Review: SCHISTOSOMA MANSONI: THE ULTRASTRUCTURE OF LARVAL MORPHOGENESIS IN BIOMPHALARIA GLABRATA AND OF ASSOCIATED HOST-PARASITE INTERACTIONS

Abstract Background The blood flukes of genus Schistosoma are the causative agent of schistosomiasis, a parasitic disease that infects more than 200 million people worldwide. Proteases of schistosomes are involved in critical steps of host–parasite interactions and are promising therapeutic targets. We recently identified and characterized a group of S1 family Schistosoma mansoni serine proteases, including SmSP1 to SmSP5. Expression levels of some SmSPs in S. mansoni are low, and by standard genome sequencing technologies they are marginally detectable at the method threshold levels. Here, we report their spatial gene expression patterns in adult S. mansoni by the high-sensitivity localization assay. Methodology Highly sensitive fluorescence in situ RNA hybridization (FISH) was modified and used for the localization of mRNAs encoding individual SmSP proteases (including low-expressed SmSPs) in tissues of adult worms. High sensitivity was obtained due to specifically prepared tissue and probes in combination with the employment of a signal amplification approach. The assay method was validated by detecting the expression patterns of a set of relevant reference genes including SmCB1, SmPOP, SmTSP-2, and Sm29 with localization formerly determined by other techniques. Results FISH analysis revealed interesting expression patterns of SmSPs distributed in multiple tissues of S. mansoni adults. The expression patterns of individual SmSPs were distinct but in part overlapping and were consistent with existing transcriptome sequencing data. The exception were genes with significantly low expression, which were also localized in tissues where they had not previously been detected by RNA sequencing methods. In general, SmSPs were found in various tissues including reproductive organs, parenchymal cells, esophagus, and the tegumental surface. Conclusions The FISH-based assay provided spatial information about the expression of five SmSPs in adult S. mansoni females and males. This highly sensitive method allowed visualization of low-abundantly expressed genes that are below the detection limits of standard in situ hybridization or by RNA sequencing. Thus, this technical approach turned out to be suitable for sensitive localization studies and may also be applicable for other trematodes. The results suggest that SmSPs may play roles in diverse processes of the parasite. Certain SmSPs expressed at the surface may be involved in host–parasite interactions. Graphic abstract

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Chronobiological aspects of the host-parasite relationships between Biomphalaria glabrata and Schistosoma mansoni: Cercarial production and infectivity, and growth kinetics of the host

Journal of Invertebrate Pathology ◽

10.1016/0022-2011(84)90014-4 ◽

1984 ◽

Vol 44 (2) ◽

pp. 209-213 ◽

Cited By ~ 9

Author(s):

A. Théron ◽

H. Moné

Keyword(s):

Schistosoma Mansoni ◽

Growth Kinetics ◽

Biomphalaria Glabrata ◽

Cercarial Production ◽

Host Parasite ◽

Kinetics Of

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Interactions between the plasma proteins of Biomphalaria glabrata (Gastropoda) and the sporocyst tegument of Schistosoma mansoni (Trematoda)

Parasitology ◽

10.1017/s0031182000065513 ◽

1986 ◽

Vol 92 (3) ◽

pp. 653-664 ◽

Cited By ~ 26

Author(s):

C. J. Bayne ◽

E. S. Loker ◽

Mary A. Yui

Keyword(s):

Schistosoma Mansoni ◽

Plasma Proteins ◽

Biomphalaria Glabrata ◽

Rabbit Antibody ◽

Tegumental Surface ◽

Immunological Interactions ◽

Resistant Strains ◽

Host Parasite ◽

Susceptibility And Resistance

SUMMARYThe tegumental surface of Schistosoma mansoni sporocysts is the site of both nutritive and immunological interactions with haemolymph cells and plasma of Biomphalaria glabrata, the schistosome intermediate host. Within minutes of being placed in host plasma, sporocysts acquire plasma antigens, and within 3 h host plasma antigens are present on the surface at near steady state. Though a wide variety of peptides is acquired, there is selection. Furthermore, some differences occur in the peptides acquired from the plasma of susceptible and resistant strains of snail. Acquired antigens are rapidly processed, and are predominantly undetectable in tegumental extracts after a few hours. In contrast, rabbit antibody on sporocysts remains in situ for at least 48 h, so under some conditions there is stable expression of certain tegumental antigenic determinants.These data, obtained using antibodies to snail plasma antigens and to sporocyst tegumental antigens, are discussed in the light of current ideas on the cellular and molecular basis of susceptibility and resistance in this host#parasite system.

