Abstract
Biological activities of a putative mature sea bass interleukin-1β peptide, produced as a recombinant protein (rIL-1β) in Escherichia coli, have been investigated. The rIL-1β contains a 6-histidine tag at the N-terminus, and protein purification has been achieved through this tag by affinity chromatography. Biological activities have been investigated both at the cellular and gene expression levels. In in vitro assays sea bass rIL-1β induced the proliferation of murine D10.G4.1 cells and increased yeast phagocytosis by sea bass head kidney leukocytes. The purified cytokine was also tested in a lymphocyte-activation factor assay, where it induced the proliferation of sea bass thymocytes. Finally, in an in vivo assay, rIL-1β administered intraperitoneally increased expression levels of the IL-1β gene and activated macrophages to produce a cyclooxygenase 2 homologue (COX-2) gene in the head kidney.
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References
Auron PE (1998). The interleukin 1 receptor: ligand interactions and signal transduction. Cytokine Growth Factor Rev. 9:221–237
Benanni N, Schmid-Alliana A, Lafaurie M (1995). Evaluation of phagocytic activity in a teleost fish, Dicentrarchus labrax. Fish Shellfish Immunol. 5:237–246
Bird S, Wang T, Zou J, Cunningham C, Secombes CJ (2002). The first cytokine sequence within cartilaginous fish: IL-1β in the small spotted catshark (Scyliorhinus canicula). J. Immunol. 168:3329–3340
Blecha F, Reddy DN, Chitko-Mckown CG, Mcvey DS, Chengappa MM, Goodband RD, Nelssen JL (1995). Influence of recombinant bovine interleukin-1β and interleukin-2 in pigs vaccinated and challenged with Streptococcus suis. Vet. Immunol. Immunopathol. 44:329–346
Buonocore F, Frugnoli D, Falasca C, Secombes CJ, Scapigliati G (2003) Peculiar gene organisation and incomplete splicing of sea bass (Dicentrarchus labrax L.) interleukin 1β. Cytokine 21:257–264
Buonocore F, Mazzini M, Forlenza M, Randelli E, Secombes CJ, Zou J, Scapigliati G (2004) Expression in E. coli and purification of sea bass (Dicentrarchus labrax) interleukin-1β, a possible immuno-adjuvant in aquaculture. Marine Biotechnology 6:53–59
Buonocore F, Randelli E, Casani D, Mazzini M, Cappuccio I, Secombes CJ, Scapigliati G (2005) cDNA cloning and expression analysis of a cyclooxygenase2 from sea bass (Dicentrarchus labrax L.) after vaccination. Aquaculture 245, 301–310
Crampe M, Farley SR, Langston A, Pulsford AL (1997) Measurement of phagocytosis: a comparative evaluation of microscopic and microplate methods. In: Methodology in Fish Diseases Research. Aberdeen: Fisheries Research Services, pp. 81–89
Dalmau SR, Freitas CS, Savino W (1993). A modified assay for measuring thymocyte co-stimulatory activity. Mem Inst Oswaldo Cruz. 88:419–425
Debets R, Timans JC, Homey B, Zurawski S, Sana TR, Lo S, Wagner J, Edwards G, Clifford T, Menon S, Bazan JF, Kastelein RA (2001). Two novel IL-1 family members, IL-1δ′ and IL-1ε, function as an antagonist and agonist of NF-κB activation through the orphan IL-1 receptor-related protein 2. J. Immunol. 167:1440–1446
Dinarello CA (1996). Biologic basis for interleukin 1 in disease. Blood 87:2095–2147
Dinarello CA (1997) Interleukin 1. Cytokine Growth Factor Rev. 8:253–265
Engelsma MY, Stet RJM, Schipper H, Verburg-van Kememade BML (2001). Regulation of interleukin-1 beta RNA expression in the common carp, Cyprinus carpio L. Dev Comp Immunol 25:195–203
Fujiki K, Shin DH, Nakao M, Yano T (2000). Molecular cloning and expression analysis of carp (Cyprinus carpio) interleukin-1β high affinity immunoglobulin E Fc receptor (β subunit and serum amyloid A. Fish Shellfish Immunol. 10:229–242
Holland JW, Pottinger TG, Cunningham C, Secombes CJ (2000) Sequencing and expression analysis of the type 1 interleukin-1 receptor gene. EMBL accession number AJ295296
Holland JW, Pottinger TG, Secombes CJ (2002). Recombinant interleukin-1 beta activates the hypothalamic-pituitary-interrenal axis in rainbow trout, Oncorhynchus mykiss. J Endocrinol 175:261–267
Hong S, Zou J, Crampe M, Peddie S, Scapigliati G, Bols N, Cunningham C, Secombes CJ (2001). The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1β. Vet Immunol Immunopathol 81:1–14
Hong S, Peddie S, Campos-Perez J, Zou J, Secombes CJ (2003). The effect of intraperitoneally administered recombinant IL-1β on immune parameters and resistance to Aeromonas salmonicida in the rainbow trout (Oncorhynchus mykiss). Dev Comp Immun 27:801–812
Hong S, Zou J, Collet B, Bols NC, Secombes CJ (2004). Analysis and characterisation of IL-1β processing in rainbow trout, Oncorhynchus mykiss. Fish Shellfish Immunol 16:453–459
Horowitz JB, Kaye J, Conrad PJ, Katz ME, Janeway JR CA (1986). Autocrine growth inhibition of a cloned line of helper T cells. Proc Natl Acad Sci USA 83:1886–1890
