: Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325:612-616.
- [55]Leuschner F, Panizzi P, Chico-Calero I, Lee WW, Ueno T, Cortez-Retamozo V, Waterman P, Gorbatov R, Marinelli B, Iwamoto Y, Chudnovskiy A, Figueiredo JL, Sosnovik DE, Pittet MJ, Swirski FK, Weissleder R, Nahrendorf M: Angiotensin-converting enzyme inhibition prevents the release of monocytes from their splenic reservoir in mice with myocardial infarction. Circ Res 2010, 107:1364-1373.
- [56]Leuschner F, Rauch PJ, Ueno T, Gorbatov R, Marinelli B, Lee WW, Dutta P, Wei Y, Robbins C, Iwamoto Y, Sena B, Chudnovskiy A, Panizzi P, Keliher E, Higgins JM, Libby P, Moskowitz MA, Pittet MJ, Swirski FK, Weissleder R, Nahrendorf M: Rapid monocyte kinetics in acute myocardial infarction are sustained by extramedullary monocytopoiesis. J Exp Med 2012, 209:123-137.
- [57]Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K: Development of monocytes, macrophages, and dendritic cells. Science 2010, 327:656-661.
- [58]Sunderkötter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, Leenen PJM: Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004, 172:4410-4417.
- [59]Woollard KJ, Geissmann F: Monocytes in atherosclerosis: subsets and functions. Nat Rev Cardiol 2010, 7:77-86.
- [60]Swirski FK, Weissleder R, Pittet MJ: Heterogeneous in vivo behavior of monocyte subsets in atherosclerosis. Arterioscler Thromb Vasc Biol 2009, 29:1424-1432.
- [61]Tacke F, Alvarez D, Kaplan T, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ: Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007, 117:185-194.
- [62]Swirski F, Libby P, Aikawa E, Alcaide P, Luscinskas F, Weissleder R, Pittet M: Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007, 117:195-205.
- [63]Bruhl H, Cihak J, Plachy J, Kunz-Schughart L, Niedermeier M, Denzel A, Rodriguez Gomez M, Talke Y, Luckow B, Stangassinger M, Mack M: Targeting of Gr-1+,CCR2+ monocytes in collagen-induced arthritis. Arthritis Rheum 2007, 56:2975-2985.
- [64]Waddell A, Ahrens R, Steinbrecher K, Donovan B, Rothenberg ME, Munitz A, Hogan SP: Colonic eosinophilic inflammation in experimental colitis is mediated by Ly6C(high) CCR2(+) inflammatory monocyte/macrophage-derived CCL11. J Immunol 2011, 186:5993-6003.
- [65]Nahrendorf M, Swirski F, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo J, Libby P, Weissleder R, Pittet M: The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007, 204:3037-3047.
- [66]King IL, Dickendesher TL, Segal BM: Circulating Ly-6C+ myeloid precursors migrate to the CNS and play a pathogenic role during autoimmune demyelinating disease. Blood 2009, 113:3190-3197.
- [67]Mildner A, Mack M, Schmidt H, Bruck W, Djukic M, Zabel MD, Hille A, Priller J, Prinz M: CCR2+Ly-6Chi monocytes are crucial for the effector phase of autoimmunity in the central nervous system. Brain 2009, 132:2487-2500.
- [68]Butovsky O, Siddiqui S, Gabriely G, Lanser AJ, Dake B, Murugaiyan G, Doykan CE, Wu PM, Gali RR, Iyer LK, Lawson R, Berry J, Krichevsky AM, Cudkowicz ME, Weiner HL: Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J Clin Invest 2012, 122:3063-3087.
- [69]Christophi GP, Hudson CA, Panos M, Gruber RC, Massa PT: Modulation of macrophage infiltration and inflammatory activity by the phosphatase SHP-1 in virus-induced demyelinating disease. J Virol 2009, 83:522-539.
- [70]Tacke F, Randolph G: Migratory fate and differentiation of blood monocyte subsets. Immunobiology 2006, 211:609-618.
- [71]Varol C, Landsman L, Fogg D, Greenshtein L, Gildor B, Margalit R, Kalchenko V, Geissmann F, Jung S: Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J Exp Med 2007, 204:171-180.
