{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T15:21:03Z","timestamp":1782746463519,"version":"3.54.5"},"reference-count":108,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2022,1,25]],"date-time":"2022-01-25T00:00:00Z","timestamp":1643068800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Blue Granary Science and Technology Innovation","award":["2019YFD0901000"],"award-info":[{"award-number":["2019YFD0901000"]}]},{"name":"Major technology innovation &amp; application projects in Shandong province-breeding of the ex-cellent trout species for open sea farming","award":["SD2019YY006"],"award-info":[{"award-number":["SD2019YY006"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Rainbow trout (Oncorhynchus mykiss) serves as one of the most important commercial fish with an annual production of around 800,000 tonnes. However, infectious diseases, such as furunculosis caused by Aeromonas salmonicida infection, results in great economic loss in trout culture. The brain and kidney are two important organs associated with \u201csickness behaviors\u201d and immunomodulation in response to disease. Therefore, we worked with 60 trout and investigated transcriptional responses and enrichment pathways between healthy and infected trout. We observed that furunculosis resulted in the activation of toll-like receptors with neuroinflammation and neural dysfunction in the brain, which might cause the \u201csickness behaviors\u201d of infected trout including anorexia and lethargy. We also showed the salmonid-specific whole genome duplication contributed to duplicated colony stimulating factor 1 (csf-1) paralogs, which play an important role in modulating brain immunomodulation. Enrichment analyses of kidneys showed up-regulated immunomodulation and down-regulated neural functions, suggesting an immune-neural interaction between the brain and kidney. Moreover, the kidney endocrine network was activated in response to A. salmonicida infection, further convincing the communications between endocrine and immune systems in regulating internal homeostasis. Our study provided a foundation for pathophysiological responses of the brain and kidney in response to furunculosis and potentially offered a reference for generating disease-resistant trout strains.<\/jats:p>","DOI":"10.3390\/ijms23031340","type":"journal-article","created":{"date-parts":[[2022,1,25]],"date-time":"2022-01-25T20:40:18Z","timestamp":1643143218000},"page":"1340","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Transcriptional Signatures of Immune, Neural, and Endocrine Functions in the Brain and Kidney of Rainbow Trout (Oncorhynchus mykiss) in Response to Aeromonas salmonicida Infection"],"prefix":"10.3390","volume":"23","author":[{"given":"Mengqun","family":"Liu","sequence":"first","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaodong","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chu","family":"Zeng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hongkui","family":"Zhao","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jifang","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhishuai","family":"Hou","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haishen","family":"Wen","sequence":"additional","affiliation":[{"name":"Key Laboratory of Mariculture, Ministry of Education (KLMME), Ocean University of China, Qingdao 266003, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,1,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1093\/embo-reports\/kve236","article-title":"Fish as food: Aquaculture\u2019s contribution","volume":"2","author":"Tidwell","year":"2001","journal-title":"EMBO Rep."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1038\/35016500","article-title":"Effect of aquaculture on world fish supplies","volume":"405","author":"Naylor","year":"2000","journal-title":"Nature"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/s41586-021-03308-6","article-title":"A 20-year retrospective review of global aquaculture","volume":"591","author":"Naylor","year":"2021","journal-title":"Nature"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.gfs.2013.10.001","article-title":"Fisheries in transition: Food and nutrition security implications for the global South","volume":"3","author":"Belton","year":"2014","journal-title":"Glob. Food Sec."