{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T22:17:04Z","timestamp":1790201824816,"version":"4.1.0"},"reference-count":77,"publisher":"Springer Science and Business Media LLC","issue":"5","license":[{"start":{"date-parts":[[2020,6,9]],"date-time":"2020-06-09T00:00:00Z","timestamp":1591660800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,6,9]],"date-time":"2020-06-09T00:00:00Z","timestamp":1591660800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100004281","name":"Narodowe Centrum Nauki","doi-asserted-by":"publisher","award":["2015\/19\/B\/NZ6\/00895"],"award-info":[{"award-number":["2015\/19\/B\/NZ6\/00895"]}],"id":[{"id":"10.13039\/501100004281","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Fish Physiol Biochem"],"published-print":{"date-parts":[[2020,10]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Inflammation is the evolutionary conserved immune response to harmful stimuli such as pathogens or damaged cells. This multistep process acts by removing injurious stimuli and initiating the healing process. Therefore, it must be tightly regulated by cytokines, chemokines, and enzymes, as well as neuroendocrine mediators. In the present work, we studied the immunoregulatory properties of 17\u03b2-estradiol (E2) in common carp. We determined the in vitro effects of E2 on the activity\/polarization of macrophages and the in vivo effects during <jats:italic>Aeromonas salmonicida<\/jats:italic>-induced inflammation. In vitro, E2 reduced the lipopolysaccharide (LPS)-stimulated expression of pro- and anti-inflammatory mediator genes but did not change the gene expression of the estrogen receptors and of aromatase CYP19. In contrast, in vivo in the head kidney of <jats:italic>A. salmonicida<\/jats:italic>-infected fish, E2-treated feeding induced an upregulation of gene expression of pro-inflammatory (<jats:italic>il-12p35<\/jats:italic> and <jats:italic>cxcb2<\/jats:italic>) and anti-inflammatory (<jats:italic>arginase 1<\/jats:italic>, <jats:italic>arginase 2<\/jats:italic>, <jats:italic>il-10<\/jats:italic>, and <jats:italic>mmp9<\/jats:italic>) mediators. Moreover, in infected fish fed with E2-treated food, a higher gene expression of the estrogen receptors and of the aromatase CYP19 was found. Our results demonstrate that estrogens can modulate the carp innate immune response, though the in vitro and in vivo effects of this hormone are contrasting. This implies that estradiol not only induces a direct effect on macrophages but rather exerts immunomodulatory actions through indirect mechanisms involving other cellular targets.<\/jats:p>","DOI":"10.1007\/s10695-020-00827-3","type":"journal-article","created":{"date-parts":[[2020,6,9]],"date-time":"2020-06-09T10:03:14Z","timestamp":1591696994000},"page":"1775-1794","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["17\u03b2-Estradiol affects the innate immune response in common carp"],"prefix":"10.1007","volume":"46","author":[{"given":"Magdalena","family":"Maciuszek","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lukasz","family":"Pijanowski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agnieszka","family":"Pekala-Safinska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B. M. Lidy Verburg-van","family":"Kemenade","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8067-6278","authenticated-orcid":false,"given":"Magdalena","family":"Chadzinska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,6,9]]},"reference":[{"key":"827_CR1","doi-asserted-by":"publisher","first-page":"273","DOI":"10.22034\/ijab.v1i6.143","volume":"1","author":"P Akbary","year":"2013","unstructured":"Akbary P, Mirvaghefi A, Akhlaghi M et al (2013) Effects of the aromatase inhibitore letrozole on serum immunoglobulin and lysozyme levels in immunized rainbow trout (Oncorhynchus mykiss Walbaum) females. Int J Aquat Biol 1:273\u2013280. https:\/\/doi.org\/10.22034\/ijab.v1i6.143","journal-title":"Int J Aquat Biol"},{"key":"827_CR2","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1016\/j.fsi.2010.07.010","volume":"29","author":"JAJ Arts","year":"2010","unstructured":"Arts JAJ, Tijhaar EJ, Chadzinska M, Savelkoul HFJ, Verburg-van Kemenade BML (2010) Functional analysis of carp interferon-\u03b3: evolutionary conservation of classical phagocyte activation. Fish Shellfish Immunol 29:793\u2013802. https:\/\/doi.org\/10.1016\/j.fsi.2010.07.010","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR3","doi-asserted-by":"publisher","first-page":"1309","DOI":"10.1172\/JCI16288","volume":"111","author":"GS Ashcroft","year":"2003","unstructured":"Ashcroft GS, Mills SJ, Lei K, Gibbons L, Jeong MJ, Taniguchi M, Burow M, Horan MA, Wahl SM, Nakayama T (2003) Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J Clin Invest 111:1309\u20131318. https:\/\/doi.org\/10.1172\/JCI16288","journal-title":"J Clin