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.
Similar content being viewed by others
Data availability
PRIDE dataset identifier PXD023681.
References
Abbas MN, Kausar S, Cui H (2019) The biological role of peroxiredoxins in innate immune responses of aquatic invertebrates. Fish Shellfish Immunol 89:91–97. https://doi.org/10.1016/j.fsi.2019.03.062
Adema CM, Hanington PC, Lun C-M, Rosenberg GH, Aragon AD, Stout BA, Richard MLL, Gross PS, Loker ES (2010) Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 47:849. https://doi.org/10.1016/j.molimm.2009.10.019
Bouchut A, Sautiere PE, Coustau C, Mitta G (2006) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Trop 98:234–246. https://doi.org/10.1016/j.actatropica.2006.05.007
Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:1–8. https://doi.org/10.3389/fimmu.2014.00459
Castillo MG, Humphries JE, Mourão MM, Marquez J, Montelongo CE, Gonzalez A, Montelongo CE (2019) Biomphalaria glabrata immunity: post-genome advances. Dev Comp Immunol 104:103557. https://doi.org/10.1016/j.dci.2019.103557
Cavalcanti MGS, Filho FC, Mendonça AMB, Duarte GR, Barbosa CCGS, De Castro CMMB, Alves LC, Brayner FA (2012) Morphological characterization of hemocytes from Biomphalaria glabrata and Biomphalaria straminea. Micron 43:285–291. https://doi.org/10.1016/j.micron.2011.09.002
Coates CJ, Decker H (2017) Immunological properties of oxygen-transport proteins: hemoglobin, hemocyanin and hemerythrin. Cell Mol Life Sci 74:293–317. https://doi.org/10.1007/s00018-016-2326-7
Coates CJ, Nairn J (2014) Diverse immune functions of hemocyanins. Dev Comp Immunol 45:43–55. https://doi.org/10.1016/j.dci.2014.01.021
Colley DG, Bustinduy AL, Secor WE, King CH (2014) Human schistosomiasis. Lancet 383:2253–2264. https://doi.org/10.1016/S0140-6736(13)61949-2
Contreras-Garduño J, Lanz-Mendoza H, Franco B, Nava A, Pedraza-Reyes M, Canales-Lazcano J (2016) Insect immune priming: ecology and experimental evidences. Ecol Entomol 41:351–366. https://doi.org/10.1111/een.12300
Coustau C, Gourbal B, Duval D, Yoshino TP, Adema CM, Mitta G (2015) 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. Fish Shellfish Immunol 46:5–16. https://doi.org/10.1016/j.fsi.2015.01.036
Cox J, Mann M (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26:1367–1372. https://doi.org/10.1038/nbt.1511
Dolashka P, Voelter W (2013) Antiviral activity of hemocyanins. Invertebr Surviv J 10:120–127
Fogarty CE, Zhao M, McManus DP, Duke MG, Cummins SF, Wang T (2019) Comparative study of excretory–secretory proteins released by Schistosoma mansoni-resistant, susceptible and naïve Biomphalaria glabrata. Parasit Vectors 12:452. https://doi.org/10.1186/s13071-019-3708-0
Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway - its role in innate immunity and evolution. Immunol Rev 198:185–202. https://doi.org/10.1111/j.0105-2896.2004.0123.x
Gordy MA, Pila EA, Hanington PC (2015) The role of fibrinogen-related proteins in the gastropod immune response. Fish Shellfish Immunol 46:39–49. https://doi.org/10.1016/j.fsi.2015.03.005
Ittiprasert W, Miller A, Myers J, Nene V, El-Sayed NM, Knight M (2010) Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Mol Biochem Parasitol 169:27–39. https://doi.org/10.1016/j.molbiopara.2009.09.009
Lin D, Zeng X, Sanogo B, He P, Xiang S, Du S, Zhang Y, Wang L, Wan S, Zeng X, Yang Y, Lv Z, Liang Y, Deng Z, Hui JHL, Yuan D, Ding T, Wu Z, Sun X (2020) The potential risk of schistosoma mansoni transmission by the invasive freshwater snail biomphalaria straminea in south china. PLoS Negl Trop Dis 14:1–19. https://doi.org/10.1371/journal.pntd.0008310
