Pathogen recognition molecules from hemocytes of Planorbarius corneus molluscs (Planorbidae, Pulmonata)
DOI:
https://doi.org/10.33910/2686-9519-2024-16-1-36-55Keywords:
Planorbarius corneus, Bilharziella polonica, trematode invasion, hemocytes, immune reactions, transcriptome, pathogen recognition molecules, lectinsAbstract
Investigations of the innate immunity of molluscs are necessary to understand the evolution of the immune system. In this work, for the first time, a transcriptome of hemocytes from Planorbarius corneus molluscs infected with Bilharziella polonica (Schistosomatidae) trematodes was obtained and analyzed. The assemblies were found to contain transcripts encoding all major groups of factors of innate immunity. Pathogen recognition molecules turned out to be the most numerous groups of immune factors. Based on the nucleotide sequences of transcripts, the study allowed to predict the domain structure of proteins encoded in them. The analysis covered the composition of lectin domains, Toll-like receptors, adhesion molecules, and toxins. The hemocyte of Planorbarius corneus molluscs was found to have a wide variety of pathogen recognition molecules. The obtained data obtained expand the knowledge about the immune responses of mollusсs to trematode invasion and make it possible to consider P. corneus a new model organism for studying the defense reactions of molluscs.
References
Adema, C. M., Hertel, L. A., Miller, R. D., Loker, E. S. (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. PNAS, vol. 94, no. 16, pp. 8691–8696. https://doi.org/10.1073/pnas.94.16.8691 (In English)
Adema, C. M., Hillier, L. W., Jones, C. S. et al. (2017) Whole genome analysis of a schistosomiasistransmitting freshwater snail. Nature Communications, vol. 16, no. 8, article 15451. https://doi.org/10.1038/ncomms15451 (In English)
Adema, C. M., Loker, E. S. (2015) Digenean-gastropod host associations inform on aspects of specific immunity in snails. Developmental and Comparative Immunology, vol. 48, no. 2, pp. 275–283. https://doi.org/10.1016/j.dci.2014.06.014 (In English)
Allan, E. R. O., Yang, L., Tennessen, J. A., Blouin, M. S. (2019) Allelic variation in a single genomic region alters the hemolymph proteome in the snail Biomphalaria glabrata. Fish and Shellfish Immunology, vol. 88, pp. 301–307. https://doi.org/10.1016/j.fsi.2019.02.065 (In English)
Angata, T., Brinkman-Van der Linden, E. C. M. (2002) I-type lectins. Biochim Biophys Acta, vol. 1572, no. 2–3, pp. 294–316. https://doi.org/10.1016/s0304-4165(02)00316-1 (In English)
Ataev, G. L., Polevshchikov, A. V. (2004) Zashchitnye reaktsii bryukhonogikh mollyuskov. 1. Kletochnye reaktsii [Protective reactions of Gastropod molluscs. 1. Cell reactions]. Parazitologiya, vol. 38, no. 4, pp. 342–351. (In Russian)
Ataev, G. L., Prokhorova, E. E., Kudryavtsev, I. V., Polevshchikov, A. V. (2016) The influence of trematode infection on the hemocyte composition in Planorbarius corneus (Gastropoda, Pulmonata). Invertebrate Survival Journal, vol. 13, no. 1, pp. 164–171. (In English)
Ataev, G. L., Prokhorova, E. E., Tokmakova, A. S. (2020) Zashchitnye reaktsii legochnykh mollyuskov pri parazitarnoj invazii [Defense reactions of pulmonate molluscs during parasitic invasion]. Parazitologiya, vol. 54, no. 5, pp. 371–401. https://doi.org/10.31857/S1234567806050028 (In Russian)
Berwin, B., Hart, J. P., Rice, S. et al. (2003) Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. The EMBO Journal, vol. 22, no. 22, pp. 6127–6136. https://doi.org/10.1093/emboj/cdg572 (In English)
