MMP-independent role of TIMP-1 at the blood brain barrier during viral encephalomyelitis

ASN Neuro

Volumn 5, Issue 5, 2013, Pages 321-331

  Savarin, Carine ^a   Bergmann, Cornelia C ^a   Hinton, David R ^b   Stohlman, Stephen A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

CD4 T cells; Coronavirus; Glia limitans; Matrix metalloproteinase; TIMP 1

Indexed keywords

CHEMOKINE; GAMMA INTERFERON; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LEUKOCYTE ANTIGEN; MESSENGER RNA; RANTES; TIMP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CORONAVIRUS INFECTION; DISEASE SEVERITY; ENCEPHALITIS VIRUS; ENCEPHALOMYELITIS; MOUSE; NONHUMAN; T LYMPHOCYTE SUBPOPULATION; TISSUE INJURY; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; C57BL MOUSE; CORONAVIRUS; DISEASE MODEL; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VIROLOGY;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; BLOOD-BRAIN BARRIER; BRAIN; CHEMOKINE CCL5; CHEMOKINE CXCL10; CORONAVIRUS; CORONAVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, VIRAL; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASE-1;

EID: 84888871910     PISSN: 17590914     EISSN: None     Source Type: Journal    
DOI: 10.1042/AN20130033     Document Type: Article

References (45)

1. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, Opdenakker G, Sorokin LM (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203:1007-1019.
2. Agrawal SM, Silva C, Wang J, Tong JP, Yong VW (2012) A novel anti-EMMPRIN function-blocking antibody reduces T cell proliferation and neurotoxicity: relevance to multiple sclerosis. J Neuroinflammation 9:64.
3. Ajami B, Bennett JL, Krieger C, McNagny KM, Rossi FM (2011) Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat Neurosci 14:1142-1149.
4. Althoff GE, Wolfer DP, Timmesfeld N, Kanzler B, Schrewe H, Pagenstecher A (2010) Long-term expression of tissue-inhibitor of matrix metalloproteinase-1 in the murine central nervous system does not alter the morphological and behavioral phenotype but alleviates the course of experimental allergic encephalomyelitis. Am J Pathol 177:840-853.
5. Bechmann I, Galea I, Perry VH (2007) What is the blood-brain barrier (not)? Trends Immunol 28:5-11.
6. Bergmann CC, Lane TE, Stohlman SA (2006) Coronavirus infection of the central nervous system: host-virus stand-off. Nat Rev Microbiol 4:121-132.
7. Bergmann CC, Marten NW, Hinton DR, Parra B, Stohlman SA (2001) CD8 T cell mediated immunity to neurotropic MHV infection. Adv Exp Med Biol 494:299-308.
8. Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477:267-283.
9. Clark RT, Nance JP, Noor S, Wilson EH (2011) T-cell production of matrix metalloproteinases and inhibition of parasite clearance by TIMP-1 during chronic Toxoplasma infection in the brain. ASN Neuro 3:e00049.
10. Crocker SJ, Whitmire JK, Frausto RF, Chertboonmuang P, Soloway PD, Whitton JL, Campbell IL (2006) Persistent macrophage/microglial activation and myelin disruption after experimental autoimmune encephalomyelitis in tissue inhibitor of metalloproteinase-1-deficient mice. Am J Pathol 169:2104-2116.
11. Dubois B, Masure S, Hurtenbach U, Paemen L, Heremans H, van den Oord J, Sciot R, Meinhardt T, Hammerling G, Opdenakker G, Arnold B (1999) Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. J Clin Invest 104:1507-1515.
12. Engelhardt B, Ransohoff RM (2012) Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol 33:579-589.
13. Fleming JO, Trousdale MD, el-Zaatari FA, Stohlman SA, Weiner LP (1986) Pathogenicity of antigenic variants of murine coronavirus JHM selected with monoclonal antibodies. J Virol 58:869-875.
14. Galea I, Bechmann I, Perry VH (2007) What is immune privilege (not)? Trends Immunol 28:12-18.
15. Gardner J, Ghorpade A (2003) Tissue inhibitor of metalloproteinase (TIMP)-1: the TIMPed balance of matrix metalloproteinases in the central nervous system. J Neurosci Res 74:801-806.
16. Greter M, Heppner FL, Lemos MP, Odermatt BM, Goebels N, Laufer T, Noelle RJ, Becher B (2005) Dendritic cells permit immune invasion of the CNS in an animal model of multiple sclerosis. Nat Med 11:328-334.
17. Jung KK, Liu XW, Chirco R, Fridman R, Kim HR (2006) Identification of CD63 as a tissue inhibitor of metalloproteinase-1 interacting cell surface protein. EMBO J 25:3934-3942.
18. Kapil P, Atkinson R, Ramakrishna C, Cua DJ, Bergmann CC, Stohlman SA (2009) Interleukin-12 (IL-12), but not IL-23, deficiency ameliorates viral encephalitis without affecting viral control. J Virol 83:5978-5986.
19. Khuth ST, Akaoka H, Pagenstecher A, Verlaeten O, Belin MF, Giraudon P, Bernard A (2001) Morbillivirus infection of the mouse central nervous system induces region-specific upregulation of MMPs and TIMPs correlated to inflammatory cytokine expression. J Virol 75:8268-8282.
20. Lee MM, Yoon BJ, Osiewicz K, Preston M, Bundy B, van Heeckeren AM, Werb Z, Soloway PD (2005) Tissue inhibitor of metalloproteinase 1 regulates resistance to infection. Infect Immun 73:661-665.
21. McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS (2006) CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol 177:8053-8064.
22. Moore CS, Milner R, Nishiyama A, Frausto RF, Serwanski DR, Pagarigan RR, Whitton JL, Miller RH, Crocker SJ (2011) Astrocytic tissue inhibitor of metalloproteinase-1 (TIMP-1) promotes oligodendrocyte differentiation and enhances CNS myelination. J Neurosci 31:6247-6254.
23. Oelmann E, Herbst H, Zuhlsdorf M, Albrecht O, Nolte A, Schmitmann C, Manzke O, Diehl V, Stein H, Berdel WE (2002) Tissue inhibitor of metalloproteinases 1 is an autocrine and paracrine survival factor, with additional immune-regulatory functions, expressed by Hodgkin/Reed-Sternberg cells. Blood 99:258-267.
24. Owens T, Bechmann I, Engelhardt B (2008) Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol 67:1113-1121.
25. Pagenstecher A, Stalder AK, Kincaid CL, Shapiro SD, Campbell IL (1998) Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am J Pathol 152:729-741.
26. Pfistershammer K, Majdic O, Stockl J, Zlabinger G, Kirchberger S, Steinberger P, Knapp W (2004) CD63 as an activation-linked T cell costimulatory element. J Immunol 173:6000-6008.
27. Phares TW, Marques CP, Stohlman SA, Hinton DR, Bergmann CC (2011) Factors supporting intrathecal humoral responses following viral encephalomyelitis. J Virol 85:2589-2598.
28. Phares TW, Stohlman SA, Hinton DR, Atkinson R, Bergmann CC (2010) Enhanced antiviral T cell function in the absence of B7-H1 is insufficient to prevent persistence but exacerbates axonal bystander damage during viral encephalomyelitis. J Immunol 185:5607-5618.
29. Phares TW, Stohlman SA, Hwang M, Min B, Hinton DR, Bergmann CC (2012) CD4 T cells promote CD8 T cell immunity at the priming and effector site during viral encephalitis. J Virol 86:2416-2427.
30. + T cell migration into the CNS parenchyma following Toxoplasma gondii infection. Brain Behav Immun 25:883-896.
31. Ransohoff RM, Engelhardt B (2012) The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 12:623-635.
32. Roderfeld M, Graf J, Giese B, Salguero-Palacios R, Tschuschner A, Muller-Newen G, Roeb E (2007) Latent MMP-9 is bound to TIMP-1 before secretion. Biol Chem 388:1227-1234.
33. Savarin C, Bergmann CC, Hinton DR, Ransohoff RM, Stohlman SA (2008) Memory CD4 + T-cell-mediated protection from lethal coronavirus encephalomyelitis. J Virol 82:12432-12440.
34. 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.
35. Savarin C, Stohlman SA, Rietsch AM, Butchi N, Ransohoff RM, Bergmann CC (2011) MMP9 deficiency does not decrease blood-brain barrier disruption, but increases astrocyte MMP3 expression during viral encephalomyelitis. Glia 59:1770-1781.
36. + T cell compartmentalization. Brain 132:1247-1258.
37. Stetler-Stevenson WG (2008) Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities. Sci Signal 1:re6.
38. Stiles LN, Hardison JL, Schaumburg CS, Whitman LM, Lane TE (2006) T cell antiviral effector function is not dependent on CXCL10 following murine coronavirus infection. J Immunol 177: 8372-8380.
39. Stiles LN, Liu MT, Kane JA, Lane TE (2009) CXCL10 and trafficking of virus-specific T cells during coronavirus-induced demyelination. Autoimmunity 42:484-491.
40. + T cells. J Immunol 160:2896-2904.
41. Stohlman SA, Hinton DR, Parra B, Atkinson R, Bergmann CC (2008) CD4 T cells contribute to virus control and pathology following central nervous system infection with neurotropic mouse hepatitis virus. J Virol 82:2130-2139.
42. Toft-Hansen H, Buist R, Sun XJ, Schellenberg A, Peeling J, Owens T (2006) Metalloproteinases control brain inflammation induced by pertussis toxin in mice overexpressing the chemokine CCL2 in the central nervous system. J Immunol 177:7242-7249.
43. Tran EH, Hoekstra K, van Rooijen N, Dijkstra CD, Owens T (1998) 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 161: 3767-3775.
44. + T cells but not interleukin-2. Viral Immunol 18:162-169.
45. Zhou J, Marten NW, Bergmann CC, Macklin WB, Hinton DR, Stohlman SA (2005b) Expression of matrix metalloproteinases and their tissue inhibitor during viral encephalitis. J Virol 79:4764-4773.