During infection, the host and the parasite “communicate” with each other through various molecules, including proteins. The aim of this study was to describe the excretory–secretory proteins from the helminth Schistocephalus solidus and its intermediate host, the three-spined stickleback Gasterosteus aculeatus L., which are likely to be involved in interactions between them.
Combined samples of washes from the G. aculeatus sticklebacks cavity infected with the S. solidus, and washes from the parasite surface were used as experimental samples, while washes from the uninfected fish body cavity were used as control. The obtained samples were analyzed using mass-spectrometry nLC–MS/MS.
As a result of mass-spectrometry analysis 215 proteins were identified. Comparative quantitative analysis revealed significant differences in LFQ intensity between experimental and control samples for 20 stickleback proteins. In the experimental samples, we found an increase in the content of serpins, plasminogen, angiotensin 1–10, complement component C9, and a decrease in the content of triosephosphate isomerase, creatine kinase, fructose-biphosphate aldolase, superoxide dismutase, peroxidoxin-1, homocysteine-binding and fatty acid-binding proteins, compared to uninfected fish samples. In the experimental group washes, 30 S. solidus proteins were found, including malate dehydrogenase, annexin family proteins, serpins, peptidyl-prolyl cis–trans isomerase and fatty acid-binding protein.
Thus, the protein composition of washes from the helminth S. solidus surface and the body cavity of infected and uninfected stickleback G. aculeatus were studied. As a result, it was shown that various components of the immune defense system predominated in the washes of infected fish and helminths.
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Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37(4):420–423. https://doi.org/10.1038/s41587-019-0036-z
Alvite G, Esteves A (2016) Echinococcus granulosus fatty acid binding proteins subcellular localization. Exp Parasitol 164:1–4. https://doi.org/10.1016/j.exppara.2016.02.002
Barber I (2007) Host–parasite interactions of the three-spined stickleback. In: Ostlund-Nilsson S, Mayer I, Huntingford F (eds) Biology of the three-spined stickleback, 1st edn. CRC Press, New York, pp 271–318. https://doi.org/10.1201/9781420004830
Barber I (2013) Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends Parasitol 29(11):556–566. https://doi.org/10.1016/j.pt.2013.09.004
Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond Ser B Biol Sci 268(1462):71–76. https://doi.org/10.1098/rspb.2000.1331
Barber I, Scharsack JP (2010) The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137(3):411–424. https://doi.org/10.1017/S0031182009991466
Bell A, Monaghan P, Page AP (2006) Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int J Parasitol 36(3):261–276. https://doi.org/10.1016/j.ijpara.2005.11.003
Bendtsen JD, Jensen LJ, Blom N, von Heijne G, Brunak S (2004) Feature based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17(4):349–356. https://doi.org/10.1093/protein/gzh037
Berger CS, Laroche J, Maaroufi H, Martin H, Moon K-M, Landry CR, Foster LJ, Aubin-Horth N (2020) The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions. bioRxiv. https://doi.org/10.1101/2020.02.03.932509
Bień J, Sałamatin R, Sulima A, Savijoki K, Conn DB, Näreaho A, Młocicki D (2016) Mass spectrometry analysis of the excretory-secretory (E-S) products of the model cestode Hymenolepis diminuta reveals their immunogenic properties and the presence of new E-S proteins in cestodes. Acta Parasitol 61(2):429–442. https://doi.org/10.1515/ap-2016-0058
