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A proteomics evaluation of the primary and secondary immune response of Biomphalaria straminea challenged by Schistosoma mansoni

  • Immunology and Host-Parasite Interactions - Original Paper
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Abstract

Biomphalaria spp. snails are intermediary hosts of Schistosoma mansoni, etiologic agent of intestinal schistosomiasis, one of the most important neglected tropical diseases. Biomphalaria straminea is an important intermediary host that possess a different phenotype to parasite infection but shows a large geographic distribution and high capacity of new ecologic niche invasion. Our purpose was to characterize for the first time the differentially expressed proteome in B. straminea during two times intervals after primary and secondary exposure to S. mansoni. The hemolymph was collected at 1 and 15 days after primary and secondary exposure of snails to the parasite. Total proteins were extracted and digested with trypsin. LC–MS/MS label-free quantification was performed and analyzed using Maxquant and Perseus software. Proteins were identified and annotated using Blast2GO tools. After 1 day of exposure, most of upregulated proteins are hemoglobin type 2, C and H type lectins, molecules related to cell adhesion, and response to oxidative stress. After 15 days, we found a similar pattern of upregulated proteins but some fibrinogen-related proteins (FREPs) and TEPs homologs were downregulated. Regarding the differentially expressed proteins during secondary response, the principal immune-related proteins upregulated were C and H type lectins, cellular adhesion molecules, biomphalysin, and FREP3. We noted a several upregulated biological processes during both responses that could be the one of the key points of efficacy in the immune response to parasite. Our data suggests different immune mechanisms used by B. straminea snails challenged with S. mansoni.

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Data availability

PRIDE dataset identifier PXD023681.

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Acknowledgements

The authors thank FIOCRUZ for using the Technological Platforms Network and Immunopathology Keizo Asami Laboratory (LIKA/UFPE).

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD023681.

Funding

This study was supported by Oswaldo Cruz Fundation (FIOCRUZ – PROEP APQ number 1658–2.13/15); Fundação de Amparo a Ciência do Estado de Pernambuco, Brazil (FACEPE, APQ number 0279–2.13/15); and in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasil (CAPES), as a fellowship.

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All authors contributed to the study conception. Nairomberg Cavalcanti Portela Junior, Luiz Carlos Alves, and Elverson Soares de Melo – conceived the design of the proposal; Nairomberg Cavalcanti Portela Junior, Elverson Soares de Melo, Iasmin Lopes de Lima, and Rubens Emanoel Tavares da Rocha performed the methodology, lab experiments, and data analysis, Roberto Afonso, and José Luiz de Lima Filho provided complementary resources and analysis. Nairomberg Cavalcanti Portela Junior – writing original draft; Nairomberg Cavalcanti Portela Junior, Luiz Carlos Alves, and Fábio André Brayner and Ana Paula Sampaio Feitosa – writing, reviewing, and editing. Luiz Carlos Alves and Fábio André Brayner – funding acquisition and research supervision.

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Correspondence to Nairomberg Cavalcanti Portela Junior.

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FIOCRUZ Ethics and Use of Animals Committee (CEUA) protocol number 104/2016.

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Conflict of interest

The authors declare no competing interests.

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Section Editor: Ramaswamy Kalyanasundaram

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Junior, N.C.P., de Melo, E.S., de Lima, I.L. et al. A proteomics evaluation of the primary and secondary immune response of Biomphalaria straminea challenged by Schistosoma mansoni. Parasitol Res 120, 4023–4035 (2021). https://doi.org/10.1007/s00436-021-07341-2

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  • DOI: https://doi.org/10.1007/s00436-021-07341-2

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