Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei

Abstract

Successful colonization of a compatible snail host by a digenetic trematode miracidium initiates a complex, proliferative development program requiring weeks to reach culmination in the form of production of cercariae which, once started, may persist for the remainder of the life span of the infected snail. How are such proliferative and invasive parasites able to circumvent host defenses and establish chronic infections? Using a microarray designed to monitor the internal defense and stress-related responses of the freshwater snail Biomphalaria glabrata, we have undertaken a time course study to monitor snail responses following exposure to two different trematode species to which the snail is susceptible: the medically important Schistosoma mansoni, exemplifying sporocyst production in its larval development, or Echinostoma paraensei, representing an emphasis on rediae production in its larval development. We sampled eight time points (0.5, 1, 2, 4, 8, 16 and 32 days p.i.) that cover the period required for cercariae to be produced. Following exposure to S. mansoni, there was a preponderance of up-regulated over down-regulated array features through 2 days p.i. but by 4 days p.i. and thereafter, this pattern was strongly reversed. For E. paraensei, there was a preponderance of down-regulated array features over up-regulated features at even 0.5 days p.i., a Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Author ManuscriptInt J Parasitol. Author manuscript; available in PMC 2011 June 1. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript pattern that persists throughout the course of infection except for 1 day p.i., when up-regulated array features slightly outnumbered down-regulated features. Examination of particular array features revealed several that were up-regulated by both parasites early in the course of infection and one, fibrinogen related protein 4 (FREP 4), that remained significantly elevated throughout the course of infection with either parasite, effectively serving as a marker of infection. Many defense-related transcripts were persistently down-regulated, including several fibrinogen-containing lectins and homologs of molecules best known from vertebrate phagocytic cells. Our results are consistent with earlier studies suggesting that both parasites are able to interfere with host defense responses, including a tendency for E. paraensei to do so more rapidly and strongly than S. mansoni They further suggest mechanisms for how trematodes are able to establish the chronic infections necessary for their cont...

Identification of differentially expressed genes in Oncomelania hupensis chronically infected with Schistosoma japonicum

“…It is clear that there are fewer forward library transcripts than reverse transcripts during a chronic infection, although many more clones from the forward library were examined. These results are consistent with those from the study of Hanington et al (2010), who found that following B. glabrata exposure to S. mansoni, there was a preponderance of up-regulated over down-regulated array features through 2 days post-infection (p.i. ); however, 4 days p.i.…”

“…The interaction between schistosome and snail begins when the free-swimming miracidium recognizes and penetrates the snail tegument or a natural opening such as branchial cavity or mouth (Xia and Jourdane, 1991). Certain factors are active immediately during acute infection while others act during chronic infection (Bayne, 2009;Hanington et al, 2010). The outcomes of schistosome-snail encounters are variable and are determined by several factors including the recognition capacity of the snail, evasion capacity of the schistosome, effectiveness of the killing activity of the snail, and counter-defense capacity of the schistosome (Bayne, 2009), and some researchers have argued that the success or failure of the snail's recognition system plays the dominant role in determining the outcomes of schistosome-snail encounters (Théron and Coustau, 2005).…”

Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection

“…Microarray analysis of the transcriptional profiles associated with size, strain, and acquired resistance models identified FREP3 as a transcript that is commonly up-regulated in resistant snails. Conversely, previous studies have demonstrated that FREP3 is a transcript that is targeted by the parasites for suppression during successful infections (21).…”

“…gnl|ti|2278068446-2278071234). pronounced during the early stages of infection (20): The parasite attempts to suppress the snail immune response (21) or to disguise itself from it (22), thereby allowing the parasite to establish. For its part, the snail host mounts humoral and cellular responses to encapsulate and kill the parasite (20,23,24).…”

Endogenous growth factor stimulation of hemocyte proliferation induces resistance to Schistosoma mansoni challenge in the snail host

“…The second, and lesser-understood, drivers are endogenous snail growth factors that, in response to infection, induce hemocyte proliferation/differentiation within the APO. Recent studies screening the transcriptome and proteome of B. glabrata have yielded promising candidates that possess canonical domains associated with hematopoietic factors of other organisms, both invertebrate and vertebrate (12).…”