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Transcriptome of the parasitic flatworm Schistosoma mansoni during intra-mammalian development

10.1101/757633 ◽

2019 ◽

Cited By ~ 3

Author(s):

Arporn Wangwiwatsin ◽

Anna V. Protasio ◽

Shona Wilson ◽

Christian Owusu ◽

Nancy E. Holroyd ◽

...

Keyword(s):

Gene Expression ◽

Schistosoma Mansoni ◽

Chronic Infection ◽

Egg Laying ◽

Mammalian Host ◽

Expression Data ◽

Mammalian Development ◽

Host Parasite Interactions ◽

Parasitic Flatworm ◽

Host Parasite

AbstractSchistosomes are parasitic blood flukes that survive for many years within the mammalian host vasculature. How the parasites establish a chronic infection in the hostile bloodstream environment, whilst evading the host immune response is poorly understood. The parasite develops morphologically and grows as it migrates to its preferred vascular niche, avoiding or repairing damage from the host immune system. In this study, we investigated temporal changes in gene expression during the intra-mammalian development of Schistosoma mansoni. RNA-seq data were analysed from parasites developing in the lung through to egg-laying mature adult worms, providing a comprehensive picture of in vivo intra-mammalian development. Remarkably, genes involved in signalling pathways, developmental control, and adaptation to oxidative stress were up-regulated in the lung stage. The data also suggested a potential role in immune evasion for a previously uncharacterised gene. This study not only provides a large and comprehensive data resource for the research community, but also reveals new directions for further characterising host–parasite interactions that could ultimately lead to new control strategies for this neglected tropical disease pathogen.Author SummaryThe life cycle of the parasitic flatworm Schistosoma mansoni is split between snail and mammalian (often human) hosts. An infection can last for more than 10 years, during which time the parasite physically interacts with its mammalian host as it moves through the bloodstream, travelling through the lungs and liver, to eventually establish a chronic infection in the blood vessels around the host gut. Throughout this complex journey, the parasite develops from a relatively simple larval form into a more complex, sexually reproducing adult. To understand the molecular basis of parasite interactions with the host during this complex journey we have produced genome-wide expression data from developing parasites. The parasites were collected from experimentally-infected mice over its developmental time-course from the poorly studied lung stage, to the fully mature egg-laying adult worm. The data highlight many genes involved in processes known to be associated with key stages of the infection. In addition, the gene expression data provide a unique view of interactions between the parasite and the immune system in the lung, including novel players in host-parasite interactions. A detailed understanding of these processes may provide new opportunities to design intervention strategies, particularly those focussed on the early stages of the infection that are not targeted by current chemotherapy.

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Transient non-susceptibility toSchistosoma mansoniassociated with atrial amoebocytic accumulations in the snail hostBiomphalaria glabrata

Parasitology ◽

10.1017/s0031182000057929 ◽

1987 ◽

Vol 95 (3) ◽

pp. 499-505 ◽

Cited By ~ 10

Author(s):

C. S. Richards ◽

D. J. Minchella

Keyword(s):

Population Dynamics ◽

Schistosoma Mansoni ◽

Genetic Control ◽

Old Age ◽

Biomphalaria Glabrata ◽

Egg Laying ◽

Snail Population ◽

Host Parasite ◽

Variable Susceptibility

SUMMARYIn someBiomphalaria glabrata–Schistosoma mansonicombinations snails are susceptible to infection as juveniles, but have variable susceptibility as adults. These snails become non-susceptible at the onset of egg-laying and typically revert to susceptibility in old age. Certain stocks ofB. glabratahave the capacity to form amoebocytic accumulations in the atrium, and this ability is under genetic control. The atrial amoebocytic accumulations are transitory, typically appearing at onset of egg-laying and disappearing after a few months. A snail stock which has genetic tendencies for both adult variable susceptibility and atrial amoebocytic accumulations was studied. An association between the time of occurrence of adult non-susceptibility and atrial accumulation is revealed as snails never became infected withS. mansoniwhen amoebocytic accumulations were present. Developing parasites, however, were not necessarily encapsulated and destroyed by amoebocytes. Some sporocysts were able to delay development until the amoebocytic accumulations disappeared. The timing of atrial amoebocytic accumulations and resulting transient non-susceptibility in this host-parasite combination could influence snail population dynamics.