Invest"},{"key":"827_CR4","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.matbio.2005.03.007","volume":"24","author":"S Bai","year":"2005","unstructured":"Bai S, Thummel R, Godwin AR et al (2005) Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1-MMP, MMP2 and TIMP2. Matrix Biol 24:247\u2013260. https:\/\/doi.org\/10.1016\/j.matbio.2005.03.007","journal-title":"Matrix Biol"},{"key":"827_CR5","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1016\/S0145-305X(01)00033-7","volume":"25","author":"CJ Bayne","year":"2001","unstructured":"Bayne CJ, Gerwick L (2001) The acute phase response and innate immunity of fish. Dev Comp Immunol 25:725\u2013743. https:\/\/doi.org\/10.1016\/S0145-305X(01)00033-7","journal-title":"Dev Comp Immunol"},{"key":"827_CR6","doi-asserted-by":"publisher","first-page":"1404","DOI":"10.1182\/blood-2003-10-3380","volume":"104","author":"\u00c5K Bengtsson","year":"2004","unstructured":"Bengtsson \u00c5K, Ryan EJ, Giordano D et al (2004) 17\u03b2-estradiol (E2) modulates cytokine and chemokine expression in human monocyte-derived dendritic cells. Blood 104:1404\u20131410. https:\/\/doi.org\/10.1182\/blood-2003-10-3380","journal-title":"Blood"},{"key":"827_CR7","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.fsi.2016.09.006","volume":"58","author":"MA Burgos-Aceves","year":"2016","unstructured":"Burgos-Aceves MA, Cohen A, Smith Y, Faggio C (2016) Estrogen regulation of gene expression in the teleost fish immune system. Fish Shellfish Immunol 58:42\u201349. https:\/\/doi.org\/10.1016\/j.fsi.2016.09.006","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR8","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1016\/j.dci.2011.09.011","volume":"36","author":"I Cabas","year":"2012","unstructured":"Cabas I, Liarte S, Garc\u00eda-Alc\u00e1zar A, Meseguer J, Mulero V, Garc\u00eda-Ayala A (2012) 17\u03b1-Ethynylestradiol alters the immune response of the teleost gilthead seabream (Sparus aurata L.) both in vivo and in vitro. Dev Comp Immunol 36:547\u2013556. https:\/\/doi.org\/10.1016\/j.dci.2011.09.011","journal-title":"Dev Comp Immunol"},{"key":"827_CR9","doi-asserted-by":"publisher","first-page":"7980","DOI":"10.4049\/jimmunol.180.12.7980","volume":"180","author":"B Calippe","year":"2008","unstructured":"Calippe B, Douin-Echinard V, Laffargue M, Laurell H, Rana-Poussine V, Pipy B, Gu\u00e9ry JC, Bayard F, Arnal JF, Gourdy P (2008) Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J Immunol 180:7980\u20137988. https:\/\/doi.org\/10.4049\/jimmunol.180.12.7980","journal-title":"J Immunol"},{"key":"827_CR10","doi-asserted-by":"publisher","first-page":"1169","DOI":"10.4049\/jimmunol.0902383","volume":"185","author":"B Calippe","year":"2010","unstructured":"Calippe B, Douin-Echinard V, Delpy L, Laffargue M, L\u00e9lu K, Krust A, Pipy B, Bayard F, Arnal JF, Gu\u00e9ry JC, Gourdy P (2010) 17\u03b2-Estradiol promotes TLR4-triggered proinflammatory mediator production through direct estrogen receptor \u03b1 signaling in macrophages in vivo. J Immunol 185:1169\u20131176. https:\/\/doi.org\/10.4049\/jimmunol.0902383","journal-title":"J Immunol"},{"key":"827_CR11","doi-asserted-by":"publisher","first-page":"1825","DOI":"10.1084\/jem.20100500","volume":"207","author":"L Campbell","year":"2010","unstructured":"Campbell L, Emmerson E, Davies F, Gilliver SC, Krust A, Chambon P, Ashcroft GS, Hardman MJ (2010) Estrogen promotes cutaneous wound healing via estrogen receptor \u03b2 independent of its antiinflammatory activities. J Exp Med 207:1825\u20131833. https:\/\/doi.org\/10.1084\/jem.20100500","journal-title":"J Exp Med"},{"key":"827_CR12","doi-asserted-by":"publisher","first-page":"2461","DOI":"10.1038\/jid.2013.164","volume":"133","author":"L Campbell","year":"2013","unstructured":"Campbell L, Saville CR, Murray PJ, Cruickshank SM, Hardman MJ (2013) Local arginase 1 activity is required for cutaneous wound healing. J Invest Dermatol 133:2461\u20132470. https:\/\/doi.org\/10.1038\/jid.2013.164","journal-title":"J Invest Dermatol"},{"key":"827_CR13","doi-asserted-by":"publisher","first-page":"2447","DOI":"10.1038\/jid.2014.175","volume":"134","author":"L Campbell","year":"2014","unstructured":"Campbell L, Emmerson E, Williams H, Saville CR, Krust A, Chambon P, Mace KA, Hardman MJ (2014) Estrogen receptor-alpha promotes alternative macrophage activation during cutaneous repair. J Invest Dermatol 134:2447\u20132457. https:\/\/doi.org\/10.1038\/jid.2014.175","journal-title":"J Invest Dermatol"},{"key":"827_CR14","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1111\/j.1365-2567.2008.02874.x","volume":"125","author":"M Chadzinska","year":"2008","unstructured":"Chadzinska M, Baginski P, Kolaczkowska E, Savelkoul HFJ, Lidy Verburg-van Kemenade BM (2008a) Expression profiles of matrix metalloproteinase 9 in teleost fish provide evidence for its active role in initiation