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

ASN Neuro. 2013 Nov 26;5(5):e00127. doi: 10.1042/AN20130033.

Abstract

Infection of the CNS (central nervous system) with a sublethal neurotropic coronavirus (JHMV) induces a vigorous inflammatory response. CD4⁺ and CD8⁺ T cells are essential to control infectious virus but at the cost of tissue damage. An enigma in understanding the contribution of T cell subsets in pathogenesis resides in their distinct migration pattern across the BBB (blood brain barrier). CD4⁺ T cells transiently accumulate within the perivascular space, whereas CD8⁺ T cells migrate directly into the CNS parenchyma. As MMPs (matrix metalloproteinases) facilitate migration across the glia limitans, specific expression of the TIMP (tissue inhibitor of MMPs)-1 by CD4⁺ T cells present in the perivascular cuffs suggested that TIMP-1 is responsible for stalling CD4⁺ T cell migration into the CNS parenchyma. Using TIMP-1 deficient mice, the present data demonstrate an increase rather than a decrease in CD4⁺ T cell accumulation within the perivascular space during JHMV infection. Whereas virus control was not affected by perivascular retention of CD4⁺ T cells, disease severity was decreased and associated with reduced IFNγ (interferon γ) production. Moreover, decreased CD4⁺ T cell recruitment into the CNS parenchyma of TIMP-1 deficient mice was not associated with impaired T cell recruiting chemokines or MMP expression, and no compensation by other TIMP molecules was identified. These data suggest an MMP-independent role of TIMP-1 in regulating CD4⁺ T cell access into the CNS parenchyma during acute JHMV encephalitis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Antigens, CD / metabolism
  • Blood-Brain Barrier / metabolism*
  • Blood-Brain Barrier / physiopathology
  • Blood-Brain Barrier / virology
  • Brain / pathology
  • Brain / virology
  • Chemokine CCL5 / metabolism
  • Chemokine CXCL10 / metabolism
  • Coronavirus / physiology
  • Coronavirus Infections / complications
  • Disease Models, Animal
  • Encephalomyelitis / etiology
  • Encephalomyelitis / pathology*
  • Encephalomyelitis / virology*
  • Flow Cytometry
  • Gene Expression Regulation, Viral / genetics
  • Matrix Metalloproteinases / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • RNA, Messenger / metabolism
  • Tissue Inhibitor of Metalloproteinase-1 / deficiency*
  • Tissue Inhibitor of Metalloproteinase-1 / genetics

Substances

  • Antigens, CD
  • Chemokine CCL5
  • Chemokine CXCL10
  • RNA, Messenger
  • Timp1 protein, mouse
  • Tissue Inhibitor of Metalloproteinase-1
  • Matrix Metalloproteinases