Abstract
This review presents the basic concepts and knowledge about the immunity of Bivalvia with an emphasis on humoral factors and a more detailed analysis of carbohydrate-binding and effector molecules, an assessment of the influence of environmental factors on their activity, and a description of application of some of them. Cellular responses and hemocytes are briefly considered as a key component of the bivalve immune system and the main source of protective molecules. Various types of classification of humoral immunity factors are provided with their further description for groups based on functional activity. Carbohydrate-binding proteins that recognize foreign components and play the role of agglutinins and opsonins, general regulatory mechanisms and signal molecules, as well as effector molecules such as lysins, antimicrobial peptides, etc. are considered in detail.
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REFERENCES
Ratcliffe, N.A., Rowley, A.F., Fitzgerald, S.W., and Rhodes, C.P., Invertebrate immunity: Basic concepts and recent advances, in International Review of Cytology, Bourne, G.H., Ed., New York: Academic, 1985, pp. 183–350.
Song, L., Wang, L., Qiu, L., and Zhang, H., Bivalve immunity, in Invertebrate Immunity, Söderhäll, K., Ed., Boston: Springer, 2010, pp. 44–65.
Vasta, G.R., Lectins as innate immune recognition factors: Structural, functional, and evolutionary aspects, in The Evolution of the Immune System, Malagoli, D., Ed., Academic, 2016, pp. 205–224.
Jack, R. and Du Pasquier, L., Innate immunity, evolutionary concepts, in Immunology, Cham: Springer, 2019, pp. 33–69.
Gerdol, M., Gomez-Chiarri, M., Castillo, M.G., Figueras, A., Fiorito, G., Moreira, R., Novoa, B., Pallavicini, A., Ponte, G., and Roumbedakis, K., Immunity in molluscs: Recognition and effector mechanisms, with a focus on Bivalvia, in Advances in Comparative Immunology, Cooper, E., Ed., Cham: Springer, 2018, pp. 225–341.
Loker, E.S. and Bayne, C.J., Molluscan immunobiology: Challenges in the anthropocene epoch, in Advances in Comparative Immunology, Cooper, E., Ed., Cham: Springer, 2018, pp. 343–407.
Criscitiello, M.F. and de Figueiredo, P., Fifty shades of immune defense, PloS Pathog., 2013, vol. 9, e1003110. https://doi.org/10.1371/journal.ppat.1003110
Mafra, L.L., Bricelj, V.M., amd Fennel, K., Domoic acid uptake and elimination kinetics in oysters and mussels in relation to body size and anatomical distribution of toxin, Aquat. Toxicol., 2010, vol. 100, pp. 17–29. https://doi.org/10.1016/j.aquatox.2010.07.002
Ben-Horin, T., Bidegain, G., Huey, L., Narvaez, D.A., and Bushek, D., Parasite transmission through suspension feeding, J. Invertebr. Pathol., 2015, vol. 131, pp. 155–176. https://doi.org/10.1016/j.jip.2015.07.006
Allam, B. and Pales Espinosa, E., Bivalve immunity and response to infections: Are we looking at the right place?, Fish Shellfish Immunol., 2016, vol. 53, pp. 4–12. https://doi.org/10.1016/j.fsi.2016.03.037
Allam, B. and Raftos, D., Immune responses to infectious diseases in bivalves, J. Invertebr. Pathol., 2015, vol. 131, pp. 121–136. https://doi.org/10.1016/j.jip.2015.05.005
Zannella, C., Mosca, F., Mariani, F., Franci, G., Folliero, V., Galdiero, Marilena, Tiscar, P.G., and Galdiero, M., Microbial diseases of bivalve mollusks: Infections, immunology and antimicrobial defense, Mar. Drugs, 2017, vol. 15, no. 6, 182. https://doi.org/10.3390/md15060182
Zhang, T., Qiu, L., Sun, Z., Wang, L., Zhou, Z., Liu, R., Yue, F., Sun, R., and Song, L., The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus, Dev. Comp. Immunol., 2014, vol. 45, pp. 141–150. https://doi.org/10.1016/j.dci.2014.02.015
Wang, Lingling, Yue, F., Song, X., and Song, L., Maternal immune transfer in mollusc, Dev. Comp. Immunol., 2015, vol. 48, pp. 354–359. https://doi.org/10.1016/j.dci.2014.05.010
Green, T.J., Raftos, D., Speck, P., and Montagnani, C., Antiviral immunity in marine molluscs, J. Gen. Virol., 2015, vol. 96, pp. 2471–2482. https://doi.org/10.1099/jgv.0.000244
Pinaud, S., Portela, J., Duval, D., Nowacki, F.C., Olive, M.-A., Allienne, J.-F., Galinier, R., Dheilly, N.M., Kieffer-Jaquinod, S., Mitta, G., Théron, A., and Gourbal, B., A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata, PloS Pathog., 2016, vol. 12, e1005361. https://doi.org/10.1371/journal.ppat.1005361
Wang, H., Song, L., Li, C., Zhao, J., Zhang, H., Ni, D., and Xu, W., Cloning and characterization of a novel C-type lectin from Zhikong scallop Chlamys farreri, Mol. Immunol., 2007, vol. 44, pp. 722–731. https://doi.org/10.1016/j.molimm.2006.04.015
Lafont, M., Petton, B., Vergnes, A., Pauletto, M., Segarra, A., Gourbal, B., and Montagnani, C., Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas, Sci. Rep., 2017, vol. 7, 13143. https://doi.org/10.1038/s41598-017-13564-0
Oubella, R., Maes, P., Paillard, C., and Auffret, M., Experimentally induced variation in hemocyte density for Ruditapes philippinarum and R. decussatus (Mollusca, Bivalvia), Dis. Aquat. Org., 1993, vol. 15, pp. 193–197.
Santarem, M., Robledo, J., and Figueras, A., Seasonal changes in hemocytes and serum defense factors in the blue mussel Mytilus galloprovincialis, Dis. Aquat. Org., 1994, vol. 18, pp. 217–222. https://doi.org/10.3354/dao018217
Carballal, Villalba, Lopez, Seasonal variation and effects of age, food availability, size, gonadal development, and parasitism on the hemogram of Mytilus galloprovincialis, J. Invertebr. Pathol., 1998, vol. 72, pp. 304–312. https://doi.org/10.1006/jipa.1998.4779
Allam, B., Paillard, C., and Ford, S.E., Pathogenicity of Vibrio tapetis, the etiological agent of brown ring disease in clams, Dis. Aquat. Org., 2002, vol. 48, pp. 221–231. https://doi.org/10.3354/dao048221
Anisimova, A.A., Morphofunctional parameters of hemocytes in the assessment of the physiological status of bivalves, Russ. J. Mar. Biol., 2013, vol. 39, pp. 381–391. https://doi.org/10.1134/S1063074013060023
Wang, L., Song, X., and Song, L., The oyster immunity, Dev. Comp. Immunol., 2018, vol. 80, pp. 99–118. https://doi.org/10.1016/j.dci.2017.05.025
Dam, T.K., Sarkar, M., Ghosal, J., and Choudhury, A., A novel galactosyl-binding lectin from the plasma of the blood clam, Anadara granosa (L) and a study of its combining site, Mol. Cell. Biochem., 1992, vol. 117, pp. 1–9. https://doi.org/10.1007/BF00230405
Romanenko, L.A., Uchino, M., Kalinovskaya, N.I., and Mikhailov, V.V., Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities, Microbiol. Res., 2008, vol. 163, pp. 633–644. https://doi.org/10.1016/j.micres.2006.10.001
Chen, Y., Li, C., Zhu, J., Xie, W., Hu, X., Song, L., Zi, J., and Yu, R., Purification and characterization of an antibacterial and anti-inflammatory polypeptide from Arca subcrenata, Int. J. Biol. Macromol., 2017, vol. 96, pp. 177–184. https://doi.org/10.1016/j.ijbiomac.2016.11.082
Balseiro, P., Falcó, A., Romero, A., Dios, S., Martínez-López, A., Figueras, A., Estepa, A., and Novoa, B., Mytilus galloprovincialis myticin C: a chemotactic molecule with antiviral activity and immunoregulatory properties, PLoS One, 2011, vol. 6, e23140. https://doi.org/10.1371/journal.pone.0023140
Zhang, L., Li, L., Guo, X., Litman, G.W., Dishaw, L.J., and Zhang, G., Massive expansion and functional divergence of innate immune genes in a protostome, Sci. Rep., 2015, vol. 5, 8693. https://doi.org/10.1038/srep08693
Sharon, N. and Lis, H., Lectins, Dordrecht: Springer, 2007.