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.worlddev.2015.11.007","article-title":"Contribution of Fisheries and Aquaculture to Food Security and Poverty Reduction: Assessing the Current Evidence","volume":"79","author":"Arthur","year":"2016","journal-title":"World Dev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.foodpol.2016.02.005","article-title":"Sustaining healthy diets: The role of capture fisheries and aquaculture for improving nutrition in the post-2015 era","volume":"61","author":"Thilsted","year":"2016","journal-title":"Food Policy"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"5804","DOI":"10.1038\/s41467-020-19679-9","article-title":"Farming fish in the sea will not nourish the world","volume":"11","author":"Belton","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"856","DOI":"10.3389\/fimmu.2018.00856","article-title":"Comparative immune- and stress-related transcript response induced by air exposure and Vibrio anguillarum bacterin in rainbow trout (Oncorhynchus mykiss) and gilthead seabream (Sparus aurata) mucosal surfaces","volume":"9","author":"Khansari","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2597","DOI":"10.3389\/fimmu.2020.567941","article-title":"Immunoglobulins, Mucosal Immunity and Vaccination in Teleost Fish","volume":"11","author":"Yu","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1016\/j.fsi.2006.08.015","article-title":"The immune response of tilapia Oreochromis mossambicus and its susceptibility to Streptococcus iniae under stress in low and high temperatures","volume":"22","author":"Ndong","year":"2007","journal-title":"Fish Shellfish Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/B978-0-12-802728-8.00010-2","article-title":"10-Stress and Disease Resistance: Immune System and Immunoendocrine Interactions","volume":"Volume 35","author":"Schreck","year":"2016","journal-title":"Biology of Stress in Fish"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1128\/CMR.00039-09","article-title":"The genus Aeromonas: Taxonomy, pathogenicity, and infection","volume":"23","author":"Janda","year":"2010","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1046\/j.1365-2672.1998.00435.x","article-title":"Identification of atypical Aeromonas salmonicida: Inter-laboratory evaluation and harmonization of methods","volume":"84","author":"Dalsgaard","year":"1998","journal-title":"J. Appl. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.4014\/jmb.2005.05040","article-title":"Recent insights into Aeromonas salmonicida and its bacteriophages in aquaculture: A comprehensive review","volume":"30","author":"Park","year":"2020","journal-title":"J. Microbiol. Biotechnol."},{"key":"ref_15","unstructured":"Austin, B., and Austin, D. (2007). Bacterial Fish Pathogens: Diseases of Farmed and Wild Fish, Springer."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"167","DOI":"10.3354\/dao02342","article-title":"Colonization of turbot tissues by virulent and avirulent Aeromonas salmonicida subsp. salmonicida strains during infection","volume":"95","author":"Farto","year":"2011","journal-title":"Dis. Aquat. Organ."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1111\/raq.12248","article-title":"The adherence and colonization of microorganisms in fish gastrointestinal tract","volume":"11","author":"Li","year":"2019","journal-title":"Rev. Aquac."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/j.rvsc.2018.06.019","article-title":"Silver Nanoparticles: Their Role as Antibacterial Agent against Aeromonas salmonicida Subsp. salmonicida in Rainbow Trout (Oncorhynchus mykiss)","volume":"119","author":"Shaalan","year":"2018","journal-title":"Res. Vet. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Bernoth, E.-M. (1997). Furunculosis: The history of the disease and of disease research. Furunculosis, Academic Press.","DOI":"10.1016\/B978-012093040-1\/50003-8"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.vetmic.2013.06.025","article-title":"Virulence, genomic features, and plasticity of Aeromonas salmonicida subsp. salmonicida, the causative agent of fish furunculosis","volume":"169","author":"Tanaka","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1016\/j.fsi.2016.04.125","article-title":"Toll-like receptors in maraena whitefish: Evolutionary relationship among salmonid fishes and patterns of response to Aeromonas salmonicida","volume":"54","author":"Altmann","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/j.fsi.2019.05.048","article-title":"A transcriptome analysis focusing on splenic immune-related mciroRNAs of rainbow trout upon Aeromonas salmonicida subsp. salmonicida infection","volume":"91","author":"Cao","year":"2019","journal-title":"Fish Shellfish