Matrix metalloproteinase-9 amplifies the immune response to Pseudomonas aeruginosa corneal infection

Invest Ophthalmol Vis Sci. 2006 Jan;47(1):256-64. doi: 10.1167/iovs.05-1050.

Abstract

Purpose: The purpose of this study was to determine the role of matrix metalloproteinases (MMP) in Pseudomonas aeruginosa keratitis.

Methods: Gene array and selective real-time PCR examined MMP expression in the cornea of susceptible (C57BL/6, B6) versus resistant (BALB/c) mice before and after infection; zymography tested enzyme activity for MMP-2 and -9. Clinical score, Langerhans cell (LC), and Neutrophil (PMN) quantitation were done in recombinant (r) MMP-9, antibody neutralized, and MMP-9(-/-) mice. The chemotactic potential of MMP-9 was tested in a Boyden chamber assay; light and transmission microscopy and immunostaining for collagen IV and MMP-9 were used to examine the effects and the source of MMP-9 after infection. ELISA was used to assess IL-1beta and MIP-2 levels.

Results: Gene array (confirmed by PCR) revealed sixfold more MMP-9, and zymography showed greater enzyme activity in the infected cornea of B6 over BALB/c mice. rMMP-9 injection of BALB/c mice enhanced, whereas MMP-9 antibody neutralization in B6 mice and its absence in MMP-9(-/-) mice decreased corneal disease. MMP-9(-/-) and antibody neutralized mice had fewer LCs in cornea; rMMP-9-treated mice had more. A myeloperoxidase (MPO) assay showed a similar pattern for PMN. MMP-9 was not chemotactic for LC or PMN. The basement membrane was more intact in MMP-9(-/-) over wild-type infected mice and correlated with staining for collagen IV; PMN was a source of MMP-9. IL-1beta and MIP-2 were increased in rMMP-9 but decreased in MMP-9 antibody neutralized and MMP-9(-/-) over control groups.

Conclusions: MMP-9 regulates immune function in cornea by proteolysis, potentiating P. aeruginosa keratitis by degrading collagen IV and upregulating chemotactic cytokines/chemokines IL-1beta and MIP-2.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibody Formation
  • Chemokine CXCL2
  • Chemokines / metabolism
  • Chemotaxis, Leukocyte / physiology
  • Collagen Type IV / metabolism
  • Corneal Ulcer / enzymology
  • Corneal Ulcer / immunology*
  • Disease Susceptibility
  • Enzyme-Linked Immunosorbent Assay
  • Eye Infections, Bacterial / enzymology
  • Eye Infections, Bacterial / immunology*
  • Female
  • Immunity, Innate
  • Interleukin-1 / metabolism
  • Langerhans Cells / immunology*
  • Matrix Metalloproteinase 9 / physiology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / immunology*
  • Oligonucleotide Array Sequence Analysis
  • Pseudomonas Infections / enzymology
  • Pseudomonas Infections / immunology*
  • Pseudomonas aeruginosa / physiology
  • Reverse Transcriptase Polymerase Chain Reaction
  • Up-Regulation

Substances

  • Chemokine CXCL2
  • Chemokines
  • Collagen Type IV
  • Cxcl2 protein, mouse
  • Interleukin-1
  • Matrix Metalloproteinase 9