{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,12]],"date-time":"2026-07-12T05:04:50Z","timestamp":1783832690817,"version":"3.55.0"},"reference-count":104,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2022,3,13]],"date-time":"2022-03-13T00:00:00Z","timestamp":1647129600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Mar2020 Operational Programme and the European Union through FEDER and by Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia (FCT)","award":["UID\/MAR\/04292\/2020; UIDB\/04423\/2020; UIDP\/04423\/2020; 2020.00290.CEECIND"],"award-info":[{"award-number":["UID\/MAR\/04292\/2020; UIDB\/04423\/2020; UIDP\/04423\/2020; 2020.00290.CEECIND"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Currently, aquaculture production of rainbow trout (Oncorhynchus mykiss) is a multibillion dollar industry; nevertheless, the development of this sector has not been exempt from pitfalls related to the recurrent presence of pathogens of bacterial origin. This is the case of Yersinia ruckeri, the etiologic agent of the infectious pathology known as Enteric Red Mouth Disease (ERM), causing serious economic losses that can be as high as 30\u201370% of production. Although several studies have been performed regarding pathogen features and virulence factors, more information is needed about the host defense mechanism activation after infection. Given this perspective, this study aimed to evaluate rainbow trout\u2019s short-term innate immune response against infection with Y. ruckeri. A series of factors linked to the innate immune response were evaluated, including determination of hematological parameters, oxidative stress biomarkers, and analysis of the expression of immune-related genes. Results showed a significant decrease in several hematological parameters (white blood cell count, hematocrit, neutrophils, monocytes, lymphocytes, and thrombocytes) and oxidative stress indicators (SOD) between the control and infected groups. In addition, there were significant differences in the level of gene expression between infected individuals and the control group. Most of these genes (il-1\u03b2, il-8, il-10, tnf-\u03b11, tnf-\u03b12, socs3, mmp-9, cath, hsp-70, saa, fer, pcb) were upregulated within the first 24 h following infection. Results from this study showed more insights into the short-term immune response of rainbow trout to infection with Y. ruckeri, which may be useful for the establishment of biomarkers that may be used for the early detection of ERM.<\/jats:p>","DOI":"10.3390\/ijms23063096","type":"journal-article","created":{"date-parts":[[2022,3,13]],"date-time":"2022-03-13T22:29:43Z","timestamp":1647210583000},"page":"3096","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Functional and Molecular Immune Response of Rainbow Trout (Oncorhynchus mykiss) Following Challenge with Yersinia ruckeri"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9403-2211","authenticated-orcid":false,"given":"Carlos","family":"Fajardo","sequence":"first","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"},{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Polytechnic Institute of Leiria, 2520-620 Peniche, Portugal"},{"name":"Department of Biology, Faculty of Marine and Environmental Sciences, Instituto Universitario de Investigaci\u00f3n Marina (INMAR), Campus de Excelencia Internacional del Mar (CEI\u00b7MAR), University of Cadiz (UCA), 11510 Puerto Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0812-4529","authenticated-orcid":false,"given":"Paulo","family":"Santos","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"},{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Polytechnic Institute of Leiria, 2520-620 Peniche, Portugal"},{"name":"Department of Aquatic Production, School of Biomedicine and Biomedical Sciences, Abel Salazar Institute of Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ricardo","family":"Passos","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Polytechnic Institute of Leiria, 2520-620 Peniche, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariana","family":"Vaz","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Polytechnic Institute of Leiria, 2520-620 Peniche, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2486-595X","authenticated-orcid":false,"given":"Rita","family":"Azeredo","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7718-5021","authenticated-orcid":false,"given":"Marina","family":"Machado","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sergio","family":"Fern\u00e1ndez-Boo","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1168-7461","authenticated-orcid":false,"given":"Teresa","family":"Baptista","sequence":"additional","affiliation":[{"name":"MARE\u2014Marine and Environmental Sciences Centre, ESTM, Polytechnic Institute of Leiria, 2520-620 Peniche, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3758-0849","authenticated-orcid":false,"given":"Benjamin","family":"Costas","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, 4450-208 Porto, Portugal"},{"name":"Department of Aquatic Production, School of Biomedicine and Biomedical Sciences, Abel Salazar Institute of Biomedical Sciences (ICBAS), University of Porto, 4050-313 Porto, Portugal"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,3,13]]},"reference":[{"key":"ref_1","unstructured":"(2020). The State of World Fisheries and Aquaculture (SOFIA), FAO."