Abstract
Interleukin-10 (IL-10) is an anti-inflammatory cytokine and negatively regulates cell-mediated immunity (CMI) induction by inhibiting cytokine production in type 1 T helper cells. IL-10 genes have been isolated from several fish, and inflammatory cytokine inhibition by IL-10 has been well examined. However, a CMI regulator of IL-10 in fish has not yet been identified. In this study, we cloned the IL-10 gene in amberjack Seriola dumerili and analyzed its function using its recombinant protein (rIL-10). In an in vitro culture experiment, gene expression of inflammatory cytokines was suppressed in leukocytes incubated with rIL-10 compared with cells that only received Nocardia seriolae stimulation. This result suggests amberjack IL-10 has conserved function as an inflammatory cytokine inhibitor. Bactericidal activity of amberjack cells against intracellular pathogen stimulation was decreased in a rIL-10 dose-dependent manner. Furthermore, a significant reduction in the T-bet/GATA-3 ratio was observed in N. seriolae living cell (LC) + rIL-10-injected fish. Taken together, these results suggest amberjack rIL-10 suppresses CMI induction both in vitro and in vivo. In addition, the number of IgM+ cells among spleen leukocytes in N. seriolae + rIL-10-injected fish was higher than in only N. seriolae LC, suggesting that Th2-dominant immunity was induced by adding rIL-10.
Similar content being viewed by others
References
Bendtsen JD, Nielsen H, Heijne GV, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Berlato C, Cassatella MA, Kinjyo I, Gatto L, Yoshimura A, Bazzoni F (2002) Involvement of suppressor of cytokine signal-3 as a mediator of the inhibitory effects of IL-10 on lipopolysaccharide-induced macrophage activation. J. Immunol 168:6404–6411
Bouaziz J, Calbo S, Maho-Vaillant M, Saussine A, Bagot M, Bensussan A, Musette P (2010) IL-10 produced by activated human B cells regulates CD4+ T-cell activation in vitro. Eur J Immunol 40:2686–2691
Briere F, Servet-Delprat C, Bridon JM, Saint-Remy JM, Banchereau J (1994) Human interleukin 10 induces naïve surface immunoglobulin D + (sIgD +) B cells to secret IgG1 and IgG3. J Exp Med 179:757–762
D’andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G (1993) Interleukin 10 (IL-10) inhibits human lymphocyte interferon-γ production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178:1041–1048
Ding Y, Qin L, Kotenko SV, Pestka S, Bromberg JS (2000) A single amino acid determines the immunostimulatory activity of interleukin 10. J Exp Med 191:213–224
Ellis AE (1977) The leucocytes of fish: a review. J Fish Biol 11:453–491
Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170:2081–2095
Grayfer L, Belosevic M (2012) Identification and molecular characterization of the interleukin-10 receptor 1 of the zebrafish (Danio rerio) and the goldfish. Dev Comp Immunol 36:401–417
Grayfer L, Hodgkingson JW, Hitchen SJ, Belosevic M (2011) Characterization and functional analysis of goldfish (Carassius auratus L.) interleukin-10. Mol Immunol 48:563–571
Grewe M, Gyufko K, Krutmann J (1995) Interleukin-10 production by cultured human keratinocytes: regulation by ultraviolet B and ultraviolet Al radiation. J Invest Dermatol 104:3–6
Huang L, Gebreselassie NG, Gagliardo LF, Ruyechan MC, Lee NA, Lee JA, Appleton JA (2014) Eosinophil-derived IL-10 supports chronic nematode infection. J Immunol 193:4178–4187
Inoue Y, Mamota S, Ito K, Yoshiura Y, Ototake M, Moritomo T, Nakanishi T (2005) Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs. Fish Shellfish Immunol 18:335–344