Immunol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"846","DOI":"10.1016\/j.fsi.2012.07.014","article-title":"The influence of dietary \u03b2-glucan, PAMP exposure and Aeromonas salmonicida on apoptosis modulation in common carp (Cyprinus carpio)","volume":"33","author":"Miest","year":"2012","journal-title":"Fish Shellfish Immunol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.3389\/fimmu.2019.01237","article-title":"Aeromonas salmonicida subsp. Salmonicida Early infection and immune response of atlantic cod (Gadus morhua L.) primary macrophages","volume":"10","author":"Hossain","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0147-619X(03)00058-1","article-title":"Three small, cryptic plasmids from Aeromonas salmonicida subsp. salmonicida A449","volume":"50","author":"Boyd","year":"2003","journal-title":"Plasmid"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2111","DOI":"10.1099\/mic.0.27926-0","article-title":"Attenuated virulence of an Aeromonas salmonicida subsp. salmonicida type III secretion mutant in a rainbow trout model","volume":"151","author":"Burr","year":"2005","journal-title":"Microbiology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1016\/j.fsi.2007.02.002","article-title":"Cytokine expression in the intestine of rainbow trout (Oncorhynchus mykiss) during infection with Aeromonas salmonicida","volume":"23","author":"Mulder","year":"2007","journal-title":"Fish Shellfish Immunol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1111\/are.14436","article-title":"Dietary \u03b2-glucan modulate haematological parameters, cytokines and gene expression in TLR and ERK pathways of rainbow trout (Oncorhynchus mykiss) during infection by Aeromonas salmonicida","volume":"51","author":"Ji","year":"2020","journal-title":"Aquac. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.dci.2008.09.012","article-title":"Expression profiles of cytokines released in intestinal epithelial cells of the rainbow trout, Oncorhynchus mykiss, in response to bacterial infection","volume":"33","author":"Komatsu","year":"2009","journal-title":"Dev. Comp. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"16810","DOI":"10.1038\/s41598-020-73999-w","article-title":"Aeromonas salmonicida activates rainbow trout IgM+ B cells signalling through Toll like receptors","volume":"10","author":"Soleto","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1192","DOI":"10.1016\/j.fsi.2013.07.032","article-title":"Novel insights into the peritoneal inflammation of rainbow trout (Oncorhynchus mykiss)","volume":"35","author":"Jaros","year":"2013","journal-title":"Fish Shellfish Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.fsi.2016.12.006","article-title":"Aeromonas salmonicida type III secretion system-effectors-mediated immune suppression in rainbow trout (Oncorhynchus mykiss)","volume":"60","author":"Origgi","year":"2017","journal-title":"Fish Shellfish Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2101","DOI":"10.1038\/s41598-019-38890-3","article-title":"Phosphoproteomic analyses of kidneys of Atlantic salmon infected with Aeromonas salmonicida","volume":"9","author":"Liu","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"292","DOI":"10.1016\/j.fsi.2016.08.055","article-title":"Metabolic profiling in kidneys of Atlantic salmon infected with Aeromonas salmonicida based on 1H NMR","volume":"58","author":"Liu","year":"2016","journal-title":"Fish Shellfish Immunol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.jprot.2015.03.031","article-title":"Transcriptomic and proteomic analyses of splenic immune mechanisms of rainbow trout (Oncorhynchus mykiss) infected by Aeromonas salmonicida subsp","volume":"122","author":"Long","year":"2015","journal-title":"salmonicida. J. Proteom."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.ecoenv.2017.03.044","article-title":"Transcriptional changes in innate immunity genes in head kidneys from Aeromonas salmonicida-challenged rainbow trout fed a mixture of polycyclic aromatic hydrocarbons","volume":"142","author":"Curtis","year":"2017","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.dci.2017.02.013","article-title":"Proteomic analysis in kidneys of Atlantic salmon infected with Aeromonas salmonicida by iTRAQ","volume":"72","author":"Liu","year":"2017","journal-title":"Dev. Comp. Immunol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"17857","DOI":"10.1038\/s41598-021-97437-7","article-title":"Whole-genome association study searching for QTL for Aeromonas salmonicida resistance in rainbow trout","volume":"11","author":"Marana","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1089\/zeb.2006.3.235","article-title":"Modulatory neurotransmitter systems and behavior: Towards zebrafish models of neurodegenerative diseases","volume":"3","author":"Panula","year":"2006","journal-title":"Zebrafish"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/j.bbi.2007.05.005","article-title":"Brain-immune communication pathways","volume":"21","author":"Quan","year":"2007","journal-title":"Brain. Behav. Immun."