},{"key":"ref_2","unstructured":"INE (Instituto Nacional de Estat\u00edstica) (2021). Estat\u00edsticas da Pesca: 2020, INE. Available online: https:\/\/www.ine.pt\/xurl\/pub\/280980980."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1111\/j.1365-2761.1989.tb00324.x","article-title":"Morphological and biochemical differences among isolates of Yersinia ruckeri obtained from wide geographical areas","volume":"12","author":"Davies","year":"1989","journal-title":"J. Fish Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1111\/j.1365-2761.2006.00723.x","article-title":"First description of non-motile Yersinia ruckeri serovar I strains causing disease in rainbow trout, Oncorhynchus mykiss (Walbaum), cultured in Spain","volume":"29","author":"Fouz","year":"2006","journal-title":"J. Fish Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"763","DOI":"10.1139\/m66-103","article-title":"Description of a bacterium associated with redmouth disease of rainbow trout (Salmo gairdneri)","volume":"12","author":"Ross","year":"1966","journal-title":"Can. J. Microbiol."},{"key":"ref_6","unstructured":"Inglis, V., Roberts, R.J., and Bromage, N.R. (1993). Isolation and Identification of Fish Bacterial Pathogens. Bacterial Diseases of Fish, Blackwell Science Ltd."},{"key":"ref_7","first-page":"1","article-title":"Utilizaci\u00f3n de la PCR para el diagn\u00f3stico en ictiopatolog\u00eda","volume":"15","author":"Gibello","year":"2001","journal-title":"Rev. AquaTiC"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"349","DOI":"10.15381\/rpb.v18i3.451","article-title":"Rapid diagnosis and identification by PCR of Yersinia ruckeri isolated of Oncorhynchus mykiss from Canta, Lima, Peru","volume":"18","year":"2011","journal-title":"Rev. Peru Biol."},{"key":"ref_9","first-page":"825","article-title":"Redmouth disease of rainbow trout (Salmo gairdneri)","volume":"65","author":"Rucker","year":"1966","journal-title":"Bull. Off. Int. Epizoot."},{"key":"ref_10","first-page":"190","article-title":"First outbreak of enteric redmouth of rainbow trout Oncorhynchus mykiss cultured in Venezuela","volume":"12","author":"Alvarez","year":"1992","journal-title":"Bull. Eur. Ass. Fish Pathol."},{"key":"ref_11","first-page":"3","article-title":"Disease reported in pen reared salmonids from Chile","volume":"21","author":"Bravo","year":"1993","journal-title":"AFS\/FHS Newsl."},{"key":"ref_12","first-page":"104","article-title":"First isolation of Yersinia ruckeri from rainbow trout (Oncorhynchus mykiss) in Peru","volume":"24","author":"Bravo","year":"2004","journal-title":"Bull. Eur. Ass. Fish Pathol."},{"key":"ref_13","first-page":"28","article-title":"Patolog\u00eda e identificaci\u00f3n de Yersinia ruckeri en trucha arco iris (Oncorhynchus mykiss) en piscigranjas de Jun\u00edn, Per\u00fa","volume":"38","author":"Sierralta","year":"2013","journal-title":"Rev. AquaTIC"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1111\/j.1365-2761.1983.tb00091.x","article-title":"Outbreak of enteric redmouth disease in rainbow trout. Salmo gairdneri Richardson, in France","volume":"6","author":"Lesel","year":"1983","journal-title":"J. Fish Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1111\/j.1365-2761.1983.tb00080.x","article-title":"An outbreak of enteric redmouth disease in West Germany","volume":"6","author":"Fuhrmann","year":"1983","journal-title":"J. Fish Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1111\/j.1365-2761.1996.tb00123.x","article-title":"Health status of salmonid aquaculture in North Portugal. First detection of IPN virus","volume":"19","author":"Sousa","year":"1996","journal-title":"J. Fish Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1078\/072320203322337416","article-title":"Recovery of a new biogroup of Yersinia ruckeri from diseased rainbow trout (Oncorhynchus mykiss, Walbaum)","volume":"26","author":"Austin","year":"2003","journal-title":"Syst. Appl. Microbiol."},{"key":"ref_18","first-page":"182","article-title":"An outbreak of enteric redmouth disease in farmed rainbow trout (Oncorynchus mykiss) in Turkey","volume":"11","author":"Timur","year":"1991","journal-title":"Bull Eur. Ass. Fish Pathol."