and resolution of inflammation. Immunology 125:601\u2013610. https:\/\/doi.org\/10.1111\/j.1365-2567.2008.02874.x","journal-title":"Immunology"},{"key":"827_CR15","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1016\/j.dci.2007.08.008","volume":"32","author":"M Chadzinska","year":"2008","unstructured":"Chadzinska M, Leon-Kloosterziel KM, Plytycz B, Verburg-van Kemenade BML (2008b) In vivo kinetics of cytokine expression during peritonitis in carp: evidence for innate and alternative macrophage polarization. Dev Comp Immunol 32:509\u2013518. https:\/\/doi.org\/10.1016\/j.dci.2007.08.008","journal-title":"Dev Comp Immunol"},{"key":"827_CR16","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.dci.2008.07.004","volume":"33","author":"M Chadzinska","year":"2009","unstructured":"Chadzinska M, Savelkoul HFJ, Verburg-van Kemenade BML (2009) Morphine affects the inflammatory response in carp by impairment of leukocyte migration. Dev Comp Immunol 33:88\u201396. https:\/\/doi.org\/10.1016\/j.dci.2008.07.004","journal-title":"Dev Comp Immunol"},{"key":"827_CR17","doi-asserted-by":"publisher","first-page":"9","DOI":"10.3390\/biology7010009","volume":"7","author":"E Chaves-Pozo","year":"2018","unstructured":"Chaves-Pozo E, Garc\u00eda-Ayala A, Cabas I (2018) Effects of sex steroids on fish leukocytes. Biology (Basel) 7:9. https:\/\/doi.org\/10.3390\/biology7010009","journal-title":"Biology (Basel)"},{"key":"827_CR18","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1016\/0022-1759(94)90027-2","volume":"174","author":"IM Corraliza","year":"1994","unstructured":"Corraliza IM, Campo ML, Soler G, Modolell M (1994) Determination of arginase activity in macrophages: a micromethod. J Immunol Methods 174:231\u2013235. https:\/\/doi.org\/10.1016\/0022-1759(94)90027-2","journal-title":"J Immunol Methods"},{"key":"827_CR19","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.molimm.2018.01.016","volume":"95","author":"RA Costa","year":"2018","unstructured":"Costa RA, Power DM (2018) Skin and scale regeneration after mechanical damage in a teleost. Mol Immunol 95:73\u201382. https:\/\/doi.org\/10.1016\/j.molimm.2018.01.016","journal-title":"Mol Immunol"},{"key":"827_CR20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0119751","volume":"10","author":"E Derlindati","year":"2015","unstructured":"Derlindati E, Cas AD, Montanini B et al (2015) Transcriptomic analysis of human polarized macrophages: more than one role of alternative activation? PLoS One 10:1\u201317. https:\/\/doi.org\/10.1371\/journal.pone.0119751","journal-title":"PLoS One"},{"key":"827_CR21","doi-asserted-by":"publisher","first-page":"2749","DOI":"10.1210\/en.2008-1569","volume":"150","author":"E Emmerson","year":"2009","unstructured":"Emmerson E, Campbell L, Ashcroft GS, Hardman MJ (2009) Unique and synergistic roles for 17\u03b2-estradiol and macrophage migration inhibitory factor during cutaneous wound closure are cell type specific. Endocrinology 150:2749\u20132757. https:\/\/doi.org\/10.1210\/en.2008-1569","journal-title":"Endocrinology"},{"key":"827_CR22","doi-asserted-by":"publisher","first-page":"1051","DOI":"10.1016\/j.fsi.2012.02.028","volume":"32","author":"A Falco","year":"2012","unstructured":"Falco A, Frost P, Miest J, Pionnier N, Irnazarow I, Hoole D (2012) Reduced inflammatory response to Aeromonas salmonicida infection in common carp (Cyprinus carpio L.) fed with \u03b2-glucan supplements. Fish Shellfish Immunol 32:1051\u20131057. https:\/\/doi.org\/10.1016\/j.fsi.2012.02.028","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR23","doi-asserted-by":"publisher","first-page":"2957","DOI":"10.1128\/mcb.25.8.2957-2968.2005","volume":"25","author":"S Ghisletti","year":"2005","unstructured":"Ghisletti S, Meda C, Maggi A, Vegeto E (2005) 17\u03b2-Estradiol inhibits inflammatory gene expression by controlling NF-kB intracellular localization. Mol Cell Biol 25:2957\u20132968. https:\/\/doi.org\/10.1128\/mcb.25.8.2957-2968.2005","journal-title":"Mol Cell Biol"},{"key":"827_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41536-017-0027-y","volume":"2","author":"JW Godwin","year":"2017","unstructured":"Godwin JW, Debuque R, Salimova E, Rosenthal NA (2017) Heart regeneration in the salamander relies on macrophage-mediated control of fibroblast activation and the extracellular landscape. NPJ Regen Med 2:1\u201311. https:\/\/doi.org\/10.1038\/s41536-017-0027-y","journal-title":"NPJ Regen Med"},{"key":"827_CR25","first-page":"137","volume":"44","author":"P Gruca","year":"1996","unstructured":"Gruca P, Chadzinska M, Lackowska B, Plytycz B (1996) Analysis of peritoneal and head kidney phagocytes during Thioglycollate-elicited peritoneal inflammation in the goldfish, Carassius auratus. Folia Biol (Praha) 44:137\u2013142","journal-title":"Folia Biol (Praha)"},{"key":"827_CR26","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1577\/1548-8659(1975)104<342:UOAFTP>2.0.CO;2","volume":"104","author":"RD Guerrero","year":"1975","unstructured":"Guerrero RD (1975) Use of androgens for the production of all-male Tilapia aurea (Steindachner). Trans Am Fish Soc 104:342\u2013348. https:\/\/doi.org\/10.1577\/1548-8659(1975)104<342:UOAFTP>2.0.CO;2","journal-title":"Trans Am Fish Soc"},{"key":"827_CR27","doi-asserted-by":"publisher","first-page":"2968","DOI":"10.1210\/en.2003-0806","volume":"145","author":"MB Hawkins","year":"2004","unstructured":"Hawkins MB, Thomas P (2004) The unusual binding properties of the third distinct teleost estrogen receptor subtype ER\u03b2a are accompanied by highly conserved amino acid changes in the ligand binding domain. Endocrinology 145:2968\u20132977. https:\/\/doi.org\/10.1210\/en.2003-0806","journal-title":"Endocrinology"},{"key":"827_CR28","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1016\/j.dci.2016.08.014","volume":"67","author":"JW Hodgkinson","year":"2017","unstructured":"Hodgkinson JW, Fibke C, Belosevic M (2017) Recombinant IL-4\/13A and IL-4\/13B induce arginase activity and down-regulate nitric oxide response of primary goldfish (Carassius auratus L.) macrophages. Dev Comp Immunol 67:377\u2013384. https:\/\/doi.org\/10.1016\/j.dci.2016.08.014","journal-title":"Dev Comp Immunol"},{"key":"827_CR29","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.mce.2010.01.002","volume":"319","author":"A Holm","year":"2010","unstructured":"Holm A, Andersson KE, Nordstr\u00f6m I, Hellstrand P, Nilsson BO (2010) Down-regulation of endothelial cell estrogen receptor expression by the inflammation promoter LPS. Mol Cell Endocrinol 319:8\u201313. https:\/\/doi.org\/10.1016\/j.mce.2010.01.002","journal-title":"Mol Cell Endocrinol"},{"key":"827_CR30","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1016\/j.devcel.2017.11.010","volume":"43","author":"SP Hui","year":"2017","unstructured":"Hui SP, Sheng DZ, Sugimoto K, Gonzalez-Rajal A, Nakagawa S, Hesselson D, Kikuchi K (2017) Zebrafish regulatory T cells mediate organ-specific regenerative programs. Dev Cell 43:659\u2013672. https:\/\/doi.org\/10.1016\/j.devcel.2017.11.010","journal-title":"Dev Cell"},{"key":"827_CR31","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1007\/s10126-013-9513-4","volume":"15","author":"A Ibarz","year":"2013","unstructured":"Ibarz A, Pinto PIS, Power DM (2013) Proteomic approach to skin regeneration in a marine teleost: modulation by oestradiol-17\u03b2. Mar Biotechnol 15:629\u2013646. https:\/\/doi.org\/10.1007\/s10126-013-9513-4","journal-title":"Mar Biotechnol"},{"key":"827_CR32","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1016\/j.fsi.2014.06.021","volume":"40","author":"LR Iwanowicz","year":"2014","unstructured":"Iwanowicz LR, Stafford JL, Pati\u00f1o R, Bengten E, Miller NW, Blazer VS (2014) Channel catfish (Ictalurus punctatus) leukocytes express estrogen receptor isoforms ER\u03b1 and ER\u03b22 and are functionally modulated by estrogens. Fish Shellfish Immunol 40:109\u2013119. https:\/\/doi.org\/10.1016\/j.fsi.2014.06.021","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR33","doi-asserted-by":"publisher","first-page":"1390","DOI":"10.1016\/j.cub.2007.07.019","volume":"17","author":"A Ja\u017awi\u0144ska","year":"2007","unstructured":"Ja\u017awi\u0144ska A, Badakov R, Keating MT (2007) Activin-\u03b2A signaling is required for zebrafish fin regeneration. Curr Biol 17:1390\u20131395. https:\/\/doi.org\/10.1016\/j.cub.2007.07.019","journal-title":"Curr Biol"},{"key":"827_CR34","doi-asserted-by":"publisher","first-page":"1116","DOI":"10.1016\/j.molimm.2005.07.022","volume":"43","author":"M Joerink","year":"2006","unstructured":"Joerink M, Savelkoul HFJ, Wiegertjes GF (2006) Evolutionary conservation of alternative activation of macrophages: structural and functional characterization of arginase 1 and 2 in carp (Cyprinus carpio L.). Mol Immunol 43:1116\u20131128. https:\/\/doi.org\/10.1016\/j.molimm.2005.07.022","journal-title":"Mol Immunol"},{"key":"827_CR35","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1002\/jat.1707","volume":"33","author":"Y Katsu","year":"2013","unstructured":"Katsu Y, Lange A, Miyagawa S, Urushitani H, Tatarazako N, Kawashima Y, Tyler CR, Iguchi T (2013) Cloning, expression and functional characterization of carp, Cyprinus carpio , estrogen receptors and their differential activations by estrogens. J Appl Toxicol 33:41\u201349. https:\/\/doi.org\/10.1002\/jat.1707","journal-title":"J Appl Toxicol"},{"key":"827_CR36","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1016\/j.ygcen.2015.01.002","volume":"212","author":"A Krasnov","year":"2015","unstructured":"Krasnov A, Wesmajervi Breiland MS, Hatlen B, Afanasyev S, Skugor S (2015) Sexual maturation and administration of 17\u03b2-estradiol and testosterone induce complex gene