Dietary manipulation to maintain fish health and reduce bacterial infection through the use of immunostimulants has been widely used worldwide. A broad range of bioactive substances capable of optimising animal health has been found in several insect species, including antimicrobial/antiviral peptides, polysaccharides such as chitin, lauric acid, and insect products such as honey. Recently, we identified a novel bioactive polysaccharide from Bombyx mori, termed silkrose-BM, that can activate innate immunity in mammalian RAW264.7 macrophages and provide effective protection against vibriosis in penaeid prawns. However, the efficacy of dietary silkrose-BM in teleosts remains unclear. Here, we investigated the effects of dietary inclusion of silkrose-BM in Japanese medaka (Oryzias latipes) after they were artificially challenged with Edwardsiella tarda. The survival of medaka after infection with E. tarda was significantly improved by dietary silkrose-BM at a concentration of 10, 100, and 1000 ng/g. RNA-seq analysis was performed in the intestine and liver of the medaka to identify changes in the transcriptional profiling evoked by silkrose-BM. The dietary silkrose-BM group showed 1,194 and 2,259 differentially expressed genes (DEGs) in the intestine and liver, respectively, when compared with the control group prior to E. tarda infection. Functional enrichment analysis of DEGs showed several putative genes involved in the Toll-like receptor/nuclear factor κB pathway, cytokine-cytokine receptor interactions, complement cascade, antimicrobial peptides, and junctional modification. Taken together, these results suggest that silkrose-BM used as an immunostimulant can improve the immune system and resistance to edwardsiellosis in teleosts.
Akira, S., Uematsu, S. and Takeuchi, O., 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. https://doi.org/10.1016/j.cell.2006.02.015
Ali, M.F.Z., Kameda, K., Kondo, F., Iwai, T., Kurniawan, R.A., Ohta, T., Ido, A., Takahashi, T., Miura, C. and Miura, T., 2021. Effects of dietary silkrose of Antheraea yamamai on gene expression profiling and disease resistance to Edwardsiella tarda in Japanese medaka (Oryzias latipes). Fish and Shellfish Immunology 114: 207-217. https://doi.org/10.1016/j.fsi.2021.05.001
Ali, M.F.Z., Ohta, T., Ido, A., Miura, C. and Miura, T., 2019. The dipterose of black soldier fly (Hermetia illucens) induces innate immune response through toll-like receptor pathway in mouse macrophage RAW264.7 cells. Biomolecules 9: 677. https://doi.org/10.3390/biom9110677
Ali, M.F.Z., Yasin, I.A., Ohta, T., Hashizume, A., Ido, A., Takahashi, T., Miura, C. and Miura, T., 2018. The silkrose of Bombyx mori effectively prevents vibriosis in penaeid prawns via the activation of innate immunity. Scientific Reports 8: 8836. https://doi.org/10.1038/s41598-018-27241-3
Arts, J.A., Tijhaar, E.J., Chadzinska, M., Savelkoul, H.F. and Verburg-Van Kemenade, B.M., 2010. Functional analysis of carp interferon-γ: evolutionary conservation of classical phagocyte activation. Fish and Shellfish Immunology 29: 793-802. https://doi.org/10.1016/j.fsi.2010.07.010
Bebak, J. and Wagner, B., 2012. Use of vaccination against enteric septicemia of catfish and columnaris disease by the U.S. Catfish Industry. Journal of Aquatic Animal Health 24: 30-36. https://doi.org/10.1080/08997659.2012.667048
Boshra, H., Li, J. and Sunyer, J.O., 2006. Recent advances on the complement system of teleost fish. Fish and Shellfish Immunology 20: 239-262. https://doi.org/10.1016/j.fsi.2005.04.004
Cabello, F.C., 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environmental Microbiology 8: 1137-1144. https://doi.org/10.1111/j.1462-2920.2006.01054.x
Castro, N., Toranzo, A.E., Núñez, S. and Magariños, B., 2008. Development of an effective Edwardsiella tarda vaccine for cultured turbot (Scophthalmus maximus). Fish and Shellfish Immunology 25: 208-212. https://doi.org/10.1016/j.fsi.2008.05.008
Chaklader, M.R., Siddik, M.A.B., Fotedar, R. and Howieson, J., 2019. Insect larvae, Hermetia illucens in poultry by-product meal for barramundi, Lates calcarifer modulates histomorphology, immunity and resistance to Vibrio harveyi. Scientific Reports 9: 16703. https://doi.org/10.1038/s41598-019-53018-3
Chernysh, S., Kim, S.I., Bekker, G., Pleskach, V.A., Filatova, N.A., Anikin, V.B., Platonov, V.G. and Bulet, P., 2002. Antiviral and antitumor peptides from insects. Proceedings of the National Academy of Sciences of the USA 99: 12628-12632. https://doi.org/10.1073/pnas.192301899
Clavijo, A.M., Conroy, G., Conroy, D.A., Santander, J. and Aponte, F., 2002. First report of Edwardsiella tarda from tilapias in Venezuela. Bulletin of the European Association of Fish Pathologists 22: 280-282.