Blanc, G., Font, B., Eichenberger, D. et al. (2007) Insights into how CUB domains can exert specific functions while sharing a common fold: conserved and specific features of the CUB1 domain contribute to the molecular basis of procollagen C-proteinase enhancer-1 activity. Journal of Biological Chemistry, vol. 282, no. 23, pp. 16924–16933. https://doi.org/10.1074/jbc.M701610200 (In English)
Bowie, A., O’Neill, L. A. J. (2000) The interleukin-1 receptor/Toll-like receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. Journal of Leukocyte Biology, vol. 67, no. 4, pp. 508–514. https://doi.org/10.1002/jlb.67.4.508 (In English)
Bridger, J. M., Brindley, P. J., Knight, M. (2018) The snail Biomphalaria glabrata as a model to interrogate the molecular basis of complex human diseases. PLoS Neglected Tropical Diseases, vol. 12, no. 8, article e0006552. https://doi.org/10.1371/journal.pntd.0006552 (In English)
Brown, R., Soldanova, M., Barrett, J., Kostadinova, A. (2011) Small-scale to large-scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe. Parasitology Research, vol. 108, pp. 137–150. https://doi.org/10.1007/s00436-010-2047-z (In English)
Chen, H., Cai, X., Li, R. et al. (2022) A novel toll-like receptor from Crassostrea gigas is involved in innate immune response to Vibrio alginolyticus. Infection, Genetics and Evolution, vol. 97, article 105159 https://doi.org/10.1016/j.meegid.2021.105159 (In English)
Clemmensen, I., Petersen, L. C., Kluft, C. (1986) Purification and characterization of a novel, oligomeric, plasminogen kringle-4 binding protein from human plasma: tetranectin. European Journal of Biochemistry, vol. 156, no. 2, pp. 327–333. https://doi.org/10.1111/j.1432-1033.1986.tb09586.x (In English)
Dheilly, N. M., Duval, D., Mouahid, G. et al. (2015) A family of variable immunoglobulin and lectin domain containing molecules in the snail Biomphalaria glabrata. Developmental and Comparative Immunology, vol. 48, no. 1, pp. 234–243. https://doi.org/10.1016/j.dci.2014.10.009 (In English)
Donaghy, L., Hong, H.-K., Lambert, C. et al. (2010) First characterisation of the populations and immunerelated activities of hemocytes from two edible gastropod species, the disk abalone, Haliotis discus discus and the spiny top shell, Turbo cornutus. Fish & Shellfish Immunology, vol. 28, no. 1, pp. 87–97. https://doi.org/10.1016/j.fsi.2009.10.006 (In English)
Du, Y., Shi, H., Guo, Q. et al. (2023) Hirudomacin: a Protein with Dual Effects of Direct Bacterial Inhibition and Regulation of Innate Immunity. Applied and Environmental Microbiology, vol. 89, no. 7, article e0052723. https://doi.org/10.1128/aem.00527-23 (In English)
Faltynkova, A., Našincova, V., Kablaskova, L. (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Systematic Parasitology, vol. 69, pp. 155–178. https://doi.org/10.1007/s11230-007-9127-1 (In English)
Fraser, I. P., Koziel, H., Ezekowitz, R. A. B. (1998) The serum mannose-binding protein and the macrophage mannose receptor are pattern recognition molecules that link innate and adaptive immunity. Seminars in Immunology, vol. 10, no. 5, pp. 363–372. https://doi.org/10.1006/smim.1998.0141 (In English)
Fu, L., Niu, B., Zhu, Z. et al. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics, vol. 28, no. 23, pp. 3150–3152. https://doi.org/10.1093/bioinformatics/bts565 (In English)
Galinier, R., Portela, J., Mone, Y. et al. (2013). Biomphalysin, a new β pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathogens, vol. 9, no. 3., article e1003216. https://doi.org/10.1371/journal.ppat.1003216 (In English)
