Components of the cultivated red seaweed Chondrus crispus enhance the immune response of Caenorhabditis elegans to Pseudomonas aeruginosa through the pmk-1, daf-2/daf-16, and skn-1 pathways

Appl Environ Microbiol. 2013 Dec;79(23):7343-50. doi: 10.1128/AEM.01927-13. Epub 2013 Sep 20.

Abstract

Marine macroalgae are rich in bioactive compounds that can, when consumed, impart beneficial effects on animal and human health. The red seaweed Chondrus crispus has been reported to have a wide range of health-promoting activities, such as antitumor and antiviral activities. Using a Caenorhabditis elegans infection model, we show that C. crispus water extract (CCWE) enhances host immunity and suppresses the expression of quorum sensing (QS) and the virulence factors of Pseudomonas aeruginosa (strain PA14). Supplementation of nematode growth medium with CCWE induced the expression of C. elegans innate immune genes, such as irg-1, irg-2, F49F1.6, hsf-1, K05D8.5, F56D6.2, C29F3.7, F28D1.3, F38A1.5 ZK6.7, lys-1, spp-1, and abf-1, by more than 2-fold, while T20G5.7 was not affected. Additionally, CCWE suppressed the expression of PA14 QS genes and virulence factors, although it did not affect the growth of the bacteria. These effects correlated with a 28% reduction in the PA14-inflicted killing of C. elegans. Kappa-carrageenan (K-CGN), a major component of CCWE, was shown to play an important role in the enhancement of host immunity. Using C. elegans mutants, we identified that pmk-1, daf-2/daf-16, and skn-1 are essential in the K-CGN-induced host immune response. In view of the conservation of innate immune pathways between C. elegans and humans, the results of this study suggest that water-soluble components of C. crispus may also play a health-promoting role in higher animals and humans.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / isolation & purification
  • Anti-Bacterial Agents / metabolism*
  • Caenorhabditis elegans / drug effects*
  • Caenorhabditis elegans / immunology
  • Caenorhabditis elegans / microbiology*
  • Caenorhabditis elegans Proteins / metabolism
  • Chondrus / chemistry*
  • DNA-Binding Proteins / metabolism
  • Forkhead Transcription Factors
  • Immunity, Innate / drug effects
  • Immunologic Factors / isolation & purification
  • Immunologic Factors / metabolism*
  • Mitogen-Activated Protein Kinases / metabolism
  • Plant Extracts / isolation & purification
  • Plant Extracts / metabolism*
  • Pseudomonas aeruginosa / drug effects
  • Pseudomonas aeruginosa / immunology*
  • Quorum Sensing / drug effects
  • Receptor, Insulin / metabolism
  • Transcription Factors / metabolism
  • Virulence Factors / biosynthesis

Substances

  • Anti-Bacterial Agents
  • Caenorhabditis elegans Proteins
  • DNA-Binding Proteins
  • Forkhead Transcription Factors
  • Immunologic Factors
  • Plant Extracts
  • Transcription Factors
  • Virulence Factors
  • daf-16 protein, C elegans
  • skn-1 protein, C elegans
  • DAF-2 protein, C elegans
  • Receptor, Insulin
  • Mitogen-Activated Protein Kinases
  • Pmk-1 protein, C elegans