},{"key":"ref_19","first-page":"173","article-title":"First report of yersiniosis-like infection in farmed rainbow trout","volume":"23","author":"Soltani","year":"1999","journal-title":"Bull. Eur. Assoc. Fish Pathol."},{"key":"ref_20","unstructured":"Raidal, S., Cross, G., Fenwick, S., Nicholls, P., Nowak, B., Ellard, K., and Stephens, E. (2004). Aquatic Animal Health: Exotic Disease Training Manual, Fisheries Research and Development Corp. and Murdoch University."},{"key":"ref_21","first-page":"5","article-title":"Isolation of Yersinia ruckeri from rainbow trout in South Africa","volume":"6","author":"Bragg","year":"1986","journal-title":"Bull. Eur. Assoc. Fish Pathol."},{"key":"ref_22","first-page":"96","article-title":"Early records of North American and Australian outbreaks of enteric redmouth disease","volume":"6","author":"Bullock","year":"1977","journal-title":"Fish Health News"},{"key":"ref_23","first-page":"455","article-title":"Enteric Redmouth Disease (Yersinia ruckeri)","volume":"Volume 3","author":"Woo","year":"1999","journal-title":"Fish Diseases and Disorders. Viral, Bacterial and Fungal Infections"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.fsi.2008.07.008","article-title":"Development of adaptive immunity in rainbow trout, Oncorhynchus mykiss (Walbaum) surviving an infection with Yersinia ruckeri","volume":"25","author":"Raida","year":"2008","journal-title":"Fish Shellfish Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"219","DOI":"10.3354\/dao02057","article-title":"Route of entry and tissue distribution of Yersinia ruckeri in experimentally infected rainbow trout Oncorhynchus mykiss","volume":"84","author":"Tobback","year":"2009","journal-title":"Dis. Aquat. Org."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.fsi.2019.05.031","article-title":"Dietary effects of Coriandrum sativum extract on growth performance, physiological and innate immune responses and resistance of rainbow trout (Oncorhynchus mykiss) against Yersinia ruckeri","volume":"91","author":"Farsani","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/j.1365-2761.2007.00816.x","article-title":"Yersinia ruckeri infections in salmonid fish","volume":"30","author":"Tobback","year":"2007","journal-title":"J. Fish Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/0959-8030(93)90031-6","article-title":"Yersinia ruckeri, the causal agent of enteric redmouth disease (ERM) in fish","volume":"3","author":"Furones","year":"1993","journal-title":"Annu. Rev. Fish Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/j.1365-2761.1985.tb00960.x","article-title":"Atypical infection of rainbow trout, (Salmo gairdneri, Richardson), with Yersinia ruckeri","volume":"8","author":"Frerichs","year":"1985","journal-title":"J. Fish Dis."},{"key":"ref_30","unstructured":"Inglis, V., Roberts, R.J., and Bromage, N.J. (1993). Enteric Redmouth (ERM) and Other Enterobacterial Infections of Fish. Bacterial Diseases of Fish, Blackwell Scientific."},{"key":"ref_31","unstructured":"Carson, J., and Wilson, T. (2009). Australia and New Zealand Standard Diagnostic Procedure Manual, Ablis."},{"key":"ref_32","first-page":"1321","article-title":"Pathological findings in rainbow trout (Oncorhynchus mykiss, Walbaum 1792) experimentally infected with Yersinia ruckeri","volume":"29","author":"Avci","year":"2005","journal-title":"Turk. J. Vet. Anim. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1111\/j.1365-2761.1983.tb00111.x","article-title":"A report of an epizootic in hatchery reared rainbow trout, Salmo gairdneri Richardson, at an English trout farm, caused by Yersinia ruckeri","volume":"6","author":"Roberts","year":"1983","journal-title":"J. Fish Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1023\/A:1015382625446","article-title":"The effect of antibiotic treatment on the establishment of persistent infection with Yersinia ruckeri Serovar II in rainbow trout Oncorhynchus mykiss (Walbaum)","volume":"9","author":"Rigos","year":"2001","journal-title":"Aquac. Int."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2429","DOI":"10.1139\/f75-279","article-title":"Establishment of an asymptomatic carrier state infection of enteric redmouth disease in rainbow trout (Salmo gairdneri)","volume":"32","author":"Busch","year":"1975","journal-title":"J. Fish Res. Board Can."},{"key":"ref_36","unstructured":"Busch, R.A. (1982). Enteric Redmouth Disease. Symposium Internatinal de Talloires. Les Antigenes des Microorganismes Pathogens des Poissons, Collection Fondation Marcel Merieux."