Central neuroinvasion and demyelination by inflammatory macrophages after peripheral virus infection is controlled by SHP-1

Viral Immunology

Volumn 22, Issue 6, 2009, Pages 371-387

  Christophi, George P ^a   Massa, Paul T ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN TYROSINE PHOSPHATASE SHP 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; BLOOD; BRAIN; CELL INVASION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEMYELINATION; DISEASE SEVERITY; ENZYME DEFECT; MACROPHAGE; MOLECULE; MONOCYTE; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; PARALYSIS; PROTEIN EXPRESSION; VIRUS INFECTION; VIRUS LOAD;

ANIMALS; CARDIOVIRUS INFECTIONS; CENTRAL NERVOUS SYSTEM; CHEMOKINE CCL2; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; CLODRONIC ACID; CYTOKINES; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; INJECTIONS, INTRAPERITONEAL; MACROPHAGES; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MICE, MUTANT STRAINS; PARALYSIS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; THEILOVIRUS; VIRAL LOAD; VIRUS REPLICATION;

MUS; THEILER'S ENCEPHALOMYELITIS VIRUS;

EID: 71449120488     PISSN: 08828245     EISSN: None     Source Type: Journal    
DOI: 10.1089/vim.2009.0052     Document Type: Article

References (94)

1. Alliot F, Rutin J, and Pessac B: Ly-6C is expressed in brain vessels endothelial cells but not in microglia of the mouse. Neurosci Lett 1998;251:37-40.
2. Amour A, Knight CG, English WR, et al.: The enzymatic activity of ADAM8 and ADAM9 is not regulated by TIMPs. FEBS Lett 2002;524:154-158.
3. Aubert C, Chamorro M, and 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.
4. Babcock AA, Kuziel WA, Rivest S, and Owens T: Chemokine expression by glial cells directs leukocytes to sites of axonal injury in the CNS. J Neurosci 2003;23:7922-7930.
5. Bauer J, Huitinga I, Zhao W, LassmannH, Hickey WF, and Dijkstra CD: The role of macrophages, perivascular cells, and microglial cells in the pathogenesis of experimental autoimmune encephalomyelitis. Glia 1995;15:437-446.
6. Bennett JL, Elhofy A, Canto MC, Tani M, Ransohoff RM, and Karpus WJ: CCL2 transgene expression in the central nervous system directs diffuse infiltration of CD45(high) CD11b(+) monocytes and enhanced Theiler's murine encephalomyelitis virus-induced demyelinating disease. JNeurovirol 2003;9:623-636.
7. Bennett JL, Elhofy A, Charo I, Miller SD, Dal Canto MC, and Karpus WJ: CCR2 regulates development of Theiler's murine encephalomyelitis virus-induced demyelinating disease. Viral Immunol 2007;20:19-33.
8. Biewenga J, van der Ende MB, Krist LF, Borst A, Ghufron M, and van Rooijen N: Macrophage depletion in the rat after intraperitoneal administration of liposome-encapsulated clodronate: depletion kinetics and accelerated repopulation of peritoneal and omental macrophages by administration of Freund's adjuvant. Cell Tissue Res 1995;280:189-196.
9. Blakemore WF, Welsh CJ, Tonks P, and Nash AA: Observations on demyelinating lesions induced by Theiler's virus in CBA mice. Acta Neuropathol 1988;76:581-589.
10. Boltz-Nitulescu G, Wiltschke C, Holzinger C, Fellinger A, Scheiner O, Gessl A, and Forster O: Differentiation of rat bone marrow cells into macrophages under the influence of mouse L929 cell supernatant. J Leukoc Biol 1987;41:83-91.
11. Bonaparte KL, Hudson CA, Wu C, and Massa PT: Inverse regulation of inducible nitric oxide synthase (iNOS) and arginase I by the protein tyrosine phosphatase SHP-1 in CNS glia. Glia 2006;53:827-835.
12. Bonetti B, Stegagno C, Cannella B, Rizzuto N, Moretto G, and Raine CS: Activation of NF-kappaB and c-jun transcription factors in multiple sclerosis lesions. Implications for oligodendrocyte pathology. Am J Pathol 1999;155:1433-1438.
13. Brahic M, Bureau JF, and Michiels T: The genetics of the persistent infection and demyelinating disease caused by Theiler's virus. Annu Rev Microbiol 2005;59:279-298.