Ito S, Ansari P, Sakatsume M, Dickensheets H, Vazquez N, Donnelly RP, Larmer AC, Finbllom DS (1999) Interleukin-10 inhibits expression of both interferon alpha- and interferon gamma-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93:1456–1463
Jeannin P, Lecoanet S, Deineste Y, Gauchat JF, Bonnefoy JY (1998) IgE versus IgG4 production can be differentially regulated by IL-10. J Immunol 160:3555–3561
Karan S, Dash P, Kaushik H, Sahoo PK, Garg LC, Dixit A (2016) Structural and functional characterization of recombinant interleukin-10 from Indian major carp Labeo rohita. J Immunol Res 2016:11
Kariya T, Kubota S, Nakamura Y, Kira K (1968) Nocardia infection in cultured yellowtails (Seriola quinqueradiata and S. purpursacens) I. Bacteriological study. Fish Pathol 3:16–23
Kato G, Kondo H, Aoki T, Hirono I (2012) Mycobacterium bovis BCG vaccine induces non-specific immune responses in Japanese flounder against Nocardia seriolae. Fish Shellfish Immunol 33:243–250
Kishore R, Krishnamurthy P, Garikipati VN, Benedict C, Nickoloff E, Khan M, Johnson J, Gumpert AM, Koch WJ, Verma SK (2015) Interleukin-10 inhibits chronic angiotensin II-induced pathological autophagy. J Mol Cell Cardiol 89:203–213
Kotenko SV, Izotova LS, Microchnitchenko OV, Esterova E, Dickensheets H, Donnelly RP, Pestka S (2001) Identification of the functional interleukin-22 (IL-22) receptor complex: the IL-10R2 chain (IL-10Rbeta) is a common chain of both the IL-10 and IL-22 (IL-10-related T cell-derived inducible factor, IL-TIF) receptor complexes. J Bio Chem 276:2725–2732
Kusuda R, Nakagawa A (1978) Nocardia Infection of cultured yellowtail. Fish Pathol 13:25–31
Larkin MA, Blackshield G, Brown NP, Chenna R, McGettingan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higging DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lund EF (2008) Cytokine-producing B lymphocytes—key regulators of immunity. Curr Opin Immunol 20:332–338
Matsumoto M, Hayashi K, Suetake H, Yamamoto A, Araki K (2016) Identification and functional characterization of multiple interleukin 12 in amberjack (Seriola dumerili). Fish Shellfish Immunol 55:281–292
Matsumoto M, Araki K, Hayashi K, Takeuchi Y, Shiozaki K, Suetake H, Yamamoto A (2017) Adjuvant effect of recombinant interleukin-12 in the nocardiosis formalin-killed vaccine of the amberjack Seriola dumerili. Fish Shellfish Immunol 67:263–269
Murray PJ, Wang L, Onufryk C, Tepper RI, Young RA (1997) T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J Immunol 158:315–321
Nakamura R, Sene A, Santeford A, Gdoura A, Kubota S, Zapata N, Apte RS (2015) IL-10 driven STAT3 signaling in senescent macrophages promotes pathological eye angiogenesis. Nat Commun 6:7847
Nawijn MC, Dingjan GM, Ferreira R, Lambrecht BN, Karis A, Grosveld F, Savelkoul H, Hendriks RW (2001) Enforced expression of GATA-3 in transgenic mice inhibits Th1 differentiation and induces the formation of a T1/ST2-expressing Th2-committed T cell compartment in vivo. J Immunol 167:724–732
Nayak SK, Shibasaki Y, Nakanishi T (2014) Immune response to live and inactivated Nocardia seriolae and protective effect of recombinant interferon gamma (rIFN-γ) against nocardiosis in ginbuna crucian carp, Carassius auratus langsdorfii. Fish Shellfish Immunol 39:354–364
O’Farrell AM, Liu Y, Moore KW, Mui AL (1998) IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat-3 dependent and independent pathways. EMBO J 17:1006–1018
Ohno S, Wolf U, Atkin NB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59:169–187
Piazzon MC, Savelkoul HS, Pietretti D, Wiegertjes GF, Forlenza M (2015a) Carp IL-10 has anti-inflammatory activities on phagocytes, promotes proliferation of memory T cells, and regulates B cell differentiation and antibody secretion. J Immunol 194:187–199