expression changes in skin and increase resistance of Atlantic salmon to ectoparasite salmon louse. Gen Comp Endocrinol 212:34\u201343. https:\/\/doi.org\/10.1016\/j.ygcen.2015.01.002","journal-title":"Gen Comp Endocrinol"},{"key":"827_CR37","doi-asserted-by":"publisher","first-page":"3149","DOI":"10.1007\/s00018-011-0778-3","volume":"68","author":"LF Lau","year":"2011","unstructured":"Lau LF (2011) CCN1\/CYR61: the very model of a modern matricellular protein. Cell Mol Life Sci 68:3149\u20133163. https:\/\/doi.org\/10.1007\/s00018-011-0778-3","journal-title":"Cell Mol Life Sci"},{"key":"827_CR38","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1006\/gcen.2000.7593","volume":"121","author":"WY Law","year":"2001","unstructured":"Law WY, Chen WH, Song YL, Dufour S, Chang CF (2001) Differential in vitro suppressive effects of steroids on leukocyte phagocytosis in two teleosts, tilapia and common carp. Gen Comp Endocrinol 121:163\u2013172. https:\/\/doi.org\/10.1006\/gcen.2000.7593","journal-title":"Gen Comp Endocrinol"},{"key":"827_CR39","doi-asserted-by":"publisher","first-page":"2136","DOI":"10.1242\/dev.121160","volume":"142","author":"DC LeBert","year":"2015","unstructured":"LeBert DC, Squirrell JM, Rindy J et al (2015) Matrix metalloproteinase 9 modulates collagen matrices and wound repair. Dev 142:2136\u20132146. https:\/\/doi.org\/10.1242\/dev.121160","journal-title":"Dev"},{"key":"827_CR40","doi-asserted-by":"publisher","first-page":"1917","DOI":"10.1016\/j.molimm.2011.05.019","volume":"48","author":"S Liarte","year":"2011","unstructured":"Liarte S, Cabas I, Chaves-Pozo E, Arizcun M, Meseguer J, Mulero V, Garc\u00eda-Ayala A (2011a) Natural and synthetic estrogens modulate the inflammatory response in the gilthead seabream (Sparus aurata L.) through the activation of endothelial cells. Mol Immunol 48:1917\u20131925. https:\/\/doi.org\/10.1016\/j.molimm.2011.05.019","journal-title":"Mol Immunol"},{"key":"827_CR41","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1016\/j.dci.2010.07.007","volume":"35","author":"S Liarte","year":"2011","unstructured":"Liarte S, Chaves-Pozo E, Abell\u00e1n E, Meseguer J, Mulero V, Garc\u00eda-Ayala A (2011b) 17\u03b2-Estradiol regulates gilthead seabream professional phagocyte responses through macrophage activation. Dev Comp Immunol 35:19\u201327. https:\/\/doi.org\/10.1016\/j.dci.2010.07.007","journal-title":"Dev Comp Immunol"},{"key":"827_CR42","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.dci.2015.06.008","volume":"53","author":"A L\u00f3pez-Mu\u00f1oz","year":"2015","unstructured":"L\u00f3pez-Mu\u00f1oz A, Liarte S, G\u00f3mez-Gonz\u00e1lez NE, Cabas I, Meseguer J, Garc\u00eda-Ayala A, Mulero V (2015) Estrogen receptor 2b deficiency impairs the antiviral response of zebrafish. Dev Comp Immunol 53:55\u201362. https:\/\/doi.org\/10.1016\/j.dci.2015.06.008","journal-title":"Dev Comp Immunol"},{"key":"827_CR43","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.fsi.2019.08.064","volume":"94","author":"M Maciuszek","year":"2019","unstructured":"Maciuszek M, Rydz L, \u015awitakowska I, Verburg-van Kemenade BML, Chadzi\u0144ska M (2019) Effects of stress and cortisol on the polarization of carp macrophages. Fish Shellfish Immunol 94:27\u201337. https:\/\/doi.org\/10.1016\/j.fsi.2019.08.064","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR44","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.fsi.2004.09.006","volume":"20","author":"B Magnad\u00f3ttir","year":"2006","unstructured":"Magnad\u00f3ttir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137\u2013151. https:\/\/doi.org\/10.1016\/j.fsi.2004.09.006","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR45","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1016\/j.fsi.2018.06.002","volume":"80","author":"K Mao","year":"2018","unstructured":"Mao K, Chen W, Mu Y, Ao J, Chen X (2018) Identification of two IL-4\/13 homologues in large yellow croaker (Larimichthys crocea) revealed their similar roles in inducing alternative activation of monocytes\/macrophages. Fish Shellfish Immunol 80:180\u2013190. https:\/\/doi.org\/10.1016\/j.fsi.2018.06.002","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR46","doi-asserted-by":"publisher","first-page":"13","DOI":"10.12703\/P6-13","volume":"6","author":"FO Martinez","year":"2014","unstructured":"Martinez FO, Gordon S (2014) The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6:13. https:\/\/doi.org\/10.12703\/P6-13","journal-title":"F1000Prime Rep"},{"key":"827_CR47","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1124\/mi.3.5.281","volume":"3","author":"J Matthews","year":"2003","unstructured":"Matthews J, Gustafsson JA (2003) Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol Interv 3:281\u2013292. https:\/\/doi.org\/10.1124\/mi.3.5.281","journal-title":"Mol