Vasta, G.R., Ahmed, H., Tasumi, S., Odom, E.W., and Saito, K., Biological roles of lectins in innate immunity: molecular and structural basis for diversity in self/non-self recognition, Adv. Exp. Med. Biol., 2007, vol. 598, pp. 389–406. https://doi.org/10.1007/978-0-387-71767-8_27
Fujita, T., Matsushita, M., and Endo, Y., The lectin-complement pathway—its role in innate immunity and evolution, Immunol. Rev., 2004, vol. 198, pp. 185–202. https://doi.org/10.1111/j.0105-2896.2004.0123.x
Vasta, G.R. and Ahmed, H., Animal Lectins: A Functional View, Boca Raton: CRC Press, 2008.
Drickamer, K., Two distinct classes of carbohydrate-recognition domains in animal lectins., J. Biol. Chem., 1988, vol. 263, pp. 9557–9560. https://doi.org/10.1016/S0021-9258(19)81549-1
Zelensky, A.N., Gready, J.E., and Gready J.E. The C-type lectin-like domain superfamily, FEBS J., 2005, vol. 272, pp. 6179–6217. https://doi.org/10.1111/j.1742-4658.2005.05031.x
Pees, B., Yang, W., Zárate-Potes, A., Schulenburg, H., and Dierking, K., High innate immune specificity through diversified C-type lectin-like domain proteins in invertebrates, J. Innate Immun., 2016, vol. 8, pp. 129–142. https://doi.org/10.1159/000441475
Zhao, L.-L., Wang, Y.-Q., Dai, Y.-J., Zhao, L.-J., Qin, Q., Lin, L., Ren, Q., and Lan, J.-F., A novel C-type lectin with four CRDs is involved in the regulation of antimicrobial peptide gene expression in Hyriopsis cumingii, Fish Shellfish Immunol., 2016, vol. 55, pp. 339–347. https://doi.org/10.1016/j.fsi.2016.06.007
Martins, E., Figueras, A., Novoa, B., Santos, R.S., Moreira, R., and Bettencourt, R., Comparative study of immune responses in the deep-sea hydrothermal vent mussel Bathymodiolus azoricus and the shallow-water mussel Mytilus galloprovincialis challenged with Vibrio bacteria, Fish Shellfish Immunol., 2014, vol. 40, pp. 485–499. https://doi.org/10.1016/j.fsi.2014.07.018
Zheng, P., Wang, H., Zhao, J., Song, L., Qiu, L., Dong, C., Wang, B., Gai, Y., Mu, C., Li, C., Ni, D., and Xing, K., A lectin (CfLec-2) aggregating Staphylococcus haemolyticus from scallop Chlamys farreri, Fish Shellfish Immunol., 2008, vol. 24, pp. 286–293. https://doi.org/10.1016/j.fsi.2007.11.014
Zhu, L., Song, L., Xu, W., and Qian, P.-Y., Molecular cloning and immune responsive expression of a novel C-type lectin gene from bay scallop Argopecten irradians, Fish Shellfish Immunol., 2008, vol. 25, pp. 231–238. https://doi.org/10.1016/j.fsi.2008.05.004
Jing, X., Espinosa, E.P., Perrigault, M., and Allam, B., Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica, Fish Shellfish Immunol., 2011, vol. 30, pp. 851–858. https://doi.org/10.1016/j.fsi.2011.01.007
Huang, M., Song, X., Zhao, J., Mu, C., Wang, L., Zhang, H., Zhou, Z., Liu, X., and Song, L., A C-type lectin (AiCTL-3) from bay scallop Argopecten irradians with mannose/galactose binding ability to bind various bacteria, Gene, 2013, vol. 531, pp. 31–38. https://doi.org/10.1016/j.gene.2013.08.042
Mu, C., Chen, L., Zhao, J., and Wang, C., Molecular cloning and expression of a C-type lectin gene from Venerupis philippinarum, Mol. Biol. Rep., 2014, vol. 41, pp. 139–144. https://doi.org/10.1007/s11033-013-2846-2
Huang, M., Zhang, H., Jiang, S., Wang, L., Liu, R., Yi, Q., and Song, L., An EPD/WSD motifs containing C-type lectin from Argopectens irradians recognizes and binds microbes with broad spectrum, Fish Shellfish Immunol., 2015, vol. 43, pp. 287–293. https://doi.org/10.1016/j.fsi.2014.12.035
Yang, J., Huang, M., Zhang, H., Wang, Lingling, Wang, H., Wang, Leilei, Qiu, L., and Song, L., CfLec-3 from scallop: an entrance to non-self recognition mechanism of invertebrate C-type lectin, Sci. Rep., 2015, vol. 5, 10068. https://doi.org/10.1038/srep10068
Li, H., Zhang, H., Jiang, S., Wang, W., Xin, L., Wang, H., Wang, L., and Song, L., A single-CRD C-type lectin from oyster Crassostrea gigas mediates immune recognition and pathogen elimination with a potential role in the activation of complement system, Fish Shellfish Immunol., 2015, vol. 44, pp. 566–575. https://doi.org/10.1016/j.fsi.2015.03.011
Wang, Lingling, Zhang, H., Wang, Leilei, Zhang, D., Lv, Z., Liu, Z., Wang, W., Zhou, Z., Qiu, L., Wang, H., Li, J., and Song, L., The RNA-seq analysis suggests a potential multi-component complement system in oyster Crassostrea gigas, Dev. Comp. Immunol., 2017, vol. 76, pp. 209–219. https://doi.org/10.1016/j.dci.2017.06.009
Vasta, G.R., Ahmed, H., Nita-Lazar, M., Banerjee, A., Pasek, M., Shridhar, S., Guha, P., and Fernández-Robledo, J.A., Galectins as self/non-self recognition receptors in innate and adaptive immunity: an unresolved paradox, Front. Immunol., 2012, vol. 3, pp. 199. https://doi.org/10.3389/fimmu.2012.00199
Vasta, G.R., Roles of galectins in infection, Nat. Rev. Microbiol., 2009, vol. 7, pp. 424–438. https://doi.org/10.1038/nrmicro2146
Vasta, G.R., Feng, C., Bianchet, M.A., Bachvaroff, T.R., and Tasumi, S., Structural, functional, and evolutionary aspects of galectins in aquatic mollusks: From a sweet tooth to the Trojan horse, Fish Shellfish Immunol., 2015, vol. 46, pp. 94–106. https://doi.org/10.1016/j.fsi.2015.05.012
Feng, C., Ghosh, A., Amin, M.N., Giomarelli, B., Shridhar, S., Banerjee, A., Fernández-Robledo, J.A., Bianchet, M.A., Wang, L.-X., Wilson, I.B.H., and Vasta, G.R., The galectin CvGal1 from the eastern oyster (Crassostrea virginica) binds to blood group A oligosaccharides on the hemocyte surface, J. Biol. Chem., 2013, vol. 288, pp. 24394–24409. https://doi.org/10.1074/jbc.M113.476531
Feng, C., Ghosh, A., Amin, M.N., Bachvaroff, T.R., Tasumi, S., Pasek, M., Banerjee, A., Shridhar, S., Wang, L.-X., Bianchet, M.A., and Vasta, G.R., Galectin CvGal2 from the Eastern oyster (Crassostrea virginica) displays unique specificity for ABH blood group oligosaccharides and differentially recognizes sympatric Perkinsus species, Biochemistry, 2015, vol. 54, pp. 4711–4730. https://doi.org/10.1021/acs.biochem.5b00362
Kurz, S., Jin, C., Hykollari, A., Gregorich, D., Giomarelli, B., Vasta, G.R., Wilson, I.B.H., and Paschinger, K., Hemocytes and plasma of the eastern oyster (Crassostrea virginica) display a diverse repertoire of sulfated and blood group A-modified N-glycans, J. Biol. Chem., 2013, vol. 288, pp. 24410–24428. https://doi.org/10.1074/jbc.M113.478933
Tasumi, S. and Vasta, G.R., A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus, J. Immunol., 2007, vol. 179, pp. 3086–3098. https://doi.org/10.4049/jimmunol.179.5.3086
Yamaura, K., Takahashi, K.G., and Suzuki, T., Identification and tissue expression analysis of C-type lectin and galectin in the Pacific oyster, Crassostrea gigas, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2008, vol. 149, pp. 168–175. https://doi.org/10.1016/j.cbpb.2007.09.004
Yoshino, T.P., Dinguirard, N., Kunert, J., and Hokke, C.H., 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, 2008, vol. 411, pp. 46–58. https://doi.org/10.1016/j.gene.2008.01.003
Song, X., Zhang, H., Zhao, J., Wang, L., Qiu, Limei, Mu, C., Liu, X., Qiu, Lihua, and Song, L., An immune responsive multidomain galectin from bay scallop Argopectens irradians, Fish Shellfish Immunol., 2010, vol. 28, pp. 326–332. https://doi.org/10.1016/j.fsi.2009.11.016
Zhang, D., Jiang, S., Hu, Y., Cui, S., Guo, H., Wu, K., Li, Y., and Su, T., A multidomain galectin involved in innate immune response of pearl oyster Pinctada fucata, Dev. Comp. Immunol., 2011, vol. 35, pp. 1–6. https://doi.org/10.1016/j.dci.2010.08.007
Bao, Y., Shen, H., Zhou, H., Dong, Y., and Lin, Z., A tandem-repeat galectin from blood clam Tegillarca granosa and its induced mRNA expression response against bacterial challenge, Genes Genomics, 2013, vol. 35, pp. 733–740.