Mitta G, Adema CM, Gourbal B, Loker ES, Theron A (2012) Compatibility polymorphism in snail/schistosome interactions: from field to theory to molecular mechanisms. Dev Comp Immunol 37:1–8. https://doi.org/10.1016/j.dci.2011.09.002
Peña JJ, Adema CM (2016) The planorbid snail biomphalaria glabrata expresses a hemocyanin-like sequence in the albumen gland. PLoS ONE 11:1–17. https://doi.org/10.1371/journal.pone.0168665
Pietrzyk-Brzezinska AJ, Bujacz A (2020) H-type lectins – structural characteristics and their applications in diagnostics, analytics and drug delivery. Int J Biol Macromol 152:735–747. https://doi.org/10.1016/j.ijbiomac.2020.02.320
Pila EA, Li H, Hambrook JR, Wu X, Hanington PC (2017) Schistosomiasis from a snail’s perspective: advances in snail immunity. Trends Parasitol 33:845–857. https://doi.org/10.1016/j.pt.2017.07.006
Pinaud S, Portela J, Duval D, Nowacki FC, Olive MA, Allienne JF, Galinier R, Dheilly NM, Kieffer-Jaquinod S, Mitta G, Théron A, Gourbal B (2016) A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathog 12:1–18. https://doi.org/10.1371/journal.ppat.1005361
Pinaud S, Portet A, Allienne JF, Belmudes L, Saint-Beat C, Arancibia N, Galinier R, Du Pasquier L, Duval D, Gourbal B (2019) Molecular characterisation of immunological memory following homologous or heterologous challenges in the schistosomiasis vector snail, Biomphalaria glabrata. Dev Comp Immunol 92:238–252. https://doi.org/10.1016/j.dci.2018.12.001
Portela J, Duval D, Rognon A, Galinier R, Boissier J, Coustau C, Mitta G, Théron A, Gourbal B (2013) Evidence for specific genotype-dependent immune priming in the lophotrochozoan biomphalaria glabrata snail. J Innate Immun 5:261–276. https://doi.org/10.1159/000345909
Qin Z, Babu VS, Wan Q, Muhammad A, Li J, Lan J, Lin L (2018) Antibacterial activity of hemocyanin from red swamp crayfish (Procambarus clarkii). Fish Shellfish Immunol 75:391–399. https://doi.org/10.1016/j.fsi.2018.02.010
Rey-Campos M, Moreira R, Gerdol M, Pallavicini A, Novoa B, Figueras A (2019) Immune tolerance in Mytilus galloprovincialis hemocytes after repeated contact with vibrio splendidus. Front Immunol 10:1–15. https://doi.org/10.3389/fimmu.2019.01894
Sanchez J-F, Lescar J, Chazalet V, Audfray A, Gagnon J, Alvarez R, Breton C, Imberty A, Mitchell EP (2006) Biochemical and structural analysis of Helix pomatia Agglutinin. J Biol Chem 281:20171–20180. https://doi.org/10.1074/jbc.M603452200
Scholte RGC, Carvalho OS, Malone JB, Utzinger J, Vounatsou P (2012) Spatial distribution of Biomphalaria spp., the intermediate host snails of Schistosoma mansoni, in Brazil. Geospat Health 6:S95–S101. https://doi.org/10.1016/j.jcv.2015.07.170
Sheehan G, Farrell G, Kavanagh K (2020) Immune priming: the secret weapon of the insect world. Virulence 11:238–246. https://doi.org/10.1080/21505594.2020.1731137
Stączek S, Zdybicka-Barabas A, Mak P, Sowa-Jasiłek A, Kedracka-Krok S, Jankowska U, Suder P, Wydrych J, Grygorczuk K, Jakubowicz T, Cytryńska M (2018) Studies on localization and protein ligands of Galleria mellonella apolipophorin III during immune response against different pathogens. J Insect Physiol 105:18–27. https://doi.org/10.1016/j.jinsphys.2017.12.009
Tetreau G, Pinaud S, Portet A, Galinier R, Gourbal B, Duval D (2017) Specific pathogen recognition by multiple innate immune sensors in an invertebrate. Front Immunol 8:1249. https://doi.org/10.3389/fimmu.2017.01249
Tyanova S, Temu T, Sinitcyn P, Carlson A, Hein MY, Geiger T, Mann M, Cox J (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods 13:731–740. https://doi.org/10.1038/nmeth.3901
