Schistosomes and snails: a molecular encounter

Abstract

Biomphalaria glabrata snails play an integral role in the transmission of Schistosoma mansoni, the causative agent for human schistosomiasis in the Western hemisphere. For the past two decades, tremendous advances have been made in research aimed at elucidating the molecular basis of the snail/parasite interaction. The growing concern that there is no vaccine to prevent schistosomiasis and only one effective drug in existence provides the impetus to develop new control strategies based on eliminating schistosomes at the snail-stage of the life cycle. To elucidate why a given snail is not always compatible to each and every schistosome it encounters, B. glabrata that are either resistant or susceptible to a given strain of S. mansoni have been employed to track molecular mechanisms governing the snail/schistosome relationship. With such snails, genetic markers for resistance and susceptibility were identified. Additionally, differential gene expression studies have led to the identification of genes that underlie these phenotypes. Lately, the role of schistosomes in mediating non-random relocation of gene loci has been identified for the first time, making B. glabrata a model organism where chromatin regulation by changes in nuclear architecture, known as spatial epigenetics, orchestrated by a major human parasite can now be investigated. This review will highlight the progress that has been made in using molecular approaches to describe snail/schistosome compatibility issues. Uncovering the signaling networks triggered by schistosomes that provide the impulse to turn genes on and off in the snail host, thereby controlling the outcome of infection, could also yield new insights into anti-parasite mechanism(s) that operate in the human host as well.

Keywords: B. glabrata; S. mansoni; compatibility; gene loci re-localization; gene-expression; intermediate snail host; resistance; susceptibility.

FIGURE 1

Temporal modulation of the transcript encoding (A) Hsp 70 or (B) Hsp 90 in susceptible NMRI and resistant (BS–90) B. glabrata snail stocks examined by qPCR after exposure (0 – 120 min) to S. mansoni miracidia. Note that expression of the transcripts occurs only in the susceptible but not in the resistant snail (Ittiprasert et al., 2010; Ittiprasert and Knight, 2012).

FIGURE 2

Biomphalaria glabrata embryonic (Bge) cells grown in vitro or ex vivo cells extracted from B. glabrata snails stained with antibodies or subjected to FISH. Antibodies raised against other species were used to reveal similar nuclear structures within snails and Bge cells; these include the nuclear lamina (A, green), fibrillarin in the nucleolus (B, green), PML bodies (F, red) and nuclear myosin (G, red). Chromatin modification was revealed using antibodies made against D. melanogaster modification that have a broad species range; histon 4 trimethylated K27 (D, green) and histone 3 trimethyl K4 (E, green). Individual chromosome territories were delineated by allowing 5-bromo-2′-deoxyuridine to be incorporated into replicating DNA and then allowing cells to divide seven times, followed by indirect immunofluorescence with an anti-5-bromo-2′-deoxyuridine antibody (C, red). Individual gene loci were revealed by FISH using labeled BAC probes (H, red). The DNA of the cells was stained with a DNA intercalating dye 4′6-diamidino-2-phenylindole. Scale bar 10 μm (Drs. Arican-Goktas, 2013 and Odoemelams′, 2009, Ph.D. thesis, Brunel University, UK) (Odoemelam, 2009; Arican-Goktas, 2013).