Dheilly, N.M., Duval, D., Mouahid, G., Emans, R., Allienne, J.-F., Galinier, R., Genthon, C., Dubois, E., Du Pasquier, L., Adema, C.M., Grunau, C., Mitta, G., and Gourbal, B., A family of variable immunoglobulin and lectin domain containing molecules in the snail Biomphalaria glabrata, Dev. Comp. Immunol., 2015, vol. 48, pp. 234–243. https://doi.org/10.1016/j.dci.2014.10.009
Bai, Z., Zhao, L., Chen, X., Li, Q., and Li, J., A galectin from Hyriopsis cumingii involved in the innate immune response against to pathogenic microorganism and its expression profiling during pearl sac formation, Fish Shellfish Immunol., 2016, vol. 56, pp. 127–135. https://doi.org/10.1016/j.fsi.2016.07.006
Cummings, R.D. and Schnaar, R.L., R-Type Lectins, in Essentials of Glycobiology, Varki, A., Ed., New York: Cold Spring Harbor Laboratory, 2015,
Jao, M., Lubkowski, J., O’Keefe, B.R., and Wlodawer, A., Structure of a lectin from the sea mussel Crenomytilus grayanus (CGL), Acta Crystallogr., Sect. F: Struct. Biol. Commun., 2015, vol. 71, pp. 1429–1436. https://doi.org/10.1107/S2053230X15019858
Chernikov, O., Kuzmich, A., Chikalovets, I., Molchanova, V., and Hua, K.-F., Lectin CGL from the sea mussel Crenomytilus grayanus induces Burkitt’s lymphoma cells death via interaction with surface glycan, Int. J. Biol. Macromol., 2017, vol. 104, pp. 508–514. https://doi.org/10.1016/j.ijbiomac.2017.06.074
Chernikov, O.V., Wong, W.-T., Li, L.-H., Chikalovets, I.V., Molchanova, V.I., Wu, S.-H., Liao, J.-H., and Hua, K.-F., A GalNAc/Gal-specific lectin from the sea mussel Crenomytilus grayanus modulates immune response in macrophages and in mice, Sci. Rep., 2017, vol. 7, pp. 6315. https://doi.org/10.1038/s41598-017-06647-5
Hasan, I., Gerdol, M., Fujii, Y., Rajia, S., Koide, Y., Yamamoto, D., Kawsar, S.M.A., and Ozeki, Y., cDNA and gene structure of MytiLec-1, a bacteriostatic R-Type lectin from the Mediterranean mussel (Mytilus galloprovincialis), Mar. Drugs, 2016, vol. 14, no. 5, 92. https://doi.org/10.3390/md14050092
Terada, D., Kawai, F., Noguchi, H., Unzai, S., Hasan, I., Fujii, Y., Park, S.-Y., Ozeki, Y., and Tame, J.R.H., Crystal structure of MytiLec, a galactose-binding lectin from the mussel Mytilus galloprovincialis with cytotoxicity against certain cancer cell types, Sci. Rep., 2016, vol. 6, 28344. https://doi.org/10.1038/srep28344
Chikalovets, I.V., Kovalchuk, S.N., Litovchenko, A.P., Molchanova, V.I., Pivkin, M.V., and Chernikov, O.V., A new Gal/GalNAc-specific lectin from the mussel Mytilus trossulus: Structure, tissue specificity, antimicrobial and antifungal activity, Fish Shellfish Immunol., 2016, vol. 50, pp. 27–33. https://doi.org/10.1016/j.fsi.2016.01.020
García-Maldonado, E., Cano-Sánchez, P., and Hernández-Santoyo, A., Molecular and functional characterization of a glycosylated Galactose-Binding lectin from Mytilus californianus, Fish Shellfish Immunol., 2017, vol. 66, pp. 564–574. https://doi.org/10.1016/j.fsi.2017.05.057
Bianchet, M.A., Odom, E.W., Vasta, G.R., and Amzel, L.M., A novel fucose recognition fold involved in innate immunity, Nat. Struct. Biol., 2002, vol. 9, pp. 628–634. https://doi.org/10.1038/nsb817
Odom, E.W. and Vasta, G.R., Characterization of a binary tandem domain F-type lectin from striped bass (Moronesaxatilis), J. Biol. Chem., 2006, vol. 281, pp. 1698–1713. https://doi.org/10.1074/jbc.M507652200
Bianchet, M.A., Odom, E.W., Vasta, G.R., and Amzel, L.M., Structure and specificity of a binary tandem domain F-lectin from striped bass (Morone saxatilis), J. Mol. Biol., 2010, vol. 401, pp. 239–252. https://doi.org/10.1016/j.jmb.2010.06.018
Vasta, G.R., Ahmed, H., Bianchet, M.A., Fernández-Robledo, J.A., and Amzel, L.M., Diversity in recognition of glycans by F-type lectins and galectins: Molecular, structural, and biophysical aspects, Ann. N. Y. Acad. Sci., 2012, vol. 1253, pp. E14–26. https://doi.org/10.1111/j.1749-6632.2012.06698.x
Bishnoi, R., Khatri, I., Subramanian, S., and Ramya, T.N.C., Prevalence of the F-type lectin domain, Glycobiology, 2015, vol. 25, pp. 888–901. https://doi.org/10.1093/glycob/cwv029
Springer, S.A., Moy, G.W., Friend, D.S., Swanson, W.J., and Vacquier, V.D., Oyster sperm bindin is a combinatorial fucose lectin with remarkable intra-species diversity, Int. J. Dev. Biol., 2008, vol. 52, pp. 759–768. https://doi.org/10.1387/ijdb.082581ss
Moy, G.W., Springer, S.A., Adams, S.L., Swanson, W.J., and Vacquier, V.D., Extraordinary intraspecific diversity in oyster sperm bindin, Proc. Natl. Acad. Sci. U. S. A., 2008, vol. 105, pp. 1993–1998. https://doi.org/10.1073/pnas.0711862105
Moy, G.W. and Vacquier, V.D., Bindin genes of the Pacific oyster Crassostrea gigas, Gene, 2008, vol. 423, pp. 215–220. https://doi.org/10.1016/j.gene.2008.07.005
Wang, A., Wang, Y., Gu, Z., Li, S., Shi, Y., and Guo, X., Development of expressed sequence tags from the pearl oyster, Pinctada martensii Dunker, Mar. Biotechnol., 2011, vol. 13, pp. 275–283. https://doi.org/10.1007/s10126-010-9296-9
Arivalagan, J., Marie, B., Sleight, V.A., Clark, M.S., Berland, S., and Marie, A., Shell matrix proteins of the clam, Mya truncata: Roles beyond shell formation through proteomic study, Mar. Genomics, 2016, vol. 27, pp. 69–74. https://doi.org/10.1016/j.margen.2016.03.005
Gestal, C., Pallavicini, A., Venier, P., Novoa, B., and Figueras, A., MgC1q, a novel C1q-domain-containing protein involved in the immune response of Mytilus galloprovincialis, Dev. Comp. Immunol., 2010, vol. 34, pp. 926–934. https://doi.org/10.1016/j.dci.2010.02.012
Gerdol, M., Manfrin, C., De Moro, G., Figueras, A., Novoa, B., Venier, P., and Pallavicini, A., The C1q domain containing proteins of the Mediterranean mussel Mytilus galloprovincialis: A widespread and diverse family of immune-related molecules, Dev. Comp. Immunol., 2011, vol. 35, pp. 635–643. https://doi.org/10.1016/j.dci.2011.01.018
Takeuchi, T., Koyanagi, R., Gyoja, F., et al., Bivalve-specific gene expansion in the pearl oyster genome: Implications of adaptation to a sessile lifestyle, Zool. Lett., 2016, vol. 2, 3. https://doi.org/10.1186/s40851-016-0039-2
Gerdol, M., Venier, P., and Pallavicini, A., The genome of the Pacific oyster Crassostrea gigas brings new insights on the massive expansion of the C1q gene family in Bivalvia, Dev. Comp. Immunol., 2015, vol. 49, pp. 59–71. https://doi.org/10.1016/j.dci.2014.11.007
Sun, Y., Zhou, Z., Wang, L., Yang, C., Jianga, S., and Song, L., The immunomodulation of a novel tumor necrosis factor (CgTNF-1) in oyster Crassostrea gigas, Dev. Comp. Immunol., 2014, vol. 45, pp. 291–299. https://doi.org/10.1016/j.dci.2014.03.007