'First report of Edwardsiella tarda from tilapias in Venezuela ' () 22 Bulletin of the European Association of Fish Pathologists : 280 -282 .
Doñate, C., Balasch, J.C., Callol, A., Bobe, J., Tort, L. and MacKenzie, S., 2010. The effects of immunostimulation through dietary manipulation in the rainbow trout: evaluation of mucosal immunity. Marine Biotechnology 12: 88-99. https://doi.org/10.1007/s10126-009-9203-4
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. and Smith, F., 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28: 350-356. https://doi.org/10.1021/ac60111a017
Ferreira, S.S., Passos, C.P., Madureira, P., Vilanova, M. and Coimbra, M.A., 2015. Structure – function relationships of immunostimulatory polysaccharides: a review. Carbohydrate Polymers 132: 378-396. https://doi.org/10.1016/j.carbpol.2015.05.079
Gasco, L., Finke, M. and Van Huis, A., 2018. Can diets containing insects promote animal health? Journal of Insects as Food and Feed 4: 1-4. https://doi.org/10.3920/JIFF2018.x001
Giri, S.S., Sen, S.S., Chi, C., Kim, H.J., Yun, S., Park, S.C. and Sukumaran, V., 2015. Chlorophytum borivilianum polysaccharide fraction provokes the immune function and disease resistance of Labeo rohita against Aeromonas hydrophila. Journal of Immunology Research, Article ID: 256510. https://doi.org/10.1155/2015/256510
Gopalakannan, A. and Arul, V., 2006. Immunomodulatory effects of dietary intake of chitin, chitosan and levamisole on the immune system of Cyprinus carpio and control of Aeromonas hydrophila infection in ponds. Aquaculture 255: 179-187. https://doi.org/10.1016/j.aquaculture.2006.01.012
Grayfer, L. and Belosevic, M., 2012. Cytokine regulation of teleost inflammatory responses. In: Turker, H. (ed.) New advances and contributions to fish biology. IntechOpen, London, UK, pp. 59-96.
'Cytokine regulation of teleost inflammatory responses ', () 59 -96 .
Harikrishnan, R., Kim, J.S., Balasundaram, C. and Heo, M.S., 2012. Dietary supplementation with chitin and chitosan on haematology and innate immune response in Epinephelus bruneus against Philasterides dicentrarchi. Experimental Parasitology 131: 116-124. https://doi.org/10.1016/j.exppara.2012.03.020
Harikrishnan, R., Kim, J.S., Balasundaram, C. and Heo, M.S., 2012. Immunomodulatory effects of chitin and chitosan enriched diets in Epinephelus bruneus against Vibrio alginolyticus infection. Aquaculture 326-329: 46-52. https://doi.org/10.1016/j.aquaculture.2011.11.034
Henry, M.A., Gai, F., Enes, P., Peréz-Jiménez, A. and Gasco L., 2018. Effect of partial dietary replacement of fishmeal by yellow mealworm (Tenebrio molitor) larvae meal on the innate immune response and intestinal antioxidant enzymes of rainbow trout (Oncorhynchus mykiss). Fish and Shellfish Immunology 83: 308-313. https://doi.org/10.1016/j.fsi.2018.09.040
Holland, M.C.H. and Lambris, J.D., 2002. The complement system in teleosts. Fish and Shellfish Immunology 12: 399-420. https://doi.org/10.1006/fsim.2001.0408
Ido, A., Iwai, T., Ito, K., Ohta, T., Mizushige, T., Kishida, T., Miura, C. and Miura, T., 2015. Dietary effects of housefly (Musca domestica) (Diptera: Muscidae) pupae on the growth performance and the resistance against bacterial pathogen in red sea bream (Pagrus major) (Perciformes: Sparidae). Applied Entomology and Zoology 50: 213-221. https://doi.org/10.1007/s13355-015-0325-z
Ido, A., Hashizume, A., Ohta, T., Takahashi, T., Miura, C. and Miura, T., 2019. Replacement of fish meal by defatted yellow mealworm (Tenebrio molitor) larvae in diet improves growth performance and disease resistance in red seabream (Pagrus major). Animals 9: 100. https://doi.org/10.3390/ani9030100
Joerink, M., Savelkoul, H.F. and Wiegertjes, G.F., 2006. Evolutionary conservation of alternative activation of macrophages: structural and functional characterization of arginase 1 and 2 in carp (Cyprinus carpio L.). Molecular Immunology 43: 1116-1128. https://doi.org/10.1016/j.molimm.2005.07.022
Katzenback, B.A., 2015. Antimicrobial peptides as mediators of innate immunity in teleosts. Biology 4: 607-639. https://doi.org/10.3390/biology4040607
Kawai, T. and Akira, S., 2010. The role of pattern-recognition receptors in innate immunity: update on toll-like receptors. Nature Immunology 11: 373-384. https://doi.org/10.1038/ni.1863
Kim, D., Paggi, J.M., Park, C., Bennett, C. and Salzberg, S.L., 2019. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology 37(8): 907-915. https://doi.org/10.1038/s41587-019-0201-4.