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/nri.2017.152","article-title":"Neuroimmunology in 2017: The central nervous system: Privileged by immune connections","volume":"18","author":"Kipnis","year":"2018","journal-title":"Nat. Rev. Immunol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbi.2015.09.003","article-title":"Inflammatory transcription factors as activation markers and functional readouts in immune-to-brain communication","volume":"54","author":"Rummel","year":"2016","journal-title":"Brain. Behav. Immun."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2089","DOI":"10.1523\/JNEUROSCI.3567-08.2009","article-title":"Cerebral microglia recruit monocytes into the brain in response to tumor necrosis factora signaling during peripheral organ inflammation","volume":"29","author":"Le","year":"2009","journal-title":"J. Neurosci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1349","DOI":"10.1007\/s10571-018-0609-2","article-title":"Mechanisms of Blood Brain Barrier Disruption by Different Types of Bacteria, and Bacterial\u2013Host Interactions Facilitate the Bacterial Pathogen Invading the Brain","volume":"38","author":"Desa","year":"2018","journal-title":"Cell. Mol. Neurobiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1111\/jfd.12697","article-title":"Blood\u2013brain barrier breakdown and myeloperoxidase activity in silver catfish experimentally infected with Pseudomonas aeruginosa","volume":"41","author":"Baldissera","year":"2018","journal-title":"J. Fish Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1942","DOI":"10.1210\/en.2015-2024","article-title":"Cross talk between growth and immunity: Coupling of the igf axis to conserved cytokine pathways in rainbow trout","volume":"157","author":"Alzaid","year":"2016","journal-title":"Endocrinology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1093\/molbev\/mst017","article-title":"Evolution of ancient functions in the vertebrate insulin-like growth factor system uncovered by study of duplicated salmonid fish genomes","volume":"30","author":"MacQueen","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"807","DOI":"10.1126\/science.1154370","article-title":"Discovery of a cytokine and its receptor by functional screening of the extracellular proteome","volume":"320","author":"Lin","year":"2008","journal-title":"Science"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1016\/j.str.2012.02.010","article-title":"Structural basis for the dual recognition of helical cytokines IL-34 and CSF-1 by CSF-1R","volume":"20","author":"Ma","year":"2012","journal-title":"Structure"},{"key":"ref_50","first-page":"96","article-title":"Molecular cloning, pathologically-correlated expression and functional characterization of the colony stimulating factor 1 receptor (CSF-1R) gene from a teleost, Plecoglossus altivelis","volume":"37","author":"Chen","year":"2016","journal-title":"Dong Wu Xue Yan Jiu Zool Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1182\/blood.V99.1.111","article-title":"Targeted disruption of the mouse colony-stimulating factor 1 receptor gene results in osteopetrosis, mononuclear phagocyte deficiency, increased primitive progenitor cell frequencies, and reproductive defects","volume":"99","author":"Dai","year":"2002","journal-title":"Blood"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1189\/jlb.1209780","article-title":"Editorial: CSF1R, CSF-1, and IL-34, a \u201cm\u00e9nage \u00e0 trois\u201d conserved across vertebrates","volume":"87","author":"Droin","year":"2010","journal-title":"J. Leukoc. Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/BF00172150","article-title":"Cloning and analysis of gene regulation of a novel LPS-inducible cDNA","volume":"41","author":"Lee","year":"1995","journal-title":"Immunogenetics"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"7820","DOI":"10.1073\/pnas.1218599110","article-title":"Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production","volume":"110","author":"Michelucci","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"822","DOI":"10.1038\/s41423-020-0489-5","article-title":"ACOD1 in immunometabolism and disease","volume":"17","author":"Wu","year":"2020","journal-title":"Cell. Mol. Immunol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"14274","DOI":"10.1074\/jbc.M115.685792","article-title":"Immunoresponsive gene 1 and itaconate inhibit succinate dehydrogenase to modulate intracellular succinate levels","volume":"291","author":"Cordes","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"152","DOI":"10.3389\/fimmu.2020.00152","article-title":"Fish Macrophages Show Distinct Metabolic Signatures Upon Polarization","volume":"11","author":"Wentzel","year":"2020","journal-title":"Front. Immunol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1007\/s00281-012-0309-9","article-title":"Roles for major histocompatibility complex glycosylation in immune function","volume":"34","author":"Ryan","year":"2012","journal-title":"Semin. Immunopathol."},{"key":"ref_59","unstructured":"Janeway, C.A., Travers, P., and Walport, M. (2001). Immunobiology: The Immune System in Health and Disease: The major histocompatibility complex and its functions. Immunobiol. Immune Syst. Health Dis., Available online: https:\/\/www.ncbi.nlm.nih.gov\/books\/NBK27156\/."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1046\/j.1365-2567.2003.01738.x","article-title":"The MHC class I antigen presentation pathway: Strategies for viral immune evasion","volume":"110","author":"Hewitt","year":"2003","journal-title":"Immunology"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1084\/jem.20021542","article-title":"Presentation of exogenous antigens on major histocompatibility complex (MHC) class I and MHC class II molecules is differentially regulated during dendritic cell maturation","volume":"198","author":"Delamarre","year":"2003","journal-title":"J. Exp. Med."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2776(02)80012-8","article-title":"Protein degradation and the generation of MHC class I-presented peptides","volume":"80","author":"Rock","year":"2002","journal-title":"Adv. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"292","DOI":"10.3389\/fimmu.2017.00292","article-title":"Major histocompatibility complex (MHC) class I and MHC class II proteins: Conformational plasticity in antigen presentation","volume":"8","author":"Wieczorek","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1111\/j.1365-3083.2007.02052.x","article-title":"The effect of specific MHC class I and class II combinations on resistance to furunculosis in Atlantic salmon (Salmo salar)","volume":"67","author":"Larsen","year":"2008","journal-title":"Scand. J. Immunol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1016\/j.fsi.2006.02.001","article-title":"How specific MHC class I and class II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon (Salmo salar)","volume":"21","author":"Larsen","year":"2006","journal-title":"Fish Shellfish Immunol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0065-2776(08)60785-3","article-title":"Mechanisms of Exogenous Antigen Presentation by MHC Class I Molecules In Vitro and In Vivo: Implications for Generating CD8+ T Cell Responses to Infectious Agents, Tumors, Transplants, and Vaccines","volume":"73","author":"Yewdell","year":"1999","journal-title":"Adv. Immunol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"3107","DOI":"10.1016\/j.molimm.2008.03.007","article-title":"Identification of MHC class II\u03b2 resistance\/susceptibility alleles to Aeromonas salmonicida in brook charr (Salvelinus fontinalis)","volume":"45","author":"Tarte","year":"2008","journal-title":"Mol. Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"270302","DOI":"10.1155\/2014\/270302","article-title":"Functional roles of Syk in macrophage-mediated inflammatory responses","volume":"2014","author":"Yi","year":"2014","journal-title":"Mediators Inflamm."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"342931","DOI":"10.1155\/2013\/342931","article-title":"Innate immunity and neuroinflammation","volume":"2013","author":"Shastri","year":"2013","journal-title":"Mediators Inflamm."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1016\/j.it.2006.11.004","article-title":"What is immune privilege (not)?","volume":"28","author":"Galea","year":"2007","journal-title":"Trends Immunol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1186\/s12974-018-1163-z","article-title":"Evidence of the impact of systemic inflammation on neuroinflammation from a non-bacterial endotoxin animal model","volume":"15","author":"Huang","year":"2018","journal-title":"J. Neuroinflamm."