Interv"},{"key":"827_CR48","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1016\/j.fsi.2016.06.044","volume":"55","author":"J Montero","year":"2016","unstructured":"Montero J, G\u00f3mez-Abell\u00e1n V, Arizcun M, Mulero V, Sepulcre MP (2016) Prostaglandin E2 promotes M2 polarization of macrophages via a cAMP\/CREB signaling pathway and deactivates granulocytes in teleost fish. Fish Shellfish Immunol 55:632\u2013641. https:\/\/doi.org\/10.1016\/j.fsi.2016.06.044","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR49","doi-asserted-by":"publisher","first-page":"6787","DOI":"10.4049\/jimmunol.177.10.6787","volume":"177","author":"K Ogawa","year":"2006","unstructured":"Ogawa K, Funaba M, Chen Y, Tsujimoto M (2006) Activin a functions as a Th2 cytokine in the promotion of the alternative activation of macrophages. J Immunol 177:6787\u20136794. https:\/\/doi.org\/10.4049\/jimmunol.177.10.6787","journal-title":"J Immunol"},{"key":"827_CR50","doi-asserted-by":"publisher","first-page":"713","DOI":"10.1016\/j.fsi.2018.11.078","volume":"86","author":"M Paiola","year":"2019","unstructured":"Paiola M, Moreira C, Duflot A, Knigge T, Monsinjon T (2019) Oestrogen differentially modulates lymphoid and myeloid cells of the European sea bass in vitro by specifically regulating their redox biology. Fish Shellfish Immunol 86:713\u2013723. https:\/\/doi.org\/10.1016\/j.fsi.2018.11.078","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR51","doi-asserted-by":"publisher","first-page":"45e","DOI":"10.1093\/nar\/29.9.e45","volume":"29","author":"MW Pfaffl","year":"2001","unstructured":"Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45e. https:\/\/doi.org\/10.1093\/nar\/29.9.e45","journal-title":"Nucleic Acids Res"},{"key":"827_CR52","doi-asserted-by":"publisher","first-page":"6284","DOI":"10.4049\/jimmunol.179.9.6284","volume":"179","author":"PA Pioli","year":"2007","unstructured":"Pioli PA, Jensen AL, Weaver LK, Amiel E, Shen Z, Shen L, Wira CR, Guyre PM (2007) Estradiol attenuates lipopolysaccharide-induced CXC chemokine ligand 8 production by human peripheral blood monocytes. J Immunol 179:6284\u20136290. https:\/\/doi.org\/10.4049\/jimmunol.179.9.6284","journal-title":"J Immunol"},{"key":"827_CR53","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1016\/j.fsi.2018.11.038","volume":"86","author":"S Rastgar","year":"2019","unstructured":"Rastgar S, Movahedinia A, Salamat N, Salati AP, Zabihi E (2019) Interruption of immune responses in primary macrophages exposed to nonylphenol provides insights into the role of ER and NF-KB in immunotoxicity of Persian sturgeon. Fish Shellfish Immunol 86:125\u2013134. https:\/\/doi.org\/10.1016\/j.fsi.2018.11.038","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR54","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fimmu.2014.00532","volume":"5","author":"M Rath","year":"2014","unstructured":"Rath M, M\u00fcller I, Kropf P et al (2014) Metabolism via arginase or nitric oxide synthase: two competing arginine pathways in macrophages. Front Immunol 5:1\u201310. https:\/\/doi.org\/10.3389\/fimmu.2014.00532","journal-title":"Front Immunol"},{"key":"827_CR55","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1016\/j.fsi.2009.03.023","volume":"26","author":"LS Robertson","year":"2009","unstructured":"Robertson LS, Iwanowicz LR, Marranca JM (2009) Identification of centrarchid hepcidins and evidence that 17\u03b2-estradiol disrupts constitutive expression of hepcidin-1 and inducible expression of hepcidin-2 in largemouth bass (Micropterus salmoides). Fish Shellfish Immunol 26:898\u2013907. https:\/\/doi.org\/10.1016\/j.fsi.2009.03.023","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR56","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1111\/j.1524-475X.2008.00440.x","volume":"17","author":"CE Routley","year":"2009","unstructured":"Routley CE, Ashcroft GS (2009) Effect of estrogen and progesterone on macrophage activation during wound healing. Wound Repair Regen 17:42\u201350. https:\/\/doi.org\/10.1111\/j.1524-475X.2008.00440.x","journal-title":"Wound Repair Regen"},{"key":"827_CR57","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.marenvres.2013.03.003","volume":"87\u201388","author":"F Seemann","year":"2013","unstructured":"Seemann F, Knigge T, Rocher B, Minier C, Monsinjon T (2013) 17\u03b2-estradiol induces changes in cytokine levels in head kidney and blood of juvenile sea bass (Dicentrarchus labrax, L., 1758). Mar Environ Res 87\u201388:44\u201351. https:\/\/doi.org\/10.1016\/j.marenvres.2013.03.003","journal-title":"Mar Environ Res"},{"key":"827_CR58","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1016\/j.cbpc.2011.11.006","volume":"155","author":"LK Shelley","year":"2012","unstructured":"Shelley LK, Ross PS, Kennedy CJ (2012) The effects of an in vitro exposure to 17\u03b2-estradiol and nonylphenol on rainbow trout (Oncorhynchus mykiss) peripheral