Whole transcriptome analysis of the Atlantic cod vaccine response reveals subtle changes in adaptive immunity

Monica Hongrø Solbakken1, Sissel Jentoft1, Trond Reitan1, Helene Mikkelsen2, Kjetill S. Jakobsen1, Marit Seppola3
1Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway
2The Northern Norway Regional Health Authority, Tromsø, Norway
3Department of Medical Biology, The Arctic University of Norway, Tromsø, Norway

Tài liệu tham khảo

Andrews Bakkemo, 2011, Intracellular localisation and innate immune responses following Francisella noatunensis infection of Atlantic cod (Gadus morhua) macrophages, Fish Shellfish Immunol., 31, 993, 10.1016/j.fsi.2011.08.020 Ballesteros, 2012, Oral immunization of rainbow trout to infectious pancreatic necrosis virus (Ipnv) induces different immune gene expression profiles in head kidney and pyloric ceca, Fish Shellfish Immunol., 33, 174, 10.1016/j.fsi.2012.03.016 Berg, 2006, Time of vaccination influences development of adhesions, growth and spinal deformities in Atlantic salmon Salmo salar, Dis. Aquat. Org., 69, 239, 10.3354/dao069239 Bindea, 2009, ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks, Bioinformatics, 25, 1091, 10.1093/bioinformatics/btp101 Bird, 2015, Teleost chemokines and their receptors, Dev. Biol. (Basel), 4, 756 Buchmann, 2014, Evolution of innate immunity: clues from invertebrates via fish to mammals, Front. Immunol., 5, 459, 10.3389/fimmu.2014.00459 Caipang, 2008, Intraperitoneal vaccination of Atlantic cod, Gadus morhua with heat-killed Listonella anguillarum enhances serum antibacterial activity and expression of immune response genes, Fish Shellfish Immunol., 24, 314, 10.1016/j.fsi.2007.11.018 Caipang, 2009, Profiling gene expression in the spleen of Atlantic cod, Gadus morhua upon vaccination with Vibrio anguillarum antigen, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 153, 261, 10.1016/j.cbpb.2009.03.005 Camacho, 2009, BLAST+: architecture and applications, BMC Bioinf., 10, 421, 10.1186/1471-2105-10-421 Chettri, 2015, Comparative evaluation of infection methods and environmental factors on challenge success: Aeromonas salmonicida infection in vaccinated rainbow trout, Fish Shellfish Immunol., 44, 485, 10.1016/j.fsi.2015.03.003 Corripio-Miyar, 2007, Vaccination experiments in the gadoid haddock, Melanogrammus aeglefinus L., against the bacterial pathogen Vibrio anguillarum, Vet. Immunol. Immunopathol., 118, 147, 10.1016/j.vetimm.2007.04.011 Ellingsen, 2011, Francisella noatunensis in Atlantic cod (Gadus morhua L.); waterborne transmission and immune responses, Fish Shellfish Immunol., 31, 326, 10.1016/j.fsi.2011.05.021 Eschmeyer, 2015 Eslamloo, 2016, Transcriptome profiling of the antiviral immune response in Atlantic cod macrophages, Dev. Comp. Immunol., 63, 187, 10.1016/j.dci.2016.05.021 Feng, 2009, Identification and analysis of differentially expressed genes in immune tissues of Atlantic cod stimulated with formalin-killed, atypical Aeromonas salmonicida, Physiol. Genomics, 37, 149, 10.1152/physiolgenomics.90373.2008 Frans, 2011, Vibrio anguillarum as a fish pathogen: virulence factors, diagnosis and prevention, J. Fish Dis., 34, 643, 10.1111/j.1365-2761.2011.01279.x Fraser, 2015, Vaccination and triploidy increase relative heart weight in farmed Atlantic salmon, Salmo salar L, J. Fish Dis., 38, 151, 10.1111/jfd.12216 Gao, 2014, A live attenuated combination vaccine evokes effective immune-mediated protection against Edwardsiella tarda and Vibrio anguillarum, Vaccine, 32, 5937, 10.1016/j.vaccine.2014.08.074 Gardiner, 2016, The cells that mediate innate immune memory and their functional significance in inflammatory and infectious diseases, Semin. Immunol., 28, 343, 10.1016/j.smim.2016.03.001 Goff Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Gudmundsdottir, 2009, Specific and natural antibody response of cod juveniles vaccinated against Vibrio anguillarum, Fish Shellfish Immunol., 26, 619, 10.1016/j.fsi.2008.09.017 Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nat. Protoc., 8, 1494, 10.1038/nprot.2013.084 Haase, 2016, Comparative transcriptomics of stickleback immune gene responses upon infection by two helminth parasites, Diplostomum pseudospathaceum and Schistocephalus solidus, Zoology (Jena), 119, 307, 10.1016/j.zool.2016.05.005 Hoare, 2017, Efficacy of a polyvalent immersion vaccine against Flavobacterium psychrophilum and evaluation of immune response to vaccination