Advances in gastropod immunity from the study of the interaction between the snail Biomphalaria glabrata and its parasites: A review of research progress over the last decade.

This review summarizes the research progress made over the past decade in the field of gastropod immunity resulting from investigations of the interaction between the snail Biomphalaria glabrata and its trematode parasites. A combination of integrated approaches, including cellular, genetic and comparative molecular and proteomic approaches have revealed novel molecular components involved in mediating Biomphalaria immune responses that provide insights into the nature of host-parasite compatibility and the mechanisms involved in parasite recognition and killing. The current overview emphasizes that the interaction between B. glabrata and its trematode parasites involves a complex molecular crosstalk between numerous antigens, immune receptors, effectors and anti-effector systems that are highly diverse structurally and extremely variable in expression between and within host and parasite populations. Ultimately, integration of these molecular signals will determine the outcome of a specific interaction between a B. glabrata individual and its interacting trematodes. Understanding these complex molecular interactions and identifying key factors that may be targeted to impairment of schistosome development in the snail host is crucial to generating new alternative schistosomiasis control strategies.

The transcriptomic analysis of Planorbarius corneus hemocytes (Gastropoda) naturally infected with Bilharziella polonica (Schistosomatidae).

The study of molluscan innate immunity is essential for understanding the evolution of the immune system. An advance in the knowledge of their immune system can be achieved by increasing the number of model species. Our study focuses on the immunity of Planorbarius corneus, a pulmonate snail widely distributed in Eurasia. These snails are intermediate hosts of many trematodes, including Bilharziella polonica (Schistosomatidae). In this paper we obtained and analyzed transcriptomes of hemocytes of uninfected snails Planorbarius corneus and snails naturally infected with Bilharziella polonica. The transcriptomes were found to contain transcripts encoding all major groups of immune factors previously described for other gastropods. Pathogen-recognition molecules were the most diverse group of immune factors. Comparison of the transcriptomes of the infected and the uninfected molluscs showed that the expression of some genes changed during infection. Our results extend the knowledge of immune responses of pulmonate snails to trematode invasion and promote P. corneus as a new model for the study of molluscan defence reactions.

Vertebrate host protective immunity drives genetic diversity and antigenic polymorphism in Schistosoma mansoni.

Schistosomes are gonochoric blood parasites with a complex life cycle responsible for a disease of considerable medical and veterinary importance in tropical and subtropical regions. Understanding the evolution of schistosome genetic diversity is clearly of fundamental importance to interpreting schistosomiasis epidemiology and disease transmission patterns of this parasite. In this article, we investigated the putative role of the host immune system in the selection of male genetic diversity. We demonstrated the link between genetic dissimilarity and the protective effect among male worms. We then compared the proteomes of three male clones with different genotypes and differing by their capacity to protect against reinfection. The identified differences correspond mainly to antigens known or supposed to be involved in the induction of protective immunity. These results underline the role played by host immune system in the selection of schistosome genetic diversity that is linked to antigenic diversity. We discuss the evolutionary consequences in the context of schistosome infection.

The compatibiuty polymorphism in invertebrate host/trematodes interactions: research of molecular determinants.

The co-evolutionary dynamics that exist in many host-parasite interactions sometimes leads to compatibility polymorphism. This phenomenon is well documented in mollusc/trematodes interactions but its molecular base is unknown. In order to identify key molecules involved in this phenomenon, we developed several molecular approaches comparing compatible or incompatible strains of mollusc or parasite. These comparisons led to the identification of numerous candidate genes listed and discussed (some of them) in the present review.

The Compatibility Between Biomphalaria glabrata Snails and Schistosoma mansoni: An Increasingly Complex Puzzle.

This review reexamines the results obtained in recent decades regarding the compatibility polymorphism between the snail, Biomphalaria glabrata, and the pathogen, Schistosoma mansoni, which is one of the agents responsible for human schistosomiasis. Some results point to the snail's resistance as explaining the incompatibility, while others support a "matching hypothesis" between the snail's immune receptors and the schistosome's antigens. We propose here that the two hypotheses are not exclusive, and that the compatible/incompatible status of a particular host/parasite couple probably reflects the balance of multiple molecular determinants that support one hypothesis or the other. Because these genes are involved in a coevolutionary arms race, we also propose that the underlying mechanisms can vary. Finally, some recent results show that environmental factors could influence compatibility. Together, these results make the compatibility between B. glabrata and S. mansoni an increasingly complex puzzle. We need to develop more integrative approaches in order to find targets that could potentially be manipulated to control the transmission of schistosomiasis.

Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes.

Because susceptibility or resistance of Biomphalaria glabrata to the trematode Echinostoma caproni correlates with differential hemocytic adhesive properties, we compared the expression of genes involved in adhesion processes between hemocytes from susceptible and resistant snails. Quantitative reverse transcriptase-PCR analysis revealed four genes whose transcripts were differentially represented between hemocytes from resistant and susceptible snails. These genes encode two dermatopontin-like, one matrilin-like and one cadherin-like proteins. Expression analyses performed following parasite exposure suggested that dermatopontins may be involved in the compatibility differences between these strains. We also investigated expression levels on whole snails of different genes potentially involved in extracellular matrix structure or coagulation. Our results support the hypothesis that susceptible snails possess a hemolymph coagulation-like system that is more potent than that of resistant snails. This system may prevent hemocyte migration towards the parasite larvae and therefore facilitate parasite settlement in susceptible snails.