Jarrous N, Kaempfer R (1994). Induction of human interleukin 1 gene expression by retinoic acid and its regulation at processing of precursor transcripts. Journ Biol Chem 269:23141–23149
Kullberg BJ, Van der Meer JWM (1995). Cytokines in the Treatment of Infectious Diseases: Options for the Modulation of the Host Defense. (Dordrecht, The Netherlands: Kluwer Academic Publishers)
Kupper T, Flood P, Coleman D, Horowitz M (1987). Growth of an interleukin 2/interleukin 4-dependent T cell line induced by granulocyte-macrophage colony-stimulating factor (GM-CSF). J. Immunol. 138:4288–4292
Mathew JA, Guo YX, Goh KP, Chan J, Verburg-Van Kemenade BML, Kwang J (2002). Characterisation of a monoclonal antibody to carp IL-1β and the development of a sensitive capture ELISA. Fish Shellfish Immunol. 13:85–95
Nicola NA (1994). Guidebook to Cytokines and Their Receptors. (Oxford, U.K.: Sambrook and Tooze)
Peddie S, Zou J, Cunningham C, Secombes CJ (2001). Rainbow trout (Oncorhynchus mykiss) recombinant IL-1β and derived peptide induce migration of head-kidney leucocytes in vitro. Fish Shellfish Immunol. 11:697–709
Pelegrin P, Garcia-Castillo J, Mulero V, Meseguer J (2001). Interleukin-1β isolated from a marine fish reveals up-regulated expression in macrophages following activation with lipopolysaccharide and lymphokines. Cytokine 16:67–72
Scapigliati G, Buonocore F, Bird S, Zou J, Pelegrin P, Falasco C, Frugnoli D, Secombes CJ (2001). Phylogeny of cytokines: molecular cloning and expression analysis of sea bass Dicentrarchus labrax interleukin-1 beta. Fish Shellfish Immunol. 11:711–726
Scapigliati G, Meloni S, Buonocore F, Bossù P, Prugnoli D, Secombes CJ (2003) Immunopurification of B lymphocytes from sea bass Dicentrarchus labrax (L.) Mar Biotechnol 5, 214–221
Scapigliati G, Costantini S, Colonna G, Facchiano A, Buonocore F, Bossù P, Cunningham C, Holland JW, Secombes CJ (2004). Modelling of fish interleukin-1 and its receptor. Dev Comp Immun 28:429–441
Sangrador-Vegas A, Martin SAM, O’Dea PG, Smith TJ (2000). Cloning and characterisation of the rainbow trout (Oncorhynchus mikyss) type II interleukin-1 receptor cDNA. Eur. J. Biochem. 267:7031–7037
Secombes CJ, Fletcher TC (1992). The role of phagocytes in the protective mechanisma of fish. Ann Rev Fish Des 2:53–71
Secombes CJ, Bird S, Cunningham C, Zou J (1999). Interleukin-1 in fish. Fish Shellfish Immunol. 9:335–343
Sims JE, Dower SK (1994). Interleukin-1 receptors. Eur Cytokine Netw 5:517–531
Smith DE, Renshaw BR, Ketchem RR, Kubin M, Garka KE, Sims JE (2000) Four new members expand the IL-1 superfamily. J Biol Chem 275:1169–1175
Smith KA, Lachman LB, Oppenheim JJ, Favata MM (1980). The functional relationship of the interleukins. J Exp Med 151:1551–1556
Solem ST, Jörgensen JB, Robertsen B (1995). Stimulation of respiratory burst and phagocytic activity in Atlantic salmon (Salmo salar L.) macrophages by lipopolysaccharide. Fish Shellfish Immunol 5:475–491
Subramaniam S, Stansberg C, Olsen L, Zou J, Secombes CJ, Cunningham C (2002). Cloning of a Salmo salar interleukin-1 receptor-like cDNA. Dev Comp Immunol 26:415–431
Tartakovsky B, Kovacs EJ, Takacs L, Durum SK (1986). T cell clone producing an IL1-like activity after stimulation by antigen-presenting B cells. J Immunol 137:160–166
Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD, Kostura MJ, Miller DK, Molineaux SM, Weidner JR, Aunins J (1992). A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356:768–774
Vega-Rubin de Celis S, Gomez P, Calduch-Giner JA, Medale F, Perez-Sanchez J (2003). Expression and characterization of European Sea Bass (Dicentrarchus labrax) somatolactin: assessment of in vivo metabolic effects. Mar Biotechnol 5:92–101
Warner SJC, Auger KR, Libby P (1987). Interleukin 1 induces interleukin 1, II. recombinant human interleukin 1 induces interleukin 1 production by adult human vascular endothelial cells. J Immun 139:1911–1917
Yin Z, Kwang J (2000). Carp interleukin 1β in the role of an immuno-adjuvant. Fish Shellfish Immunol 10:375–378
Zou J, Grabowski PS, Cunningham C, Secombes CJ. (1999). Molecular cloning of interleukin 1β from rainbow trout Oncorhynchus mykiss reveals no evidence of an ICE cut site. Cytokine 11:552–560
Zou J, Neumann NF, Holland JW, Belosevic M, Cunningham C, Secombes CJ, Rowley F (1999a). Fish macrophages express a cyclo-oxygenase-2 homologue after activation. Biochem. J. 340:153–159
Zou J, Holland J, Pleguezuelos O, Cunningham C, Secombes CJ (2000). Factors influencing the expression of interleukin-1β in rainbow trout. Dev. Comp. Immunol. 24:575–582
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Buonocore, F., Forlenza, M., Randelli, E. et al. Biological Activity of Sea Bass (Dicentrarchus labrax L.) Recombinant Interleukin-1β. Mar Biotechnol 7, 609–617 (2005). https://doi.org/10.1007/s10126-004-5131-5
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DOI: https://doi.org/10.1007/s10126-004-5131-5