Transgenic CCL2 expression in the central nervous system results in a dysregulated immune response and enhanced lethality after coronavirus infection

Journal of Virology

Volumn 87, Issue 5, 2013, Pages 2376-2389

  Trujillo, Jonathan A ^a   Fleming, Erica L ^a   Perlmana, Stanley ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CORONAVIRUS INFECTION; CYTOKINE RESPONSE; DEMYELINATING DISEASE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; IMMUNOREGULATION; INNATE IMMUNITY; LETHALITY; MACROPHAGE ACTIVATION; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRAL CLEARANCE; VIRUS ENCEPHALITIS; VIRUS IMMUNITY; VIRUS STRAIN; WILD TYPE;

ANIMALS; ANTIGENS, CD40; ANTIGENS, CD86; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINE CCL2; CORONAVIRUS INFECTIONS; DOXORUBICIN; FORKHEAD TRANSCRIPTION FACTORS; HISTOCOMPATIBILITY ANTIGENS CLASS II; IMMUNOSUPPRESSION; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; MURINE HEPATITIS VIRUS; NITRIC OXIDE;

EID: 84874737246     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03089-12     Document Type: Article

References (55)

1. Deshmane SL, Kremlev S, Amini S, Sawaya BE. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29:313-326.
2. -/- mice. J. Cereb. Blood Flow Metab. 30:769-782.
3. Semple BD, Kossmann T, Morganti-Kossmann MC. 2010. Role of chemokines in CNS health and pathology: a focus on the CCL2/CCR2 and CXCL8/CXCR2 networks. J. Cereb. Blood Flow Metab. 30:459-473.
4. Chen Y, Hallenbeck JM, Ruetzler C, Bol D, Thomas K, Berman NE, Vogel SN. 2003. Overexpression of monocyte chemoattractant protein 1 in the brain exacerbates ischemic brain injury and is associated with recruitment of inflammatory cells. J. Cereb. Blood Flow Metab. 23:748-755.
5. Mahad DJ, Ransohoff RM. 2003. The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin. Immunol. 15:23-32.
6. Bennett JL, Elhofy A, Canto MC, Tani M, Ransohoff RM, Karpus WJ. 2003. CCL2 transgene expression in the central nervous system directs diffuse infiltration of CD45high CD11b+ monocytes and enhanced Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Neurovirol. 9:623-636.
7. Getts DR, Terry RL, Getts MT, Muller M, Rana S, Shrestha B, Radford J, Van Rooijen N, Campbell IL, King NJ. 2008. Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J. Exp. Med. 205:2319-2337.
8. Leuschner F, Dutta P, Gorbatov R, Novobrantseva TI, Donahoe JS, Courties G, Lee KM, Kim JI, Markmann JF, Marinelli B, Panizzi P, Lee WW, Iwamoto Y, Milstein S, Epstein-Barash H, Cantley W, Wong J, Cortez-Retamozo V, Newton A, Love K, Libby P, Pittet MJ, Swirski FK, Koteliansky V, Langer R, Weissleder R, Anderson DG, Nahrendorf M. 2011. Therapeutic siRNA silencing in inflammatory monocytes in mice. Nat. Biotechnol. 29:1005-1010.
9. Izikson L, Klein RS, Luster AD, Weiner HL. 2002. Targeting monocyte recruitment in CNS autoimmune disease. Clin. Immunol. 103:125-131.
10. Kiyota T, Yamamoto M, Schroder B, Jacobsen MT, Swan RJ, Lambert MP, Klein WL, Gendelman HE, Ransohoff RM, Ikezu T. 2009. AAV1/2-mediated CNS gene delivery of dominant-negative CCL2 mutant suppresses gliosis, beta-amyloidosis, and learning impairment of APP/PS1 mice. Mol. Ther. 17:803-809.
11. Chensue SW, Warmington KS, Ruth JH, Sanghi PS, Lincoln P, Kunkel SL. 1996. Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J. Immunol. 157:4602-4608.
12. Luther SA, Cyster JG. 2001. Chemokines as regulators of T cell differentiation. Nat. Immunol. 2:102-107.
13. Huang DR, Wang J, Kivisakk P, Rollins BJ, Ransohoff RM. 2001. Absence of monocyte chemoattractant protein 1 in mice leads to decreased local macrophage recruitment and antigen-specific T helper cell type 1 immune response in experimental autoimmune encephalomyelitis. J. Exp. Med. 193:713-726.