14. Breij EC, Brink BP, Veerhuis R, et al.: Homogeneity of active demyelinating lesions in established multiple sclerosis. Ann Neurol 2008;63:16-25.
15. Bruck W, Porada P, Poser S, Rieckmann P, Hanefeld F, Kretzschmar HA, and Lassmann H: Monocyte/macrophage differentiation in early multiple sclerosis lesions. Ann Neurol 1995;38:788-796.
16. Bruck W, Sommermeier N, Bergmann M, Zettl U, Goebel HH, Kretzschmar HA, and Lassmann H: Macrophages in multiple sclerosis. Immunobiology 1996;195:588-600.
17. Christophi GP. Hudson CA, Gruber R, Christophi CP, and Massa PT: Promoter-specific induction of the phosphatase SHP-1 by viral infection and cytokines in CNS glia. J Neurochem 2008;105:2511-2523.
18. Christophi GP, Hudson CA, Panos M, Gruber RC, and Massa PT: Modulation of macrophage infiltration and inflammatory activity by the phosphatase SHP-1 in virusinduced demyelinating disease. J Virol 2009;83:522-539.
19. Christophi GP, Isackson PJ, Blaber S, Blaber M, Rodriguez M, and Scarisbrick IA: Distinct promoters regulate tissuespecific and differential expression of kallikrein 6 in CNS demyelinating disease. J Neurochem 2004;91:1439-1449.
20. Christophi GP, Panos M, Hudson CA, et al.: Macrophages of multiple sclerosis patients display deficient SHP-1 expression and enhanced inflammatory phenotype. Lab Invest 2009;89:742-759.
21. Christophi GP, Panos M, Hudson CA, Tsikkou C, Mihai C, Mejico LJ, Jubelt B, and Massa PT: Interferon-beta treatment in multiple sclerosis attenuates inflammatory gene expression through inducible activity of the phosphatase SHP-1. Clinical Immunology 2009;133:27-44.
22. Clatch RJ, Lipton HL, and Miller SD: Characterization of Theiler's murine encephalomyelitis virus (TMEV)-specific delayed-type hypersensitivity responses in TMEV-induced demyelinating disease: correlation with clinical signs. J Immunol 1986;136:920-927.
23. Clatch RJ, Miller SD, Metzner R, Dal Canto MC, and Lipton HL: Monocytes/macrophages isolated from the mouse central nervous system contain infectious Theiler's murine encephalomyelitis virus (TMEV). Virology 1990;176:244-254.
24. Croker BA, Lawson BR, Berger M, et al.: Inflammation and autoimmunity caused by a SHP1 mutation depend on IL-1, MyD88, and a microbial trigger. Proc Natl Acad Sci USA 2008;105:15028-15033.
25. Cua DJ, Hinton DR, Kirkman L, and Stohlman SA: Macrophages regulate induction of delayed-type hypersensitivity and experimental allergic encephalomyelitis in SJL mice. Eur J Immunol 1995;25:2318-2324.
26. Dal Canto MC, Kim BS, Miller SD, and Melvold RW: Theiler's murine encephalomyelitis virus (TMEV)-induced demyelination: A model for human multiple sclerosis. Methods 1996;10:453-461.
27. Dal Canto MC, and Lipton HL: Ultrastructural immunohistochemical localization of virus in acute and chronic demyelinating Theiler's virus infection. Am J Pathol 1982;106: 20-29.
28. David M, Chen HE, Goelz S, Larner AC, and Neel BG: Differential regulation of the alpha/beta interferon-stimulated Jak/Stat pathway by the SH2 domain-containing tyrosine phosphatase SHPTP1. Mol Cell Biol 1995;15:7050-7058.
29. Dogan RN, and Karpus WJ: Chemokines and chemokine receptors in autoimmune encephalomyelitis as a model for central nervous system inflammatory disease regulation. Front Biosci 2004;9:1500-1505.
30. Drescher KM, and Sosnowska D: Being a mouse in a man's world: what TMEV has taught us about human disease. Front Biosci 2008;13:3775-3785.
31. Forget G, Matte C, Siminovitch KA, Rivest S, Pouliot P, and Olivier M: Regulation of the Leishmania-induced innate inflammatory response by the protein tyrosine phosphatase SHP-1. Eur J Immunol 2005;35:1906-1917.
32. Frohman EM, Racke MK, and Raine CS: Multiple sclerosis- the plaque and its pathogenesis. N Engl J Med 2006;354:942-955.