Binns D, Dimmer E, Huntley R, Barrell D, O’Donovan C, Apweiler R (2009) QuickGO: a web-based tool for gene ontology searching. Bioinformatics 25(22):3045–3046. https://doi.org/10.1093/bioinformatics/btp536
Brown NA, Antoniw J, Hammond-Kosack KE (2012) The predicted secretome of the plant pathogenic Fungus Fusarium graminearum: a refined comparative analysis. PLoS ONE 7(4):e33731. https://doi.org/10.1371/journal.pone.0033731
Cantacessi C, Seddon JM, Miller TL, Leow CY, Thomas L, Mason L, Willis C, Walker G, Loukas A, Gasser RB (2013) A genome-wide analysis of annexins from parasitic organisms and their vectors. Sci Rep 3:2898. https://doi.org/10.1038/srep02893
Chappell LH (1969) Parasites of three-spined stickleback Gasterosteus aculeatus L. from a Yorkshire pond 1. Seasonal variation of parasite fauna. J Fish Biol 1:137–152. https://doi.org/10.1111/j.1095-8649.1969.tb03848.x
Chen R, Kang R, Fan X, Tang D (2014) Release and activity of histone in diseases. Cell Death Dis 5:e1370. https://doi.org/10.1038/cddis.2014.337
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Coombs GH, Mottram JC (1997) Parasite proteinases and amino acid metabolism: possibilities for chemotherapeutic exploitation. Parasitology 114(Suppl):S61–S80
Cox JM (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
de Castro E, Sigrist CJA, Gattiker A, Bulliard V, Langendijk-Genevaux PS, Gasteiger E, Bairoch A, Hulo N (2006) ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res 34:W362–W365. https://doi.org/10.1093/Nar/Gkl124
Ehsan M, Wang W, Gadahi JA, Hasan MW, Lu MM, Wang YJ, Liu XC, Haseeb M, Yan RF, Xu LX, Song XK, Li XR (2018) The serine/threonine-protein phosphatase 1 from haemonchus contortus is actively involved in suppressive regulatory roles on immune functions of goat peripheral blood mononuclear cells. Front Immunol 9:1627. https://doi.org/10.3389/fimmu.2018.01627
Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300(4):1005–1016. https://doi.org/10.1006/jmbi.2000.3903
Farjo KM, Farjo RA, Halsey S, Moiseyev G, Ma JX (2012) Retinol-binding protein 4 induces inflammation in human endothelial cells by an NADPH oxidase- and nuclear factor kappa B-dependent and retinol-independent mechanism. Mol Cell Biol 32(24):5103–5115. https://doi.org/10.1128/MCB.00820-12
Folstad I, Hope AM, Andrew Karter A, Skorping A (1994) Sexually selected color in male sticklebacks—a signal of both parasite exposure and parasite resistance? Oikos 69(3):511–515. https://doi.org/10.2307/3545863
Fu Y-W, Zhu C-K, Zhang Q-Z, Hou T-L (2019) Molecular characterization, expression analysis, and ontogeny of complement component C9 in southern catfish (Silurus meridionalis). Fish Shellfish Immunol 86:449–458. https://doi.org/10.1016/j.fsi.2018.11.069
Giles N (1983) Behavioral effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback Gasterosteus aculeatus L. Anim Behav 31(4):1192–1194. https://doi.org/10.1016/S0003-3472(83)80025-6
Gomez S, Adalid-Peralta L, Palafox-Fonseca H, Cantu-Robles VA, Soberón X, Sciutto E, Fragoso G, Bobes RJ, Laclette JP, Yauner Ldel P, Ochoa-Leyva A (2015) Genome analysis of Excretory/Secretory proteins in Taenia solium reveals their Abundance of Antigenic Regions (AAR). Sci Rep 5:9683. https://doi.org/10.1038/srep09683
Hammerschmidt K, Kurtz J (2005) Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences. Int J Parasitol 35(14):1499–1507. https://doi.org/10.1016/j.ijpara.2005.08.011