Kumar, R., Kaur, N. and Kamilya, D., 2019. Chitin modulates immunity and resistance of Labeo rohita (Hamilton, 1822) against gill monogeneans. Aquaculture 498: 522-527. https://doi.org/10.1016/j.aquaculture.2018.09.013
Lee, C.G., Da Silva, C.A., Lee, J.Y., Hartl, D. and Elias, J.A., 2008. Chitin regulation of immune responses: an old molecule with new roles. Current Opinion in Immunology 20: 684-689. https://doi.org/10.1016/j.coi.2008.10.002
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R. and 1000 Genome Project Data Processing Subgroup, 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25(16): 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
Li, H., Zhang, F., Guo, H., Zhu, Y., Yuan, J., Yang, G. and An, L., 2013. Molecular characterization of hepcidin gene in common carp (Cyprinus carpio L.) and its expression pattern responding to bacterial challenge. Fish and Shellfish Immunology 35: 1030-1038. https://doi.org/10.1016/j.fsi.2013.07.001
Li, H.X., Lu, X.J., Li, C.H. and Chen, J., 2015. Molecular characterization of the liver-expressed antimicrobial peptide 2 (LEAP-2) in a teleost fish, Plecoglossus altivelis: antimicrobial activity and molecular mechanism. Molecular Immunology 65: 406-415. https://doi.org/10.1016/j.molimm.2015.02.022
Li, M.Y., Zhu, X.M., Niu, X.T., Chen, X.M., Tian, J.X., Kong, Y.D., Zhang, D.M., Zhao, L. and Wang, G.Q., 2019. Effects of dietary Allium mongolicum Regel polysaccharide on growth, lipopolysaccharide-induced antioxidant responses and immune responses in Channa argus. Molecular Biology Reports 46: 2221-2230. https://doi.org/10.1007/s11033-019-04677-y
Liao, Y., Smyth, G.K. and Shi, W., 2014. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30(7): 923-930. https://doi.org/10.1093/bioinformatics/btt656
Livak, K.J. and Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
Makkar, H.P.S., Tran, G., Heuzé, V. and Ankers, P., 2014. State-of-the-art on use of insects as animal feed. Animal Feed Science and Technology 197: 1-33. https://doi.org/10.1016/j.anifeedsci.2014.07.008
Martin, M., 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17(1): 10-12. https://doi.org/10.14806/ej.17.1.200
Martin, S.A.M., Dehler, C.E. and Król, E., 2016. Transcriptomic responses in the fish intestine. Developmental and Comparative Immunology 64: 103-117. https://doi.org/10.1016/j.dci.2016.03.014
Matsuyama, T., Kamaishi, T., Ooseko, N., Kurohara, K. and Iida T., 2005. Pathogenicity of motile and non-motile Edwardsiella tarda to some marine fish. Fish Pathology 40: 133-135. https://doi.org/10.3147/JSFP.40.133
Meyer, F.P. and Bullock, G.L., 1973. Edwardsiella tarda, a new pathogen of channel catfish (Ictalurus punctatus). Applied Microbiology 25: 155-156. https://doi.org/10.1128/am.25.1.155-156.1973
Michelucci, A., Cordes, T., Ghelfi, J., Pailot, A., Reiling, N., Goldmann, O., Binz, T., Wegner, A., Tallam, A., Rausell, A., Buttini, M., Linster, C.L., Medina, E., Balling, R. and Hiller, K., 2013. Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proceedings of the National Academy of Sciences of the USA 110: 7820-7825. https://doi.org/10.1073/pnas.1218599110
Mohanty, B.R. and Sahoo, P.K., 2007. Edwardsiellosis in fish: a brief review. Journal of Biosciences 32: 1331-1344. https://doi.org/10.1007/s12038-007-0125-x
Morimoto, N., Kono, T., Sakai, M. and Hikima, J.I., 2021. Inflammasomes in teleosts: structures and mechanisms that induce pyroptosis during bacterial infection. International Journal of Molecular Sciences 22: 4389. https://doi.org/10.3390/ijms22094389