33. Getts DR, Terry RL, Getts MT, et al.: Ly6c+"inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med 2008;205:2319-2337.
34. Gveric D, Kaltschmidt C, Cuzner ML, and Newcombe J: Transcription factor NF-kappaB and inhibitor I kappaBalpha are localized in macrophages in active multiple sclerosis lesions. J Neuropathol Exp Neurol 1998;57:168-178.
35. Ha-Lee YM, Dillon K, Kosaras B, Sidman R, Revell P, Fujinami R, and Chow M: Mode of spread to and within the central nervous system after oral infection of neonatal mice with the DA strain of Theiler's murine encephalomyelitis virus. J Virol 1995;69:7354-7361.
36. Hanson EM, Dickensheets H, Qu CK, Donnelly RP, and Keegan AD: Regulation of the dephosphorylation of Stat6. Participation of Tyr-713 in the interleukin-4 receptor alpha, the tyrosine phosphatase SHP-1, and the proteasome. J Biol Chem 2003;278:3903-3911.
37. Hendriks JJ, Teunissen CE, de Vries HE, and Dijkstra CD: Macrophages and neurodegeneration. Brain Res Brain Res Rev 2005;48:185-195.
38. Huang ZY, Hunter S, Kim MK, Indik ZK, and Schreiber AD: The effect of phosphatases SHP-1 and SHIP-1 on signaling by the ITIM- and ITAM-containing Fcgamma receptors FcgammaRIIB and FcgammaRIIA. J Leukoc Biol 2003;73: 823-829.
39. Huitinga I, Damoiseaux JG, van Rooijen N, Dopp EA, and Dijkstra CD: Liposome mediated affection of monocytes. Immunobiology 1992;185:11-19.
40. Huitinga I, Ruuls SR, Jung S, Van Rooijen N, Hartung HP, and Dijkstra CD: Macrophages in T cell line-mediated, demyelinating, and chronic relapsing experimental autoimmune encephalomyelitis in Lewis rats. Clin Exp Immunol 1995;100:344-351.
41. Ito A, Suganami T, Yamauchi A, et al.: Role of CC chemokine receptor 2 in bone marrow cells in the recruitment of macrophages into obese adipose tissue. J Biol Chem 2008;283: 35715-35723.
42. Izikson L, Klein RS, Luster AD, and Weiner HL: Targeting monocyte recruitment in CNS autoimmune disease. Clin Immunol 2002;103:125-131.
43. Kant AM, De P, Peng X, Yi T, Rawlings DJ, Kim JS, and Durden DL: SHP-1 regulates Fcgamma receptor-mediated phagocytosis and the activation of RAC. Blood 2002;100: 1852-1859.
44. Karpus WJ, Kennedy KJ, Fife BT, Bennett JL, Dal Canto MC, Kunkel SL, and Lukacs NW: Anti-CCL2 treatment inhibits Theiler's murine encephalomyelitis virus-induced demyelinating disease. J Neurovirol 2006;12:251-261.
45. Khaled AR, Butfiloski EJ, Sobel ES, and Schiffenbauer J: Functional consequences of the SHP-1 defect in motheaten viable mice: role of NF-kappa B. Cell Immunol 1998;185:49-58.
46. Kim CH, Qu CK, Hangoc G, Cooper S, Anzai N, Feng GS, and Broxmeyer HE: Abnormal chemokine-induced responses of immature and mature hematopoietic cells from motheaten mice implicate the protein tyrosine phosphatase SHP-1 in chemokine responses. J Exp Med 1999;190:681-690.
47. Kim WK, Corey S, Alvarez X, and Williams K: Monocyte/macrophage traffic in HIV and SIV encephalitis. J Leukoc Biol 2003;74:650-656.
48. Kornek B, and Lassmann H: Neuropathology of multiple sclerosis-new concepts. Brain Res Bull 2003;61:321-326.
49. Lipton HL, and Dal Canto MC: Chronic neurologic disease in Theiler's virus infection of SJL/J mice. J Neurol Sci 1976; 30:201-207.
50. Lipton HL, and Jelachich ML: Molecular pathogenesis of Theiler's murine encephalomyelitis virus-induced demyelinating disease in mice. Intervirology 1997;40:143-152.
51. Lipton HL, Kallio P, and Jelachich ML: Simplified quantitative analysis of spinal cord cells from Theiler's virusinfected mice without the requirement for myelin debris removal. J Immunol Methods 2005;299:107-115.
