Advertisement

Immunogenetics

, Volume 55, Issue 5, pp 325–335 | Cite as

Characterisation, expression and promoter analysis of an interleukin 10 homologue in the puffer fish, Fugu rubripes

  • Jun Zou
  • Melody S. Clark
  • Chris J. SecombesEmail author
Original Paper

Abstract

Using computer-based tools, an interleukin (IL) 10 homologue has been identified from the puffer fish (Fugu rubripes) genome database. This is the first report on the existence of an IL-10 homologue in a non-mammalian vertebrate species. The Fugu IL-10 gene is located within a 2790-bp fragment including 549 bp of coding sequence which translates into an 183-amino-acid protein. It is predicted to contain five exons and four introns, sharing the same organization with the mammalian IL-10 genes. The size of the introns in the Fugu IL-10 gene is much smaller compared to mammalian IL-10 genes, whilst the size of the exons is similar. The deduced protein sequence shares 44–50% homology with the mammalian IL-10 sequences, 39–42% with the viral IL-10 sequences and 37–42% with other members of the IL-10 family, IL-20 and IL-22. Southern blot analysis indicates that a single copy of the IL-10 gene is present in the Fugu genome. A very low level of constitutive expression was detected in tissues of healthy fish including liver, kidney, gut and spinal cord, whilst no expression was detectable in spleen, gill, brain, gonad and eye. Analysis of the transcription regulation elements in the promoter region revealed that trans elements are located in the region between 1 bp and 721 bp, cis elements between 934 bp and 1114 bp and a tumour necrosis factor alpha responsive transcription element was located 92 bp upstream of the TATA box.

Keywords

Comparative immunology/evolution Cytokine Fish Gene regulation 

Notes

Acknowledgements

This work is supported by a grant from European Union (CT1999–00799). Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession number AJ539537.