- [72]Davison AM, King NJ: Accelerated dendritic cell differentiation from migrating Ly6C(lo) bone marrow monocytes in early dermal West Nile virus infection. J Immunol 2011, 186:2382-2396.
- [73]Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F: Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
- [74]Saederup N, Cardona A, Croft K, Mizutani M, Cotleur A, Tsou C, Ransohoff R, Charo I: Selective chemokine receptor usage by central nervous system myeloid cells in CCR2-red fluorescent protein knock-in mice. PLoS One 2010, 5:e13693.
- [75]Nagasawa T, Hirota S, Tachibana K, Takakura N, Nishikawa S, Kitamura Y, Yoshida N, Kikutani H, Kishimoto T: Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature 1996, 382:635-638.
- [76]Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR: Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 1998, 393:595-599.
- [77]Hidalgo A, Sanz-Rodriguez F, Rodriguez-Fernandez JL, Albella B, Blaya C, Wright N, Cabanas C, Prosper F, Gutierrez-Ramos JC, Teixido J: Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-dependent adhesion to fibronectin and VCAM-1 on bone marrow hematopoietic progenitor cells. Exp Hematol 2001, 29:345-355.
- [78]Bleul CC, Fuhlbrigge RC, Casasnovas JM, Aiuti A, Springer TA: A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1). J Exp Med 1996, 184:1101-1109.
- [79]Katayama Y, Hidalgo A, Peired A, Frenette PS: Integrin alpha4beta7 and its counterreceptor MAdCAM-1 contribute to hematopoietic progenitor recruitment into bone marrow following transplantation. Blood 2004, 104:2020-2026.
- [80]Sanz-Rodriguez F, Hidalgo A, Teixido J: Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-mediated multiple myeloma cell adhesion to CS-1/fibronectin and VCAM-1. Blood 2001, 97:346-351.
- [81]Serbina N, Pamer E: Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 2006, 7:311-317.
- [82]Shi C, Velazquez P, Hohl T, Leiner I, Dustin M, Pamer E: Monocyte trafficking to hepatic sites of bacterial infection is chemokine independent and directed by focal intercellular adhesion molecule-1 expression. J Immunol 2010, 184:6266-6274.
- [83]Jia T, Serbina NV, Brandl K, Zhong MX, Leiner IM, Charo IF, Pamer EG: Additive roles for MCP-1 and MCP-3 in CCR2-mediated recruitment of inflammatory monocytes during Listeria monocytogenes infection. J Immunol 2008, 180:6846-6853.
- [84]Engel D, Maurer J, Tittel A, Weisheit C, Cavlar T, Schumak B, Limmer A, van Rooijen N, Trautwein C, Tacke F, Kurts C: CCR2 mediates homeostatic and inflammatory release of Gr1(high) monocytes from the bone marrow, but is dispensable for bladder infiltration in bacterial urinary tract infection. J Immunol 2008, 181:5579-5586.
- [85]Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, Charo IF: Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J Clin Invest 2007, 117:902-909.
- [86]Wang Y, Cui L, Gonsiorek W, Min SH, Anilkumar G, Rosenblum S, Kozlowski J, Lundell D, Fine JS, Grant EP: CCR2 and CXCR4 regulate peripheral blood monocyte pharmacodynamics and link to efficacy in experimental autoimmune encephalomyelitis. J Inflamm (Lond) 2009, 6:32. BioMed Central Full Text
- [87]Boivin N, Menasria R, Gosselin D, Rivest S, Boivin G: Impact of deficiency in CCR2 and CX3CR1 receptors on monocytes trafficking in herpes simplex virus encephalitis. J Gen Virol 2012, 93:1294-1304.
- [88]Chen BP, Kuziel WA, Lane TE: Lack of CCR2 results in increased mortality and impaired leukocyte activation and trafficking following infection of the central nervous system with a neurotropic coronavirus. J Immunol 2001, 167:4585-4592.
- [89]Ruzek D, Salat J, Singh SK, Kopecky J: Breakdown of the blood–brain barrier during tick-borne encephalitis in mice is not dependent on CD8+ T-cells. PLoS One 2011, 6:e20472.