Harnett W (2014) Secretory products of helminth parasites as immunomodulators. Mol Biochem Parasitol 195(2):130–136. https://doi.org/10.1016/j.molbiopara.2014.03.007
He L, Ren MY, Chen XQ, Wang XY, Li S, Lin JS, Liang C, Liang P, Hu Y, Lei HL (2008) Calcium-dependent proapoptotic effect of Taenia solium metacestodes annexin B1 on human eosinophils: a novel strategy to prevent host immune response. Int J Biochem Cell Biol 40:2151–2163. https://doi.org/10.1016/j.biocel.2008.02.018
He L, Ren MY, Chen XQ, Wang XY, Li S, Lin JS, Liang C, Liang P, Hu Y, Lei HL (2014) Biochemical and immunological characterization of annexin B30 from Clonorchis sinensis excretory/secretory products. Parasitol Res 113:2743–2755. https://doi.org/10.1007/s00436-014-3935-4
Hébert FO, Grambauer S, Barber I, Landry CR, Aubin-Horth N (2017) Major host transitions are modulated through transcriptome-wide reprogramming events in Schistocephalus solidus, a threespine stickleback parasite. Mol Ecol 26(4):1118–1130. https://doi.org/10.1111/mec.13970
Hoffman M, Pratt CW, Corbin LW, Church FC (1990) Characteristics of the chemotactic activity of heparin cofactor II proteolysis products. J Leukoc Biol 48(2):156–162. https://doi.org/10.1002/jlb.48.2.156
Hotamisligil GS, Bernlohr DA (2015) Metabolic functions of FABPs–mechanisms and therapeutic implications. Nat Rev Endocrinol 11(10):592–605. https://doi.org/10.1038/nrendo.2015.122
Hund AK, Fuess LE, Kenney ML, Maciejewski MF, Marini JM, Shim KC, Bolnick DI (2020) Rapid evolution of parasite resistance via improved recognition and accelerated immune activation and deactivation. bioRxiv. https://doi.org/10.1101/2020.07.03.186569
Kalle M, Papareddy P, Kasetty G, Tollefsen DM, Malmsten M, Mörgelin M, Schmidtchen A (2013) Proteolytic activation transforms heparin cofactor II into a host defense molecule. J Immunol 190(12):6303–6310. https://doi.org/10.4049/jimmunol.120303
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30. https://doi.org/10.1093/nar/28.1.27
Kobayashi Y, Yang T, Yu C-T, Ume C, Kubota H, Shimakura K, Shiomi K, Hamada-Sato N (2016) Quantification of major allergen parvalbumin in 22 species of fish by SDS-PAGE. Food Chem 194:345–353. https://doi.org/10.1016/j.foodchem.2015.08.037
Konijnendijk N, Raeymaekers J, Vandeuren S, Jacquemin L, Volckaert F (2013) Testing for local adaptation in the Gasterosteus-Gyrodactylus host–parasite system. Evol Ecol Res 15:489–502
Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. https://doi.org/10.1006/jmbi.2000.4315
Kuehn A, Scheuermann T, Hilger C, Hentges F (2010) Important variations in parvalbumin content in common fish species: a factor possibly contributing to variable allergenicity. Int Arch Allergy Immunol 153(4):359–366. https://doi.org/10.1159/000316346
Kurtz J, Kalbe M, Aeschlimann PB, Häberli MA, Wegner KM, Reusch TBH, Milinski M (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond Ser B Biol Sci 271:197–204. https://doi.org/10.1098/rspb.2003.2567
Li Y, Liu S, Qin Z, Yao J, Jiang C, Song L, Dunham R, Liu Z (2015) The serpin superfamily in channel catfish: identification, phylogenetic analysis and expression profiling in mucosal tissues after bacterial infections. Dev Comp Immunol 49(2):267–277. https://doi.org/10.1016/j.dci.2014.12.006
Lubzens E, Lissauer L, Levavi-Sivan B, Avarre JC, Sammar M (2003) Carotenoid and retinoid transport to fish oocytes and eggs: what is the role of retinol binding protein? Mol Aspects Med 24(6):441–457. https://doi.org/10.1016/s0098-2997(03)00040-2
Milinski M (1985) Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93(1/4):203–216
Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333
Mitchell AL, Attwood TK, Babbitt PC, Blum M, Bork P, Bridge A, Brown SD, Hsin-Yu C, El-Gebali S, Fraser MI, Julian Gough J, Haft DR, Huang H, Letunic I, Lopez R, Luciani A, Madeira F, Marchler-Bauer A, Mi H, Natale DA, Necci M, Nuka G, Orengo C, Pandurangan AP, Paysan-Lafosse T, Pesseat S, Potter SC, Qureshi MA, Rawlings ND, Redaschi N, Richardson LJ, Rivoire C, Salazar GA, Sangrador-Vegas A, Sigrist CJA, Sillitoe I, Sutton GG, Thanki N, Thomas PD, Tosatto SCE, Yong S-Y, Finn RD (2019) InterPro in 2019: improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res 47(Database issue):D351–D360. https://doi.org/10.1093/nar/gky1100
Molehin AJ, Gobert GN, McManus DP (2012) Serine protease inhibitors of parasitic helminthes. Parasitology 139(6):681–695. https://doi.org/10.1017/S0031182011002435
Nie A, Sun B, Fu Z, Dongsheng Y (2019) Roles of aminoacyl-tRNA synthetases in immune regulation and immune diseases. Cell Death Dis 10(12):901. https://doi.org/10.1038/s41419-019-2145-5
Ong JLY, Woo JM, Hiong KC, Ching B, Wong WP, Chew SF, Ip YK (2015) Molecular characterization of betaine-homocysteine methyltransferase 1 from the liver, and effects of aestivation on its expressions and homocysteine concentrations in the liver, kidney and muscle, of the African lungfish, Protopterus annectens. Comp Biochem Physiol B Biochem Mol Biol 183:30–41. https://doi.org/10.1016/j.cbpb.2014.12.007
Pennycuick L (1971) Differences in parasite infections in threespined sticklebacks (Gasterosteus aculeatus L.) of different sex, age and size. Parasitology 63(3):407–418. https://doi.org/10.1017/S0031182000079932
Pierleoni A, Martelli PL, Casadio R (2008) PredGPI: a GPI-anchor predictor. BMC Bioinform 9:392. https://doi.org/10.1186/1471-2105-9-392
Poulin R, Blanar CA, Thieltges DW, Marcogliese DJ (2011) The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34:540–551. https://doi.org/10.1111/j.1600-0587.2010.06826.x
Russell MJ, Klemmer AM, Olson KR (2001) Angiotensin signaling and receptor types in teleost fish. Comp Biochem Physiol A Mol Integr Physiol 128(1):41–51. https://doi.org/10.1016/s1095-6433(00)00296-8
Scharsack JP, Kalbe M, Derner R, Kurtz J, Milinski M (2004) Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Dis Aquat Organ 59(2):141–150. https://doi.org/10.3354/dao059141
Scharsack JP, Koch K, Hammerschmidt K (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host? Proc Biol Sci 274(1629):3151–3158. https://doi.org/10.1098/rspb.2007.1148
Scharsack JP, Gossens A, Franke F, Kurtz J (2013) Excretory products of the cestode, Schistocephalus solidus, modulate in vitro responses of leukocytes from its specific host, the three-spined stickleback (Gasterosteus aculeatus). Fish Shellfish Immunol 35(6):1779–1787. https://doi.org/10.1016/j.fsi.2013.08.029
Sekito A, Koide-Yoshida S, Niki T, Taira T, Iguchi-Ariga SM, Ariga H (2006) DJ-1 interacts with HIPK1 and affects H2O2-induced cell death. Free Radic Res 40(2):155–165. https://doi.org/10.1080/10715760500456847
Shawa PE (2002) Peptidyl-prolyl isomerases: a new twist to transcription. EMBO Rep 3(6):521–526. https://doi.org/10.1093/embo-reports/kvf118
Smyth DJ (1946) Studies on tapeworm physiology, the cultivation of Schistocephalus solidus in vitro. J Exp Biol 23:47–70
Song X, Hu D, Zhong X, Wang N, Gu X, Wang T, Peng X, Yang G (2016) Characterization of a secretory annexin in Echinococcus granulosus. Am J Trop Med Hyg 94(3):626–633. https://doi.org/10.4269/ajtmh.15-0452