Powell, D., Subramanian, S., Suwansa-ard, S., Zhao, M., O’Connor, W., Raftos, D., and Elizur, A., The genome of the oyster Saccostrea offers insight into the environmental resilience of bivalves, DNA Res., 2018, vol. 25, pp. 655–665. https://doi.org/10.1093/dnares/dsy032
Gerdol, M., Greco, S., and Pallavicini, A., Extensive tandem duplication events drive the expansion of the C1q-domain-containing gene family in Bivalves, Mar. Drugs, 2019, vol. 17, no. 10, 583. https://doi.org/10.3390/md17100583
Mun, S., Kim, Y.-J., Markkandan, K., et al., The Whole-genome and transcriptome of the Manila clam (Ruditapes philippinarum), Genome Biol. Evol., 2017, vol. 9, pp. 1487–1498. https://doi.org/10.1093/gbe/evx096
Xu, T., Xie, J., Li, J., Luo, M., Ye, S., and Wu, X., Identification of expressed genes in cDNA library of hemocytes from the RLO-challenged oyster, Crassostrea ariakensis Gould with special functional implication of three complement-related fragments (CaC1q1, CaC1q2 and CaC3), Fish Shellfish Immunol., 2012, vol. 32, pp. 1106–1116. https://doi.org/10.1016/j.fsi.2012.03.012
Leite, R.B., Milan, M., Coppe, A., et al., mRNA-Seq and microarray development for the Grooved Carpet shell clam, Ruditapes decussatus: A functional approach to unravel host-parasite interaction, BMC Genomics, 2013, vol. 14, 741. https://doi.org/10.1186/1471-2164-14-741
Allam, B., Pales Espinosa, E., Tanguy, A., Jeffroy, F., Le Bris, C., and Paillard, C., Transcriptional changes in Manila clam (Ruditapes philippinarum) in response to Brown Ring Disease, Fish Shellfish Immunol., 2014, vol. 41, pp. 2–11. https://doi.org/10.1016/j.fsi.2014.05.022
Kong, P., Zhang, H., Wang, Lingling, Zhou, Z., Yang, J., Zhang, Y., Qiu, L., Wang, Leilei, and Song, L., AiC1qDC-1, a novel gC1q-domain-containing protein from bay scallop Argopecten irradians with fungi agglutinating activity, Dev. Comp. Immunol., 2010, vol. 34, pp. 837–846. https://doi.org/10.1016/j.dci.2010.03.006
Li, C., Yu, S., Zhao, J., Su, X., and Li, T., Cloning and characterization of a sialic acid binding lectins (SABL) from Manila clam Venerupis philippinarum, Fish Shellfish Immunol., 2011, vol. 30, pp. 1202–1206. https://doi.org/10.1016/j.fsi.2011.02.022
Jiang, S., Li, H., Zhang, D., Zhang, H., Wang, L., Sun, J., and Song, L., A C1q domain containing protein from Crassostrea gigas serves as pattern recognition receptor and opsonin with high binding affinity to LPS, Fish Shellfish Immunol., 2015, vol. 45, pp. 583–591. https://doi.org/10.1016/j.fsi.2015.05.021
Wang, Leilei, Wang, Lingling, Kong, P., Yang, J., Zhang, H., Wang, M., Zhou, Z., Qiu, L., and Song, L., A novel C1qDC protein acting as pattern recognition receptor in scallop Argopecten irradians, Fish Shellfish Immunol., 2012, vol. 33, pp. 427–435. https://doi.org/10.1016/j.fsi.2012.05.032
Wang, Leilei, Wang, Lingling, Zhang, H., Zhou, Z., Siva, V.S., and Song, L., A C1q domain containing protein from scallop Chlamys farreri serving as pattern recognition receptor with heat-aggregated IgG binding activity, PLoS One, 2012, vol. 7, e43289. https://doi.org/10.1371/journal.pone.0043289
Zhang, H., Song, L., Li, C., Zhao, J., Wang, H., Qiu, L., Ni, D., and Zhang, Y., A novel C1q-domain-containing protein from Zhikong scallop Chlamys farreri with lipopolysaccharide binding activity, Fish Shellfish Immunol., 2008, vol. 25, pp. 281–289. https://doi.org/10.1016/j.fsi.2008.06.003
Yang, J., Wei, X., Liu, X., Xu, J., Yang, D., Yang, Jianmin, Fang, J., and Hu, X., Cloning and transcriptional analysis of two sialic acid-binding lectins (SABLs) from razor clam Solen grandis, Fish Shellfish Immunol., 2012, vol. 32, pp. 578–585. https://doi.org/10.1016/j.fsi.2012.01.012
Wang, Leilei, Wang, Lingling, Zhang, D., Jiang, Q., Sun, R., Wang, H., Zhang, H., and Song, L., A novel multi-domain C1qDC protein from Zhikong scallop Chlamys farreri provides new insights into the function of invertebrate C1qDC proteins, Dev. Comp. Immunol., 2015, vol. 52, pp. 202–214. https://doi.org/10.1016/j.dci.2015.05.009
Zhao, L.-L., Jin, M., Li, X.-C., Ren, Q., and Lan, J.-F., Four C1q domain-containing proteins involved in the innate immune response in Hyriopsis cumingii, Fish Shellfish Immunol., 2016, vol. 55, pp. 323–331. https://doi.org/10.1016/j.fsi.2016.06.003
Huang, Y., Wang, W., and Ren, Q., Identification and function of a novel C1q domain-containing (C1qDC) protein in triangle-shell pearl mussel (Hyriopsis cumingii), Fish Shellfish Immunol., 2016, vol. 58, pp. 612–621. https://doi.org/10.1016/j.fsi.2016.10.010
He, X., Zhang, Y., Yu, F., and Yu, Z., A novel sialic acid binding lectin with anti-bacterial activity from the Hong Kong oyster (Crassostrea hongkongensis), Fish Shellfish Immunol., 2011, vol. 31, pp. 1247–1250. https://doi.org/10.1016/j.fsi.2011.08.021
Pezzati, E., Canesi, L., Damonte, G., et al., Susceptibility of Vibrio aestuarianus 01/032 to the antibacterial activity of Mytilus haemolymph: Identification of a serum opsonin involved in mannose-sensitive interactions, Environ. Microbiol., 2015, vol. 17, pp. 4271–4279. https://doi.org/10.1111/1462-2920.12750
Zhang, H., Wang, L., Song, L., Song, X., Wang, B., Mu, C., and Zhang, Y., A fibrinogen-related protein from bay scallop Argopecten irradians involved in innate immunity as pattern recognition receptor, Fish Shellfish Immunol., 2009, vol. 26, pp. 56–64. https://doi.org/10.1016/j.fsi.2008.07.019
Yang, C., Wang, Leilei, Zhang, H., Wang, Lingling, Huang, M., Sun, Z., Sun, Y., and Song, L., A new fibrinogen-related protein from Argopecten irradians (AiFREP-2) with broad recognition spectrum and bacteria agglutination activity, Fish Shellfish Immunol., 2014, vol. 38, pp. 221–229. https://doi.org/10.1016/j.fsi.2014.03.025
Xiang, Z., Qu, F., Wang, F., Li, J., Zhang, Y., and Yu, Z., Characteristic and functional analysis of a ficolin-like protein from the oyster Crassostrea hongkongensis, Fish Shellfish Immunol., 2014, vol. 40, pp. 514–523. https://doi.org/10.1016/j.fsi.2014.08.006
Gorbushin, A.M. and Iakovleva, N.V., A new gene family of single fibrinogen domain lectins in Mytilus, Fish Shellfish Immunol., 2011, vol. 30, pp. 434–438. https://doi.org/10.1016/j.fsi.2010.10.002
Huang, B., Zhang, L., Li, L., Tang, X., and Zhang, G., Highly diverse fibrinogen-related proteins in the Pacific oyster Crassostrea gigas, Fish Shellfish Immunol., 2015, vol. 43, pp. 485–490. https://doi.org/10.1016/j.fsi.2015.01.021
