Primed Immune Responses Triggered by Ingested Bacteria Lead to Systemic Infection Tolerance in Silkworms

PLoS One. 2015 Jun 24;10(6):e0130486. doi: 10.1371/journal.pone.0130486. eCollection 2015.

Abstract

In the present study, we examined whether microorganisms collaterally ingested by insects with their food activate the innate immune system to confer systemic resistance against subsequent bacterial invasion. Silkworms orally administered heat-killed Pseudomonas aeruginosa cells showed resistance against intra-hemolymph infection by P. aeruginosa. Oral administration of peptidoglycans, cell wall components of P. aeruginosa, conferred protective effects against P. aeruginosa infection, whereas oral administration of lipopolysaccharides, bacterial surface components, did not. In silkworms orally administered heat-killed P. aeruginosa cells, P. aeruginosa growth was inhibited in the hemolymph, and mRNA amounts of the antimicrobial peptides cecropin A and moricin were increased in the hemocytes and fat body. Furthermore, the amount of paralytic peptide, an insect cytokine that activates innate immune reactions, was increased in the hemolymph of silkworms orally administered heat-killed P. aeruginosa cells. These findings suggest that insects sense bacteria present in their food by peptidoglycan recognition, which activates systemic immune reactions to defend the insects against a second round of infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity*
  • Administration, Oral
  • Animals
  • Antimicrobial Cationic Peptides / biosynthesis
  • Antimicrobial Cationic Peptides / genetics
  • Antimicrobial Cationic Peptides / immunology*
  • Bombyx / genetics
  • Bombyx / immunology*
  • Bombyx / microbiology
  • Fat Body / cytology
  • Fat Body / immunology
  • Fat Body / microbiology
  • Gene Expression
  • Hemocytes / cytology
  • Hemocytes / immunology
  • Hemocytes / microbiology
  • Hemolymph / cytology
  • Hemolymph / immunology
  • Hemolymph / microbiology
  • Hot Temperature
  • Insect Proteins / biosynthesis
  • Insect Proteins / genetics
  • Insect Proteins / immunology*
  • Larva / genetics
  • Larva / immunology
  • Larva / microbiology
  • Lipopolysaccharides / pharmacology
  • Neuropeptides / biosynthesis
  • Neuropeptides / genetics
  • Neuropeptides / immunology*
  • Pseudomonas aeruginosa / chemistry
  • Pseudomonas aeruginosa / immunology

Substances

  • Antimicrobial Cationic Peptides
  • Insect Proteins
  • Lipopolysaccharides
  • Neuropeptides
  • moricin protein, Bombyx mori
  • paralytic peptide, insect
  • cecropin A

Grants and funding

This study was supported by Grants-in-Aid for Scientific Research 23249009, 24590519, 25117507, 26670025 and Japan Society for the Promotion of Science Research Fellowships for Young Scientists Grant 25-8664 (to A.M.). This study was supported in part by the Genome Pharmaceutical Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.