Signals triggered by a bacterial pore-forming toxin contribute to toll-like receptor redundancy in gram-positive bacterial recognition

J Infect Dis. 2009 Jan 1;199(1):124-33. doi: 10.1086/595562.

Abstract

Background: Toll-like receptor (TLR) 2 is the principal recognition receptor for gram-positive microbes. However, in some gram-positive bacterial infections, TLR2 is dispensable. One of the outstanding questions regarding host-bacteria interactions is why TLR2 is essential in some infections but dispensable in others.

Methods: We used a combination of bacterial plating, flow cytometry, enzyme-linked immunosorbent assay, and reverse-transcriptase polymerase chain reaction to analyze the inflammatory responses induced by Listeria monocytogenes and its toxin listeriolysin O (LLO) in vitro and in vivo. We analyzed wild-type, TLR2(-/-)-, TLR4(-/-)-, MyD88(-/-)-, interleukin (IL)-1beta(-/-)-, and IL-18(-/-)-deficient mice and the bone marrow-derived mast cells obtained from these respective groups.

Results: TLR2(-/-) mice had unaltered L. monocytogenes clearance and did not experience impairment of cytokine/chemokine induction and neutrophil mobilization by L. monocytogenes or purified LLO, but they were unresponsive to the LLO-deficient mutant L. monocytogenes (LmDeltahly). We show that L. monocytogenes and LLO mediate such responses in part via interleukin (IL)-1beta and IL-18-MyD88 pathways.

Conclusions: The results illustrate that signals triggered by LLO contribute to TLR2 redundancy in recognition of L. monocytogenes. Under normal conditions, multiple and, sometimes, redundant pathways cooperate to induce a rapid antimicrobial defense. When one signaling pathway-in this case, TLR2-is removed from the system, the other pathways are still capable of mounting a sufficient response to ensure survival of the host.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacterial Toxins / toxicity*
  • Bone Marrow / physiology
  • DNA Primers
  • Heat-Shock Proteins / toxicity*
  • Hemolysin Proteins / toxicity*
  • Inflammation / microbiology
  • Interleukin-18 / deficiency
  • Interleukin-18 / genetics
  • Interleukin-1beta / deficiency
  • Interleukin-1beta / genetics
  • Listeria monocytogenes / isolation & purification*
  • Listeriosis / genetics
  • Listeriosis / physiopathology*
  • Mast Cells / physiology
  • Mice
  • Mice, Knockout
  • Myeloid Differentiation Factor 88 / deficiency
  • Myeloid Differentiation Factor 88 / genetics
  • RNA, Messenger / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Toll-Like Receptor 2 / deficiency*
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 4 / deficiency*
  • Toll-Like Receptor 4 / genetics

Substances

  • Bacterial Toxins
  • DNA Primers
  • Heat-Shock Proteins
  • Hemolysin Proteins
  • Interleukin-18
  • Interleukin-1beta
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • RNA, Messenger
  • Tlr2 protein, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 2
  • Toll-Like Receptor 4
  • hlyA protein, Listeria monocytogenes