Gerdol, M. and Venier, P., An updated molecular basis for mussel immunity, Fish Shellfish Immunol., 2015, vol. 46, pp. 17–38. https://doi.org/10.1016/j.fsi.2015.02.013
Catanzaro, E., Calcabrini, C., Bishayee, A., and Fimognari, C., Antitumor potential of marine and freshwater lectins, Mar. Drugs, 2020, vol. 18, 11. https://doi.org/10.3390/md18010011
Callewaert, L. and Michiels, C.W., Lysozymes in the animal kingdom, J. Biosci., 2010, vol. 35, pp. 127–160. https://doi.org/10.1007/s12038-010-0015-5
Nilsen, I.W., Øverbø, K., Sandsdalen, E., Sandaker, E., Sletten, K., and Myrnes, B., Protein purification and gene isolation of chlamysin, a cold-active lysozyme-like enzyme with antibacterial activity, FEBS Lett., 1999, vol. 464, pp. 153–158. https://doi.org/10.1016/s0014-5793(99)01693-2
Matsumoto, T., Nakamura, A.M., and Takahashi, K.G., Cloning of cDNAs and hybridization analysis of lysozymes from two oyster species, Crassostrea gigas and Ostrea edulis, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2006, vol. 145, pp. 325–330. https://doi.org/10.1016/j.cbpb.2006.08.003
La Peyre, J.F., Xue, Q.-G., Itoh, N., Li, Y., and Cooper, R.K., Serine protease inhibitor cvSI-1 potential role in the eastern oyster host defense against the protozoan parasite Perkinsus marinus, Dev. Comp. Immunol., 2010, vol. 34, pp. 84–92. https://doi.org/10.1016/j.dci.2009.08.007
Yue, X., Liu, B., and Xue, Q., An i-type lysozyme from the Asiatic hard clam Meretrix meretrix potentially functioning in host immunity, Fish Shellfish Immunol., 2011, vol. 30, pp. 550–558. https://doi.org/10.1016/j.fsi.2010.11.022
Ren, Q., Qi, Y.-L., Hui, K.-M., Zhang, Z., Zhang, C.-Y., and Wang, W., Four invertebrate-type lysozyme genes from triangle-shell pearl mussel (Hyriopsis cumingii), Fish Shellfish Immunol., 2012, vol. 33, pp. 909–915. https://doi.org/10.1016/j.fsi.2012.07.019
Bachali, S., Jager, M., Hassanin, A., Schoentgen, F., Jollès, P., Fiala-Medioni, A., and Deutsch, J.S., Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function, J. Mol. Evol., 2002, vol. 54, pp. 652–664. https://doi.org/10.1007/s00239-001-0061-6
Detree, C., Chabenat, A., Lallier, F.H., Satoh, N., Shoguchi, E., Tanguy, A., and Mary, J., Multiple I-type lysozymes in the hydrothermal vent mussel Bathymodiolus azoricus and their role in symbiotic plasticity, PLoS One, 2016, vol. 11, e0148988. https://doi.org/10.1371/journal.pone.0148988
Venier, P., De Pitta, C., Bernante, F., et al., MytiBase: A knowledgebase of mussel (M. galloprovincialis) transcribed sequences, BMC Genomics, 2009, vol. 10, 72. https://doi.org/10.1186/1471-2164-10-72
Wang, Q., Wang, C., Mu, C., Wu, H., Zhang, L., and Zhao, J., A novel C-type lysozyme from Mytilus galloprovincialis: Insight into innate immunity and molecular evolution of invertebrate C-type lysozymes, PLoS One, 2013, vol. 8, e67469. https://doi.org/10.1371/journal.pone.0067469
Zhao, J., Song, L., Li, C., Zou, H., Ni, D., Wang, W., and Xu, W., Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein, Mol. Immunol., 2007, vol. 44, pp. 1198–1208. https://doi.org/10.1016/j.molimm.2006.06.008
Li, J., Zhang, Yang, Zhang, Yuehuan, Xiang, Z., Tong, Y., Qu, F., and Yu, Z., Genomic organization, polymorphisms and molecular evolution of the goose-type lysozyme gene from Zhikong scallop Chlamys farreri, Gene, 2013, vol. 513, pp. 40–52. https://doi.org/10.1016/j.fsi.2014.07.026
He, C., Yu, H., Liu, W., Su, H., Shan, Z., Bao, X., Li, Y., Fu, L., and Gao, X., A goose-type lysozyme gene in Japanese scallop (Mizuhopecten yessoensis): cDNA cloning, mRNA expression and promoter sequence analysis, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2012, vol. 162, pp. 34–43. https://doi.org/10.1016/j.cbpb.2012.02.002
Itoh, N. and Takahashi, K.G., A novel peptidoglycan recognition protein containing a goose-type lysozyme domain from the Pacific oyster, Crassostrea gigas, Mol. Immunol., 2009, vol. 46, pp. 1768–1774. https://doi.org/10.1016/j.molimm.2009.01.022
Ding, J., Wang, R., Yang, F., Zhao, L., Qin, Y., Zhang, G., and Yan, X., Identification and characterization of a novel phage-type like lysozyme from Manila clam, Ruditapes philippinarum, Dev. Comp. Immunol., 2014, vol. 47, pp. 81–89. https://doi.org/10.1016/j.dci.2014.06.013
Ren, Q., Wang, C., Jin, M., Lan, J., Ye, T., Hui, K., Tan, J., Wang, Z., Wyckoff, G.J., Wang, W., and Han, G.-Z., Co-option of bacteriophage lysozyme genes by bivalve genomes, Open Biol., 2017, vol. 7, 160285. https://doi.org/10.1098/rsob.160285
Gonzalez, M., Gueguen, Y., Destoumieux-Garzón, D., Romestand, B., Fievet, J., Pugniere, M., Roquet, F., Escoubas, J.-M., Vandenbulcke, F., Levy, O., Sauné, L., Bulet, P., and Bachere, E., Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI, Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, pp. 17759–17764. https://doi.org/10.1073/pnas.0702281104
Zhang, Y., He, X., Li, X., Fu, D., Chen, J., and Yu, Z., The second bactericidal permeability increasing protein (BPI) and its revelation of the gene duplication in the Pacific oyster, Crassostrea gigas, Fish Shellfish Immunol., 2011, vol. 30, pp. 954–963. https://doi.org/10.1016/j.fsi.2011.01.031
Moreira, R., Balseiro, P., Planas, J.V., Fuste, B., Beltran, S., Novoa, B., and Figueras, A., Transcriptomics of in vitro immune-stimulated hemocytes from the Manila clam Ruditapes philippinarum using high-throughput sequencing, PLoS One, 2012, vol. 7, e35009. https://doi.org/10.1371/journal.pone.0035009
Zhang, L., Li, L., Zhu, Y., Zhang, G., and Guo, X., Transcriptome analysis reveals a rich gene set related to innate immunity in the Eastern oyster (Crassostrea virginica), Mar. Biotechnol., 2014, vol. 16, pp. 17–33. https://doi.org/10.1007/s10126-013-9526-z
Prado-Alvarez, M., Rotllant, J., Gestal, C., Novoa, B., and Figueras, A., Characterization of a C3 and a factor B-like in the carpet-shell clam, Ruditapes decussatus, Fish Shellfish Immunol., 2009, vol. 26, pp. 305–315. https://doi.org/10.1016/j.fsi.2008.11.015
Peng, K., Wang, J., Sheng, J., Zeng, L., and Hong, Y., Molecular characterization and immune analysis of a defensin from freshwater pearl mussel, Hyriopsis schlegelii, Aquaculture, 2012, vol. 334–337, pp. 45–50. https://doi.org/10.1016/j.aquaculture.2011.12.039
Hubert, F., Noel, T., and Roch, P., A member of the arthropod defensin family from edible Mediterranean mussels (Mytilus galloprovincialis), Eur. J. Biochem., 1996, vol. 240, pp. 302–306.
