{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,26]],"date-time":"2026-06-26T17:33:56Z","timestamp":1782495236370,"version":"3.54.5"},"reference-count":37,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,2,2]],"date-time":"2023-02-02T00:00:00Z","timestamp":1675296000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:sec><jats:title>Introduction<\/jats:title><jats:p>Temporal elevation of water temperature positively affects immune activity and disease resistance in poikilothermic teleost fish. The ayu, <jats:italic>Plecoglossus altivelis<\/jats:italic>, an important fish species for Japanese freshwater fisheries, is usually produced under higher water temperatures than the natural conditions to facilitate rapid growth. However, it has been reported that rearing fish at higher water temperatures inhibits the development of the thymus, suggesting that resistance to infectious diseases is reduced in ayu reared at higher water temperatures. Here, we show that decreased resistance to bacterial cold-water disease and excessive inflammatory responses occurred in ayu reared at 22\u00b0C compared with those reared at lower temperatures.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Ayu larvae were reared at 12\u00b0C, 15\u00b0C and 22\u00b0C for 77 days and fed 3% of their body weight. Thymus index and condition factor was calculated after the fish rearing. Then, ayu reared at the different temperatures were challenged with Flavobacterium psychrophilum and the fish were sampled for histopathology and gene expression analyses. Further, the fish were vaccinated with formalin-killed F. psychrophilum and continuously reared at the three different water temperatures. Serum antibody titer was determined by ELISA and cumulative mortality in each group was recorded after the bacterial challenge.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Ayu reared at 22\u00b0C showed a significantly lower thymus index and higher condition factor than those reared at lower temperatures. Infiltrated leukocytes and many melanin pigments were frequently observed in the adipose tissues and spleens of ayu reared at  22\u00b0C, respectively, but not in those reared at 12\u00b0C. The gene expression levels of inflammatory cytokines such as IL-1\u03b2, IL-8 and TNF\u03b1 in the spleen were significantly higher in the 22\u00b0C group than in the 12\u00b0C group. The cumulative survival rate after challenge with <jats:italic>Flavobacterium psychrophilum<\/jats:italic> was 51.7%, 40.0% and 13.3% in the 12\u00b0C, 15\u00b0C and 22\u00b0C groups, respectively. The relative percent survival values of vaccinated fish reared at 15\u00b0C and 22\u00b0C groups were lower than those reared at 12\u00b0C. Moreover, the specific antibody titer of the vaccinated fish was the lowest in the 22\u00b0C group and the highest in the 12\u00b0C group. <\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>These results suggest that rearing the fish under high water temperature causes excessive inflammatory responses similar to metabolic inflammation in human obesity, resulting in a decrease of disease resistance. In addition, thymic involution induced by higher water temperature probably leads the poor response to vaccination. The present study provides insights into the physiological and immunological changes of fish under global warming.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fimmu.2023.1101491","type":"journal-article","created":{"date-parts":[[2023,2,2]],"date-time":"2023-02-02T05:20:08Z","timestamp":1675315208000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Decreased resistance to bacterial cold-water disease and excessive inflammatory response in ayu (Plecoglossus altivelis) reared at high water temperature"],"prefix":"10.3389","volume":"14","author":[{"given":"Goshi","family":"Kato","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hayato","family":"Nakajima","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyuma","family":"Suzuki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuhei","family":"Kanzawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chihaya","family":"Nakayasu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kosei","family":"Taguchi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Osamu","family":"Kurata","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Motohiko","family":"Sano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,2,2]]},"reference":[{"key":"B1","article-title":"Elevation in body temperature to fever range enhances and prolongs subsequent responsiveness of macrophages to endotoxin challenge","volume":"7","author":"Lee","year":"2012","journal-title":"PloS One"},{"key":"B2","doi-asserted-by":"crossref","DOI":"10.1073\/pnas.1803609115","article-title":"Temperature regulates NF-\u03baB dynamics and function through timing of A20 transcription","volume":"115","author":"Harper","year":"2018","journal-title":"PNAS"},{"key":"B3","doi-asserted-by":"crossref","DOI":"10.1016\/j.fsi.2011.12.005","article-title":"The