Motte, C., Rios, A., Lefebvre, T., Do, H., Henry, M. and Jintasataporn, O., 2019. Replacing fish meal with defatted insect meal (Yellow mealworm Tenebrio molitor) improves the growth and immunity of pacific white shrimp (Litopenaeus vannamei). Animals 9: 258. https://doi.org/10.3390/ani9050258
Ohta, T., Ido, A., Kusano, K., Miura, C. and Miura, T., 2014. A novel polysaccharide in insects activates the innate immune system in mouse macrophage RAW264 cells. PLoS ONE 9: e114823. https://doi.org/10.1371/journal.pone.0114823
Ohta, T., Kusano, K., Ido, A., Miura, C. and Miura, T., 2015. Silkrose: a novel acidic polysaccharide from the silkmoth that can stimulate the innate immune response. Carbohydrate Polymers 136: 995-1001. https://doi.org/10.1016/j.carbpol.2015.09.070
Padrós, F., Zarza, C., Dopazo, L., Cuadrado, M. and Crespo, S., 2006. Pathology of Edwardsiella tarda infection in turbot, Scophthalmus maximus (L.). Journal of Fish Diseases 29: 87-94. https://doi.org/10.1111/j.1365-2761.2006.00685.x
Park, S.B, Aoki, T. and Jung, T.S., 2012. Pathogenesis of and strategies for preventing Edwardsiella tarda infection in fish. Veterinary Research 43: 67. https://doi.org/10.1186/1297-9716-43-67
Peatman, E., Lange, M., Zhao, H. and Beck, B.H., 2015. Physiology and immunology of mucosal barriers in catfish (Ictalurus spp.). Tissue Barriers 3: e1068907. https://doi.org/10.1080/21688370.2015.1068907
Ping, K.G. and Jie, G.X., 2011. Overview of silkworm pathology in China. African Journal of Biotechnology 10: 18046-18056. https://doi.org/10.5897/AJB10.263
Pooley, N.J., Tacchi, L., Secombes, C.J. amd Martin, S.A., 2013. Inflammatory responses in primary muscle cell cultures in Atlantic salmon (Salmo salar). BMC Genomics 14: 747. https://doi.org/10.1186/1471-2164-14-747
Rahimnejad, S., Hu, S., Song, K., Wang, L., Lu, K., Wu, R. and Zhang, C., 2019. Replacement of fish meal with defatted silkworm (Bombyx mori L.) pupae meal in diets for Pacific white shrimp (Litopenaeus vannamei). Aquaculture 510: 150-159. https://doi.org/10.1016/j.aquaculture.2019.05.054
Ratcliffe, N., Azambuja, P. and Mello., C.B., 2014. Recent advances in developing insect natural products as potential modern day medicines. Evidence-Based Complementary and Alternative Medicine, Article ID 904958. https://doi.org/10.1155/2014/904958
R Core Team, 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/.
Sakai, M., 1999. Current research status of fish immunostimulants. Aquaculture 172: 63-92. https://doi.org/10.1016/S0044-8486(98)00436-0
Salinas, I. and Magadán, S., 2017. Omics in fish mucosal immunity. Developmental and Comparative Immunology 75: 99-108. https://doi.org/10.1016/j.dci.2017.02.010
Shanthi Mari, L.S., Jagruthi, C., Anbazahan, S.M., Yogeshwari, G., Thirumurugan, R., Arockiaraj, J., Mariappan, P., Balasundaram, C. and Harikrishnan, R., 2014. Protective effect of chitin and chitosan enriched diets on immunity and disease resistance in Cirrhina mrigala against Aphanomyces invadans. Fish and Shellfish Immunology 39: 378-385. https://doi.org/10.1016/j.fsi.2014.05.027
Sun, J., Nishiyama, T., Shimizu, K. and Kadota, K., 2013. TCC: an R package for comparing tag count data with robust normalization strategies. BMC Bioinformatics 14: 219.
'TCC: an R package for comparing tag count data with robust normalization strategies ' () 14 BMC Bioinformatics : 219 .
