{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T12:31:22Z","timestamp":1781872282088,"version":"3.54.5"},"reference-count":98,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,3,28]],"date-time":"2020-03-28T00:00:00Z","timestamp":1585353600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology, Taiwan","doi-asserted-by":"publisher","award":["MOST 107-2313-B-020-012-MY3."],"award-info":[{"award-number":["MOST 107-2313-B-020-012-MY3."]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Vaccines"],"abstract":"<jats:p>DNA vaccines have been widely employed in controlling viral and bacterial infections in mammals and teleost fish. Co-injection of molecular adjuvants, including chemokines, cytokines, and immune co-stimulatory molecules, is one of the potential strategies used to improve DNA vaccine efficacy. In mammals and teleost fish, interleukin-34 (IL-34) had been described as a multifunctional cytokine and its immunological role had been confirmed; however, the adjuvant capacity of IL-34 remains to be elucidated. In this study, IL-34 was identified in largemouth bass. A recombinant plasmid of IL-34 (pcIL-34) was constructed and co-administered with a DNA vaccine encoding hypoxic response protein 1 (Hrp1; pcHrp1) to evaluate the adjuvant capacity of pcIL-34 against Nocardia seriolae infection. Our results indicated that pcIL-34 co-injected with pcHrp1 not only triggered innate immunity and a specific antibody response, but also enhanced the mRNA expression level of immune-related genes encoding for cytokines, chemokines, and humoral and cell-mediated immunity. Moreover, pcIL-34 enhanced the protection of pcHrp1 against N. seriolae challenge and conferred the relative percent survival of 82.14%. Collectively, IL-34 is a promising adjuvant in a DNA vaccine against nocardiosis in fish.<\/jats:p>","DOI":"10.3390\/vaccines8020151","type":"journal-article","created":{"date-parts":[[2020,3,31]],"date-time":"2020-03-31T10:29:38Z","timestamp":1585650578000},"page":"151","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Interleukin 34 Serves as a Novel Molecular Adjuvant against Nocardia Seriolae Infection in Largemouth Bass (Micropterus Salmoides)"],"prefix":"10.3390","volume":"8","author":[{"given":"Huy Hoa","family":"Hoang","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine, College of Veterinary Medicine, National Pingtung University of Science and Technology, No. 1 Shuefu Road, Neipu, Pingtung 91201, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pei-Chi","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, College of Veterinary Medicine, National Pingtung University of Science and Technology, No. 1 Shuefu Road, Neipu, Pingtung 91201, Taiwan"},{"name":"Southern Taiwan Fish Disease Centre, National Pingtung University of Science and Technology, No. 1 Shuefu Road, Neipu, Pingtung 91201, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2885-9370","authenticated-orcid":false,"given":"Shih-Chu","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine, College of Veterinary Medicine, National Pingtung University of Science and Technology, No. 1 Shuefu Road, Neipu, Pingtung 91201, Taiwan"},{"name":"Southern Taiwan Fish Disease Centre, National Pingtung University of Science and Technology, No. 1 Shuefu Road, Neipu, Pingtung 91201, Taiwan"},{"name":"International Degree Program of Ornamental Fish Science and Technology, International College, National Pingtung University of Science and Technology, No. 1, Shuefu Road, Neipu, Pingtung 91201, Taiwan"},{"name":"Research Centre for Animal Biologics, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,3,28]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"16","DOI":"10.3147\/jsfp.3.16","article-title":"Nocardia infection in cultured yellowtails (Seriola quinqueradiata and S. purpursacens) I. Bacteriological study","volume":"3","author":"Kariya","year":"1968","journal-title":"Fish Pathol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1046\/j.1365-2761.2000.00217.x","article-title":"Nocardiosis in sea bass, Lateolabrax japonicus, in Taiwan","volume":"23","author":"Chen","year":"2000","journal-title":"J. Fish Dis."},{"key":"ref_3","first-page":"61","article-title":"Isolation and characterization of the pathogenic bacterium, Nocardia seriolae, from female broodstock of striped mullet (Mugil cephalus)","volume":"12","author":"Huang","year":"2004","journal-title":"J. Fish. Res."