blood leukocytes. Comp Biochem Physiol - C Toxicol Pharmacol 155:440\u2013446. https:\/\/doi.org\/10.1016\/j.cbpc.2011.11.006","journal-title":"Comp Biochem Physiol - C Toxicol Pharmacol"},{"key":"827_CR59","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.ygcen.2012.09.014","volume":"180","author":"LK Shelley","year":"2013","unstructured":"Shelley LK, Osachoff HL, van Aggelen GC, Ross PS, Kennedy CJ (2013) Alteration of immune function endpoints and differential expression of estrogen receptor isoforms in leukocytes from 17\u03b2-estradiol exposed rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 180:24\u201332. https:\/\/doi.org\/10.1016\/j.ygcen.2012.09.014","journal-title":"Gen Comp Endocrinol"},{"key":"827_CR60","doi-asserted-by":"publisher","first-page":"659","DOI":"10.1002\/glia.20644","volume":"56","author":"A Sierra","year":"2008","unstructured":"Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K (2008) Steroid hormone receptor expression and function in microglia. Glia 56:659\u2013674. https:\/\/doi.org\/10.1002\/glia.20644","journal-title":"Glia"},{"key":"827_CR61","doi-asserted-by":"publisher","first-page":"6391","DOI":"10.4049\/jimmunol.174.10.6391","volume":"174","author":"G Soucy","year":"2005","unstructured":"Soucy G, Boivin G, Labrie F, Rivest S (2005) Estradiol is required for a proper immune response to bacterial and viral pathogens in the female brain. J Immunol 174:6391\u20136398. https:\/\/doi.org\/10.4049\/jimmunol.174.10.6391","journal-title":"J Immunol"},{"key":"827_CR62","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.dci.2016.04.003","volume":"66","author":"E Szwejser","year":"2017","unstructured":"Szwejser E, Maciuszek M, Casanova-Nakayama A, Segner H, Verburg-van Kemenade BML, Chadzinska M (2017a) A role for multiple estrogen receptors in immune regulation of common carp. Dev Comp Immunol 66:61\u201372. https:\/\/doi.org\/10.1016\/j.dci.2016.04.003","journal-title":"Dev Comp Immunol"},{"key":"827_CR63","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1016\/j.fsi.2017.07.011","volume":"68","author":"E Szwejser","year":"2017","unstructured":"Szwejser E, Pijanowski L, Maciuszek M, Ptak A, Wartalski K, Duda M, Segner H, Verburg-van Kemenade BML, Chadzinska M (2017b) Stress differentially affects the systemic and leukocyte estrogen network in common carp. Fish Shellfish Immunol 68:190\u2013201. https:\/\/doi.org\/10.1016\/j.fsi.2017.07.011","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR64","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.yhbeh.2016.10.007","volume":"88","author":"E Szwejser","year":"2017","unstructured":"Szwejser E, Verburg-van Kemenade BML, Maciuszek M, Chadzinska M (2017c) Estrogen-dependent seasonal adaptations in the immune response of fish. Horm Behav 88:15\u201324. https:\/\/doi.org\/10.1016\/j.yhbeh.2016.10.007","journal-title":"Horm Behav"},{"key":"827_CR65","doi-asserted-by":"publisher","first-page":"1722","DOI":"10.1897\/08-642.1","volume":"28","author":"H Thilagam","year":"2009","unstructured":"Thilagam H, Gopalakrishnan S, Bo J, Wang KJ (2009) Effect of 17\u03b2-estradiol on the immunocompetence of Japanese sea bass (Lateolabrax japonicus). Environ Toxicol Chem 28:1722\u20131731. https:\/\/doi.org\/10.1897\/08-642.1","journal-title":"Environ Toxicol Chem"},{"key":"827_CR66","doi-asserted-by":"publisher","first-page":"741","DOI":"10.1016\/j.dci.2011.11.011","volume":"36","author":"LM van der Aa","year":"2012","unstructured":"van der Aa LM, Chadzinska M, Golbach LA, Ribeiro CMS, Lidy Verburg-van Kemenade BM (2012) Pro-inflammatory functions of carp CXCL8-like and CXCb chemokines. Dev Comp Immunol 36:741\u2013750. https:\/\/doi.org\/10.1016\/j.dci.2011.11.011","journal-title":"Dev Comp Immunol"},{"key":"827_CR67","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.jsbmb.2004.02.004","volume":"91","author":"E Vegeto","year":"2004","unstructured":"Vegeto E, Ghisletti S, Meda C, Etteri S, Belcredito S, Maggi A (2004) Regulation of the lipopolysaccharide signal transduction pathway by 17\u03b2-estradiol in macrophage cells. J Steroid Biochem Mol Biol 91:59\u201366. https:\/\/doi.org\/10.1016\/j.jsbmb.2004.02.004","journal-title":"J Steroid Biochem Mol Biol"},{"key":"827_CR68","first-page":"143158","volume":"187","author":"BML Verburg-van Kemenade","year":"1994","unstructured":"Verburg-van Kemenade BML, Groeneveld A, van Rens BTTM, Rombout JHWM (1994) Characterization of macrophages and neutrophilic granulocytes from the pronephros of carp (Cyprinus carpio). J Exp Biol 187:143158 http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/9317515","journal-title":"J Exp Biol"},{"key":"827_CR69","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.dci.2016.05.015","volume":"66","author":"BML Verburg-van Kemenade","year":"2017","unstructured":"Verburg-van Kemenade BML, Cohen N, Chadzinska