Piazzon MC, Wentzel AS, Tijhaar EJ, Rakus KL, Vanderplasschen A, Wiegertjes GF, Forlenza M (2015b) Cyprinid herpesvirus 3 IL-10 inhibits inflammatory activates of carp macrophages and promotes proliferation of IgM+ B cells and memory T cell in manner similar to carp IL-10. J Immunol 195:3694–3704
Piazzon MC, Wentzel AS, Wiegerties GF, Forlenza M (2017) Carp IL-10a and IL-10b exert identical biological activities in vitro, but are differentially regulated in vivo. Dev Comp Immunol 67:350–360
Pinto RD, Nascimento DS, Reis MI, do Vale A, Dos Santos NM (2007) Molecular characterization, 3D modeling and expression analysis of sea bass (Dicentrarchus labrax L.) interleukin-10. Mol Immunol 44:2056–2065
Sahoo BR, Swain B, Basu M, Panda P, Maiti NK, Samanata M (2012) 3D modeling and molecular dynamics stimulation of an immune-regulatory cytokine, interleukin-10, from the Indian major carp, Catla catla. J Mol Model 18:1713–1722
Savan R, Igawa D, Sakai M (2003) Cloning, characterization and expression analysis of interleukin-10 from the common carp, Cyprinus carpio L. Eur J Biochem 270:4647–4654
Seppola M, Larsen AN, Steiro K, Robertsen B, Jensen I (2008) Characterization and expression analysis of interleukin genes, IL-1beta, IL-8 and IL-10, in Atlantic cod (Gadus morhua L.). Mol Immunol 45:887–897
Sieg S, King C, Huang Y, Kaplan D (1996) The role of interleukin-10 in the inhibition of T-cell proliferation and apoptosis mediated by parainfluenza virus type 3. J Virol 70:4845–4848
Vieira P, de Waal-Malefyt R, Dang MN, Jhonson KE, Kastelein R, Fiorentino DF, deVries JE, Roncarolo MG, Mosmann TR, Moore KW (1991) Isolation and expression of human cytokine synthesis inhibitory factor cDNA clones: homology to Epstein-Barr virus open reading frame BCRFI. Proc Natl Acad Sci USA 88:1172–1176
Wang T, Secombes CJ (2013) The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 35:1703–1718
Weber-Nordt RM, Riley JK, Greenlund AC, Moore KW, Darmell JE, Schreiber RD (1996) Stat3 recruitment by two distinct ligand-induced, tyrosine-phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J Biol Chem 271:27954–27961
Wei H, Yang M, Zhao T, Wang X, Zhou H (2013) Functional expression and characterization of glass carp IL-10: an essential mediator of TGF-β1 immune regulator in peripheral blood lymphocytes. Mol Biol 53:313–320
Wei H, Yin L, Feng S, Wang X, Yang K, Zhang A, Zhou H (2015) Dual-parallel inhibition of IL-10 and TGF-β1 controls LPS-induced inflammatory response via NF-kB signaling in garass carp monocytes/macrophages. Fish Shellfish Immunol 44:445–452
Zdanov A, Schalk-Hihi C, Gustchina A, Tsang M, Weatherbee J, Wlodawer A (1995) Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon γ. Structure 3:591–601
Zhang DC, Shao YQ, Huang YQ, Jiang SG (2005) Cloning, characterization and expression analysis of interleukin-10 from the zebrafish (Danio rerion). J Biochem Mol Biol 38:571–576
Zou J, Clark MS, Secombes CJ (2003) Characterization, expression and promoter analysis of an interleukin 10 homologue in the puffer fish, Fugu rubripes. Immunogenetics 55:325–335
Acknowledgements
We thank Mr. Soetsu Yanagi and Mr. Yoshiaki Imaoka (Kagoshima Prefectural Fisheries Technology and Development Center, Japan) for assistance with fish maintenance. This work was supported by JSPS KAKENHI (Grant Nos. 25292129 and 25450305).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Matsumoto, M., Amer, M.T., Araki, K. et al. Amberjack Seriola dumerili interleukin-10 negatively suppresses host cell-mediated immunity. Fish Sci 84, 857–867 (2018). https://doi.org/10.1007/s12562-018-1223-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12562-018-1223-4