Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin

PLoS Pathog. 2015 Jul 31;11(7):e1005015. doi: 10.1371/journal.ppat.1005015. eCollection 2015 Jul.

Abstract

Insect immune systems can recognize specific pathogens and prime offspring immunity. High specificity of immune priming can be achieved when insect females transfer immune elicitors into developing oocytes. The molecular mechanism behind this transfer has been a mystery. Here, we establish that the egg-yolk protein vitellogenin is the carrier of immune elicitors. Using the honey bee, Apis mellifera, model system, we demonstrate with microscopy and western blotting that vitellogenin binds to bacteria, both Paenibacillus larvae--the gram-positive bacterium causing American foulbrood disease--and to Escherichia coli that represents gram-negative bacteria. Next, we verify that vitellogenin binds to pathogen-associated molecular patterns; lipopolysaccharide, peptidoglycan and zymosan, using surface plasmon resonance. We document that vitellogenin is required for transport of cell-wall pieces of E. coli into eggs by imaging tissue sections. These experiments identify vitellogenin, which is distributed widely in oviparous species, as the carrier of immune-priming signals. This work reveals a molecular explanation for trans-generational immunity in insects and a previously undescribed role for vitellogenin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / immunology*
  • Blotting, Western
  • Egg Proteins / immunology*
  • Female
  • Ovum / immunology*
  • Surface Plasmon Resonance
  • Vitellogenins / immunology*

Substances

  • Egg Proteins
  • Vitellogenins

Grants and funding

HS was funded by Academy of Finland grant number 265971. www.aka.fi/en-GB/A/ GVA was funded by Norwegian Research Council grant number 180504 and 191699. www.forskningsradet.no/en/Home_page/1177315753906 DF was funded by Academy of Finland grant number 251337 and 252411. HS and DF were also supported by University of Helsinki www.helsinki.fi/university. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.