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Cloning, Characterization and Expression Analysis of Interleukin-10 from the Zebrafish (Danio rerion)

  • Zhang, Dian-Chang (Aquaculture and Biotechnology Division, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Science) ;
  • Shao, Yan-Qing (Shanghai Fisheries University) ;
  • Huang, Yan-Qin (Shanghai Fisheries University) ;
  • Jiang, Shi-Gui (Aquaculture and Biotechnology Division, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Science)
  • Published : 2005.09.30

Abstract

Cytokines are proteins produced by many different cells of the immune system and play a significant role in initiating and regulating the inflammatory process. In this research, an important cytokine, interleukin-10 (IL-10) gene, has been identified and characterized from zebrafish (Danio rerio) genome database. Zebrafish IL-10 is located within a 2690 bp fragment and contains five exons and four introns, sharing the same organization with mammalian IL-10 genes. An open reading frame of 543 bp was found to encode a putative 180 amino acid protein with a signal peptide of 22 amino acids, which shares 29.7-80.9% homology with amino acid sequences of other known IL-10. The signature motif of IL-10 is also conserved in zebrafish IL-10. The predicted transcript was finally confirmed by sequencing of cDNA clones. Multi-tissue reverse transcriptase PCR (RT-PCR) was performed to examine the tissue distribution and expression regulation of this gene in seven organs of normal and lipopolysaccharide (LPS) stimulation zebrafish. The results demonstrated that this gene was expressed slightly in normal kidney, gill and gut, no expression was detected in other four tissues. The expression was clearly upregulated after LPS stimulation. Using the ideal zebrafish model, further study of IL-10 characterization and function may provide insight on the understanding of the innate immune system.