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1186\/s12974-015-0332-6","article-title":"Systemic inflammation and microglial activation: Systematic review of animal experiments","volume":"12","author":"Hoogland","year":"2015","journal-title":"J. Neuroinflamm."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2677","DOI":"10.1093\/brain\/awt210","article-title":"Inflammatory components in human Alzheimer\u2019s disease and after active amyloid-\u03b242 immunization","volume":"136","author":"Zotova","year":"2013","journal-title":"Brain"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1126\/science.aag2590","article-title":"How neuroinflammation contributes to neurodegeneration","volume":"353","author":"Ransohoff","year":"2016","journal-title":"Science"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.pharmthera.2011.01.014","article-title":"Immune system to brain signaling: Neuropsychopharmacological implications","volume":"130","author":"Capuron","year":"2011","journal-title":"Pharmacol. Ther."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/j.biopsych.2009.09.033","article-title":"A Meta-Analysis of Cytokines in Major Depression","volume":"67","author":"Dowlati","year":"2010","journal-title":"Biol. Psychiatry"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1097\/PSY.0b013e3181907c1b","article-title":"Associations of depression with c-reactive protein, IL-1, and IL-6: A meta-analysis","volume":"71","author":"Howren","year":"2009","journal-title":"Psychosom. Med."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.jneuroim.2019.03.012","article-title":"Toll-like receptors in the pathogenesis of neuroinflammation","volume":"332","author":"Kumar","year":"2019","journal-title":"J. Neuroimmunol."},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Lim, K.H., and Staudt, L.M. (2013). Toll-Like receptor signaling. Cold Spring Harb. Perspect. Biol., 5.","DOI":"10.1101\/cshperspect.a011247"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"461","DOI":"10.3389\/fimmu.2014.00461","article-title":"Toll-like receptor signaling pathways","volume":"5","author":"Kawasaki","year":"2014","journal-title":"Front. Immunol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.fsi.2019.12.022","article-title":"Comparative transcriptome analysis reveals the mechanism of \u03b2-glucan in protecting rainbow trout (Oncorhynchus mykiss) from Aeromonas salmonicida infection","volume":"98","author":"Ji","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1016\/j.dci.2006.08.007","article-title":"Characterization of twin toll-like receptors from rainbow trout (Oncorhynchus mykiss): Evolutionary relationship and induced expression by Aeromonas salmonicida salmonicida","volume":"31","author":"Rebl","year":"2007","journal-title":"Dev. Comp. Immunol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1210\/edrv-17-1-64","article-title":"Immune-neuro-endocrine interactions: Facts and hypotheses","volume":"17","author":"Besedovsky","year":"1996","journal-title":"Endocr. Rev."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0165-2427(00)00235-X","article-title":"Modulation of the fish immune system by hormones","volume":"77","author":"Harris","year":"2000","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1016\/j.dci.2011.07.002","article-title":"Stress and immune modulation in fish","volume":"35","author":"Tort","year":"2011","journal-title":"Dev. Comp. Immunol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1159\/000452902","article-title":"Immune-Neuro-Endocrine Reflexes, Circuits, and Networks: Physiologic and Evolutionary Implications","volume":"48","author":"Besedovsky","year":"2017","journal-title":"Front. Horm. Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1002\/eji.201847895","article-title":"\u2018Beauty and the beast\u2019 in infection: How immune\u2013endocrine interactions regulate systemic metabolism in the context of infection","volume":"49","author":"Wensveen","year":"2019","journal-title":"Eur. J. Immunol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1007\/s10646-010-0588-7","article-title":"The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: A review","volume":"20","author":"Milla","year":"2011","journal-title":"Ecotoxicology"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1016\/j.dci.2018.08.001","article-title":"Role of estrogens in fish immunity with special emphasis on GPER1","volume":"89","author":"Cabas","year":"2018","journal-title":"Dev. Comp. Immunol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1126\/science.1178331","article-title":"Development of monocytes, macrophages, and dendritic cells","volume":"327","author":"Geissmann","year":"2010","journal-title":"Science"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1189\/jlb.72.4.621","article-title":"The mononuclear phagocyte system revisited","volume":"72","author":"Hume","year":"2002","journal-title":"J. Leukoc. Biol."