14. Fife BT, Huffnagle GB, Kuziel WA, Karpus WJ. 2000. CC chemokine receptor 2 is critical for induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 192:899-905.
15. Gu L, Tseng S, Horner RM, Tam C, Loda M, Rollins BJ. 2000. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404:407-411.
16. Zisman DA, Kunkel SL, Strieter RM, Tsai WC, Bucknell K, Wilkowski J, Standiford TJ. 1997. MCP-1 protects mice in lethal endotoxemia. J. Clin. Invest. 99:2832-2836.
17. Kriegel MA, Rathinam C, Flavell RA. 2012. Pancreatic islet expression of chemokine CCL2 suppresses autoimmune diabetes via tolerogenic CD11c+ CD11b+ dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 109:3457-3462.
18. Elhofy A, Wang J, Tani M, Fife BT, Kennedy KJ, Bennett J, Huang D, Ransohoff RM, Karpus WJ. 2005. Transgenic expression of CCL2 in the central nervous system prevents experimental autoimmune encephalomyelitis. J. Leukoc. Biol. 77:229-237.
19. Lane TE, Asensio VC, Yu N, Paoletti AD, Campbell IL, Buchmeier MJ. 1998. Dynamic regulation of alpha-and beta-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J. Immunol. 160:970-978.
20. Held KS, Chen BP, Kuziel WA, Rollins BJ, Lane TE. 2004. Differential roles of CCL2 and CCR2 in host defense to coronavirus infection. Virology 329:251-260.
21. Savarin C, Stohlman SA, Atkinson R, Ransohoff RM, Bergmann CC. 2010. Monocytes regulate T cell migration through the glia limitans during acute viral encephalitis. J. Virol. 84:4878-4888.
22. Chen BP, Kuziel WA, Lane TE. 2001. 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. 167:4585-4592.
23. Fuentes ME, Durham SK, Swerdel MR, Lewin AC, Barton DS, Megill JR, Bravo R, Lira SA. 1995. Controlled recruitment of monocytes and macrophages to specific organs through transgenic expression of monocyte chemoattractant protein-1. J. Immunol. 155:5769-5776.
24. Bergmann CC, Lane TE, Stohlman SA. 2006. Coronavirus infection of the central nervous system: host-virus stand-off. Nat. Rev. Microbiol. 4:121-132.
25. Dandekar AA, Wu GF, Pewe L, Perlman S. 2001. Axonal damage is T cell mediated and occurs concomitantly with demyelination in mice infected with a neurotropic coronavirus. J. Virol. 75:6115-6120.
26. Wu GF, Perlman S. 1999. Macrophage infiltration, but not apoptosis, is correlated with immune-mediated demyelination following murine infection with a neurotropic coronavirus. J. Virol. 73:8771-8780.
27. -/- mice infected with a neurotropic coronavirus. J. Virol. 79:7113-7120.
28. Perlman S, Schelper R, Bolger E, Ries D. 1987. Late onset, symptomatic, demyelinating encephalomyelitis in mice infected with MHV-JHM in the presence of maternal antibody. Microb. Pathog. 2:185-194.
29. Zhao J, Zhao J, Perlman S. 2009. De novo recruitment of antigenexperienced and naive T cells contributes to the long-term maintenance of antiviral T cell populations in the persistently infected central nervous system. J. Immunol. 183:5163-5170.
30. Wu GF, Dandekar AA, Pewe L, Perlman S. 2000. CD4 and CD8 T cells have redundant but not identical roles in virus-induced demyelination. J. Immunol. 165:2278-2286.
31. Zhou H, Perlman S. 2006. Preferential infection of mature dendritic cells by mouse hepatitis virus strain JHM. J. Virol. 80:2506-2514.
32. Kruse N, Pette M, Toyka K, Rieckmann P. 1997. Quantification of cytokine mRNA expression by RT-PCR in samples of previously frozen blood. J. Immunol. Methods 210:195-203.
33. Furtado GC, Pina B, Tacke F, Gaupp S, van Rooijen N, Moran TM, Randolph GJ, Ransohoff RM, Chensue SW, Raine CS, Lira SA. 2006. A novel model of demyelinating encephalomyelitis induced by monocytes and dendritic cells. J. Immunol. 177:6871-6879.