- [90]Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM: Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 2005, 202:1087-1098.
- [91]Glass WG, Liu MT, Kuziel WA, Lane TE: Reduced macrophage infiltration and demyelination in mice lacking the chemokine receptor CCR5 following infection with a neurotropic coronavirus. Virology 2001, 288:8-17.
- [92]Vilela MC, Mansur DS, Lacerda-Queiroz N, Rodrigues DH, Lima GK, Arantes RM, Kroon EG, Da Silva Campos MA, Teixeira MM, Teixeira AL: The chemokine CCL5 is essential for leukocyte recruitment in a model of severe Herpes simplex encephalitis. Ann N Y Acad Sci 2009, 1153:256-263.
- [93]Malik M, Chen YY, Kienzle MF, Tomkowicz BE, Collman RG, Ptasznik A: Monocyte migration and LFA-1-mediated attachment to brain microvascular endothelia is regulated by SDF-1 alpha through Lyn kinase. J Immunol 2008, 181:4632-4637.
- [94]McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS: CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol 2006, 177:8053-8064.
- [95]Peng H, Erdmann N, Whitney N, Dou H, Gorantla S, Gendelman HE, Ghorpade A, Zheng J: HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 2006, 54:619-629.
- [96]McCandless EE, Zhang B, Diamond MS, Klein RS: CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc Natl Acad Sci USA 2008, 105:11270-11275.
- [97]D'Mello C, Le T, Swain M: Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factoralpha signaling during peripheral organ inflammation. J Neurosci 2009, 29:2089-2102.
- [98]Hickman S, El Khoury J: Mechanisms of mononuclear phagocyte recruitment in Alzheimer's disease. CNS Neurol Disord Drug Targets 2010, 9:168-173.
- [99]Mildner A, Schlevogt B, Kierdorf K, Bottcher C, Erny D, Kummer MP, Quinn M, Bruck W, Bechmann I, Heneka MT, Priller J, Prinz M: Distinct and Non-Redundant Roles of Microglia and Myeloid Subsets in Mouse Models of Alzheimer's Disease. J Neurosci 2011, 31:11159-11171.
- [100]Izikson L, Klein RS, Charo IF, Weiner HL, Luster AD: Resistance to experimental autoimmune encephalomyelitis in mice lacking the CC chemokine receptor (CCR)2. J Exp Med 2000, 192:1075-1080.
- [101]Dogan RN, Elhofy A, Karpus WJ: Production of CCL2 by central nervous system cells regulates development of murine experimental autoimmune encephalomyelitis through the recruitment of TNF- and iNOS-expressing macrophages and myeloid dendritic cells. J Immunol 2008, 180:7376-7384.
- [102]Wuest TR, Carr DJ: The role of chemokines during herpes simplex virus-1 infection. Front Biosci 2008, 13:4862-4872.
- [103]Persidsky Y, Ghorpade A, Rasmussen J, Limoges J, Liu XJ, Stins M, Fiala M, Way D, Kim KS, Witte MH, Weinand M, Carhart L, Gendelman HE: Microglial and astrocyte chemokines regulate monocyte migration through the blood–brain barrier in human immunodeficiency virus-1 encephalitis. Am J Pathol 1999, 155:1599-1611.
- [104]Marques CP, Hu S, Sheng W, Lokensgard JR: Microglial cells initiate vigorous yet non-protective immune responses during HSV-1 brain infection. Virus Res 2006, 121:1-10.
- [105]Savarin C, Stohlman SA, Atkinson R, Ransohoff RM, Bergmann CC: Monocytes regulate T cell migration through the glia limitans during acute viral encephalitis. J Virol 2010, 84:4878-4888.
- [106]Held KS, Chen BP, Kuziel WA, Rollins BJ, Lane TE: Differential roles of CCL2 and CCR2 in host defense to coronavirus infection. Virology 2004, 329:251-260.
- [107]Lane TE, Hosking MP: The pathogenesis of murine coronavirus infection of the central nervous system. Crit Rev Immunol 2010, 30:119-130.