},{"key":"ref_4","unstructured":"Reantaso, M.G.B., Mohan, V., Crumlish, M., and Subasinghe, R.P. (2008). Nocardial infections in fish: An emerging problem in both freshwater and marine aquaculture systems in Asia. Diseases in Asian Aquaculture VI, Fish Health Section, Asian Fisheries Society."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"173","DOI":"10.3354\/dao03023","article-title":"Isolation and genetic characterization of Nocardia seriolae from snubnose pompano Trachinotus blochii in Vietnam","volume":"120","author":"Duong","year":"2016","journal-title":"Dis. Aquat. Org."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.aquaculture.2009.06.017","article-title":"Genotypic and phenotypic analysis of fish pathogen, Nocardia seriolae, isolated in Taiwan","volume":"294","author":"Shimahara","year":"2009","journal-title":"Aquaculture"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5559","DOI":"10.1016\/j.vaccine.2017.08.067","article-title":"DNA vaccines against leptospirosis: A literature review","volume":"35","author":"Silveira","year":"2017","journal-title":"Vaccine"},{"key":"ref_8","first-page":"254","article-title":"DNA Vaccines for Prostate Cancer","volume":"8","author":"McNeel","year":"2012","journal-title":"Curr. Cancer Ther. Rev."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.fsi.2019.03.045","article-title":"Construction and characterization of a DNA vaccine encoding the SagH against Streptococcus iniae","volume":"89","author":"Liu","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.fsi.2018.11.073","article-title":"Intramuscular administration of a DNA vaccine encoding OmpK antigen induces humoral and cellular immune responses in flounder (Paralichthys olivaceus) and improves protection against Vibrio anguillarum","volume":"86","author":"Xu","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"499","DOI":"10.3389\/fimmu.2019.00499","article-title":"A DNA Vaccine Encoding the VAA Gene of Vibrio anguillarum Induces a Protective Immune Response in Flounder","volume":"10","author":"Xing","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"5195","DOI":"10.1016\/j.vaccine.2009.06.071","article-title":"Construction and evaluation of DNA vaccines encoding Edwardsiella tarda antigens","volume":"27","author":"Jiao","year":"2009","journal-title":"Vaccine"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2051","DOI":"10.1016\/j.vaccine.2011.01.013","article-title":"Comparative study of the immune effect of an Edwardsiella tarda antigen in two forms: Subunit vaccine vs DNA vaccine","volume":"29","author":"Sun","year":"2011","journal-title":"Vaccine"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.fsi.2016.10.029","article-title":"Design and evaluation of an Edwardsiella tarda DNA vaccine co-encoding antigenic and adjuvant peptide","volume":"59","author":"Liu","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"165","DOI":"10.3147\/jsfp.49.165","article-title":"Development of DNA vaccines against Nocardia seriolae infection in fish","volume":"49","author":"Kato","year":"2014","journal-title":"Fish Pathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.fsi.2019.10.024","article-title":"Comparison of protective efficacy between two DNA vaccines encoding DnaK and GroEL against fish nocardiosis","volume":"95","author":"Chen","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_17","first-page":"635","article-title":"The road to licensure of a DNA vaccine","volume":"8","author":"Salonius","year":"2007","journal-title":"Curr. Opin. Investig. Drugs"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/jfd.12727","article-title":"DNA vaccines for fish: Review and perspectives on correlates of protection","volume":"41","author":"Dalmo","year":"2018","journal-title":"J. Fish Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1586\/erv.10.57","article-title":"DNA vaccines for targeting bacterial infections","volume":"9","author":"Ingolotti","year":"2010","journal-title":"Expert Rev. Vaccines"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Reynes-Cerpa, S., Maisey, K., Reyes-L\u00f3pez, F., Toro-Ascuy, D., Sandino, A.M., and Imarai, M. (2012). Fish cytokines and immune response. New Adv. Contrib. Fish Biol., 3\u201357.","DOI":"10.5772\/53504"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1016\/j.fsi.2013.02.029","article-title":"Adjuvants and immunostimulants in fish vaccines: Current knowledge and future perspectives","volume":"35","author":"Tafalla","year":"2013","journal-title":"Fish Shellfish Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Guo, M., Tang, X., Sheng, X., Xing, J., and Zhan, W. (2017). The Immune Adjuvant Effects of Flounder (Paralichthys olivaceus) Interleukin-6 on E. tarda Subunit Vaccine OmpV. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18071445"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"83938","DOI":"10.18632\/oncotarget.13728","article-title":"Interleukin-8 holds promise to serve as a molecular adjuvant in DNA vaccination model against Streptococcus iniae infection in fish","volume":"7","author":"Wang","year":"2016","journal-title":"Oncotarget"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"112222","DOI":"10.18632\/oncotarget.23095","article-title":"Effects of different cytokines on immune responses of rainbow trout in a virus DNA vaccination model","volume":"8","author":"Cao","year":"2017","journal-title":"Oncotarget"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1016\/j.fsi.2018.04.009","article-title":"The effects of IL-1\u03b2, IL-8, G-CSF and TNF-\u03b1 as molecular adjuvant on the immune response to an E. tarda subunit vaccine in flounder (Paralichthys olivaceus)","volume":"77","author":"Guo","year":"2018","journal-title":"Fish Shellfish Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1016\/j.fsi.2019.08.052","article-title":"Generation and functional evaluation of a DNA vaccine co-expressing Vibrio anguillarum VAA protein and flounder interleukin-2","volume":"93","author":"Xu","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.fsi.2019.01.007","article-title":"Molecular characterization, phylogenetic analysis and adjuvant effect of channel catfish interleukin-1\u03b2s against Streptococcus iniae","volume":"87","author":"Wang","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/j.fsi.2017.06.025","article-title":"Adjuvant effect of recombinant interleukin-12 in the Nocardiosis formalin-killed vaccine of the amberjack Seriola dumerili","volume":"67","author":"Matsumoto","year":"2017","journal-title":"Fish Shellfish Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"103492","DOI":"10.1016\/j.dci.2019.103492","article-title":"The effects of CCL3, CCL4, CCL19 and CCL21 as molecular adjuvants on the immune response to VAA DNA vaccine in flounder (Paralichthys olivaceus)","volume":"103","author":"Xu","year":"2019","journal-title":"Dev. Comp. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.aquaculture.2017.11.052","article-title":"Bicistronic DNA vaccine against Edwardsiella tarda infection in Labeo rohita: Construction and comparative evaluation of its protective efficacy against monocistronic DNA vaccine","volume":"485","author":"Kumari","year":"2018","journal-title":"Aquaculture"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1835","DOI":"10.7150\/ijbs.35070","article-title":"Immunomodulation of interleukin-34 and its potential significance as a disease Biomarker and Therapeutic target","volume":"15","author":"Ge","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1016\/j.molimm.2012.09.008","article-title":"Identification of IL-34 in teleost fish: Differential expression of rainbow trout IL-34, MCSF1 and MCSF2, ligands of the MCSF receptor","volume":"53","author":"Wang","year":"2013","journal-title":"Mol. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.fsi.2014.12.023","article-title":"Grouper (Epinephelus coioides) IL-34\/MCSF2 and MCSFR1\/MCSFR2 were involved in mononuclear phagocytes activation against Cryptocaryon irritans infection","volume":"67","author":"Mo","year":"2015","journal-title":"Fish Shellfish Immunol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.fsi.2017.12.041","article-title":"Molecular characterization and expression analysis of large yellow croaker (Larimichthys crocea) interleukin-12A, 16 and 34 after poly I:C and Vibrio anguillarum challenge","volume":"74","author":"Wang","year":"2018","journal-title":"Fish Shellfish Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.fsi.2019.05.059","article-title":"Functional characterisation of interleukin 34 in grass carp Ctenopharyngodon idella","volume":"92","author":"Xue","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"93","DOI":"10.3147\/jsfp.38.93","article-title":"A