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Compatibility Polymorphism Based on Long-Term Host-Parasite Relationships: Cross Talking Between Biomphalaria glabrata and the Trematode Schistosoma mansoni From Endemic Areas in Brazil

Frontiers in Immunology ◽

10.3389/fimmu.2019.00328 ◽

2019 ◽

Vol 10 ◽

Cited By ~ 4

Author(s):

Mariana G. Lima ◽

Lângia C. Montresor ◽

Joana Pontes ◽

Ronaldo de C. Augusto ◽

Jairo Pinheiro da Silva ◽

...

Keyword(s):

Schistosoma Mansoni ◽

Biomphalaria Glabrata ◽

Endemic Areas ◽

Host Parasite

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Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation

Parasitology ◽

10.1017/s0031182006000412 ◽

2006 ◽

Vol 133 (3) ◽

pp. 313-319 ◽

Cited By ~ 17

Author(s):

F. PRUGNOLLE ◽

T. DE MEEÛS ◽

J.P. POINTIER ◽

P. DURAND ◽

A. ROGNON ◽

...

Keyword(s):

Schistosoma Mansoni ◽

Local Adaptation ◽

Genetic Factors ◽

Biomphalaria Glabrata ◽

Metapopulation Dynamics ◽

Geographical Variations ◽

Transplantation Experiment ◽

Host Parasite ◽

Parasite Populations ◽

Transplantation Experiments

We investigated local adaptation in the spatially structured natural Biomphalaria glabrata/Schistosoma mansoni host-parasite system in the marshy forest focus of Guadeloupe using cross-transplantation experiments. We demonstrated strong and highly significant variations in susceptibility/infectivity of host and parasite populations, respectively, but found no evidence of local adaptation neither for S. mansoni nor for B. glabrata. Environmental as well as genetic factors are discussed to explain susceptibility/infectivity variations between both host and parasite populations. The absence of local adaptation is discussed in relation to the metapopulation dynamics of both host and parasite, in particular their relative rates of dispersal at the scale under scrutiny. Our study constitutes the first cross-transplantation experiment concerning this host-parasite system of which both hosts and parasites came directly from the wild, excluding laboratory generations and experimental host passages.

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Observations on two biological races of Schistosoma mansoni

Memórias do Instituto Oswaldo Cruz ◽

10.1590/s0074-02761981000300006 ◽

1981 ◽

Vol 76 (3) ◽

pp. 287-291 ◽

Cited By ~ 36

Author(s):

W. Lobato Paraense ◽

Lygia R. Corrêa

Keyword(s):

Comparative Study ◽

Schistosoma Mansoni ◽

Biomphalaria Glabrata ◽

Prepatent Period ◽

Snail Species ◽

Infection Rates ◽

Paulo State ◽

Minas Gerais State ◽

Belo Horizonte ◽

Host Parasite

A comparative study of the BH strain of Schistosoma mansoni from Belo Horizonte, Minas Gerais state, infective to Biomphalaria glabrata from the same locality, and the SJ strain from São José dos Campos, São Paulo state, infective to B. tenagophila from the latter locality, showed the following differences: 1. Length of adult worms and size of eggs significantly larger in the BH strain. 2. Higher infection rates in the B. glabrata-BH strain association than in the B. tenagophila-SJ strain association, following exposure of each snail to 1 or 10 miracidia. 3.Longer prepatent period (from penetration of miracidium to first shedding of cercariae) in the B. tenagophila-SJ strain association. 4. Infection of both Biomphalaria species when exposed to hybrid miracidia from crosses between the two strains, at lower levels than those resulting from exposure of each snail species to miracidia of the pure sympatric strain. (Both Biomphalaria populations are practically refractory to infection with the allopatric strain). These results are interpreted as pointing to a better host-parasite adjustment in the B. glabrata-BH strain association than in the B. tenagophila-SJ association. The interfertility between the two strains, which produced viable hybrids infective to both Biomphalaria species, supports the conclusion that the observed differences are merely intraspecific, and that the two strains may be considered distinct biological races of Schistosoma mansoni.

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