Charlet, M., Chernysh, S., Philippe, H., Hetru, C., Hoffmann, J.A., and Bulet, P., Innate immunity. Isolation of several cysteine-rich antimicrobial peptides from the blood of a mollusc, Mytilus edulis, J. Biol. Chem., 1996, vol. 271, pp. 21808–21813. https://doi.org/10.1074/jbc.271.36.21808
Mitta, G., Vandenbulcke, F., Noel, T., Romestand, B., Beauvillain, J.C., Salzet, M., and Roch, P., Differential distribution and defence involvement of antimicrobial peptides in mussel, J. Cell Sci., 2000, vol. 113, pp. 2759–2769.
Mitta, G., Hubert, F., Dyrynda, E.A., Boudry, P., and Roch, P., Mytilin B and MGD2, two antimicrobial peptides of marine mussels: Gene structure and expression analysis, Dev. Comp. Immunol., 2000, vol. 24, pp. 381–393. https://doi.org/10.1016/s0145-305x(99)00084-1
Mitta, G., Vandenbulcke, F., Hubert, F., Salzet, M., and Roch, P., Involvement of mytilins in mussel antimicrobial defense, J. Biol. Chem., 2000, vol. 275, pp. 12954–12962. https://doi.org/10.1074/jbc.275.17.12954
Mitta, G., Hubert, F., Noël, T., and Roch, P., Myticin, a novel cysteine-rich antimicrobial peptide isolated from haemocytes and plasma of the mussel Mytilus galloprovincialis, Eur. J. Biochem., 1999, vol. 265, pp. 71–78. https://doi.org/10.1046/j.1432-1327.1999.00654.x
Martinez-Lopez, A., Encinar, J.A., Medina-Gali, R.M., Balseiro, P., Garcia-Valtanen, P., Figueras, A., Novoa, B., and Estepa, A., pH-dependent solution structure and activity of a reduced form of the host-defense peptide myticin C (Myt C) from the mussel Mytilus galloprovincialis, Mar. Drugs, 2013, vol. 11, pp. 2328–2346. https://doi.org/10.3390/md11072328
Domeneghetti, S., Franzoi, M., Damiano, N., Norante, R., El Halfawy, N.M., Mammi, S., Marin, O., Bellanda, M., and Venier, P., Structural and antimicrobial features of peptides related to myticin C, a special defense molecule from the Mediterranean mussel Mytilus galloprovincialis, J. Agric. Food Chem., 2015, vol. 63, pp. 9251–9259. https://doi.org/10.1021/acs.jafc.5b03491
Novoa, B., Romero, A., Álvarez, Á.L., Moreira, R., Pereiro, P., Costa, M.M., Dios, S., Estepa, A., Parra, F., and Figueras, A., Antiviral activity of myticin C peptide from mussel: An ancient defense against herpesviruses, J. Virol., 2016, vol. 90, pp. 7692–7702. https://doi.org/10.1128/JVI.00591-16
Li, H., Venier, P., Prado-Alvárez, M., Gestal, C., Toubiana, M., Quartesan, R., Borghesan, F., Novoa, B., Figueras, A., and Roch, P., Expression of Mytilus immune genes in response to experimental challenges varied according to the site of collection, Fish Shellfish Immunol., 2010, vol. 28, pp. 640–648. https://doi.org/10.1016/j.fsi.2009.12.022
Gueguen, Y., Herpin, A., Aumelas, A., Garnier, J., Fievet, J., Escoubas, J.-M., Bulet, P., Gonzalez, M., Lelong, C., Favrel, P., and Bachère, E., Characterization of a defensin from the oyster Crassostrea gigas. Recombinant production, folding, solution structure, antimicrobial activities, and gene expression, J. Biol. Chem., 2006, vol. 281, pp. 313–323. https://doi.org/10.1074/jbc.M510850200
Gonzalez, M., Gueguen, Y., Desserre, G., de Lorgeril, J., Romestand, B., and Bachère, E., Molecular characterization of two isoforms of defensin from hemocytes of the oyster Crassostrea gigas, Dev. Comp. Immunol., 2007, vol. 31, pp. 332–339. https://doi.org/10.1016/j.dci.2006.07.006
Xu, W. and Faisal, M., Defensin of the zebra mussel (Dreissena polymorpha): Molecular structure, in vitro expression, antimicrobial activity, and potential functions, Mol. Immunol., 2010, vol. 47, pp. 2138–2147. https://doi.org/10.1016/j.molimm.2010.01.025
Seo, J.-K., Lee, M.J., Nam, B.-H., and Park, N.G., cgMolluscidin, a novel dibasic residue repeat rich antimicrobial peptide, purified from the gill of the Pacific oyster, Crassostrea gigas, Fish Shellfish Immunol., 2013, vol. 35, pp. 480–488. https://doi.org/10.1016/j.fsi.2013.05.010
Wang, Q., Zhang, L., Yang, D., Yu, Q., Li, F., Cong, M., Ji, C., Wu, H., and Zhao, J., Molecular diversity and evolution of defensins in the manila clam Ruditapes philippinarum, Fish Shellfish Immunol., 2015, vol. 47, pp. 302–312. https://doi.org/10.1016/j.fsi.2015.09.008
Gerdol, M., De Moro, G., Manfrin, C., Venier, P., and Pallavicini, A., Big defensins and mytimacins, new AMP families of the Mediterranean mussel Mytilus galloprovincialis, Dev. Comp. Immunol., 2012, vol. 36, pp. 390–399. https://doi.org/10.1016/j.dci.2011.08.003
Zhao, J., Li, C., Chen, A., Li, L., Su, X., and Li, T., Molecular characterization of a novel big defensin from clam Venerupis philippinarum, PLoS One, 2010, vol. 5, e13480. https://doi.org/10.1371/journal.pone.0013480
Rosa, R.D., Santini, A., Fievet, J., Bulet, P., Destoumieux-Garzón, D., and Bachère, E., Big defensins, a diverse family of antimicrobial peptides that follows different patterns of expression in hemocytes of the oyster Crassostrea gigas, PLoS One, 2011, vol. 6, e25594. https://doi.org/10.1371/journal.pone.0025594
Li, M., Zhu, L., Zhou, C., Sun, S., Fan, Y., and Zhuang, Z., Molecular characterization and expression of a novel big defensin (Sb-BDef1) from ark shell, Scapharca broughtonii, Fish Shellfish Immunol., 2012, vol. 33, pp. 1167–1173. https://doi.org/10.1016/j.fsi.2012.09.008
Wang, G.-L., Xia, X.-L., Li, X.-L., Dong, S.-J., and Li, J.-L., Molecular characterization and expression patterns of the big defensin gene in freshwater mussel (Hyriopsis cumingii), GMR, Genet. Mol. Res., 2014, vol. 13, pp. 704–715. https://doi.org/10.4238/2014.January.29.1
Yang, J., Luo, J., Zheng, H., Lu, Y., and Zhang, H., Cloning of a big defensin gene and its response to Vibrio parahaemolyticus challenge in the noble scallop Chlamys nobilis (Bivalve: Pectinidae), Fish Shellfish Immunol., 2016, vol. 56, pp. 445–449. https://doi.org/10.1016/j.fsi.2016.07.030
González, R., Brokordt, K., Cárcamo, et al., Molecular characterization and protein localization of the antimicrobial peptide big defensin from the scallop Argopecten purpuratus after Vibrio splendidus challenge, Fish Shellfish Immunol., 2017, vol. 68, pp. 173–179. https://doi.org/10.1016/j.fsi.2017.07.010