Gong, H., Kobayashi, K., Sugi, T. et al. (2012) A novel PAN/apple domain-containing protein from Toxoplasma gondii: characterization and receptor identification. PLoS One, vol. 7, no. 1, article e30169. https://doi.org/10.1371/journal.pone.0030169 (In English)
Gordy, M. A., Pila, E. A., Hanington, P. C. (2015) The role of fibrinogen-related proteins in the gastropod immune response. Fish & Shellfish Immunology, vol. 46, no. 1, pp. 39–49. https://doi.org/10.1016/j.fsi.2015.03.005 (In English)
Gough, P. J., Gordon, S. (2000) The role of scavenger receptors in the innate immune system. Microbes and Infections, vol. 2, no. 3, pp. 305–311. https://doi.org/10.1016/s1286-4579(00)00297-5 (In English)
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z. et al. (2011). Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature biotechnology, vol. 29, pp. 644–652. https://doi.org/10.1038/nbt.1883 (In English)
Graversen, J. H., Sigurskjold, B. W., Thogersen, H. C., Etzerodt, M. (2000) Tetranectin-binding site on plasminogen kringle-4 involves the lysine-binding pocket and at least one additional amino acid residue. Biochemistry, vol. 39, no. 25, pp. 7414–7419. https://doi.org/10.1021/bi000155j (In English)
Hall, T. A. (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, vol. 41, no. 2, pp. 95–98. (In English)
Hanington, P. C., Forys, M. A., Dragoo, J. W. et al. (2010a) Role for a somatically diversified lectin in the resistance of an invertebrate to parasite infection. PNAS, vol. 107, no. 49, pp. 21087–21092. https://doi.org/10.1073/pnas.1011242107 (In English)
Hanington, P. C., Forys, M. A., Loker, E. S. (2012) A somatically diversified defense factor, FREP3, is a determinant of snail resistance to Schistosome infection. PLoS Neglected Tropical Diseases, vol. 6, no. 3, article e1591. https://doi.org/10.1371/journal.pntd.0001591 (In English)
Hanington, P. C., Lun, C.-M., Adema, C. M., Loker, E. S. (2010b) Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. International Journal of Parasitology, vol. 40, no. 7, pp. 819–831. https://doi.org/10.1016/j.ijpara.2009.12.005 (In English)
Hashimoto, C., Hudson, K. L., Anderson, K. V. (1988) The Toll gene of Drosophila, required for dorsalventral embryonic polarity, appears to encode a transmembrane protein. Cell, vol. 52, no. 2, pp. 269–279. https://doi.org/10.1016/0092-8674(88)90516-8 (In English)
Hernandez, J. D., Baum, L. G. (2002) Ah, sweet mystery of death! Galectins and control of cell fate. Glycobiology, vol. 12, no. 10, pp. 127R–136R. https://doi.org/10.1093/glycob/cwf081 (In English)
Huang, M., Song, X., Zhao, J. et al (2013) A C-type lectin (AiCTL-3) from bay scallop Argopecten irradians with mannose/galactose binding ability to bind various bacteria. Gene, vol. 531, no. 1, pp. 31–38. https://doi.org/10.1016/j.gene.2013.08.042 (In English)
Inohara, N., Nunez, G. (2002) ML — a conserved domain involved in innate immunity and lipid metabolism. Trends in Biochemical Sciences, vol. 27, no. 5, pp. 219–221. https://doi.org/10.1016/s0968-0004(02)02084-4 (In English)
Ittiprasert, W., Miller, A., Myers, J. et al. (2010) Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Molecular and biochemical parasitology, vol. 169, no. 1, pp. 27–39. https://doi.org/j.molbiopara.2009.09.009 (In English)
Janeway, C. A. Jr., Medzhitov, R. (2002). Innate immune recognition. Annual Review of Immunology, vol. 20, pp. 197–216. https://doi.org/10.1146/annurev.immunol.20.083001.084359 (In English)
Jung, S., Sonnichsen, F. D., Hung, C.-W. et al. (2012) Macin family of antimicrobial proteins combines antimicrobial and nerve repair activities. Journal of Biological Chemistry, vol. 287, no. 17, pp. 14246–14258. https://doi.org/10.1074/jbc.M111.336495 (In English)