M (2017) Neuroendocrine-immune interaction: evolutionarily conserved mechanisms that maintain allostasis in an ever-changing environment. Dev Comp Immunol 66:2\u201323. https:\/\/doi.org\/10.1016\/j.dci.2016.05.015","journal-title":"Dev Comp Immunol"},{"key":"827_CR70","doi-asserted-by":"publisher","first-page":"15224","DOI":"10.1038\/srep15224","volume":"5","author":"A Villa","year":"2015","unstructured":"Villa A, Rizzi N, Vegeto E, Ciana P, Maggi A (2015) Estrogen accelerates the resolution of inflammation in macrophagic cells. Sci Rep 5:15224. https:\/\/doi.org\/10.1038\/srep15224","journal-title":"Sci Rep"},{"key":"827_CR71","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1016\/0145-305x(94)90003-5","volume":"18","author":"R Wang","year":"1994","unstructured":"Wang R, Belosevic M (1994) Estradiol increases susceptibility of goldfish to Trypanosoma danilewskyi. Dev Comp Immunol 18:377\u2013387. https:\/\/doi.org\/10.1016\/0145-305x(94)90003-5","journal-title":"Dev Comp Immunol"},{"key":"827_CR72","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/0145-305x(95)00018-o","volume":"19","author":"R Wang","year":"1995","unstructured":"Wang R, Belosevic M (1995) The in vitro effects of estradiol and cortisol on the function of a long-term goldfish macrophage cell line. Dev Comp Immunol 19:327\u2013336. https:\/\/doi.org\/10.1016\/0145-305x(95)00018-o","journal-title":"Dev Comp Immunol"},{"key":"827_CR73","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1016\/S1532-0456(02)00100-X","volume":"132","author":"H Watanuki","year":"2002","unstructured":"Watanuki H, Yamaguchi T, Sakai M (2002) Suppression in function of phagocytic cells in common carp Cyprinus carpio L. injected with estradiol, progesterone or 11-ketotestosterone. Comp Biochem Physiol C Toxicol Pharmacol 132:407\u2013413. https:\/\/doi.org\/10.1016\/S1532-0456(02)00100-X","journal-title":"Comp Biochem Physiol C Toxicol Pharmacol"},{"key":"827_CR74","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1016\/j.fsi.2011.04.007","volume":"31","author":"M Wenger","year":"2011","unstructured":"Wenger M, Sattler U, Goldschmidt-Clermont E, Segner H (2011) 17Beta-estradiol affects the response of complement components and survival of rainbow trout (Oncorhynchus mykiss) challenged by bacterial infection. Fish Shellfish Immunol 31:90\u201397. https:\/\/doi.org\/10.1016\/j.fsi.2011.04.007","journal-title":"Fish Shellfish Immunol"},{"key":"827_CR75","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/S1532-0456(01)00176-4","volume":"129","author":"T Yamaguchi","year":"2001","unstructured":"Yamaguchi T, Watanuki H, Sakai M (2001) Effects of estradiol, progesterone and testosterone on the function of carp, Cyprinus carpio, phagocytes in vitro. Comp Biochem Physiol C Toxicol Pharmacol 129:49\u201355. https:\/\/doi.org\/10.1016\/S1532-0456(01)00176-4","journal-title":"Comp Biochem Physiol C Toxicol Pharmacol"},{"key":"827_CR76","doi-asserted-by":"publisher","first-page":"40140","DOI":"10.1074\/jbc.M112.348763","volume":"287","author":"W Yang","year":"2012","unstructured":"Yang W, Lu Y, Xu Y, Xu L, Zheng W, Wu Y, Li L, Shen P (2012) Estrogen represses hepatocellular carcinoma (HCC) growth via inhibiting alternative activation of tumor-associated macrophages (TAMs). J Biol Chem 287:40140\u201340149. https:\/\/doi.org\/10.1074\/jbc.M112.348763","journal-title":"J Biol Chem"},{"key":"827_CR77","doi-asserted-by":"publisher","first-page":"232","DOI":"10.1016\/S1001-0742(07)60038-2","volume":"19","author":"D Yin","year":"2007","unstructured":"Yin D, Hu S, Gu Y et al (2007) Immunotoxicity of bisphenol A to Carassius auratus lymphocytes and macrophages following in vitro exposure. J Environ Sci 19:232\u2013237. https:\/\/doi.org\/10.1016\/S1001-0742(07)60038-2","journal-title":"J Environ Sci"}],"container-title":["Fish Physiology and Biochemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10695-020-00827-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s10695-020-00827-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s10695-020-00827-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,6,9]],"date-time":"2021-06-09T00:03:53Z","timestamp":1623197033000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s10695-020-00827-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,9]]},"references-count":77,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2020,10]]}},"alternative-id":["827"],"URL":"https:\/\/doi.org\/10.1007\/s10695-020-00827-3","relation":{},"ISSN":["0920-1742","1573-5168"],"issn-type":[{"value":"0920-1742","type":"print"},{"value":"1573-5168","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,9]]},"assertion":[{"value":"12 February 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 May 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"9 June 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}