Sonthi, M., Toubiana, M., Pallavicini, A., Venier, P., and Roch, P., Diversity of coding sequences and gene structures of the antifungal peptide mytimycin (MytM) from the Mediterranean mussel, Mytilus galloprovincialis, Mar. Biotechnol., 2011, vol. 13, pp. 857–867. https://doi.org/10.1007/s10126-010-9345-4
Gueguen, Y., Bernard, R., Julie, F., Paulina, S., Delphine, D.-G., Franck, V., Philippe, B., and Evelyne, B., Oyster hemocytes express a proline-rich peptide displaying synergistic antimicrobial activity with a defensin, Mol. Immunol., 2009, vol. 46, pp. 516–522. https://doi.org/10.1016/j.molimm.2008.07.021
Leoni, G., De Poli, A., Mardirossian, M., et al., Myticalins: A novel multigenic family of linear, cationic antimicrobial peptides from marine mussels (Mytilus spp.), Mar. Drugs, 2017, vol. 15, p. 261. https://doi.org/10.3390/md15080261
Seo, J.-K., Stephenson, J., and Noga, E.J., Multiple antibacterial histone H2B proteins are expressed in tissues of American oyster, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2011, vol. 158, pp. 223–229. https://doi.org/10.1016/j.cbpb.2010.11.011
Royet, J. and Dziarski, R., Peptidoglycan recognition proteins: Pleiotropic sensors and effectors of antim crobial defences, Nat. Rev. Microbiol., 2007, vol. 5, pp. 264–277. https://doi.org/10.1038/nrmicro1620
Montaño, A.M., Tsujino, F., Takahata, N., and Satta, Y., Evolutionary origin of peptidoglycan recognition proteins in vertebrate innate immune system, BMC Evol. Biol., 2011, vol. 11, 79. https://doi.org/10.1186/1471-2148-11-79
Su, J., Ni, D., Song, L., Zhao, J., and Qiu, L., Molecular cloning and characterization of a short type peptidoglycan recognition protein (CfPGRP-S1) cDNA from Zhikong scallop Chlamys farreri, Fish Shellfish Immunol., 2007, vol. 23, pp. 646–656. https://doi.org/10.1016/j.fsi.2007.01.023
Yang, Z., Li, J., Li, Y., Wu, H., and Wang, X., Molecular cloning and functional characterization of a short peptidoglycan recognition protein (HcPGRPS1) from the freshwater mussel, Hyriopsis cumingi, Mol. Immunol., 2013, vol. 56, pp. 729–738. https://doi.org/10.1016/j.molimm.2013.06.019
Wei, X., Yang, Jianmin, Yang, D., Xu, J., Liu, X., Yang, Jialong, Fang, J., and Qiao, H., Molecular cloning and mRNA expression of two peptidoglycan recognition protein (PGRP) genes from mollusk Solen grandis, Fish Shellfish Immunol., 2012, vol. 32, pp. 178–185. https://doi.org/10.1016/j.fsi.2011.11.009
Christensen, B.M., Li, J., Chen, C.-C., and Nappi, A.J., Melanization immune responses in mosquito vectors, Trends Parasitol., 2005, vol. 21, pp. 192–199. https://doi.org/10.1016/j.pt.2005.02.007
Tang, H., Regulation and function of the melanization reaction in Drosophila, Fly, 2009, vol. 3, pp. 105–111. https://doi.org/10.4161/fly.3.1.7747
Luna-Acosta, A., Breitwieser, M., Renault, T., and Thomas-Guyon, H., Recent findings on phenoloxidases in bivalves, Mar. Pollut. Bull., 2017, vol. 122, pp. 5–16. https://doi.org/10.1016/j.marpolbul.2017.06.031
Waite, J.H. and Wilbur, K.M., Phenoloxidase in the periostracum of the marine bivalve Modiolus demissus Dillwyn, J. Exp. Zool., 1976, vol. 195, pp. 359–367.
Ford, S.E. and Borrero, F.J., Epizootiology and pathology of juvenile oyster disease in the Eastern oyster, Crassostrea virginica, J. Invertebr. Pathol., 2001, vol. 78, pp. 141–154. https://doi.org/10.1006/jipa.2001.5052
Paillard, C., A short-review of brown ring disease, a vibriosis affecting clams, Ruditapes philippinarum and Ruditapes decussatus, Aquat. Living Resour., 2004, vol. 17, pp. 467–475. https://doi.org/10.1051/alr:2004053
Butt, D. and Raftos, D., Phenoloxidase-associated cellular defence in the Sydney rock oyster, Saccostrea glomerata, provides resistance against QX disease infections, Dev. Comp. Immunol., 2008, vol. 32, pp. 299–306. https://doi.org/10.1016/j.dci.2007.06.006
Asokan, R., Arumugam, M., and Mullainadhan, P., Activation of prophenoloxidase in the plasma and haemocytes of the marine mussel Perna viridis Linnaeus, Dev. Comp. Immunol., 1997, vol. 21, pp. 1–12. https://doi.org/10.1016/s0145-305x(97)00004-9
Hellio, C., Bado-Nilles, A., Gagnaire, B., Renault, T., and Thomas-Guyon, H., Demonstration of a true phenoloxidase activity and activation of a ProPO cascade in Pacific oyster, Crassostrea gigas (Thunberg) in vitro, Fish Shellfish Immunol., 2007, vol. 22, pp. 433–440. https://doi.org/10.1016/j.fsi.2006.06.014
Raftos, D.A., Kuchel, R., Aladaileh, S., and Butt, D., Infectious microbial diseases and host defense responses in Sydney rock oysters, Front. Aquat. Microbiol., 2014, vol. 5, pp. 135. https://doi.org/10.3389/fmicb.2014.00135
Xing, J., Jiang, J., and Zhan, W., Phenoloxidase in the scallop Chlamys farreri: Purification and antibacterial activity of its reaction products generated in vitro, Fish Shellfish Immunol., 2012, vol. 32, pp. 89–93. https://doi.org/10.1016/j.fsi.2011.10.025
Jiang, J., Xing, J., Sheng, X., and Zhan, W., Characterization of phenoloxidase from the bay scallop Argopecten irradians, J. Shellfish Res., 2011, vol. 30, pp. 273–277. https://doi.org/10.2983/035.030.0212
Niu, D., Jin, K., Wang, L., Feng, B., and Li, J., Molecular characterization and expression analysis of four cathepsin L genes in the razor clam, Sinonovacula constricta, Fish Shellfish Immunol., 2013, vol. 35, pp. 581–588. https://doi.org/10.1016/j.fsi.2013.06.001
Niu, D., Xie, S., Bai, Z., Wang, L., Jin, K., and Li, J., Identification of cathepsin B in the razor clam Sinonovacula constricta and its role in innate immune responses, Dev. Comp. Immunol., 2013, vol. 41, pp. 94–99. https://doi.org/10.1016/j.dci.2014.04.012
Niu D., et al., Identification, expression, and responses to bacterial challenge of the cathepsin C gene from the razor clam Sinonovacula constricta, Dev. Comp. Immunol., 2014, vol. 46, pp. 241–245.