Kanzok, S. M., Hoa, N. T., Bonizzoni, M. et al. (2004) Origin of Toll-like receptor-mediated innate immunity. Journal of Molecular Evolution, vol. 58, pp. 442–448. https://doi.org/10.1007/s00239-003-2565-8 (In English)
Kim, D., Langmead, B., Salzberg, S. L. (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods, vol. 12, no. 4, pp. 357–360. https://doi.org/10.1038/nmeth.3317 (In English)
Kim, J. Y., Kim, Y. M., Cho, S. K. et al. (2008) Noble tandem-repeat galectin of Manila clam Ruditapes philippinarum is induced upon infection with the protozoan parasite Perkinsus olseni. Developmental and comparative immunology, vol. 32, no. 10, pp. 1131–1141. https://doi.org/10.1016/j.dci.2008.03.002 (In English)
Kohda, D., Morton, C. J., Parkar, A. A. et al. (1996) Solution structure of the link module: a hyaluronanbinding domain involved in extracellular matrix stability and cell migration. Cell, vol. 86, no. 5, pp. 767–775. https://doi.org/10.1016/s0092-8674(00)80151-8 (In English)
Kokryakov, V. N. (2006) Ocherki o vrozhdennom immunitete [Essays on innate immunity]. Saint-Petersburg: Nauka Publ., 261 p. (In Russian)
Kron, N. S. (2022) In search of the Aplysia immunome: an in silico study. BMC Genomics, vol. 23, article 543. https://doi.org/10.1186/s12864-022-08780-6 (In English)
Kumar, H., Kawai, T., Akira, S. (2011) Pathogen recognition by the innate immune system. International Reviews of Immunology, vol. 30, no. 1, pp. 16–34. https://doi.org/10.3109/08830185.2010.529976 (In English)
Lemaitre, B., Nicolas, E., Michaut, L. et al. (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell, vol. 86, no. 6, pp. 973–983. https://doi.org/10.1016/S0092-8674(00)80172-5 (In English)
Letunic, I., Khedkar, S., Bork, P. (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Research, vol. 49, no. D1, pp. D458–D460. https://doi.org/10.1093/nar/gkaa937 (In English)
Li, H., Gharamah, A. A., Hambrook, J. R. et al. (2022) Single-cell RNA-seq profiling of individual Biomphalaria glabrata immune cells with a focus on immunologically relevant transcripts. Immunogenetics, vol. 74, pp. 77–98. https://doi.org/10.1007/s00251-021-01236-3 (In English)
Li, H., Hambrook, J. R., Pila, E. A. et al. (2020) Coordination of humoral immune factors dictates compatibility between Schistosoma mansoni and Biomphalaria glabrata. eLife, vol. 9, article e51708. https://doi.org/10.7554/eLife.51708 (In English)
Liu, C., Jiang, S., Wang, M. et al. (2016) A novel siglec (CgSiglec-1) from the Pacific oyster (Crassostrea gigas) with broad recognition spectrum and inhibitory activity to apoptosis, phagocytosis and cytokine release. Developmental and Comparative Immunology, vol. 61, pp. 136–144. https://doi.org/10.1016/j.dci.2016.03.026 (In English)
Liu, L., Yang, J., Qiu, L. et al. (2011) A novel scavenger receptor-cysteine-rich (SRCR) domain containing scavenger receptor identified from mollusk mediated PAMP recognition and binding. Developmental and Comparative Immunology, vol. 35, no. 2, pp. 227–239 https://doi.org/10.1016/j.dci.2010.09.010 (In English)
Loker, E. S., Adema, C. M., Zhang, S.-M., Kepler, T. (2004) Invertebrate immune systems — not homogeneous, not simple, not well understood. Immunological Reviews, vol. 198, no. 1, pp. 10–24. https://doi.org/10.1111/j.0105-2896.2004.0117.x (In English)
Lu, L., Bu, L., Zhang, S.-M. et al. (2022) An Overview of Transcriptional Responses of Schistosome-Susceptible (M line) or -Resistant (BS-90) Biomphalaria glabrata Exposed or Not to Schistosoma mansoni Infection. Frontiers in Immunology, vol. 12, article 805882. https://doi.org/10.3389/fimmu.2021.805882 (In English)