use of warmed water treatment to induce protective immunity against the bacterial cold-water disease pathogen flavobacterium psychrophilum in ayu plecoglossus altivelis","volume":"32","author":"Sugahara","year":"2012","journal-title":"Fish Shellfish Immunol"},{"key":"B4","doi-asserted-by":"crossref","first-page":"193","DOI":"10.3354\/dao02759","article-title":"Effects of experimentally induced infections of goldfish carassius auratus with cyprinid herpesvirus 2 CyHV-2. at various water temperatures","volume":"110","author":"Ito","year":"2014","journal-title":"Dis Aquat Organ"},{"key":"B5","doi-asserted-by":"crossref","DOI":"10.1080\/23328940.2020.1765950","article-title":"Effects of temperature on feeding and digestive processes in fish","volume":"7","author":"Volkoff","year":"2020","journal-title":"Temperature"},{"key":"B6","article-title":"Migration behaviors of sea-run ayu plecoglossus altivelis pisces. in toyama bay, Japan","volume":"68","author":"Tago","year":"2000","journal-title":"Nippon Suisan Gakkaishi"},{"key":"B7","article-title":"An ecological study of the anadromous \u201cayu\u201d, plecoglossus altivelis t. et s. -II. seasonal variations in the composition of the anadromous ayu schools in the river okumo, Kyoto","volume":"29","author":"Kusuda","year":"1963","journal-title":"Nippon Suisan Gakkaishi"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.3147\/jsfp.54.40","article-title":"A survey of water temperature for production of juvenile ayu plecoglossus altivelis","volume":"54","author":"Kato","year":"2019","journal-title":"Fish Pathol"},{"key":"B9","article-title":"Studies on the artificial production of ayu fish seedling\u2013LXI. the influence of water temperature on the early survival of yolk-sac fry of ayu fish","volume":"5","author":"Ito","year":"1968","journal-title":"Res Rep Kisosansen Surv Team"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.2331\/suisan.77.237","article-title":"Effect of different feeding and water temperature conditions on the growth of ayu, plecoglossus altivelis altivelis, in brackish water under rearing conditions","volume":"77","author":"Sakano","year":"2011","journal-title":"Nippon Suisan Gakkaishi"},{"key":"B11","doi-asserted-by":"crossref","first-page":"39","DOI":"10.3390\/biology6040039","article-title":"Impacts of low temperature on the teleost immune system","volume":"6","author":"Abram","year":"2017","journal-title":"Biol Basel."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1016\/S0044-848602.00661-0","article-title":"Impairment of thymus development in cultured osmerid fish, the ayu, plecoglossus altivelis","volume":"221","author":"Miwa","year":"2003","journal-title":"Aquaculture"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.2331\/SUISAN.72.182","article-title":"Influence of water temperature and rearing density on thymus development of cultured ayu plecoglossus altivelis altivelis, and relation between the thymus volume","volume":"72","author":"Hara","year":"2006","journal-title":"Nippon Suisan Gakkaishi"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3147\/jsfp.55.31","article-title":"Subsequent changes in the thymus of ayu plecoglossus altivelis reared from juveniles with temperature-induced differential thymus growth","volume":"55","author":"Takada","year":"2020","journal-title":"Fish Pathol"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.3147\/jsfp.29.101","article-title":"A study on serotyping of cytophaga psychrophila isolated from fishes in Japan","volume":"29","author":"Wakabayashi","year":"1994","journal-title":"Fish Pathol"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.3147\/jsfp.51.153","article-title":"Bacterial cold-water disease in salmonid fish and ayu","volume":"51","author":"Kumagai","year":"2016","journal-title":"Fish Pathol"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3147\/jsfp.31.157","article-title":"Outbreaks of coldwater disease in wild ayu and pale chub","volume":"31","author":"Iida","year":"1996","journal-title":"Fish Pathol"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2761.2007.00809.x","article-title":"Molecular typing by pulsed-field gel electrophoresis of flavobacterium psychrophilum isolates derived from Japanese fish","volume":"30","author":"Arai","year":"2007","journal-title":"J Fish Dis"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.2331\/SUISAN.40.751","article-title":"Characteristics of myxobacteria associated with some freshwater fish diseases in Japan","volume":"40","author":"Wakabayashi","year":"1974","journal-title":"Nippon Suisan Gakkaishi"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1111\/1755-0998.12108","article-title":"Preservation of RNA and DNA from mammal samples under field conditions","volume":"13","author":"Camacho-Sanchez","year":"2013","journal-title":"Mol Ecol Resour"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1016\/j.margen.2015.06.011","article-title":"Expressed sequence tag