},{"key":"ref_92","first-page":"5026","article-title":"Differential processing of colony-stimulating factor 1 precursors encoded by two human cDNAs","volume":"8","author":"Rettenmier","year":"1988","journal-title":"Mol. Cell. Biol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"103586","DOI":"10.1016\/j.dci.2019.103586","article-title":"Regulation and function of macrophage colony-stimulating factor (CSF1) in the chicken immune system","volume":"105","author":"Wu","year":"2020","journal-title":"Dev. Comp. Immunol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"31865","DOI":"10.1074\/jbc.M706278200","article-title":"Growth factors of lower vertebrates: Characterization of goldfish (Carassius auratus L.) macrophage colony-stimulating factor-1","volume":"282","author":"Hanington","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_95","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_96","doi-asserted-by":"crossref","first-page":"123","DOI":"10.24272\/j.issn.2095-8137.2020.026","article-title":"Mudskipper interleukin-34 modulates the functions of monocytes\/macrophages via the colony-stimulating factor-1 receptor 1","volume":"41","author":"Shen","year":"2020","journal-title":"Zool. Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"3657","DOI":"10.1038\/ncomms4657","article-title":"The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates","volume":"5","author":"Berthelot","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"103920","DOI":"10.1016\/j.dci.2020.103920","article-title":"Macrophage colony stimulating factor (MCSF) of Japanese flounder (Paralichthys olivaceus): Immunoregulatory property, anti-infectious function, and interaction with MCSF receptor","volume":"116","author":"Gu","year":"2021","journal-title":"Dev. Comp. Immunol."},{"key":"ref_99","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":"43","author":"Mo","year":"2015","journal-title":"Fish Shellfish Immunol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"103987","DOI":"10.1016\/j.dci.2020.103987","article-title":"Identification and characterization of caspases genes in rainbow trout (Oncorhynchus mykiss) and their expression profiles after Aeromonas salmonicida and Vibrio anguillarum infection","volume":"118","author":"Zeng","year":"2021","journal-title":"Dev. Comp. Immunol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: A fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat. Methods"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"ref_104","first-page":"f1000research","article-title":"Differential expression of RNA-Seq data at the gene level\u2014The DESeq package","volume":"10","author":"Anders","year":"2012","journal-title":"Heidelberg, Ger. Eur. Mol. Biol. Lab."},{"key":"ref_105","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\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1016\/j.aquaculture.2019.01.003","article-title":"Transcriptome and physiological analysis reveal alterations in muscle metabolisms and immune responses of grass carp (Ctenopharyngodon idellus) cultured at different stocking densities","volume":"503","author":"Zhao","year":"2019","journal-title":"Aquaculture"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00395-019-0715-4","article-title":"Fibroblast polarization over the myocardial infarction time continuum shifts roles from inflammation to angiogenesis","volume":"114","author":"Mouton","year":"2019","journal-title":"Basic Res. Cardiol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/cpbi.86","article-title":"Using MetaboAnalyst 4.0 for Comprehensive and Integrative Metabolomics Data Analysis","volume":"68","author":"Chong","year":"2019","journal-title":"Curr. Protoc. Bioinform."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/3\/1340\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:07:18Z","timestamp":1760134038000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/3\/1340"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,25]]},"references-count":108,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["ijms23031340"],"URL":"https:\/\/doi.org\/10.3390\/ijms23031340","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,25]]}}}