PCR method to detect Nocardia seriolae in fish samples","volume":"38","author":"Miyoshi","year":"2003","journal-title":"Fish Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/S0378-1119(01)00819-8","article-title":"ORF-FINDER: A vector for high-throughput gene identification","volume":"282","author":"Rombel","year":"2002","journal-title":"Gene"},{"key":"ref_38","first-page":"531","article-title":"Protein identification and analysis tools in the ExPASy server","volume":"112","author":"Wilkins","year":"1999","journal-title":"Methods Mol. Biol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1038\/s41587-019-0036-z","article-title":"SignalP 5.0 improves signal peptide predictions using deep neural networks","volume":"37","author":"Tsirigos","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"15975","DOI":"10.1038\/s41598-019-52341-z","article-title":"N-GlyDE: A two-stage N-linked glycosylation site prediction incorporating gapped dipeptides and pattern-based encoding","volume":"9","author":"Pitti","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"W6","DOI":"10.1093\/nar\/gkl164","article-title":"BLAST: Improvements for better sequence analysis","volume":"34","author":"Ye","year":"2006","journal-title":"Nucleic Acids Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"19867","DOI":"10.1016\/S0021-9258(18)54860-2","article-title":"Structural features in eukaryotic mRNAs that modulate the initiation of translation","volume":"266","author":"Kozak","year":"1991","journal-title":"Biol. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Hoang, H.H., Wang, P.C., and Chen, S.C. (2020). The protective efficacy of recombinant hypoxic response protein 1 of Nocardia seriolae in largemouth bass (Micropterus salmoides). Vaccine, in press.","DOI":"10.1016\/j.vaccine.2020.02.062"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.fsi.2017.06.014","article-title":"Identification and expression analysis of two pro-inflammatory cytokines, TNF-alpha and IL-8, in cobia (Rachycentron canadum L.) in response to Streptococcus dysgalactiae infection","volume":"67","author":"Nguyen","year":"2017","journal-title":"Fish Shellfish Immunol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Byadgi, O., Chen, C.W., Wang, P.C., Tsai, M.A., and Chen, S.C. (2016). De Novo Transcriptome Analysis of Differential Functional Gene Expression in Largemouth Bass (Micropterus salmoides) after Challenge with Nocardia seriolae. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17081315"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Panzarin, V., Toffan, A., Abbadi, M., Buratin, A., Mancin, M., Braaen, S., Olsen, C.M., Bargelloni, L., Rimstad, E., and Cattoli, G. (2016). Molecular Basis for Antigenic Diversity of Genus Betanodavirus. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0158814"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1016\/j.fsi.2017.05.021","article-title":"Immunogenicity and efficacy of DNA vaccine encoding antigenic AcfA via addition of the molecular adjuvant Myd88 against Vibrio alginolyticus in Epinephelus coioides","volume":"66","author":"Huang","year":"2017","journal-title":"Fish Shellfish Immunol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1111\/j.1472-765X.2011.03062.x","article-title":"Identification and evaluation of an outer membrane protein OmpU from a pathogenic Vibrio harveyi isolate as vaccine candidate in turbot (Scophthalmus maximus)","volume":"53","author":"Wang","year":"2011","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"5700","DOI":"10.1038\/s41598-017-06143-w","article-title":"Bivalent DNA vaccine induces significant immune responses against infectious hematopoietic necrosis virus and infectious pancreatic necrosis virus in rainbow trout","volume":"7","author":"Xu","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1349","DOI":"10.1111\/jfd.12828","article-title":"Enhanced immune responses and effectiveness of refined outer membrane protein vaccines against Vibrio harveyi in orange-spotted grouper (Epinephelus coioides)","volume":"41","author":"Nguyen","year":"2018","journal-title":"J. Fish Dis."},{"key":"ref_51","first-page":"101","article-title":"Lysozyme Assays","volume":"1","author":"Ellis","year":"1990","journal-title":"InTech. Fish Immunol."