Hu, Xiaojuan, Hu, Xiangping, Hu, B., Wen, C., Xie, Y., Wu, D., Tao, Z., Li, A., and Gao, Q., Molecular cloning and characterization of cathepsin L from freshwater mussel, Cristaria plicata, Fish Shellfish Immunol., 2014, vol. 40, pp. 446–454. https://doi.org/10.1016/j.fsi.2014.07.005
Ertl, N.G., O’Connor, W.A., Papanicolaou, A., Wiegand, A.N., and Elizur, A., Transcriptome analysis of the sydney Rock oyster, Saccostrea glomerata: Insights into molluscan immunity, PLoS One, 2016, vol. 11, e0156649. https://doi.org/10.1371/journal.pone.0156649
Xue, Q.-G., Waldrop, G.L., Schey, K.L., Itoh, N., Ogawa, M., Cooper, R.K., Losso, J.N., and La Peyre, J.F., A novel slow-tight binding serine protease inhibitor from eastern oyster (Crassostrea virginica) plasma inhibits perkinsin, the major extracellular protease of the oyster protozoan parasite Perkinsus marinus, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 2006, vol. 145, pp. 16–26. https://doi.org/10.1016/j.cbpb.2006.05.010
Gutiérrez-Rivera, J.N., Arcos-Ortega, G.F., Luna-González, A., et al., Differential expression of serine protease inhibitors 1 and 2 in Crassostrea corteziensis and C. virginica infected with Perkinsus marinus, Dis. Aquat. Org., 2015, vol. 112, pp. 185–197. https://doi.org/10.3354/dao02808
Zhu, L., Song, L., Chang, Y., Xu, W., and Wu, L., Molecular cloning, characterization and expression of a novel serine proteinase inhibitor gene in bay scallops (Argopecten irradians, Lamarck 1819), FishShellfish Immunol., 2006, vol. 20, pp. 320–331. https://doi.org/10.1016/j.fsi.2005.05.009
Wang, B., Zhao, J., Song, L., et al., Molecular cloning and expression of a novel Kazal-type serine proteinase inhibitor gene from Zhikong scallop Chlamys farreri, and the inhibitory activity of its recombinant domain, Fish Shellfish Immunol., 2008, vol. 24, pp. 629–637. https://doi.org/10.1016/j.fsi.2008.01.017
Maldonado-Aguayo, W., Núñez-Acuña, G., Valenzuela-Muñoz, V., Chávez-Mardones, J., and Gallardo-Escárate, C., Molecular characterization of two Kazal-type serine proteinase inhibitor genes in the surf clam Mesodesma donacium exposed to Vibrio anguillarum, Fish Shellfish Immunol., 2013, vol. 34, pp. 1448–1454. https://doi.org/10.1016/j.fsi.2013.03.356
Yu, Q., Yang, D., Wang, Q., Zhang, Y., Cong, M., Wu, H., Ji, C., Li, F., and Zhao, J., Molecular characterization, expression and functional analysis of two Kazal-type serine protease inhibitors from Venerupis philippinarum, Fish Shellfish Immunol., 2017, vol. 70, pp. 156–163. https://doi.org/10.1016/j.fsi.2017.09.018
Montagnani, C., Le Roux, F., Berthe, F., and Escoubas, J.M., Cg-TIMP, an inducible tissue inhibitor of metalloproteinase from the Pacific oyster Crassostrea gigas with a potential role in wound healing and defense mechanisms, FEBS Lett., 2001, vol. 500, pp. 64–70. https://doi.org/10.1016/s0014-5793(01)02559-5
Roberts, S., Gueguen, Y., de Lorgeril, J., and Goetz, F., Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure, Dev. Comp. Immunol., 2008, vol. 32, pp. 1099–1104. https://doi.org/10.1016/j.dci.2008.02.006
Wu, S.-Z., Huang, X.-D., Li, Q., and He, M.-X., Interleukin-17 in pearl oyster (Pinctada fucata): Molecular cloning and functional characterization, Fish Shellfish Immunol., 2013. vol. 34, pp. 1050–1056. https://doi.org/10.1016/j.fsi.2013.01.005
Moreira, R., Milan, M., Balseiro, P., et al., Gene expression profile analysis of Manila clam (Ruditapes philippinarum) hemocytes after a Vibrio alginolyticus challenge using an immune-enriched oligo-microarray, BMC Genomics, 2014, vol. 15, 267. https://doi.org/10.1186/1471-2164-15-267
Xin, L., Zhang, H., Du, X., Li, Y., Li, M., Wang, L., Wang, H., Qiu, L., and Song, L., The systematic regulation of oyster CgIL17-1 and CgIL17-5 in response to air exposure, Dev. Comp. Immunol., 2016, vol. 63, pp. 144–155.https://doi.org/10.1016/j.dci.2016.06.001
Li, J., Zhang, Yang, Zhang, Yuehuan, Xiang, Z., Tong, Y., Qu, F., and Yu, Z., Genomic characterization and expression analysis of five novel IL-17 genes in the Pacific oyster, Crassostrea gigas, Fish Shellfish Immunol., 2014, vol. 40, pp. 455–465. https://doi.org/10.1016/j.fsi.2014.07.026
Parisi, M.-G., Toubiana, M., Mangano, V., Parrinello, N., Cammarata, M., and Roch, P., MIF from mussel: Coding sequence, phylogeny, polymorphism, 3D model and regulation of expression, Dev. Comp. Immunol., 2012, vol. 36, pp. 688–696. https://doi.org/10.1016/j.dci.2011.10.014
Li, J., Chen, J., Zhang, Y., and Yu, Z., Expression of allograft inflammatory factor-1 (AIF-1) in response to bacterial challenge and tissue injury in the pearl oyster, Pinctada martensii, Fish Shellfish Immunol., 2013, vol. 34, pp. 365–371. https://doi.org/10.1016/j.fsi.2012.11.012
Martin-Gomez, L., Villalba, A., Carballal, M.J., and Abollo, E., Molecular characterisation of TNF, AIF, dermatopontin and VAMP genes of the flat oyster Ostrea edulis and analysis of their modulation by diseases, Gene, 2014, vol. 533, pp. 208–217. https://doi.org/10.1016/j.gene.2013.09.085
Zhang, Y., Li, J., Yu, F., He, X., and Yu, Z., Allograft inflammatory factor-1 stimulates hemocyte immune activation by enhancing phagocytosis and expression of inflammatory cytokines in Crassostrea gigas, Fish Shellfish Immunol., 2013, vol. 34, pp. 1071–1077. https://doi.org/10.1016/j.fsi.2013.01.014
Qu, F., Xiang, Z., Zhang, Yang, Li, J., Xiao, S., Zhang, Yuehuan, Qin, Y., Zhou, Y., and Yu, Z., Molecular identification and functional characterization of a tumor necrosis factor (TNF) gene in Crassostrea hongkongensis, Immunobiology, 2017, vol. 222, pp. 751–758. https://doi.org/10.1016/j.imbio.2017.02.002
Liao, Z., Wang, X., Liu, H., Fan, M., Sun, J., and Shen, W., Molecular characterization of a novel antimicrobial peptide from Mytilus coruscus, Fish Shellfish Immunol., 2013, vol. 34, pp. 610–616. https://doi.org/10.1016/j.fsi.2012.11.030
Qin, C., Huang, W., Zhou, S., Wang, X., Liu, H., Fan, M., Wang, R., Gao, P., and Liao, Z., Characterization of a novel antimicrobial peptide with chitin-biding domain from Mytilus coruscus, Fish Shellfish Immunol., 2014, vol. 41, pp. 362–370. https://doi.org/10.1016/j.fsi.2014.09.019
Gerdol, M., Puillandre, N., De Moro, G., et al., Identification and characterization of a novel family of cysteine-rich peptides (MgCRP-I) from Mytilus galloprovincialis, Genome Biol. Evol., 2015, vol. 7, pp. 2203–2219. https://doi.org/10.1093/gbe/evv133
ACKNOWLEDGMENTS
The authors are grateful the CKP Primorsky aquarium, Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences (Vladivostok, Russia).
Funding
This study was supported by the RF Ministry of Science and Higher Education (project no. 0657-2020-0004).
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Grinchenko, A.V., Kumeiko, V.V. Bivalves Humoral Immunity: Key Molecules and Their Functions. Russ J Mar Biol 48, 399–417 (2022). https://doi.org/10.1134/S1063074022060062
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DOI: https://doi.org/10.1134/S1063074022060062