A Shift from Cellular to Humoral Responses Contributes to Innate Immune Memory in the Vector Snail Biomphalaria glabrata

PLoS Pathog. 2016 Jan 6;12(1):e1005361. doi: 10.1371/journal.ppat.1005361. eCollection 2016 Jan.

Abstract

Discoveries made over the past ten years have provided evidence that invertebrate antiparasitic responses may be primed in a sustainable manner, leading to the failure of a secondary encounter with the same pathogen. This phenomenon called "immune priming" or "innate immune memory" was mainly phenomenological. The demonstration of this process remains to be obtained and the underlying mechanisms remain to be discovered and exhaustively tested with rigorous functional and molecular methods, to eliminate all alternative explanations. In order to achieve this ambitious aim, the present study focuses on the Lophotrochozoan snail, Biomphalaria glabrata, in which innate immune memory was recently reported. We provide herein the first evidence that a shift from a cellular immune response (encapsulation) to a humoral immune response (biomphalysin) occurs during the development of innate memory. The molecular characterisation of this process in Biomphalaria/Schistosoma system was undertaken to reconcile mechanisms with phenomena, opening the way to a better comprehension of innate immune memory in invertebrates. This prompted us to revisit the artificial dichotomy between innate and memory immunity in invertebrate systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomphalaria / immunology*
  • Biomphalaria / parasitology
  • Disease Vectors
  • Host-Parasite Interactions / immunology*
  • Immunity, Cellular / immunology*
  • Immunity, Humoral / immunology*
  • Immunity, Innate / immunology
  • Immunologic Memory / immunology*
  • RNA, Small Interfering
  • Real-Time Polymerase Chain Reaction
  • Schistosoma mansoni / immunology
  • Schistosomiasis mansoni / immunology
  • Schistosomiasis mansoni / veterinary
  • Transfection

Substances

  • RNA, Small Interfering

Grants and funding

BG acknowledges support from ANR JCJC INVIMORY (number ANR-13-JSV7-0009). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.