- [108]Bennett JL, Elhofy A, Charo I, Miller SD, Dal Canto MC, Karpus WJ: CCR2 regulates development of Theiler's murine encephalomyelitis virus-induced demyelinating disease. Viral Immunol 2007, 20:19-33.
- [109]Yednock TA, Cannon C, Fritz LC, Sanchez-Madrid F, Steinman L, Karin N: Prevention of experimental autoimmune encephalomyelitis by antibodies against alpha 4 beta 1 integrin. Nature 1992, 356:63-66.
- [110]Gordon EJ, Myers KJ, Dougherty JP, Rosen H, Ron Y: Both anti-CD11a (LFA-1) and anti-CD11b (MAC-1) therapy delay the onset and diminish the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 1995, 62:153-160.
- [111]Ceulemans AG, Zgavc T, Kooijman R, Hachimi-Idrissi S, Sarre S, Michotte Y: The dual role of the neuroinflammatory response after ischemic stroke: modulatory effects of hypothermia. J Neuroinflammation 2010, 7:74. BioMed Central Full Text
- [112]Persidsky Y, Buttini M, Limoges J, Bock P, Gendelman HE: An analysis of HIV-1-associated inflammatory products in brain tissue of humans and SCID mice with HIV-1 encephalitis. J Neurovirol 1997, 3:401-416.
- [113]Lewandowski G, Hobbs MV: Evidence for deficiencies in intracerebral cytokine production, adhesion molecule induction, and T cell recruitment in herpes simplex virus type-2 infected mice. J Neuroimmunol 1998, 81:58-65.
- [114]Sharma A, Bhomia M, Honnold SP, Maheshwari RK: Role of adhesion molecules and inflammation in Venezuelan equine encephalitis virus infected mouse brain. Virol J 2011, 8:197. BioMed Central Full Text
- [115]Mishra MK, Dutta K, Saheb SK, Basu A: Understanding the molecular mechanism of blood–brain barrier damage in an experimental model of Japanese encephalitis: correlation with minocycline administration as a therapeutic agent. Neurochem Int 2009, 55:717-723.
- [116]Cybulsky MI, Iiyama K, Li H, Zhu S, Chen M, Iiyama M, Davis V, Gutierrez-Ramos JC, Connelly PW, Milstone DS: A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 2001, 107:1255-1262.
- [117]Barringhaus KG, Phillips JW, Thatte JS, Sanders JM, Czarnik AC, Bennett DK, Ley KF, Sarembock IJ: Alpha4beta1 integrin (VLA-4) blockade attenuates both early and late leukocyte recruitment and neointimal growth following carotid injury in apolipoprotein E (−/−) mice. J Vasc Res 2004, 41:252-260.
- [118]Huo Y, Hafezi-Moghadam A, Ley K: Role of vascular cell adhesion molecule-1 and fibronectin connecting segment-1 in monocyte rolling and adhesion on early atherosclerotic lesions. Circ Res 2000, 87:153-159.
- [119]Henderson RB, Hobbs JA, Mathies M, Hogg N: Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 2003, 102:328-335.
- [120]Fleming JC, Bao F, Chen Y, Hamilton EF, Gonzalez-Lara LE, Foster PJ, Weaver LC: Timing and duration of anti-alpha4beta1 integrin treatment after spinal cord injury: effect on therapeutic efficacy. J Neurosurg Spine 2009, 11:575-587.
- [121]Watanabe T, Fan J: Atherosclerosis and inflammation mononuclear cell recruitment and adhesion molecules with reference to the implication of ICAM-1/LFA-1 pathway in atherogenesis. Int J Cardiol 1998, 66(1):S45-S53. discussion S55
- [122]Patel SS, Thiagarajan R, Willerson JT, Yeh ET: Inhibition of alpha4 integrin and ICAM-1 markedly attenuate macrophage homing to atherosclerotic plaques in ApoE-deficient mice. Circulation 1998, 97:75-81.
- [123]Alliot F, Godin I, Pessac B: Microglia derive from progenitors, originating from the yolk sac, and which proliferate in the brain. Brain Res Dev Brain Res 1999, 117:145-152.