Sun, Y.Y. and Sun, L., 2016. A teleost bactericidal permeability-increasing protein kills gram-negative bacteria, modulates innate immune response, and enhances resistance against bacterial and viral infection. PLoS ONE 11: e0154045. https://doi.org/10.1371/journal.pone.0154045
Sunyer, J.O. and Tort, L., 1995. Natural hemolytic and bactericidal activities of sea bream Sparus aurata serum are effected by the alternative complement pathway. Veterinary Immunology and Immunopathology 45: 333-345. https://doi.org/10.1016/0165-2427(94)05430-z
Supek, F., Bošnjak, M., Škunca, N. and Šmuc, T., 2011. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6: e21800. https://doi.org/10.1371/journal.pone.0021800
Vallejos-Vidal, E., Reyes-López, F., Teles, M. and MacKenzie, S., 2016. The response of fish to immunostimulant diets. Fish and Shellfish Immunology 56: 34-69. https://doi.org/10.1016/j.fsi.2016.06.028
Van Huis, A., 2021. Prospects of insects as food and feed. Organic Agriculture 11: 301-308. https://doi.org/10.1007/s13165-020-00290-7
Wang, T., Bird, S., Koussounadis, A., Holland, J.W., Carrington, A., Zou, J. and Secombes, C.J., 2009. Identification of a novel IL-1 cytokine family member in teleost fish. The Journal of Immunology 183: 962-974. https://doi.org/10.4049/jimmunol.0802953
Xiao, X., Jin, P., Zheng, L., Cai, M., Yu, Z., Yu, J. and Zhang, J., 2018. Effects of black soldier fly (Hermetia illucens) larvae meal protein as a fishmeal replacement on the growth and immune index of yellow catfish (Pelteobagrus fulvidraco). Aquaculture Research 49: 1569-1577. https://doi.org/10.1111/are.13611
Yang, X., Guo, J.L., Ye, J.Y., Zhang, Y.X. and Wang, W., 2015. The effects of Ficus carica polysaccharide on immune response and expression of some immune-related genes in grass carp, Ctenopharyngodon idella. Fish and Shellfish Immunology 42: 132-137. https://doi.org/10.1016/j.fsi.2014.10.037
Ye, H., Lin, Q. and Luo, H., 2018. Applications of transcriptomics and proteomics in understanding fish immunity. Fish and Shellfish Immunology 77: 319-327. https://doi.org/10.1016/j.fsi.2018.03.046
Yu, G., Wang, L.G., Han, Y. and He, Q.Y., 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5): 284-287. https://doi.org/10.1089/omi.2011.0118
Yuan, C., Pan, X., Gong, Y., Xia, A., Wu, G., Tang, J. and Han, X., 2008. Effects of Astragalus polysaccharides (APS) on the expression of immune response genes in head kidney, gill and spleen of the common carp, Cyprinus carpio L. International Immunopharmacology 8: 51-58. https://doi.org/10.1016/j.intimp.2007.10.009
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 0 | 0 | 0 |
Full Text Views | 102 | 102 | 48 |
PDF Views & Downloads | 81 | 81 | 20 |
Dietary manipulation to maintain fish health and reduce bacterial infection through the use of immunostimulants has been widely used worldwide. A broad range of bioactive substances capable of optimising animal health has been found in several insect species, including antimicrobial/antiviral peptides, polysaccharides such as chitin, lauric acid, and insect products such as honey. Recently, we identified a novel bioactive polysaccharide from Bombyx mori, termed silkrose-BM, that can activate innate immunity in mammalian RAW264.7 macrophages and provide effective protection against vibriosis in penaeid prawns. However, the efficacy of dietary silkrose-BM in teleosts remains unclear. Here, we investigated the effects of dietary inclusion of silkrose-BM in Japanese medaka (Oryzias latipes) after they were artificially challenged with Edwardsiella tarda. The survival of medaka after infection with E. tarda was significantly improved by dietary silkrose-BM at a concentration of 10, 100, and 1000 ng/g. RNA-seq analysis was performed in the intestine and liver of the medaka to identify changes in the transcriptional profiling evoked by silkrose-BM. The dietary silkrose-BM group showed 1,194 and 2,259 differentially expressed genes (DEGs) in the intestine and liver, respectively, when compared with the control group prior to E. tarda infection. Functional enrichment analysis of DEGs showed several putative genes involved in the Toll-like receptor/nuclear factor κB pathway, cytokine-cytokine receptor interactions, complement cascade, antimicrobial peptides, and junctional modification. Taken together, these results suggest that silkrose-BM used as an immunostimulant can improve the immune system and resistance to edwardsiellosis in teleosts.
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 0 | 0 | 0 |
Full Text Views | 102 | 102 | 48 |
PDF Views & Downloads | 81 | 81 | 20 |