Tararam CA, Farias LP, Wilson RA, de Cerqueira Leite LC (2010) Schistosoma mansoni annexin 2: molecular characterization and immunolocalization. Exp Parasitol 126:146–155. https://doi.org/10.1016/j.exppara.2010.04.008
Välikangas T, Suomi T, Elo LL (2018) A comprehensive evaluation of popular proteomics software workflows for label-free proteome quantification and imputation. Brief Bioinform 19(6):1344–1355. https://doi.org/10.1093/bib/bbx054
Venold FF, Penn MH, Thorsen J, Gu J, Kortner TM, Krogdahl A, Bakke AM (2013) Intestinal fatty acid binding protein (fabp2) in Atlantic salmon (Salmo salar): localization and alteration of expression during development of diet induced enteritis. Comp Biochem Physiol A Mol Integr Physiol 164(1):229–240. https://doi.org/10.1016/j.cbpa.2012.09.009
Vrtílek M, Bolnick DI (2020) Phylogenetically conserved peritoneal fibrosis response to an immunologic adjuvant in ray-finned fishes. bioRxiv. https://doi.org/10.1101/2020.07.08.191601
Wang H, Ding C, Wang J, Zhao X, Jin S, Liang J, Luo H, Li D, Li R, Li Y, Xiao T (2019) Molecular cloning and expression analysis of coagulation factor VIII and plasminogen involved in immune response to GCRV, and immunity activity comparison of grass carp Ctenopharyngodon idella with different viral resistance. Fish Shellfish Immunol 86:794–804. https://doi.org/10.1016/j.fsi.2018.12.024
Wang S, Wei W, Cai X (2015) Genome-wide analysis of excretory/secretory proteins in Echinococcus multilocularis: insights into functional characteristics of the tapeworm secretome. Parasit Vectors 8:666. https://doi.org/10.1186/s13071-015-1282-7
Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232. https://doi.org/10.1046/j.1420-9101.2003.00519.x
Zheng Y, Blair D, Bradley J (2013) Phyletic distribution of fatty acid-binding protein genes. PLoS ONE 8(10):e77636. https://doi.org/10.1371/journal.pone.0077636
Zi M, Xu Y (2018) Involvement of cystatin C in immunity and apoptosis. Immunol Lett 196:80–90. https://doi.org/10.1016/j.imlet.2018.01.006
The reported study was funded by Russian Foundation for Basic Research (project number 19-34-90095). The research was carried out using the equipment of the Core Facility of the Karelian Research Centre of the Russian Academy of Sciences. The mass-spectrometric analysis was performed using equipment of “Human proteome” Core Facility (IBMC, Moscow, Russia). The sex and age determination of G. aculeatus was performed by Dr. Sterligova Olga (Laboratory for Fish and Water Invertebrate Ecology of Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences). We also express our gratitude to PhD Balan Olga (Laboratory for Genetics Institute of Biology KarRC RAS) for the assistance provided in conducting this research.
The reported study was funded by Russian Foundation for Basic Research (project number 19-34-90095).
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All animal handling procedures were approved by the Ethics and Animal Care Committee of the Institute of Biology, Karelian Research Centre of the Russian Academy of Sciences, following EU-established norms and procedures.
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Kochneva, A., Borvinskaya, E. & Smirnov, L. Zone of Interaction Between the Parasite and the Host: Protein Profile of the Body Cavity Fluid of Gasterosteus aculeatus L. Infected with the Cestode Schistocephalus solidus (Muller, 1776). Acta Parasit. (2021). https://doi.org/10.1007/s11686-020-00318-8
- Schistocephalus solidus
- Gasterosteus aculeatus
- Host–parasite interaction
- Excretory–secretory proteins