},{"key":"ref_52","first-page":"140","article-title":"High contaminant loads in Lake Apopka\u2019s riparian wetland disrupt gene networks involved in reproduction and immune function in largemouth bass","volume":"19","author":"Martyniuk","year":"2016","journal-title":"Comp. Biochem. Physiol. D Genom. Proteom."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1002\/JLB.MR1117-457R","article-title":"Interleukin-34, a comprehensive review","volume":"104","author":"Baghdadi","year":"2018","journal-title":"J. Leukoc. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/j.bbapap.2012.04.012","article-title":"The mechanism of shared but distinct CSF-1R signaling by the non-homologous cytokines IL-34 and CSF-1","volume":"1824","author":"Liu","year":"2012","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/1297-9716-45-21","article-title":"Strategies and hurdles using DNA vaccines to fish","volume":"45","author":"Myhr","year":"2014","journal-title":"Vet. Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1128\/IAI.01137-06","article-title":"Immunogenicity of eight dormancy regulon-encoded proteins of Mycobacterium tuberculosis in DNA-vaccinated and tuberculosis-infected mice","volume":"75","author":"Roupie","year":"2007","journal-title":"Infect. Immun."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1111\/j.1365-2567.2009.03196.x","article-title":"Mycobacterium tuberculosis conserved hypothetical protein rRv2626c modulates macrophage effector functions","volume":"130","author":"Bashir","year":"2010","journal-title":"Immunology"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.cimid.2018.11.016","article-title":"Rv2626c and Rv2032 activate TH1 response and downregulate regulatory T cells in peripheral blood mononuclear cells of tuberculosis patients","volume":"62","author":"Singh","year":"2019","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.fsi.2011.11.003","article-title":"A sequential study of incomplete Freund\u2019s adjuvant-induced peritonitis in Atlantic cod","volume":"32","author":"Gjessing","year":"2012","journal-title":"Fish Shellfish Immunol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.molimm.2017.05.026","article-title":"Analysis of adipose tissue immune gene expression after vaccination of rainbow trout with adjuvanted bacterins reveals an association with side effects","volume":"88","author":"Veenstra","year":"2017","journal-title":"Mol. Immunol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.fsi.2018.09.024","article-title":"Efficacy of MontanideTM ISA 763 A VG as aquatic adjuvant administrated with an inactivated Vibrio harveyi vaccine in turbot (Scophthalmus maximus L.)","volume":"84","author":"Xu","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.fsi.2020.01.031","article-title":"A CpG-riched plasmids as vaccine adjuvant reduce antigen dose of an inactivated Vibrio anguillarum vaccine in turbot (Scophthalamus maximus L.)","volume":"98","author":"Sun","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2484","DOI":"10.4049\/jimmunol.175.4.2484","article-title":"Identification and bioactivities of IFN-\u03b3 in rainbow trout Oncorhynchus mykiss: The first Th1-type cytokine characterized functionally in fish","volume":"175","author":"Zou","year":"2005","journal-title":"J. Immunol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fsi.2008.03.007","article-title":"What happens to the DNA vaccine in fish? A review of current knowledge","volume":"25","author":"Tonheim","year":"2008","journal-title":"Fish Shellfish Immunol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.fsi.2019.12.014","article-title":"Development of DNA vaccines encoding ribosomal proteins (RplL and RpsA) against Nocardia seriolae infection in fish","volume":"96","author":"Chen","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1303","DOI":"10.1016\/j.fsi.2012.10.004","article-title":"Construction and comparative study of monovalent and multivalent DNA vaccines against Streptococcus iniae","volume":"33","author":"Sun","year":"2012","journal-title":"Fish Shellfish Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1568","DOI":"10.3389\/fimmu.2018.01568","article-title":"A Review of DNA Vaccines Against Influenza","volume":"9","author":"Lee","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Ragland, S.A., and Criss, A.K. (2017). From bacterial killing to immune modulation: Recent insights to the function of lysozyme. PLoS Pathog., 21.","DOI":"10.1371\/journal.ppat.1006512"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Brott, A.S., and Clarke, A.J. (2019). Peptidoglycan O-Acetylation as a Virulence Factor: Its Effect on Lysozyme in the Innate Immune System. Antibiotics (Basel), 8.","DOI":"10.3390\/antibiotics8030094"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1111\/j.1365-2109.2007.01883.x","article-title":"Lysozyme: An important defence molecule of fish innate immune system","volume":"39","author":"Saurabh","year":"2008","journal-title":"Aquac. Res."