Lv, Z., Qiu, L., Wang, W. et al. (2020) The Members of the Highly Diverse Crassostrea gigas Integrin Family Cooperate for the Generation of Various Immune Responses. Frontiers in Immunology, vol. 11, article 1420. https://doi.org/10.3389/fimmu.2020.01420 (In English)
Marcel, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal, vol. 17, no. 1, pp. 10–12. https://doi.org/10.14806/ej.17.1.200 (In English)
Mone, Y., Gourbal, B., Duval, D. et al. (2010) A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Neglected Tropical Diseases, vol. 4, no. 9, article e813. https://doi.org/10.1371/journal.pntd.0000813 (In English)
Murphy, J. E., Tedbury, P. R., Homer-Vanniasinkam, S. et al. (2005) Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis, vol. 182, no. 1, pp. 1–15. https://doi.org/10.1016/j.atherosclerosis.2005.03.036. (In English)
Natarajan, K., Mage, M. G., Margulies, D. H. (2015) Immunoglobulin Superfamily. [Online]. Available at: https://doi.org/10.1002/9780470015902.a0000926.pub2 (accessed 12.12.2023) (In English)
Oreste, U., Ametrano, A., Coscia, M. R. (2021) On Origin and Evolution of the Antibody Molecule. Biology, vol. 10, no. 2, article 140. https://doi.org/10.3390/biology10020140 (In English)
Orlov, I. A., Ataev, G. L., Gourbal, B. et al. (2023) The transcriptomic analysis of Planorbarius corneus hemocytes (Gastropoda) naturally infected with Bilharziella polonica (Schistosomatidae). Developmental and Comparative Immunology, vol. 140, article 104607. https://doi.org/10.1016/j.dci.2022.104607 (In English)
Patro, R., Duggal, G., Love, M. I. et al. (2017) Salmon provides fast and bias-aware quantification of transcript expression. Nature Methods, vol. 14, pp. 417–419. https://doi.org/10.1038/nmeth.4197 (In English)
Peterson, N. A., Hokke, C. H., Deelder, A. M., Yoshino, T. P. (2009) Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: Differential expression during the miracidiumto-sporocyst transformation. International Journal for Parasitology, vol. 39, no. 12, pp. 1331–1344. https://doi.org/10.1016/j.ijpara.2009.06.002 (In English)
Pila, E. A., Li, H., Hambrook, J. R. et al. (2017) Schistosomiasis from a Snail’s Perspective: Advances in Snail Immunity. Trends in parasitology, vol. 33, no. 11, pp. 845–857. https://doi.org/10.1016/j.pt.2017.07.006 (In English)
Pinaud, S., Portela, J., Duval, D. et al. (2016) A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata. PLOS Pathogens. Vol. 12, no. 1, article e1005361. https://doi.org/10.1371/journal.ppat.1005361 (In English)
Pinaud, S., Portet, A., Allienne, J.-F. et al. (2019) Molecular characterisation of immunological memory following homologous or heterologous challenges in the schistosomiasis vector snail, Biomphalaria glabrata. Developmental and Comparative Immunology, vol. 92, pp. 238–252. https://doi.org/10.1016/j.dci.2018.12.001 (In English)
Portela, J., Duval, D., Rognon, A. et al. (2013) Evidence for specific genotype-dependent immune priming in the Lophotrochozoan Biomphalaria glabrata snail. Journal of Innate Immunity, vol. 5, no. 3, pp. 261–276. https://doi.org/10.1159/000345909 (In English)
Prabhudas, M., Bowdish, D., Drickamer, K. et al. (2014) Standardizing scavenger receptor nomenclature. Journal of Immunology, vol. 192, no. 5, pp. 1997–2006. https://doi.org/10.4049/jimmunol.1490003 (In English)