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/j.1365-2761.1992.tb00650.x","article-title":"Occurrence and pathogenicity of Yersinia ruckeri at fish farms in northern and central Finland","volume":"15","author":"Valtonen","year":"1992","journal-title":"J. Fish Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1111\/1758-2229.12030","article-title":"In vivo monitoring of Yersinia ruckeri in fish tissues: Progression and virulence gene expression","volume":"5","author":"Mendez","year":"2013","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"624","DOI":"10.1016\/j.fsi.2014.08.021","article-title":"Diet type dictates the gut microbiota and the immune response against Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss)","volume":"40","author":"Ingerslev","year":"2014","journal-title":"Fish Shellfish Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/j.micpath.2013.03.001","article-title":"Tissue specific uptake of inactivated and live Yersinia ruckeri in rainbow trout (Oncorhynchus mykiss): Visualization by immunohistochemistry and in situ hybridization","volume":"59\u201360","author":"Khimmakthong","year":"2013","journal-title":"Microb. Pathog."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Beck, B.H., and Peatman, E. (2015). Fish Mucosal Immunity: Gill. Mucosal Health in Aquaculture, Academic Press.","DOI":"10.1016\/B978-0-12-417186-2.00013-3"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1006\/fsim.1998.0192","article-title":"Immunity to bacteria in fish","volume":"9","author":"Ellis","year":"1999","journal-title":"Fish Shellfish Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1111\/jfd.12047","article-title":"Gut microbiota changes in rainbow trout, Oncorhynchus mykiss (Walbaum), during organic acid feed supplementation and Yersinia ruckeri infection","volume":"36","author":"Jaafar","year":"2013","journal-title":"J. Fish Dis."},{"key":"ref_44","first-page":"117","article-title":"Immunization with Bacterial Antigens: Yersiniosis","volume":"Volume 90","author":"Gudding","year":"1997","journal-title":"Fish Vaccinology. Developments in Biological Standardization"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/s10695-014-0014-9","article-title":"Growth performance and antioxidant enzyme activities in rainbow trout (Oncorhynchus mykiss) juveniles fed diets supplemented with sage, mint and thyme oils","volume":"41","author":"Bilen","year":"2015","journal-title":"Fish Physiol. Biochem."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1007\/s10695-007-9146-5","article-title":"Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+","volume":"34","author":"Ates","year":"2008","journal-title":"Fish Physiol. Biochem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1126","DOI":"10.1089\/ars.2012.5149","article-title":"Reactive oxygen species in inflammation and tissue injury","volume":"20","author":"Mittal","year":"2014","journal-title":"Antioxid. Redox Signal."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Liu, T., Wei, W.Y., Wang, K.Y., Wang, E.L., and Yang, Q. (2019). A Yersinia ruckeri TIR domain-containing protein (STIR-2) mediates immune evasion by targeting the MyD88 adaptor. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20184409"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1006\/fsim.1998.0181","article-title":"The morphology of the immune system in teleost fishes","volume":"9","author":"Press","year":"1999","journal-title":"Fish Shellfish Immunol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"48588","DOI":"10.1074\/jbc.M407634200","article-title":"Sensing bacterial flagellin by membrane and soluble orthologs of Toll-like receptor 5 in rainbow trout (Oncorhynchus mykiss)","volume":"279","author":"Tsujita","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.fsi.2016.06.049","article-title":"Molecular and functional characterization of Toll-like receptor (Tlr)1 and Tlr2 in common carp (Cyprinus carpio)","volume":"56","author":"Fink","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.dci.2015.08.012","article-title":"Structurally diverse genes encode Tlr2 in rainbow trout: The conserved receptor cannot be stimulated by classical ligands to activate NF-kB in vitro","volume":"54","author":"Brietzke","year":"2016","journal-title":"Dev. Comp. Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1146\/annurev.immunol.21.120601.141126","article-title":"Toll-like receptors","volume":"21","author":"Takeda","year":"2003","journal-title":"Annu. Rev. Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1016\/S0145-305X(03)00056-9","article-title":"The effect of intraperitoneally administered recombinant IL-1 beta on immune parameters and resistance to Aeromonas salmonicida in the rainbow trout (Oncorhynchus mykiss)","volume":"27","author":"Hong","year":"2003","journal-title":"Dev. Comp. Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Martin, S., Zou, J., Houlihan, D., and Secombes, C. (2007). Directional responses following recombinant cytokine stimulation of rainbow trout (Oncorhynchus mykiss) RTS-11 macrophage cells as revealed by transcriptome profiling. BMC Genom., 8.","DOI":"10.1186\/1471-2164-8-150"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2018","DOI":"10.4049\/jimmunol.175.3.2018","article-title":"IL-1 receptor antagonist-mediated therapeutic effect in murine myasthenia gravis is associated with suppressed serum proinflammatory cytokines, C3, and antiacetylcholine receptor IgG1","volume":"175","author":"Yang","year":"2005","journal-title":"J. Immunol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1016\/j.dci.2006.06.010","article-title":"Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: Inflammatory responses to injury mimicking infection with ectoparasites","volume":"31","author":"Gonzalez","year":"2007","journal-title":"Dev. Comp. Immunol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/j.dci.2004.12.001","article-title":"Expression of genes related to the early immune response in rainbow trout (Oncorhynchus mykiss) after viral haemorrhagic septicemia virus (VHSV) infection","volume":"29","author":"Tafalla","year":"2005","journal-title":"Dev. Comp. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"41","DOI":"10.3354\/dao01808","article-title":"Temperature-dependent expression of immunerelevant genes in rainbow trout following Yersinia ruckeri vaccination","volume":"77","author":"Raida","year":"2007","journal-title":"Dis. Aqua Org."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1016\/S0145-305X(03)00077-6","article-title":"Functional characterisation of the recombinant tumor necrosis factors in rainbow trout, Oncorhynchus mykiss","volume":"27","author":"Zou","year":"2003","journal-title":"Dev. Comp. Immunol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1046\/j.1432-1327.2001.01996.x","article-title":"Cloning and expression analysis of rainbow trout Oncorhynchus mykiss tumor necrosis factor-alpha","volume":"268","author":"Laing","year":"2001","journal-title":"Eur. J. Biochem."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/S0145-305X(01)00058-1","article-title":"Differential expression of two tumor necrosis factor genes in rainbow trout, Oncorhynchus mykiss","volume":"26","author":"Zou","year":"2002","journal-title":"Dev. Comp. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1165\/ajrcmb.26.4.4681","article-title":"Tumor necrosis factor-alpha-induced secretion of RANTES and interleukin-6 from human airway smooth muscle cells\u2013modulation by glucocorticoids and beta agonists","volume":"26","author":"Ammit","year":"2002","journal-title":"Am. J. Respir. Cell Mol. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1006\/fsim.2001.0399","article-title":"Molecular cloning and genomic structure of an interleukin-8 receptor-like gene from homozygous clones of rainbow trout (Oncorhynchus mykiss)","volume":"13","author":"Zhang","year":"2002","journal-title":"Fish Shellfish Immunol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"5615","DOI":"10.1016\/j.vaccine.2006.04.061","article-title":"Co-injection of interleukin 8 with the glycoprotein gene from viral haemorrhagic septicemia virus (VHSV) modulates the cytokine response in rainbow trout (Oncorhynchus mykiss)","volume":"24","author":"Jimenez","year":"2006","journal-title":"Vaccine"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1007\/s00251-006-0084-7","article-title":"Identification of novel rainbow trout (Oncorhynchus mykiss) chemokines, CXCd1 and CXCd2: mRNA expression after Yersinia ruckeri vaccination and challenge","volume":"58","author":"Wiens","year":"2006","journal-title":"Immunogenetics"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1016\/j.fsi.2004.08.004","article-title":"Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs","volume":"18","author":"Inoue","year":"2005","journal-title":"Fish Shellfish Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1449","DOI":"10.1016\/j.molimm.2007.08.016","article-title":"Rainbow trout suppressor of cytokine signalling (SOCS)-1, 2 and 3: Molecular identification, expression and modulation","volume":"45","author":"Wang","year":"2008","journal-title":"Mol. Immunol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"146","DOI":"10.1016\/j.molimm.2015.09.026","article-title":"Polarization of immune responses in fish: The \u2032macrophages first\u2019 point of view","volume":"69","author":"Wiegertjes","year":"2016","journal-title":"Mol. Immunol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Marro, J., Pfefferli, C., de Preux, C.A.S., Bise, T., and Ja\u017awi\u0144ska, A. (2016). Collagen XII contributes to epicardial and connective tissues in the zebrafish heart during ontogenesis and regeneration. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0165497"},{"key":"ref_71","first-page":"2645","article-title":"Transforming growth factor beta-1 (TGF-beta1) stimulates collagen synthesis in cultured rainbow trout cardiac fibroblasts","volume":"220","author":"Johnston","year":"2017","journal-title":"J. Exp. Biol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"jeb189167","DOI":"10.1242\/jeb.189167","article-title":"Transforming growth factor-\u03b21 induces differentiation of rainbow trout (Oncorhynchus mykiss) cardiac fibroblasts into myofibroblasts","volume":"221","author":"Johnston","year":"2018","journal-title":"J. Exp. Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1038\/80819","article-title":"Uncoupling of inflammatory chemokine receptors by IL-10: Generation of functional decoys","volume":"1","author":"Frascaroli","year":"2000","journal-title":"Nat. Immunol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1814","DOI":"10.4049\/jimmunol.164.4.1814","article-title":"Cloning and characterization of IL-10-related T cell-derived inducible factor (IL-TIF), a novel cytokine structurally related to IL-10 and inducible by IL-9","volume":"164","author":"Dumoutier","year":"2000","journal-title":"J. Immunol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1111\/j.1365-2567.2008.02874.x","article-title":"Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation","volume":"125","author":"Chadzinska","year":"2008","journal-title":"Immunology"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"L1006","DOI":"10.1152\/ajplung.00015.2014","article-title":"Matrix metalloproteinase-9 activates TGF-\u03b2 and stimulates fibroblast contraction of collagen gels","volume":"306","author":"Kobayashi","year":"2014","journal-title":"Am. J. Physiol. Lung Cell. Mol. Physiol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/0014-5793(89)81093-2","article-title":"Primary structure of a new cysteine proteinase inhibitor from pig leucocytes","volume":"255","author":"Ritonja","year":"1989","journal-title":"FEBS Lett."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1128\/AAC.50.1.185-195.2006","article-title":"Two cathelicidin genes are present in both rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar)","volume":"50","author":"Chang","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"5053","DOI":"10.1128\/IAI.73.8.5053-5064.2005","article-title":"Identification of a novel cathelicidin gene in rainbow trout Oncorhynchus mykiss","volume":"73","author":"Chang","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S0145-305X(00)00057-4","article-title":"Immune-relevant (including acute phase) genes identified in the livers of rainbow trout, Oncorhynchus mykiss, by suppression subtractive hybridization","volume":"25","author":"Bayne","year":"2001","journal-title":"Dev. Comp. Immunol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1016\/S0145-305X(00)00022-7","article-title":"Serum amyloid A transcription in Atlantic salmon (Salmo salar L.) hepatocytes is enhanced by stimulation with macrophage factors, recombinant human IL-1 beta, IL-6 and TNF alpha or bacterial lipopolysaccharide","volume":"24","author":"Jorgensen","year":"2000","journal-title":"Dev. Comp. Immunol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1038\/381571a0","article-title":"Molecular chaperones in cellular protein folding","volume":"381","author":"Hartl","year":"1996","journal-title":"Nature"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1016\/S0145-305X(00)00016-1","article-title":"A precerebellin-like protein is part of the acute phase response in rainbow trout, Oncorhynchus mykiss","volume":"24","author":"Gerwick","year":"2000","journal-title":"Dev. Comp. Immunol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.dci.2008.07.001","article-title":"Innate immune response in rainbow trout (Oncorhynchus mykiss) against primary and secondary infections with Yersinia ruckeri O1","volume":"33","author":"Raida","year":"2009","journal-title":"Dev. Comp. Immunol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"6333","DOI":"10.1523\/JNEUROSCI.20-17-06333.2000","article-title":"Cbln3, a novel member of the precerebellin family that binds specifically to Cbln1","volume":"20","author":"Pang","year":"2000","journal-title":"J. Neurosci."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1007\/s10695-005-4588-0","article-title":"Intracranial injections induce local transcription of a gene encoding precerebellin-like protein","volume":"31","author":"Gerwick","year":"2005","journal-title":"Fish Physiol. Biochem."