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"2337","DOI":"10.1016\/j.vaccine.2018.03.022","article-title":"Recombinant NADP-dependent isocitrate dehydrogenase of Edwardsiella tarda induces both Th1 and Th2 type immune responses and evokes protective efficacy against edwardsiellosis","volume":"36","author":"Tang","year":"2018","journal-title":"Vaccine"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Prados-Rosales, R., Carre\u00f1o, L., Cheng, T., Blanc, C., Weinrick, B., Malek, A., Lowary, T., Baena, A., Joe, M., and Bai, Y. (2017). Enhanced control of Mycobacterium tuberculosis extrapulmonary dissermination in mice by an arabinomannan-protein conjugate vaccine. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006250"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"3206","DOI":"10.1128\/IAI.01847-14","article-title":"Burkholderia pseudomallei capsular polysaccharide conjugates provide protection against acute melioidosis","volume":"82","author":"Scott","year":"2014","journal-title":"Infect. Immun."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"5548","DOI":"10.4049\/jimmunol.180.8.5548","article-title":"Utilization of Fc receptors as a mucosal vaccine strategy against an intracellular bacterium, Francisella tularensis","volume":"180","author":"Rawool","year":"2008","journal-title":"J. Immunol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1016\/j.vaccine.2014.01.044","article-title":"A recombinant bivalent fusion protein rVE confers active and passive protection against Yersinia enterocolitica infection in mice","volume":"32","author":"Singh","year":"2014","journal-title":"Vaccine"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/S1074-7613(00)80165-X","article-title":"Chemokines: A new classification system and their role in immunity","volume":"12","author":"Zlotnik","year":"2000","journal-title":"Immunity"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1111\/j.1574-6968.2002.tb11038.x","article-title":"Current status of immune mechanism of killing of intracellular microorganisms","volume":"207","author":"Ismail","year":"2002","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"276","DOI":"10.3389\/fimmu.2012.00276","article-title":"Antimicrobial chemokines","volume":"3","author":"Yung","year":"2012","journal-title":"Front. Immunol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1097\/SHK.0b013e31827802b5","article-title":"Bacterial clearance in septic mice is modulated by MCP-1\/CCL2 and nitric oxide","volume":"39","author":"Gomes","year":"2013","journal-title":"Shock"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"6514","DOI":"10.1128\/IAI.73.10.6514-6522.2005","article-title":"The chemokine CCL2 is required for control of murine gastric Salmonella enterica infection","volume":"73","author":"Depaolo","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.jri.2008.08.003","article-title":"Constitutive expression of the antibacterial CXC chemokine GCP-2\/CXCL6 by epithelial cells of male reproductive tract","volume":"79","author":"Collin","year":"2008","journal-title":"J. Reprod. Immunol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"12958","DOI":"10.3390\/ijms160612958","article-title":"Chemokine-derived peptides: Novel antimicrobial and antineoplastic agents","volume":"16","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"S\u00f6birk, S.K., M\u00f6rgelin, M., Egesten, A., Bates, P., Shannon, O., and Collin, M. (2013). Human chemokines as antimicrobial peptides with direct parasiticidal effect on Leishmania mexicana in vitro. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0058129"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1017\/S0031182013001984","article-title":"The role of chemokines in severe malaria: More than meets the eye","volume":"141","author":"Ioannidis","year":"2014","journal-title":"Parasitology"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Domingo-Gonzalez, R., Prince, O., Cooper, A., and Khader, S.A. (2016). Cytokines and Chemokines in Mycobacterium tuberculosis Infection. Microbiol. Spectr., 4.","DOI":"10.1128\/microbiolspec.TBTB2-0018-2016"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1111\/imm.12660","article-title":"Functions of interleukin-34 and its emerging association with rheumatoid arthritis","volume":"149","author":"Zhou","year":"2016","journal-title":"Immunology"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Truong, A.D., Hong, Y., Lee, J., Lee, K., Kil, D.Y., Lillehoj, H.S., and Hong, Y.H. (2018). Interleukin-34 Regulates Th1 and Th17 Cytokine Production by Activating Multiple Signaling Pathways through CSF-1R in Chicken Cell Lines. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19061665"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"e584","DOI":"10.1097\/CCM.0000000000003017","article-title":"Interleukin-34 ameliorates survival and bacterial clearance in polymicrobial sepsis","volume":"46","author":"Lin","year":"2018","journal-title":"Crit. Care Med."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"11","DOI":"10.3354\/dao060011","article-title":"Protection of atlantic salmon Salmo salar against infectious pancreatic necrosis after DNA vaccination","volume":"60","author":"Mikalsen","year":"2004","journal-title":"Dis. Aquat. Organ."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"4927","DOI":"10.1016\/j.vaccine.2006.03.062","article-title":"DNA Vaccination Can Protect Cyprinus Carpio Against Spring Viraemia of Carp Virus","volume":"24","author":"Kanellos","year":"2006","journal-title":"Vaccine"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.fsi.2005.10.012","article-title":"Genetic Vaccines Protect Red Seabream, Pagrus Major, Upon Challenge With Red Seabream Iridovirus (RSIV)","volume":"21","author":"Caipang","year":"2006","journal-title":"Fish Shellfish Immunol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"33","DOI":"10.3354\/dao073033","article-title":"Immune and histopathologic responses of DNA-vaccinated hybrid striped bass Morone Saxatilis X M. Chrysops after acute Mycobacterium marinum infection","volume":"73","author":"Pasnik","year":"2006","journal-title":"Dis. Aquat. Organ."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.fsi.2019.09.038","article-title":"Identification of common antigens of three pathogenic Nocardia species and development of DNA vaccine against fish nocardiosis","volume":"95","author":"Chen","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.fsi.2018.03.060","article-title":"Correlates of protective immunity of fish vaccines","volume":"85","author":"Evensen","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/j.fsi.2012.11.051","article-title":"Expression and immunogenicity analysis of accessory colonization factor A from Vibrio alginolyticus strain HY9901","volume":"43","author":"Cai","year":"2013","journal-title":"Fish Shellfish Immunol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.micpath.2017.03.027","article-title":"Protective efficacy of six immunogenic recombinant proteins of Vibrio anguillarum and evaluation them as vaccine candidate for flounder (Paralichthys olivaceus)","volume":"107","author":"Xing","year":"2017","journal-title":"Microb. Pathog."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"3196","DOI":"10.1016\/j.vaccine.2017.04.071","article-title":"Identification of immunogenic proteins and evaluation of four recombinant proteins as potential vaccine antigens from Vibrio anguillarum in flounder (Paralichthys olivaceus)","volume":"35","author":"Xing","year":"2017","journal-title":"Vaccine"}],"container-title":["Vaccines"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-393X\/8\/2\/151\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:12:58Z","timestamp":1760173978000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-393X\/8\/2\/151"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,28]]},"references-count":98,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["vaccines8020151"],"URL":"https:\/\/doi.org\/10.3390\/vaccines8020151","relation":{},"ISSN":["2076-393X"],"issn-type":[{"value":"2076-393X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,28]]}}}