Ren, Y., Liu, H., Fu, S. et al. (2021) Transcriptome-wide identification and characterization of toll-like receptors response to Vibrio anguillarum infection in Manila clam (Ruditapes philippinarum). Fish & Shellfish Immunology, vol. 111, pp. 49–58. https://doi.org/10.1016/j.fsi.2021.01.007 (In English)
Saco, A., Novoa, B., Greco, S. et al. (2023) Bivalves Present the Largest and Most Diversified Repertoire of Toll-Like Receptors in the Animal Kingdom, Suggesting Broad-Spectrum Pathogen Recognition in Marine Waters. Molecular Biology and Evolution, vol. 40, no. 6, article msad133. https://doi.org/10.1093/molbev/msad133 (In English)
Schikorski, D., Cuvillier-Hot, V., Leippe, M. et al. (2008) Microbial challenge promotes the regenerative process of the injured central nervous system of the medicinal leech by inducing the synthesis of antimicrobial peptides in neurons and microglia. Journal of Immunology, vol. 181, no. 2, pp. 1083–1095. https://doi.org/10.4049/jimmunol.181.2.1083 (In English)
Schumacher, C., Wang, H., Honer, C. et al. (2000) The SCAN domain mediates selective oligomerization. The Journal of Biological Chemistry, vol. 275, no. 22, pp. 17173–17179. https://doi.org/10.1074/jbc.M000119200 (In English)
Seppala, O., Walser, J.-C., Cereghetti, T. et al. (2021) Transcriptome profiling of Lymnaea stagnalis (Gastropoda) for ecoimmunological research. BMC Genomics, vol. 22, article 144. https://doi.org/10.1186/s12864-021-07428-1 (In English)
Seppey, M., Manni, M., Zdobnov, E. M. (2019). BUSCO: assessing genome assembly and annotation completeness. Methods in Molecular Biology, vol. 1962, pp. 227-245. https://doi.org/10.1007/978-1-4939-9173-0_14 (In English)
Serebryakova, M. K., Tokmakova, A. S., Prokhorova, E. E., Ataev, G. L. (2022) Changes in the cell composition of the hemolymph in the snail Planorbarius corneus after infection with the trematode Plagiorchis sp. Invertebrate Biology, vol. 141, no. 4, article e12389. https://doi.org/10.1111/ivb.12389 (In English)
Schultz, J. H., Bu, L., Adema, C, M. (2018) Comparative immunological study of the snail Physella acuta (Hygrophila, Pulmonata) reveals shared and unique aspects of gastropod immunobiology. Molecular Immunology, vol. 101, pp. 108–119. https://doi.org/10.1016/j.molimm.2018.05.029 (In English)
Sivakamavalli, J., Park, K., Kwak, I.-S., Vaseeharan, B. (2021) Purification and partial characterization of carbohydrate-recognition protein C-type lectin from Hemifusus pugilinus. Carbohydrate Research, vol. 499, article 108224. https://doi.org/10.1016/j.carres.2020.108224 (In English)
Sminia, T, van der Knaap, W. P. W. (1987) Cells and molecules in molluscan immunology. Developmental and Comparative Immunology, vol. 11, no. 1, pp. 17–28. https://doi.org/10.1016/0145-305x(87)90004-8 (In English)
Smith-Unna, R., Boursnell, C., Patro, R. et al. (2016) TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Research, vol. 26, no. 8, pp. 1134–1144. https://doi.org/10.1101/gr.196469.115 (In English)
Tenner, A. J. (1998) C1q receptors: regulating specific functions of phagocytic cells. Immunobiology, vol. 199, no. 2, pp. 250–264. https://doi.org/10.1016/S0171-2985(98)80031-4 (In English)
Tetreau, G., Pinaud, S., Portet, A. et al. (2017) Specific pathogen recognition by multiple innate immune sensors in an invertebrate. Frontiers In Immunology, vol. 8, article 1249. https://doi.org/10.3389/fimmu.2017.01249
Unno, H., Matsuyama, K., Tsuji, Y. et al. (2016) Identification, Characterization, and X-ray Crystallographic Analysis of a Novel Type of Mannose-Specific Lectin CGL1 from the Pacific Oyster Crassostrea gigas. Scientific reports, vol. 6, article 29135. https://doi.org/10.1038/srep29135 (In English)