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1111\/j.1574-6968.1991.tb04647.x","article-title":"Evidence that Yersinia ruckeri possesses a high affinity iron uptake system","volume":"80","author":"Romalde","year":"1991","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"5199","DOI":"10.1128\/AEM.70.9.5199-5207.2004","article-title":"Identification of specific in vivo-induced (ivi) genes in Yersinia ruckeri and analysis of ruckerbactin, a catecholate siderophore iron acquisition system","volume":"70","author":"Fernandez","year":"2004","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_89","unstructured":"Janeway, C.A., Travers, P., Walport, M., and Shlomchik, M.J. (2005). Immunobiology: The Immune System in Health and Disease, Garland Science Publishing. [6th ed.]."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1182\/blood.V26.2.215.215","article-title":"Simplified myeloperoxidase stain using benzidine dihychloride","volume":"26","author":"Kaplow","year":"1965","journal-title":"Blood"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"27","DOI":"10.3354\/dao034027","article-title":"Neutrophil and macrophage responses to inflammation in the peritoneal cavity of rainbow trout Oncorhynchus mykiss: A light and electron microscopic cytochemical study","volume":"34","author":"Afonso","year":"1998","journal-title":"Dis. Aquat. Organ."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/S0165-2427(97)00048-2","article-title":"A Rapid, direct assay to measure degranulation of bovine neutrophil primary granules","volume":"58","author":"Quade","year":"1997","journal-title":"Vet. Immunol. Immunop."},{"key":"ref_93","unstructured":"Stolen, J.S., Fletcher, T.C., Anderson, D.P., Roberson, B.S., and van Muiswinkel, W.B. (1990). Serum Antiproteases in Fish. Techniques in Fish Immunology, SOS Publications. [1st ed.]."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/j.fsi.2014.11.024","article-title":"Dietary tryptophan and methionine as modulators of European seabass (Dicentrarchus labrax) immune status and inflammatory response","volume":"42","author":"Machado","year":"2015","journal-title":"Fish Shellfish Immunol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1016\/j.fsi.2011.07.024","article-title":"Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858)","volume":"31","author":"Costas","year":"2011","journal-title":"Fish Shellfish Immunol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"2241","DOI":"10.1007\/s10811-021-02431-1","article-title":"Microalgal biomasses have potential as ingredients in microdiets for Senegalese sole (Solea senegalensis) post-larvae","volume":"33","author":"Peixoto","year":"2021","journal-title":"J. Appl. Phycol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.fsi.2014.05.032","article-title":"Gilthead seabream (Sparus aurata) immune responses are modulated after feeding with purified antinutrients","volume":"41","author":"Costas","year":"2014","journal-title":"Fish Shellfish Immunol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/S0076-6879(84)05038-2","article-title":"Comparative studies on different methods of malonaldehyde determination","volume":"105","author":"Bird","year":"1984","journal-title":"Method. Enzymol."},{"key":"ref_99","unstructured":"Greenwald, R.A. (1985). Catalase Activity. Handbook of Methods of Oxygen Radical Research, CRC Press."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1007\/s10646-010-0523-y","article-title":"Linking behavioural alterations with biomarkers responses in the European seabass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion","volume":"19","author":"Almeida","year":"2010","journal-title":"Ecotoxicology"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"7130","DOI":"10.1016\/S0021-9258(19)42083-8","article-title":"Glutathione-S-transferases, the first enzymatic step in mercapturic acid formation","volume":"249","author":"Habig","year":"1974","journal-title":"J. Biol. Chem."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1023\/A:1025457831923","article-title":"Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulate","volume":"26","author":"Frasco","year":"2002","journal-title":"Fish Physiol. Biochem."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT\u2013PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"W147","DOI":"10.1093\/nar\/gkw419","article-title":"Heatmapper: Web-enabled heat mapping for all","volume":"44","author":"Babicki","year":"2016","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/6\/3096\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:35:52Z","timestamp":1760135752000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/6\/3096"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,3,13]]},"references-count":104,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2022,3]]}},"alternative-id":["ijms23063096"],"URL":"https:\/\/doi.org\/10.3390\/ijms23063096","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,3,13]]}}}