analyses of three leukocyte subpopulations in ayu plecoglossus altivelis altivelis, separated by monoclonal antibodies","volume":"23","author":"Kato","year":"2015","journal-title":"Mar Genomics"},{"key":"B22","first-page":"33","article-title":"The thymus development with growth of Japanese smelt, hypomesus nipponensis and the influence of water temperature on the gland volume","volume":"3","author":"Hasegawa","year":"2005","journal-title":"J Mar Sci Technol"},{"key":"B23","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511983375.010","article-title":"Temperature and growth: Modulation of growth rate via temperature change","volume-title":"Global warming: Implications for freshwater and marine fish. society for experimental biology seminar series","author":"Jobling","year":"1997"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1038\/s41574-018-0126-x","article-title":"The obese adipose tissue microenvironment in cancer development and progression","volume":"15","author":"Quail","year":"2019","journal-title":"Nat Rev Endocrinol"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1161\/01.ATV.0000183883.72263.13","article-title":"A paracrine loop between adipocytes and macrophages aggravates inflammatory changes: Role of free fatty acids and tumor necrosis factor \u03b1","volume":"25","author":"Suganami","year":"2005","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1172\/JCI29881","article-title":"Obesity induces a phenotypic switch in adipose tissue macrophage polarization","volume":"117","author":"Lumeng","year":"2007","journal-title":"J Clin Invest"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1007\/s00125-013-3139-y","article-title":"Local proliferation of macrophages in adipose tissue during obesity-induced inflammation","volume":"57","author":"Haase","year":"2014","journal-title":"Diabetologia"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1038\/cmi.2009.113","article-title":"Premetastatic milieu explained by TLR4 agonist-mediated homeostatic inflammation","volume":"7","author":"Maru","year":"2010","journal-title":"Cell Mol Immunol"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.3390\/biom9060223","article-title":"Chronic inflammation as an immunological abnormality and effectiveness of exercise","volume":"9","author":"Suzuki","year":"2019","journal-title":"Biomolecules"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3390\/ijms22073456","article-title":"The inflammatory profile of obesity and the role on pulmonary","volume":"22","author":"Hornung","year":"2021","journal-title":"Int J Mol Sci"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1111\/j.1749-6632.1992.tb27458.x","article-title":"Thymic involution in aging. prospects for correction","volume":"673","author":"Hadden","year":"1992","journal-title":"Ann N Y Acad Sci"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1007\/s11357-013-9564-5","article-title":"Thymus and aging: morphological, radiological, and functional overview","volume":"36","author":"Rezzani","year":"2014","journal-title":"AGE"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1111\/j.1399-3038.2004.00032.x","article-title":"T-Lymphocytes subsets, thymic size and breastfeeding in infancy","volume":"15","author":"Jeppesen","year":"2004","journal-title":"Pediatr Allergy Immunol"},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.4049\/jimmunol.1201235","article-title":"Lymphopenia-driven homeostatic regulation of na\u00efve T cells in elderly and thymectomized young adults","volume":"189","author":"Sauce","year":"2012","journal-title":"J Immunol"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1002\/eji.201747431","article-title":"CXCR3high CD8+ T cells with na\u00efve phenotype and high capacity for IFN-\u03b3 production are generated during homeostatic T-cell proliferation","volume":"48","author":"Kato","year":"2018","journal-title":"Eur J Immunol"},{"key":"B36","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1186\/s12979-019-0154-y","article-title":"Effect of homeostatic T-cell proliferation in the vaccine responsiveness against influenza in elderly people","volume":"16","author":"Herrero-Fern\u00e1ndez","year":"2019","journal-title":"Immune Aging"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1186\/1742-4933-11-9","article-title":"Impact of ageing on the response and repertoire of influenza virus-specific CD4 T cells","volume":"11","author":"Lanzer","year":"2014","journal-title":"Immun Aging"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2023.1101491\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,2,2]],"date-time":"2023-02-02T05:20:21Z","timestamp":1675315221000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2023.1101491\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,2]]},"references-count":37,"alternative-id":["10.3389\/fimmu.2023.1101491"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2023.1101491","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,2]]},"article-number":"1101491"}}