52. Lipton HL, Kumar AS, and Trottier M: Theiler's virus persistence in the central nervous system of mice is associated with continuous viral replication and a difference in outcome of infection of infiltrating macrophages versus oligodendrocytes. Virus Res 2005;111:214-223.
53. Lipton HL, Liang Z, Hertzler S, and Son KN: A specific viral cause of multiple sclerosis: one virus, one disease. Ann Neurol 2007;61:514-523.
54. Lipton HL, Twaddle G, and 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.
55. Lucchinetti C, Bruck W, Parisi J, Scheithauer B, Rodriguez M, and Lassmann H: Heterogeneity of multiple sclerosis lesions: implications for the pathogenesis of demyelination. Ann Neurol 2000;47:707-717.
56. Mahad DJ, and Ransohoff RM: The role of MCP-1 (CCL2) and CCR2 in multiple sclerosis and experimental autoimmune encephalomyelitis (EAE). Semin Immunol 2003;15:23-32.
57. Man S, Ubogu EE, and Ransohoff RM: Inflammatory cell migration into the central nervous system: a few new twists on an old tale. Brain Pathol 2007;17:243-250.
58. Martin AP, Rankin S, Pitchford S, Charo IF, Furtado GC, and Lira SA: Increased expression of CCL2 in insulin-producing cells of transgenic mice promotes mobilization of myeloid cells from the bone marrow, marked insulitis, and diabetes. Diabetes 2008;57:3025-3033.
59. Martinat C, Mena I, and Brahic M: Theiler's virus infection of primary cultures of bone marrow-derived monocytes/ macrophages. J Virol 2002;76:12823-12833.
60. Massa PT, Ropka SL, Saha S, Fecenko KL, and Beuler KL: Critical role for protein tyrosine phosphatase SHP-1 in controlling infection of central nervous system glia and demyelination by Theiler's murine encephalomyelitis virus. J Virol 2002;76:8335-8346.
61. Massa PT, and Wu C: Increased inducible activation of NFkappaB and responsive genes in astrocytes deficient in the protein tyrosine phosphatase SHP-1. J Interferon Cytokine Res 1998;18:499-507.
62. Massa PT, and Wu C: The role of protein tyrosine phosphatase SHP-1 in the regulation of IFN-gamma signaling in neural cells. J Immunol 1996;157:5139-5144.
63. McManus C, Berman JW, Brett FM, Staunton H, Farrell M, and Brosnan CF: MCP-1, MCP-2 and MCP-3 expression in multiple sclerosis lesions: an immunohistochemical and in situ hybridization study. J Neuroimmunol 1998;86:20-29.
64. Mena I, Roussarie JP, and Brahic M: Infection of macrophage primary cultures by persistent and nonpersistent strains of Theiler's virus: role of capsid and noncapsid viral determinants. J Virol 2004;78:13356-13361.
65. Munz C, Lunemann JD, Getts MT, and Miller SD: Antiviral immune responses: triggers of or triggered by autoimmunity? Nat Rev Immunol 2009;9:246-258.
66. Noseworthy JH, Lucchinetti C, Rodriguez M, and Weinshenker BG: Multiple sclerosis. N Engl J Med 2000;343:938-952.
67. Oldenborg PA, Gresham HD, and Lindberg FP: CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med 2001;193:855-862.
68. Oleszak EL, Chang JR, Friedman H, Katsetos CD, and Platsoucas CD: Theiler's virus infection: a model for multiple sclerosis. Clin Microbiol Rev 2004;17:174-207.
69. Pelchen-Matthews A, Kramer B, and Marsh M: Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 2003;162:443-455.
70. Polfliet MM, Goede PH, van Kesteren-Hendrikx EM, van Rooijen N, Dijkstra CD, and van den Berg TK: A method for the selective depletion of perivascular and meningeal macrophages in the central nervous system. J Neuroimmunol 2001;116:188-195. (Pubitemid 32588631)
71. Ren W, Markel DC, Schwendener R, Ding Y, Wu B, and Wooley PH: Macrophage depletion diminishes implantwear- induced inflammatory osteolysis in a mouse model. J Biomed Mater Res A 2008;85:1043-1051.
72. Richens J, Fairclough L, Ghaemmaghami AM, Mahdavi J, Shakib F, and Sewell HF: The detection of ADAM8 protein on cells of the human immune system and the demonstration of its expression on peripheral blood B cells, dendritic cells and monocyte subsets. Immunobiology 2007;212:29-38.