References

  1. Aste-Amezaga M, Ma X, Sartori A, Trinchieri G (1998) Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J Immunol 160:5936–5944PubMedGoogle Scholar
  2. Bobe J, Goetz FW (2000) A tumor necrosis factor decoy receptor homologue is up-regulated in the brook trout (Salvelinus fontinalis) ovary at the completion of ovulation. Biol Reprod 62:420–426PubMedGoogle Scholar
  3. Bogdan C, Vodovotz Y, Nathan C (1991) Macrophage deactivation by interleukin 10. J Exp Med 174:1549–1555PubMedGoogle Scholar
  4. Collet B, Secombes CJ (2001) The rainbow trout (Oncorhynchus mykiss) Mx1 promoter. Structural and functional characterization. Eur J Biochem 268:1577–1584PubMedGoogle Scholar
  5. de Waal MR, Yssel H, de Vries JE (1993) Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J Immunol 150:4754–4765PubMedGoogle Scholar
  6. Eskdale J, Keijsers V, Huizinga T, Gallagher G (1999) Microsatellite alleles and single nucleotide polymorphisms (SNP) combine to form four major haplotype families at the human interleukin-10 (IL-10) locus. Genes Immunol 1(2):151–155CrossRefGoogle Scholar
  7. Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565PubMedGoogle Scholar
  8. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A (1991) IL-10 inhibits cytokine production by activated macrophages. J Immunol 147:3815–3822PubMedGoogle Scholar
  9. Gazzinelli RT, Oswald IP, James SL, Sher A (1992) IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J Immunol 148:1792–1796PubMedGoogle Scholar
  10. Gesser B, Leffers H, Jinquan T, Vestergaard C, Kirstein N, Sindet-Pedersen S, Jensen SL, Thestrup-Pedersen K, Larsen CG (1997) Identification of functional domains on human interleukin 10. Proc Natl Acad Sci USA 94:14620–14625CrossRefPubMedGoogle Scholar
  11. Groux H, Bigler M, de Vries JE, Roncarolo MG (1998) Inhibitory and stimulatory effects of IL-10 on human CD8+ T cells. J Immunol 160:3188–3193PubMedGoogle Scholar
  12. Hash SM, Brown WC, Rice-Ficht AC (1994) Characterization of a cDNA encoding bovine interleukin 10: kinetics of expression in bovine lymphocytes. Gene 139:257–261CrossRefPubMedGoogle Scholar
  13. Hirono I, Nam BH, Kurobe T, Aoki T (2000) Molecular cloning, characterization, and expression of TNF cDNA and gene from Japanese flounder Paralychthys olivaceus. J Immunol 165:4423–4427PubMedGoogle Scholar
  14. 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-1 beta. Vet Immunol Immunopathol 81:1–14CrossRefPubMedGoogle Scholar
  15. Howell WM, Turner SJ, Bateman AC, Theaker JM (2001) IL-10 promoter polymorphisms influence tumour development in cutaneous malignant melanoma. Genes Immunol 2(1):25–31CrossRefGoogle Scholar
  16. Hsu DH, de Waal MR, Fiorentino DF, Dang MN, Vieira P, de Vries J, Spits H, Mosmann TR, Moore KW (1990) Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science 250:830–832PubMedGoogle Scholar
  17. Huang JY, Brutlag DL (2001) The EMOTIF database. Nucleic Acids Res 29:202–204CrossRefPubMedGoogle Scholar
  18. Kotenko SV, Saccani S, Izotova LS, Mirochnitchenko OV, Pestka S (2000) Human cytomegalovirus harbors its own unique IL-10 homolog (cmvIL-10). Proc Natl Acad Sci USA 97:1695–1700PubMedGoogle Scholar
  19. Kube D, Platzer C, von Knethen A, Straub H, Bohlen H, Hafner M, Tesch H (1995) Isolation of the human interleukin 10 promoter. Characterization of the promoter activity in Burkitt's lymphoma cell lines. Cytokine 7:1–7CrossRefPubMedGoogle Scholar
  20. Laing KJ, Cunningham C, Secombes CJ (2000) Genes for three different isoforms of transforming growth factor-beta are present in plaice (Pleuronectes platessa) DNA. Fish Shellfish Immunol 10:261–271CrossRefPubMedGoogle Scholar
  21. Liu Y, Wei SH, Ho AS, de Waal MR, Moore KW (1994) Expression cloning and characterization of a human IL-10 receptor. J Immunol 152:1821–1829PubMedGoogle Scholar
  22. McFarlane SM, Pashmi G, Connell MC, Littlejohn AF, Tucker SJ, Vandenabeele P, MacEwan DJ (2002) Differential activation of nuclear factor-kappaB by tumour necrosis factor receptor subtypes. TNFR1 predominates whereas TNFR2 activates transcription poorly. FEBS Lett 515:119–126CrossRefPubMedGoogle Scholar
  23. Meisel C, Vogt K, Platzer C, Randow F, Liebenthal C, Volk HD (1996) Differential regulation of monocytic tumor necrosis factor-alpha and interleukin-10 expression. Eur J Immunol 26:1580–1586PubMedGoogle Scholar
  24. Mertz PM, DeWitt DL, Stetler-Stevenson WG, Wahl LM (1994) Interleukin 10 suppression of monocyte prostaglandin H synthase-2. Mechanism of inhibition of prostaglandin-dependent matrix metalloproteinase production. J Biol Chem 269:21322–21329PubMedGoogle Scholar
  25. Moore KW, de Waal RL Coffman RL, O'Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765Google Scholar
  26. Najakshin AM, Mechetina LV, Alabyev BY, Taranin AV (1999) Identification of an IL-8 homolog in lamprey (Lampetra fluviatilis): early evolutionary divergence of chemokines. Eur J Immunol 29:375–382CrossRefPubMedGoogle Scholar
  27. Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453PubMedGoogle Scholar
  28. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6Google Scholar
  29. Niiro H, Otsuka T, Kuga S, Nemoto Y, Abe M, Hara N, Nakano T, Ogo T, Niho Y (1994) IL-10 inhibits prostaglandin E2 production by lipopolysaccharide-stimulated monocytes. Int Immunol 6:661–664PubMedGoogle Scholar
  30. Prestridge DS (1995) Predicting Pol II promoter sequences using transcription factor binding sites. J Mol Biol 249:923–932PubMedGoogle Scholar
  31. Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res 23:4878–4884PubMedGoogle Scholar
  32. Reboul J, Gardiner K, Monneron D, Uze G, Lutfalla G (1999) Comparative genomic analysis of the interferon/interleukin-10 receptor gene cluster. Genome Res 9:242–250PubMedGoogle Scholar
  33. Sangrador-Vegas A, Martin SA, O'Dea PG, Smith TJ (2000) Cloning and characterization of the rainbow trout (Oncorhynchus mykiss) type II interleukin-1 receptor cDNA. Eur J Biochem 267:7031–7037CrossRefPubMedGoogle Scholar
  34. Schmitt C, Tonnelle C, Dalloul A, Chabannon C, Debre P, Rebollo A (2002) Aiolos and Ikaros: regulators of lymphocyte development, homeostasis and lymphoproliferation. Apoptosis 7:277–284CrossRefPubMedGoogle Scholar
  35. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedGoogle Scholar
  36. Vieira P, Waal-Malefyt R, Dang MN, Johnson 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 88:1172–1176PubMedGoogle Scholar
  37. Villinger F, Brar SS, Mayne A, Chikkala N, Ansari AA (1995) Comparative sequence analysis of cytokine genes from human and nonhuman primates. J Immunol 155:3946–3954PubMedGoogle Scholar
  38. Walter MR, Nagabhushan TL (1995) Crystal structure of interleukin 10 reveals an interferon gamma-like fold. Biochemistry 34:12118–12125PubMedGoogle Scholar
  39. Wang T, Secombes CJ (2001) Cloning and expression of a putative common cytokine receptor gamma chain (gammaC) gene in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 11:233–244CrossRefPubMedGoogle Scholar
  40. Wingender E, Chen X, Hehl R, Karas H, Liebich I, Matys V, Meinhardt T, Pruss M, Reuter I, Schacherer F (2000) TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res 28:316–319PubMedGoogle Scholar
  41. Wolf K, Quimby MC, Carlson CP (1969) Infectious pancreatic necrosis virus: lyophilization and subsequent stability in storage at 4 C. Appl Microbiol 17:623–624PubMedGoogle Scholar
  42. Zdanov A, Schalk-Hihi C, Wlodawer A (1996) Crystal structure of human interleukin-10 at 1.6 A resolution and a model of a complex with its soluble receptor. Protein Sci 5:1955–1962PubMedGoogle Scholar
  43. Zou J, Cunningham C, Secombes CJ (1999a) The rainbow trout Oncorhynchus mykiss interleukin-1 beta gene has a differ organization to mammals and undergoes incomplete splicing. Eur J Biochem 259:901–908CrossRefPubMedGoogle Scholar
  44. Zou J, Grabowski PS, Cunningham C, Secombes CJ (1999b) Molecular cloning of interleukin 1beta from rainbow trout Oncorhynchus mykiss reveals no evidence of an ice cut site. Cytokine 11:552–560CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Scottish Fish Immunology Research Centre, School of Biological Sciences, Zoology BuildingUniversity of AberdeenAberdeenUK
  2. 2.HGMP Resource CentreCambridgeUK

Personalised recommendations