in rainbow trout fry (Onchorynchus mykiss L.), Vet. Res., 48, 43, 10.1186/s13567-017-0448-z Hoffman, 2016, variancePartition: interpreting drivers of variation in complex gene expression studies, BMC Bioinf., 17, 483, 10.1186/s12859-016-1323-z Hwang, 2017, RNA-Seq transcriptome analysis of the olive flounder (Paralichthys olivaceus) kidney response to vaccination with heat-inactivated viral hemorrhagic septicemia virus, Fish Shellfish Immunol., 62, 221, 10.1016/j.fsi.2017.01.016 Jameson, 2009, Diversity in T cell memory: an embarrassment of riches, Immunity, 31, 859, 10.1016/j.immuni.2009.11.007 Jiang, 2014, Differential transcriptomic response in the spleen and head kidney following vaccination and infection of Asian seabass with Streptococcus iniae, PLoS One, 9, 10.1371/journal.pone.0099128 Jiang, 2016, Transcriptome signatures in common carp spleen in response to Aeromonas hydrophila infection, Fish Shellfish Immunol., 57, 41, 10.1016/j.fsi.2016.08.013 Joshi Kumar, 2016, MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets, Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054 Lauvau, 2016, Memory CD8(+) T cells: innate-like sensors and orchestrators of protection, Trends Immunol., 37, 375, 10.1016/j.it.2016.04.001 Liu, 2015, Profiling immune response in zebrafish intestine, skin, spleen and kidney bath-vaccinated with a live attenuated Vibrio anguillarum vaccine, Fish Shellfish Immunol., 45, 342, 10.1016/j.fsi.2015.04.028 Lund, 2007, Specificity and durability of antibody responses in Atlantic cod (Gadus morhua L.) immunised with Vibrio anguillarum O2b, Fish Shellfish Immunol., 23, 906, 10.1016/j.fsi.2007.04.006 Lund, 2008, Atypical furunculosis vaccines for Atlantic cod (Gadus morhua); vaccine efficacy and antibody responses, Vaccine, 26, 6791, 10.1016/j.vaccine.2008.10.012 Maekawa, 2017, Transcriptome analysis of immune response against Vibrio harveyi infection in orange-spotted grouper (Epinephelus coioides), Fish Shellfish Immunol., 70, 628, 10.1016/j.fsi.2017.09.052 Magnadottir, 2009, Natural antibodies of cod (Gadus morhua L.): specificity, activity and affinity, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 154, 309, 10.1016/j.cbpb.2009.07.005 Magor, 2015, Antibody affinity maturation in fishes-our current understanding, Dev. Biol. (Basel), 4, 512 Makesh, 2015, Systemic and mucosal immune response of rainbow trout to immunization with an attenuated Flavobacterium psychrophilum vaccine strain by different routes, Fish Shellfish Immunol., 44, 156, 10.1016/j.fsi.2015.02.003 Malmstrøm, 2013, Unraveling the evolution of the Atlantic cod's (Gadus morhua L.) alternative immune strategy, PLoS One, 8, 10.1371/journal.pone.0074004 Malmstrøm, 2016, Evolution of the immune system influences speciation rates in teleost fishes, Nat. Genet., 48, 1204, 10.1038/ng.3645 Martin, 2012, Cutadapt removes adapter sequences from high-throughput sequencing reads, Bioinform. Act., 17, 10 Mikkelsen, 2013, Response to vaccination of Atlantic cod (Gadus morhua L.) progenies from families with different estimated family breeding values for vibriosis resistance, Fish Shellfish Immunol., 34, 387, 10.1016/j.fsi.2012.10.010 Mikkelsen, 2011, Vibriosis vaccines based on various sero-subgroups of Vibrio anguillarum O2 induce specific protection in Atlantic cod (Gadus morhua L.) juveniles, Fish Shellfish Immunol., 30, 330, 10.1016/j.fsi.2010.11.007 Neefjes, 2011, Towards a systems understanding of MHC class I and MHC class II antigen presentation, Nat. Rev. Immunol., 11, 823, 10.1038/nri3084 Netea, 2016, Trained immunity: a program of innate immune memory in health and disease, Science, 352, aaf1098, 10.1126/science.aaf1098 Nymo, 2016, Experimental challenge of Atlantic cod (Gadus morhua) with a Brucella pinnipedialis strain from hooded seal (Cystophora cristata), PLoS One, 11, 10.1371/journal.pone.0159272 Parra, 2015, Mucosal immunity and B cells in teleosts: effect of vaccination and stress, Front. Immunol., 6, 354, 10.3389/fimmu.2015.00354 Pridgeon, 2012, Global gene expression in channel catfish after vaccination with an attenuated Edwardsiella ictaluri, Fish Shellfish Immunol., 32, 524, 10.1016/j.fsi.2011.12.013 Raeber, 2018, The role of cytokines in T-cell memory in health and disease, Immunol. Rev., 283, 176, 10.1111/imr.12644 R-Core-Team Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Rombout, 2014, Adaptive immune responses at mucosal surfaces of teleost fish, Fish