Van der Knaap, W. P. W. (1981) Recognition of foreignness in the internal defense system of the freshwater gastropod Lymnaea stagnalis. In: J. B. Solomon (ed.). Aspects of Developmental and Comparative Immunology. Proceedings of the 1st Congress of Developmental and Comparative Immunology, 27 July — 1 August 1980, Aberdeen. Aberdeen: Pergamon Press, pp. 91–97. https://doi.org/10.1016/B978-0-08-025922-2.50018-8 (In English)
Varki, A., Cummings, R. D., Esko, J. D., et al. (eds.). (2022) Essentials of Glycobiology. 4th ed. New York: Cold Spring Harbor Laboratory Press, 859 p. https://pubmed.ncbi.nlm.nih.gov/35536922 (In English)
Vasta, G. R., Ahmed. H. (eds.). (2008) Animal lectins. A functional view. Boca Raton: CRC Press, 596 p. https://doi.org/10.1201/9781420006971 (In English)
Vogel, C., Teichmann, S. A., Chothia, C. (2003) The immunoglobulin superfamily in Drosophila melanogaster and Caenorhabditis elegans and the evolution of complexity. Development, vol. 130, no. 25, pp. 6317–6328. https://doi.org/10.1242/dev.00848 (In English)
Wang, P., Zhang, Z., Xu, Z. et al. (2019) A novel invertebrate toll-like receptor with broad recognition spectrum from thick shell mussel Mytilus coruscus. Fish & Shellfish Immunology, vol. 89, pp. 132–140. https://doi.org/10.1016/j.fsi.2019.03.059 (In English)
Wang, W., Song, X., Wang, L., Song, L. (2018) Pathogen-Derived Carbohydrate Recognition in Molluscs Immune Defense. International Journal of Molecular Sciences, vol. 19, no. 3, article 721. https://doi.org/10.3390/ijms19030721 (In English)
Watson, A., Agius, J., Ackerly, D. et al. (2022) The Role of Anti-Viral Effector Molecules in Mollusc Hemolymph. Biomolecules, vol. 12, no. 3, article 345. https://doi.org/10.3390/biom12030345 (In English)
Worthley, D. L., Bardy, P. G., Mullighan, C. G. (2005) Mannose-binding lectin: biology and clinical implications. Internal Medicine Journal, vol. 35, no. 9, pp. 548–555. https://doi.org/10.1111/j.1445-5994.2005.00908.x (In English)
Wu, R., Patocka, J., Nepovimova, E, et al.(2021) Marine Invertebrate Peptides: Antimicrobial Peptides. Frontiers In Microbiology, vol. 12, article 785085. https://doi.org/10.1016/10.3389/fmicb.2021.785085 (In English)
Yoshino, T. P., Dinguirard, N., Kunert, J., Hokke, C. H. (2008) Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene, vol. 411, no. 1–2, pp. 46–58. https://doi.org/10.1016/j.gene.2008.01.003 (In English)
Żbikowska, E. (2004) Infection of snails with bird schistosomes and the threat of swimmer’s itch in selected Polish lakes. Parasitology Research, vol. 92, pp. 30–35. https://doi.org/10.1007/s00436-003-0997-0 (In English)
Zelensky, A. N., Gready, J. E. (2005) The C-type lectin-like domain superfamily. FEBS Journal, vol. 272, pp. 6179–6217. https://doi.org/10.1111/j.1742-4658.2005.05031.x (In English)
Zhang, Q., Zmasek, C. M., Godzik, A. (2010) Domain architecture evolution of pattern-recognition receptors. Immunogenetics, vol. 62, no. 5, pp. 263–272. https://pubmed.ncbi.nlm.nih.gov/20195594 (In English)
Zhang, S.-M., Zeng, Y., Loker, E. S. (2008) Expression profiling and binding properties of fibrinogenrelated proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immunity, vol. 14, no. 3, pp. 175–189. https://doi.org/10.1177/1753425908093800 (In English)
Zhao, Q. P., Gao, Q., Zhang, Y. et al. (2018) Identification of Toll-like receptor family members in Oncomelania hupensis and their role in defense against Schistosoma japonicum. Acta Tropica, vol. 181, pp. 69–78. https://doi.org/10.1016/j.actatropica.2018.01.008 (In English)
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