Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein

Gastroenterology. 2007 Sep;133(3):862-74. doi: 10.1053/j.gastro.2007.06.018. Epub 2007 Jun 20.

Abstract

Background & aims: The low calcium response V (LcrV) protein synthesized by gram-negative, pathogenic yersiniae participates in bacterial evasion of the host's innate immune response by stimulating synthesis of the anti-inflammatory interleukin (IL)-10 and preventing the activation of proinflammatory cytokines.

Methods: We genetically engineered the food-grade bacterium Lactococcus lactis to secrete the LcrV protein from the enteropathogenic species Yersinia pseudotuberculosis. The protective and therapeutic potential of orally administered LcrV-secreting L lactis was evaluated in 2 models of acute experimental colitis (induced by trinitrobenzene sulfonic acid [TNBS] and dextran sodium sulfate [DSS], respectively) in wild-type and knockout mice.

Results: Oral administration of LcrV-secreting L lactis led to active delivery of LcrV and induction of IL-10 (via a Toll-like receptor 2-dependent pathway) in the colon and prevented TNBS-induced colitis, in contrast to the L lactis control not producing LcrV. Down-regulation of tissue inflammatory markers correlated well with the reduction in damage to the colonic mucosa. In contrast, TNBS-induced colitis was not prevented in IL-10(-/-) mice pretreated with LcrV-secreting L lactis, thus showing that IL-10 is required for LcrV protection. Administration of LcrV-secreting L lactis also proved to be very effective in preventing and treating acute DSS-induced colitis.

Conclusions: LcrV-secreting L lactis decreased experimentally induced intestinal inflammation in 2 murine models of colitis. This novel approach highlights the potential of using pathogen-derived immunomodulating molecules in vivo as novel therapeutics for inflammatory bowel diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Administration, Oral
  • Animals
  • Antigens, Bacterial / administration & dosage
  • Antigens, Bacterial / metabolism*
  • Antigens, Bacterial / therapeutic use*
  • Cells, Cultured
  • Colitis / chemically induced
  • Colitis / drug therapy*
  • Colitis / prevention & control*
  • Dextran Sulfate
  • Disease Models, Animal
  • Female
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / pathology
  • Lactococcus lactis / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pore Forming Cytotoxic Proteins / administration & dosage
  • Pore Forming Cytotoxic Proteins / metabolism*
  • Pore Forming Cytotoxic Proteins / therapeutic use*
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / metabolism
  • Trinitrobenzenesulfonic Acid

Substances

  • Antigens, Bacterial
  • LcrV protein, Yersinia
  • Pore Forming Cytotoxic Proteins
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • Interleukin-10
  • Trinitrobenzenesulfonic Acid
  • Dextran Sulfate