Histomorphological study of the preputial and clitoral glands in BALB/c mice with experimental Taenia crassiceps infections.

Male preputial and female clitoral glands of mice undergo development that depends on the level of hormones in the animal. Experimental infection with Taenia crassiceps cysticerci results in significant physiological modifications in the host. Here, we investigated the histomorphological alterations induced by the parasite in these pheromonal glands. Preputial and clitoral glands were recovered from mice at 15, 35, 50, and 70 days postinfection (DPI). The glands were examined macroscopically and microscopically after histological preparation. Male preputial glands show a marked atrophy 35 days after infection. This atrophy is the result of a disorganization of the acinus tissue structure. During the course of infection, the basal, intermediate, and mature acinar cell layers are reduced, and finally, at 70 DPI, the gland includes only the duct system and fibrotic structures. In contrast, females are not affected by the infection because no modifications were observed in the morphology or histology of the clitoral glands. A probable cause for such a divergence between infected male and female mice might be related to a sex steroid imbalance as described during T. crassiceps infection.

Multi-parasite host susceptibility and multi-host parasite infectivity: a new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism.

In this study, we analyze the degree of susceptibility/un-susceptibility of five strains of Biomphalaria glabrata from different geographical origins successively challenged with a panel of 4 Schistosoma mansoni strains. A total of 20 homopatric and heteropatric host-parasite combinations were tested with exposure doses of 1, 10, 20, 30 and 50 miracidia per individual host. By doing this, we characterized each B. glabrata strain by its "multi-parasite susceptibility phenotype" that reflects better the efficiency of their defense mechanism against not only one, but a diversity of schistosome stocks. In the same time, all the S. mansoni strains used were characterized, by their "multi-host infectivity phenotype" that reflects the level of infectivity they display when confronted to diverse snail populations. Based on these results it is possible to select different homogenous stocks of snails with different spectrum of susceptibility/un-susceptibility for several parasite strains. This will be a useful tool for future functional studies conducted to understand the genetics and molecular basis of the compatibility polymorphism in this host/parasite model.

Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms.

Coevolutionary dynamics in host-parasite interactions potentially lead to an arms race that results in compatibility polymorphism. The mechanisms underlying compatibility have remained largely unknown in the interactions between the snail Biomphalaria glabrata and Schistosoma mansoni, one of the agents of human schistosomiasis. This review presents a combination of data obtained from field and laboratory studies arguing in favor of a matching phenotype model to explain compatibility polymorphism. Investigations focused on the molecular determinants of compatibility have revealed two repertoires of polymorphic and/or diversified molecules that have been shown to interact: the parasite antigens S. mansoni polymorphic mucins and the B. glabrata fibrinogen-related proteins immune receptors. We hypothesize their interactions define the compatible/incompatible status of a specific snail/schistosome combination. This line of thought suggests concrete approaches amenable to testing in field-oriented studies attempting to control schistosomiasis by disrupting schistosome-snail compatibility.

Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach.

In order to elucidate mechanisms underlying snail/echinostome compatibility, numerous molecular studies comparing transcripts and proteins of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni were undertaken. These studies focused on plasma and haemocytes of the two strains and revealed that some transcripts and/or proteins were differentially expressed between strains. The aim of the present study was to develop a complementary transcriptomic approach by constructing subtractive libraries. This work revealed some candidate transcripts already identified in previous studies (calcium-binding proteins and glycolytic enzymes) as well as novel candidate transcripts that were differentially represented between strains of B. glabrata. Among these newly identified genes, we revealed several genes potentially involved in immune processes encoding proteases, protease inhibitors, a lectin, an aplysianin-like molecule, and cell adhesion molecules.

Parasite-altered host behavior in the face of a predator: manipulation or not?

Parasitologists have generally accepted the idea that parasite-induced alterations in host behavior increase the chance for parasite survival and transmission or ensure the completion of its life cycle. The aim of the present study was to investigate modifications in the behavior of Taenia crassiceps-infected BALB/c mice in the face of a predator. The experiments showed modifications in the response of infected mice in comparison with uninfected controls on exposure to a predator final host. However, different studies lead us to suggest that the observed modifications are likely to be a secondary effect of the impact of the parasite on host physiology and immunity that favors its development and proliferation.

Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice.

Behavioural dominance relationships in mouse populations are based upon fighting and antagonistic behaviour. Social rank is affected by the physiological states present in the mice. Experimental infection by Taenia crassiceps cysticerci induced physiological disorders and disrupted the dominant-subordinate status. Infected male mice showed strong perturbations in territorial behaviour and aggressiveness. Infected dominant male mice did not show a significant reversal of dominance order compared to uninfected mice. In addition, during confrontation between naive infected and healthy mice, infected animals more often assumed a subordinate status than healthy ones. The effects of the infection by T. crassiceps were more likely to prevent adult male mice from becoming behaviourally dominant than to reverse existing dominance relationships. The results are discussed on the basis of the parasite manipulation hypothesis and host optimal foraging and decision-making theories.

Characterization of cDNA encoding a L37a ribosomal protein from Taenia crassiceps and its potential use in phylogenetic reconstructions.

In this study, we characterized for the first time the complete sequence of a L37a cDNA from a cestode specie: Taenia crassiceps. A phylogenetic analysis of L37a ribosomal proteins from distant animal species is presented and the potential use of such proteins in molecule-based phylogeny is discussed.