Systematically improved in vitro culture conditions reveal new insights into the reproductive biology of the human parasite Schistosoma mansoni

PLoS Biol. 2019 May 8;17(5):e3000254. doi: 10.1371/journal.pbio.3000254. eCollection 2019 May.

Abstract

Schistosomes infect over 200 million people. The prodigious egg output of these parasites is the sole driver of pathology due to infection, yet our understanding of sexual reproduction by schistosomes is limited because normal egg production is not sustained for more than a few days in vitro. Here, we describe culture conditions that support schistosome sexual development and sustained egg production in vitro. Female schistosomes rely on continuous pairing with male worms to fuel the maturation of their reproductive organs. Exploiting these new culture conditions, we explore the process of male-stimulated female maturation and demonstrate that physical contact with a male worm, and not insemination, is sufficient to induce female development and the production of viable parthenogenetic haploid embryos. We further report the characterization of a nuclear receptor (NR), which we call Vitellogenic Factor 1 (VF1), that is essential for female sexual development following pairing with a male worm. Taken together, these results provide a platform to study the fascinating sexual biology of these parasites on a molecular level, illuminating new strategies to control schistosome egg production.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ascorbic Acid / pharmacology
  • Cell Culture Techniques / methods*
  • Cholesterol / pharmacology
  • Embryo, Nonmammalian / drug effects
  • Embryo, Nonmammalian / metabolism
  • Erythrocytes / drug effects
  • Erythrocytes / metabolism
  • Female
  • Haploidy
  • Humans
  • Male
  • Mice
  • Ovum / drug effects
  • Ovum / physiology
  • Parasites / growth & development*
  • Parthenogenesis / drug effects
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Reproduction / drug effects
  • Schistosoma mansoni / drug effects
  • Schistosoma mansoni / growth & development*
  • Sexual Maturation / drug effects

Substances

  • Receptors, Cytoplasmic and Nuclear
  • Cholesterol
  • Ascorbic Acid