- [124]Takahashi K, Naito M, Takeya M: Development and heterogeneity of macrophages and their related cells through their differentiation pathways. Pathol Int 1996, 46:473-485.
- [125]Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M: Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010, 330:841-845.
- [126]Sedgwick JD, Schwender S, Imrich H, Dorries R, Butcher GW, ter Meulen V: Isolation and direct characterization of resident microglial cells from the normal and inflamed central nervous system. Proc Natl Acad Sci USA 1991, 88:7438-7442.
- [127]Mack CL, Vanderlugt-Castaneda CL, Neville KL, Miller SD: Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler's virus model of multiple sclerosis. J Neuroimmunol 2003, 144:68-79.
- [128]Simard AR, Soulet D, Gowing G, Julien JP, Rivest S: Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006, 49:489-502.
- [129]Malm TM, Koistinaho M, Parepalo M, Vatanen T, Ooka A, Karlsson S, Koistinaho J: Bone-marrow-derived cells contribute to the recruitment of microglial cells in response to beta-amyloid deposition in APP/PS1 double transgenic Alzheimer mice. Neurobiol Dis 2005, 18:134-142.
- [130]Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hovelmeyer N, Waisman A, Rulicke T, Prinz M, Priller J, Becher B, Aguzzi A: Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med 2005, 11:146-152.
- [131]Kokovay E, Cunningham LA: Bone marrow-derived microglia contribute to the neuroinflammatory response and express iNOS in the MPTP mouse model of Parkinson's disease. Neurobiol Dis 2005, 19:471-478.
- [132]Priller J, Prinz M, Heikenwalder M, Zeller N, Schwarz P, Heppner FL, Aguzzi A: Early and rapid engraftment of bone marrow-derived microglia in scrapie. J Neurosci 2006, 26:11753-11762.
- [133]Djukic M, Mildner A, Schmidt H, Czesnik D, Bruck W, Priller J, Nau R, Prinz M: Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 2006, 129:2394-2403.
- [134]Stalder AK, Ermini F, Bondolfi L, Krenger W, Burbach GJ, Deller T, Coomaraswamy J, Staufenbiel M, Landmann R, Jucker M: Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J Neurosci 2005, 25:11125-11132.
- [135]El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD: Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 2007, 13:432-438.
- [136]Mildner A, Schmidt H, Nitsche M, Merkler D, Hanisch UK, Mack M, Heikenwalder M, Bruck W, Priller J, Prinz M: Microglia in the adult brain arise from Ly-6C(hi)CCR2(+) monocytes only under defined host conditions. Nat Neurosci 2007, 10:1544-1553.
- [137]Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM: Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 2011, 14:1142-1149.
- [138]Ajami B, Bennett JL, Krieger C, Tetzlaff W, Rossi FM: Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat Neurosci 2007, 10:1538-1543.
- [139]Robben PM, LaRegina M, Kuziel WA, Sibley LD: Recruitment of Gr-1+ monocytes is essential for control of acute toxoplasmosis. J Exp Med 2005, 201:1761-1769.
- [140]Dunay IR, Fuchs A, Sibley LD: Inflammatory monocytes but not neutrophils are necessary to control infection with Toxoplasma gondii in mice. Infect Immun 2010, 78:1564-1570.
- [141]Serbina NV, Salazar-Mather TP, Biron CA, Kuziel WA, Pamer EG: TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003, 19:59-70.
- [142]Osterholzer JJ, Curtis JL, Polak T, Ames T, Chen GH, McDonald R, Huffnagle GB, Toews GB: CCR2 mediates conventional dendritic cell recruitment and the formation of bronchovascular mononuclear cell infiltrates in the lungs of mice infected with Cryptococcus neoformans. J Immunol 2008, 181:610-620.
- [143]Traynor TR, Kuziel WA, Toews GB, Huffnagle GB: CCR2 expression determines T1 versus T2 polarization during pulmonary Cryptococcus neoformans infection. J Immunol 2000, 164:2021-2027.