73. Rios M, Zhang MJ, Grinev A, et al.: Monocytes-macrophages are a potential target in human infection with West Nile virus through blood transfusion. Transfusion 2006;46:659-667.
74. Rodriguez M: Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathol 2007;17:219-229.
75. Rodriguez M, Leibowitz JL, and Lampert PW: Persistent infection of oligodendrocytes in Theiler's virus-induced encephalomyelitis. Ann Neurol 1983;13:426-433.
76. Rosenthal A, Fujinami RS, and Lampert PW: Mechanism of Theiler's virus-induced demyelination in nude mice. Lab Invest 1986;54:515-522.
77. Rossi CP, Delcroix M, Huitinga I, McAllister A, van Rooijen N, Claassen E, and Brahic M: Role of macrophages during Theiler's virus infection. J Virol 1997;71:3336-3340.
78. Scarisbrick IA, Blaber SI, Lucchinetti CF, Genain CP, Blaber M, and Rodriguez M: Activity of a newly identified serine protease in CNS demyelination. Brain 2002;125:1283-1296.
79. Scarisbrick IA, Linbo R, Vandell AG, et al.: Kallikreins are associated with secondary progressive multiple sclerosis and promote neurodegeneration. Biol Chem 2008;389:739-745.
80. Schlitt BP, Felrice M, Jelachich ML, and Lipton HL: Apoptotic cells, including macrophages, are prominent in Theiler's virus-induced inflammatory, demyelinating lesions. J Virol 2003;77:4383-4388.
81. Simpson JE, Newcombe J, Cuzner ML, and Woodroofe MN: Expression of monocyte chemoattractant protein-1 and other beta-chemokines by resident glia and inflammatory cells in multiple sclerosis lesions. J Neuroimmunol 1998;84: 238-249.
82. Su D, and Van Rooijen N: The role of macrophages in the immunoadjuvant action of liposomes: effects of elimination of splenic macrophages on the immune response against intravenously injected liposome-associated albumin antigen. Immunology 1989;66:466-470.
83. Sunderkotter C, Nikolic T, Dillon MJ, Van Rooijen N, Stehling M, Drevets DA, and Leenen PJ: Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J Immunol 2004;172:4410-4417.
84. Templeton SP, Kim TS, O'Malley K, and Perlman S: Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathol 2008;18:40-51.
85. Templeton SP, and Perlman S: Pathogenesis of acute and chronic central nervous system infection with variants of mouse hepatitis virus, strain JHM. Immunol Res 2007;39: 160-172.
86. Theiler M: Spontaneous encephalomyelitis of mice-a new virus disease. Science 1934;80:122.
87. Tran EH, Hoekstra K, van Rooijen N, Dijkstra CD, and Owens T: Immune invasion of the central nervous system parenchyma and experimental allergic encephalomyelitis, but not leukocyte extravasation from blood, are prevented in macrophage-depleted mice. J Immunol 1998;161:3767-3775.
88. Trebst C, Sorensen TL, Kivisakk P, et al.: CCR1+/ CCR5+ mononuclear phagocytes accumulate in the central nervous system of patients with multiple sclerosis. Am J Pathol 2001;159:1701-1710.
89. Tsou CL, Peters W, Si Y, Slaymaker S, Aslanian AM, Weisberg SP, Mack M, and 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.
90. Ubogu EE, Cossoy MB, and Ransohoff RM: The expression and function of chemokines involved in CNS inflammation. Trends Pharmacol Sci 2006;27:48-55.
91. van der Goes A, Boorsma W, Hoekstra K, Montagne L, de Groot CJ, and Dijkstra CD: Determination of the sequential degradation of myelin proteins by macrophages. J Neuroimmunol 2005;161:12-20.
92. Wishcamper CA, Coffin JD, and Lurie DI: Lack of the protein tyrosine phosphatase SHP-1 results in decreased numbers of glia within the motheaten (me/me) mouse brain. J Comp Neurol 2001;441:118-133.
93. Yamamoto S, Higuchi Y, Yoshiyama K, Shimizu E, Kataoka M, Hijiya N, and Matsuura K: ADAM family proteins in the immune system. Immunol Today 1999;20:278-284.
94. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer-Hofer K, and Schwendener RA: Clodronateliposome- mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 2006;95:272-281.