Vergote D, Bouchut A, Sautière PE, Roger E, Galinier R, Rognon A, Coustau C, Salzet M, Mitta G (2005) Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 35:215–224. https://doi.org/10.1016/j.ijpara.2004.11.006
Wang L, Huang M, Zhang H, Song L (2011) The immune role of C-type lectins in molluscs. ISJ-Invertebrate Surviv J 8:241–246
Wang X-W, Zhao X-F, Wang J-X (2014) C-type lectin binds to β-integrin to promote hemocytic phagocytosis in an invertebrate. J Biol Chem 289:2405–2414. https://doi.org/10.1074/jbc.M113.528885
Wu X, Dinguirard N, Sabat G, Lui H, Gonzalez L, Gehring M, Bickham-wright U, Yoshino TP (2017) Proteomic analysis of Biomphalaria glabrata plasma proteins with binding affinity to those expressed by early developing larval Schistosoma mansoni. PLoS Pathog 13:1–30. https://doi.org/10.6019/PXD004942
Yang Ya, Cheng W, Wu X, Huang S, Deng Z, Zeng X, Yuan D, Yang Yu, Wu Z, Chen Y, Zhou Y, Jiang Q (2018) Prediction of the potential global distribution for Biomphalaria straminea, an intermediate host for Schistosoma mansoni. PLoS Negl Trop Dis 12:1–16. https://doi.org/10.1371/journal.pntd.0006548
Bender RC, Broderick EJ, Goodall CP, Christopher J, Bender RC, Broderick EJ, Goodall CP, Bayne CJ (2005) Respiratory burst of biomphalaria glabrata hemocytes : Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails published by : Allen Press on behalf of The American Society of Parasitologists Stable URL : https://www.js. J. Parasitol. 91, 275–279
Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M (2011) Andromeda : A peptide search engine integrated into the MaxQuant environment. J. Proteome reserach 1794–1805. https://doi.org/10.1021/pr101065j
de Melo ES, Brayner FA, Junior NCP, França IRS, Alves LC (2019) Investigation of defense response and immune priming in Biomphalaria glabrata and Biomphalaria straminea, two species with different susceptibility to Schistosoma mansoni. Parasitol. Res. 189–201. https://doi.org/10.1007/s00436-019-06495-4
Dinguirard N, Cavalcanti MGS, Wu X-J, Bickham-Wright U, Sabat G, Yoshino TP, S Cavalcanti MG, Wu X-J, Bickham-Wright U, Sabat G, Yoshino TP (2018) Proteomic analysis of Biomphalaria glabrata hemocytes during in vitro encapsulation of Schistosoma mansoni Sporocysts. Front Immunol 9, 1–17. https://doi.org/10.3389/fimmu.2018.02773
Galinier R, Portela J, Moné Y, Allienne JF, Henri H, Delbecq S, Mitta G, Gourbal B, Duval D (2013) Biomphalysin, a new β pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathog. 9. https://doi.org/10.1371/journal.ppat.1003216
Hanington PC, Forys MA, Loker ES (2012) A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl Trop Dis 6. https://doi.org/10.1371/journal.pntd.0001591
Li H, Hambrook JR, Pila EA, Gharamah AA, Fang J, Wu X, Hanington P (2020) Coordination of humoral immune factors dictates compatibility between Schistosoma mansoni and Biomphalaria glabrata. Elife 9. https://doi.org/10.7554/eLife.51708
Mitta G, Gourbal B, Grunau C, Knight M, Bridger JM, Théron A (2017) The compatibility between biomphalaria glabrata snails and Schistosoma mansoni, in: Advances in Parasitology. pp. 111–145. https://doi.org/10.1016/bs.apar.2016.08.006
Negrão-Corrêa D, Mattos ACA, Pereira CAJ, Martins-Souza RL, Coelho PMZ (2012) Interaction of schistosoma mansoni sporocysts and hemocytes of biomphalaria. J Parasitol Res 6. https://doi.org/10.1155/2012/743920
Rodrigues J, Brayner FA, Alves LC (2010) Innate immune memory in. Science (80-. ). 329, 1353–1356
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Ethics approval
FIOCRUZ Ethics and Use of Animals Committee (CEUA) protocol number 104/2016.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Ramaswamy Kalyanasundaram
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07341-2