- [144]Ye Z, Uittenbogaard AM, Cohen DA, Kaplan AM, Ambati J, Straley SC: Distinct CCR2(+) Gr1(+) cells control growth of the Yersinia pestis DeltayopM mutant in liver and spleen during systemic plague. Infect Immun 2011, 79:674-687.
- [145]Iijima N, Mattei LM, Iwasaki A: Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc Natl Acad Sci USA 2011, 108:284-289.
- [146]Sheahan T, Morrison TE, Funkhouser W, Uematsu S, Akira S, Baric RS, Heise MT: MyD88 is required for protection from lethal infection with a mouse-adapted SARS-CoV. PLoS Pathog 2008, 4:e1000240.
- [147]Martinat C, Mena I, Brahic M: Theiler's virus infection of primary cultures of bone marrow-derived monocytes/macrophages. J Virol 2002, 76:12823-12833.
- [148]Lipton HL, Twaddle G, Jelachich ML: The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus-induced demyelinating disease. J Virol 1995, 69:2525-2533.
- [149]Clatch RJ, Miller SD, Metzner R, Dal Canto MC, Lipton HL: Monocytes/macrophages isolated from the mouse central nervous system contain infectious Theiler's murine encephalomyelitis virus (TMEV). Virology 1990, 176:244-254.
- [150]Blakemore WF, Welsh CJ, Tonks P, Nash AA: Observations on demyelinating lesions induced by Theiler's virus in CBA mice. Acta Neuropathol 1988, 76:581-589.
- [151]Aubert C, Chamorro M, Brahic M: Identification of Theiler's virus infected cells in the central nervous system of the mouse during demyelinating disease. Microb Pathog 1987, 3:319-326.
- [152]Wang H, Sun J, Goldstein H: Human immunodeficiency virus type 1 infection increases the in vivo capacity of peripheral monocytes to cross the blood–brain barrier into the brain and the in vivo sensitivity of the blood–brain barrier to disruption by lipopolysaccharide. J Virol 2008, 82:7591-7600.
- [153]Drevets DA, Dillon MJ, Schawang JS, Van Rooijen N, Ehrchen J, Sunderkotter C, Leenen PJ: The Ly-6Chigh monocyte subpopulation transports Listeria monocytogenes into the brain during systemic infection of mice. J Immunol 2004, 172:4418-4424.
- [154]Drevets D, Dillon M, Schawang J, Stoner J, Leenen P: IFN-gamma triggers CCR2-independent monocyte entry into the brain during systemic infection by virulent Listeria monocytogenes. Brain Behav Immun 2010, 24:919-929.
- [155]Charlier C, Nielsen K, Daou S, Brigitte M, Chretien F, Dromer F: Evidence of a role for monocytes in dissemination and brain invasion by Cryptococcus neoformans. Infect Immun 2009, 77:120-127.
- [156]Courret N, Darche S, Sonigo P, Milon G, Buzoni-Gatel D, Tardieux I: CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 2006, 107:309-316.
- [157]Schilling M, Strecker JK, Ringelstein EB, Schabitz WR, Kiefer R: The role of CC chemokine receptor 2 on microglia activation and blood-borne cell recruitment after transient focal cerebral ischemia in mice. Brain Res 2009, 1289:79-84.
- [158]Schilling M, Strecker JK, Schabitz WR, Ringelstein EB, Kiefer R: Effects of monocyte chemoattractant protein 1 on blood-borne cell recruitment after transient focal cerebral ischemia in mice. Neuroscience 2009, 161:806-812.
- [159]Semple BD, Bye N, Rancan M, Ziebell JM, Morganti-Kossmann MC: Role of CCL2 (MCP-1) in traumatic brain injury (TBI): evidence from severe TBI patients and CCL2−/− mice. J Cereb Blood Flow Metab 2010, 30:769-782.
- [160]Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ: CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J Exp Med 2000, 192:899-905.
- [161]Kennedy KJ, Strieter RM, Kunkel SL, Lukacs NW, Karpus WJ: Acute and relapsing experimental autoimmune encephalomyelitis are regulated by differential expression of the CC chemokines macrophage inflammatory protein-1alpha and monocyte chemotactic protein-1. J Neuroimmunol 1998, 92:98-108.