Shellfish Immunol., 40, 634, 10.1016/j.fsi.2014.08.020 Salinas, 2015, The mucosal immune system of teleost fish, Dev. Biol. (Basel), 4, 525 Sarropoulou, 2012, Characterization of European sea bass transcripts by RNA SEQ after oral vaccine against V. anguillarum, Mar. Biotechnol. (N.Y.), 14, 634, 10.1007/s10126-012-9466-z Scapigliati, 2018, Fish lymphocytes: an evolutionary equivalent of mammalian innate-like lymphocytes?, Front. Immunol., vol. 9, 971, 10.3389/fimmu.2018.00971 Schrøder, 2006, Early vaccination and protection of Atlantic cod (Gadus morhua L.) juveniles against classical vibriosis, Aquaculture, 254, 46, 10.1016/j.aquaculture.2005.10.015 Schrøder, 2009, Comparison of antibody responses in Atlantic cod (Gadus morhua L.) to Vibrio anguillarum, Aeromonas salmonicida and Francisella sp, Fish Shellfish Immunol., 27, 112, 10.1016/j.fsi.2008.11.016 Seppola, 2015, Ultrapure LPS induces inflammatory and antibacterial responses attenuated in vitro by exogenous sera in Atlantic cod and Atlantic salmon, Fish Shellfish Immunol., 44, 66, 10.1016/j.fsi.2015.01.018 Seternes, 2007, Specific endocytosis and degradation of naked DNA in the endocardial cells of cod (Gadus morhua L.), J. Exp. Biol., 2091, 10.1242/jeb.003186 Shannon, 2003, Cytoscape: a software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Sheridan, 2013, Gammadelta T cells exhibit multifunctional and protective memory in intestinal tissues, Immunity, 39, 184, 10.1016/j.immuni.2013.06.015 Solbakken, 2016, Evolutionary redesign of the Atlantic cod (Gadus morhua L.) toll-like receptor repertoire by gene losses and expansions, Sci. Rep., 6, 10.1038/srep25211 Solbakken, 2016, Successive losses of central immune genes characterize the Gadiformes' alternate immunity, Genome Biol. Evol., 8, 3508, 10.1093/gbe/evw250 Solbakken, 2017, Linking species habitat and past palaeoclimatic events to evolution of the teleost innate immune system, Proc. Biol. Sci., 284, 10.1098/rspb.2016.2810 Solbakken, 2019, Disentangling the immune response and host-pathogen interactions in Francisella noatunensis infected Atlantic cod, Comp. Biochem. Physiol. Part D Genomics Proteomics, 30, 333, 10.1016/j.cbd.2019.04.004 Star, 2011, The genome sequence of Atlantic cod reveals a unique immune system, Nature, 477, 207, 10.1038/nature10342 Tang, 2018, Recombinant NADP-dependent isocitrate dehydrogenase of Edwardsiella tarda induces both Th1 and Th2 type immune responses and evokes protective efficacy against edwardsiellosis, Vaccine, 36, 2337, 10.1016/j.vaccine.2018.03.022 Tørresen, 2017, An improved genome assembly uncovers prolific tandem repeats in Atlantic cod, BMC Genomics, 18, 95, 10.1186/s12864-016-3448-x Tørresen, 2018, Genomic architecture of haddock (Melanogrammus aeglefinus) shows expansions of innate immune genes and short tandem repeats, BMC Genomics, 19, 240, 10.1186/s12864-018-4616-y Trapani, 2002, Functional significance of the perforin/granzyme cell death pathway, Nat. Rev. Immunol., 2, 735, 10.1038/nri911 Trapnell, 2012, Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks, Nat. Protoc., 7, 562, 10.1038/nprot.2012.016 UniProt, C, 2015, UniProt: a hub for protein information, Nucleic Acids Res., 43, D204 Vestvik, 2013, Francisella noatunensis subsp. noatunensis replicates within Atlantic cod (Gadus morhua L.) leucocytes and inhibits respiratory burst activity, Fish Shellfish Immunol., 35, 725, 10.1016/j.fsi.2013.06.002 Vinuesa, 2013, Innate B cell helpers reveal novel types of antibody responses, Nat. Immunol., 14, 119, 10.1038/ni.2511 Vivier, 2016, The evolution of innate lymphoid cells, Nat. Immunol., 17, 790, 10.1038/ni.3459 Wan, 2016, Characterization of gammadelta T cells from zebrafish provides insights into their important role in adaptive humoral immunity, Front. Immunol., 7, 675 Zehner, 2015, Sec61 in antigen cross-presentation, Oncotarget, 6, 19954, 10.18632/oncotarget.4587 Zhang, 2013, Transcriptome profiling reveals Th17-like immune responses induced in zebrafish bath-vaccinated with a live attenuated Vibrio anguillarum, PLoS One, 8 Zhang, 2017, More than just antibodies: protective mechanisms of a mucosal vaccine against fish pathogen Flavobacterium columnare, Fish Shellfish Immunol., 71, 160, 10.1016/j.fsi.2017.10.001 Zhu, 2013, Advances in research of fish immune-relevant genes: a comparative overview of innate and adaptive immunity in teleosts, Dev. Comp. Immunol., 39, 39, 10.1016/j.dci.2012.04.001