34. Ransohoff RM, Engelhardt B. 2012. The anatomical and cellular basis of immune surveillance in the central nervous system. Nat. Rev. Immunol. 12:623-635.
35. Bradford BM, Sester DP, Hume DA, Mabbott NA. 2011. Defining the anatomical localization of subsets of the murine mononuclear phagocyte system using integrin alpha X (Itgax, CD11c) and colony-stimulating factor 1 receptor (Csf1r, CD115) expression fails to discriminate dendritic cells from macrophages. Immunobiology 216:1228-1237.
36. Drutman SB, Kendall JC, Trombetta ES. 2012. Inflammatory spleen monocytes can upregulate CD11c expression without converting into dendritic cells. J. Immunol. 188:3603-3610.
37. Bennett CL, Clausen BE. 2007. DC ablation in mice: promises, pitfalls, and challenges. Trends Immunol. 28:525-531.
38. Stoermer KA, Burrack A, Oko L, Montgomery SA, Borst LB, Gill RG, Morrison TE. 2012. Genetic ablation of arginase 1 in macrophages and neutrophils enhances clearance of an arthritogenic alphavirus. J. Immunol. 189:4047-4059.
39. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, Henao-Tamayo M, Basaraba RJ, Konig T, Schleicher U, Koo MS, Kaplan G, Fitzgerald KA, Tuomanen EI, Orme IM, Kanneganti TD, Bogdan C, Wynn TA, Murray PJ. 2008. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 9:1399-1406.
40. Martinez FO, Helming L, Gordon S. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27:451-483.
41. Bronte V, Zanovello P. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5:641-654.
42. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. 1998. Macrophagederived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J. Immunol. 160:5729-5734.
43. Huehn J, Hamann A. 2005. Homing to suppress: address codes for Treg migration. Trends Immunol. 26:632-636.
44. Geissmann F, Jung S, Littman DR. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82.
45. Anghelina D, Zhao J, Trandem K, Perlman S. 2009. Role of regulatory T cells in coronavirus-induced acute encephalitis. Virology 385:358-367.
46. Vass K, Lassmann H. 1990. Intrathecal application of interferon gamma. Progressive appearance of MHC antigens within the rat nervous system. Am. J. Pathol. 137:789-800.
47. Trandem K, Anghelina D, Zhao J, Perlman S. 2010. Regulatory T cells inhibit T cell proliferation and decrease demyelination in mice chronically infected with a coronavirus. J. Immunol. 184:4391-4400.
48. Zhao J, Zhao J, Fett C, Trandem K, Fleming E, Perlman S. 2011. IFN-gamma-and IL-10-expressing virus epitope-specific Foxp3+ T reg cells in the central nervous system during encephalomyelitis. J. Exp. Med. 208:1571-1577.
49. Li S, Gowans EJ, Chougnet C, Plebanski M, Dittmer U. 2008. Natural regulatory T cells and persistent viral infection. J. Virol. 82:21-30.
50. Gabrilovich DI, Nagaraj S. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9:162-174.
51. Mazzoni A, Bronte V, Visintin A, Spitzer JH, Apolloni E, Serafini P, Zanovello P, Segal DM. 2002. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 168:689-695.
52. Kusmartsev S, Gabrilovich DI. 2005. STAT1 signaling regulates tumorassociated macrophage-mediated T cell deletion. J. Immunol. 174:4880-4891.
53. Daley-Bauer LP, Wynn GM, Mocarski ES. 2012. Cytomegalovirus impairs antiviral CD8+ T cell immunity by recruiting inflammatory monocytes. Immunity 37:122-133.
54. Chang NC, Hung SI, Hwa KY, Kato I, Chen JE, Liu CH, Chang AC. 2001. A macrophage protein, Ym1, transiently expressed during inflammation is a novel mammalian lectin. J. Biol. Chem. 276:17497-17506.
55. Liu Q, Cheng LI, Yi L, Zhu N, Wood A, Changpriroa CM, Ward JM, Jackson SH. 2009. p47phox deficiency induces macrophage dysfunction resulting in progressive crystalline macrophage pneumonia. Am. J. Pathol. 174:153-163.