Keywords

References

  1. Asadullah, K., Sterry, W. and Volk, H. D. (2003) Interleukin-10 therapy-review of a new approach. Pharmacol. Rev. 55, 241-269 https://doi.org/10.1124/pr.55.2.4
  2. Alexander, Z. (2004) Structural features of the interleukin-10 family of cytokines. Curr. Pharm. Des. 10, 3873-3884 https://doi.org/10.2174/1381612043382602
  3. Altmann, S. M., Mellon, M. T., Distel, D. L. and Kim, C. H. (2003) Molecular and functional analysis of an interferon gene from zebrafish, Danio rerio. J. Virol. 77, 1992-2002 https://doi.org/10.1128/JVI.77.3.1992-2002.2003
  4. Brown, C. Y., Lagnado, C. A., Vadas, M. A. and Goodall, G. J. (1996) Differential regulation of the stability of cytokine mRNAs in lipopolysaccharide-activated blood monocytes in respones to interleukin-10. J. Bio. Chem. 271, 20108-20112 https://doi.org/10.1074/jbc.271.33.20108
  5. Bendtsen, J. D., Nielsen, H., Heijne, G. V. and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783-795 https://doi.org/10.1016/j.jmb.2004.05.028
  6. David, C. W. (2003) Role of interleukin-10 in the induction and function of natural and antigen-induced regulatory T cells. J. Autoimmun. 20, 273-275 https://doi.org/10.1016/S0896-8411(03)00046-5
  7. de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G. and de Vries, J. E. (1991) Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by nonocyte. J. Exp. Med. 174, 1209-1220 https://doi.org/10.1084/jem.174.5.1209
  8. Ding, Y., Qin, L., Kotenko, S. V., Pestka, S. and Bromberg, J. S. (2000) A single amino acid determines the immunostimulatory activity of interleukin-10. J. Exp. Med. 191, 213-224 https://doi.org/10.1084/jem.191.2.213
  9. Dumoutier, L., Louahed, J. and Renauld, J. C. (2000) Cloning and characterization of IL-10-related T cell-derived inducible factor (IL-TIF), a novel cytokine structurally related to IL-10 and inducible by IL-19. J. immunol. 164, 1814-1819 https://doi.org/10.4049/jimmunol.164.4.1814
  10. Fiorentino, D. F., Bond, M. W. and Mosmann, T. R. (1989) Two types of mouse T-helper IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med. 170, 2081-2095 https://doi.org/10.1084/jem.170.6.2081
  11. Goodman, R. E., Oblak, J. and Bell, R. G. (1992) Synthesis and characterization of rat interleukin-10 (IL-10) cDNA clones from the RNA of cultured OX8-OX222-thoracic duct T cells. Bioche. Biophys. Res. Commun. 30, 1-7 https://doi.org/10.1016/0006-291X(68)90703-1
  12. Herve, G. and Francoise, C. (2003) The complex role of interleukin-10 in autoimmunity. J. Autoimmun. 20, 281-285 https://doi.org/10.1016/S0896-8411(03)00044-1
  13. John, J. H., Nayef, E. S. and Bared, S. G. (2003) Interleukin-10 and the regulation of mitogen-activated protein kinase: are these signaling modules targets for the anti-inflammatory action of this cytokine? Cell. Signal. 15, 255-267 https://doi.org/10.1016/S0898-6568(02)00075-X
  14. Higgins, D., Thompson J., Gibson, T., Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressivemultiple sequence alignment through sequence weighting,position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 https://doi.org/10.1093/nar/22.22.4673
  15. Kim, J. M., Brannan, C. I., Copeland, N. G., Jenkins, N. A., Khan, T. A. and Moore, K. W. (1992) Structure of the mouse IL-10 gene and chromosomal localization of the mouse and human genes. J. Immunol. 148, 3618-3623
  16. Kumar, S., Tamura, K. and Nei, M. (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5,150-163 https://doi.org/10.1093/bib/5.2.150
  17. Laing, K. J., Holland, J., Bonilla, S., Cunningham, C. and Secombes, C. J. (2001) Cloning and sequencing of caspase 6 in rainbow trout, Ohcorhynchus mykiss, and analysis of its expression under conditions known to induce apoptosis. Dev. Comp. Immunol. 25, 303-312 https://doi.org/10.1016/S0145-305X(00)00061-6
  18. Inoue, Y., Kamota, S., Ito, K., Yoshiura, Y., Ototake, M., Moritomo, T. and Nakanishi, T. (2005) Molecular cloning and expression analysis of rainbow trout (Oncorhynchus mykiss) interleukin-10 cDNAs. Fish shellfish Immunol. 18, 335-344 https://doi.org/10.1016/j.fsi.2004.08.004
  19. Moore, K. W., Viera, P., Fiorentino, D. F., Trounstine, M. L., Khan, T. A. and Mosmann, T. R. (1990) Homology of cytokine synthesis inhibitory factor (IL-10) to the Epstein-Barr virus gene BCRFI. Science 8, 1230-1234
  20. Moore, K. W., O'Garra, A., de Waal Malefyt, R., Vieira, P. and Mosmann, T. R. (1993) Interleukin-10. Annu. Rev. Immunol. 11, 165-190 https://doi.org/10.1146/annurev.iy.11.040193.001121
  21. Rousset, F., Garcia, E., Defrance, T., Peronne, C., Vezzio, N., Hsu, D. H., Kastelein, R., Moore, K. W. and Banchereau, J. (1992) Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc. Natl. Acad. Sci. USA 89, 1890-1893
  22. Rothwell, L., Young, J. R., Zoorob, R., Whittaker, C. A., Hesketh, P., Archer, A., Smith, A. L. and Kaiser, P. (2004) Cloning and characterization of chicken IL-10 and its role in the immune response to Eimeria maxima. J. Immunol. 173, 2675-2682 https://doi.org/10.4049/jimmunol.173.4.2675
  23. Savan, R., Igawa, D. and Sakai, M. (2003) Cloning, characterization and expression analysis of interleukin-10 from the common carp, Cyprinus carpio L. Eur. J. Biochem. 270, 4647-4654 https://doi.org/10.1046/j.1432-1033.2003.03854.x
  24. Shaw, G. and Kamen, R. (1986) A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659-667 https://doi.org/10.1016/0092-8674(86)90341-7
  25. Vieira, P., de Waal-Malefyt, R., Dang, M. N., Johnson, K. E., Kastelein, R., Fiorentino, D. F., de Vries, J. E., Roncarolo, M. G., Mosmann, T. R. and Moore, K. W. (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
  26. Walter, M. R. and Nagabhushan, T. L. (1995) Crystal structure of interleukin-10 reveals an interferon gamma-like fold. Biochemisty 34, 12118-12125 https://doi.org/10.1021/bi00038a004
  27. Zou, J., Clark, M. S. and Scombes, C. J. (2003) Characterization, expression and promoter analysis of an interleukin-10 homologue in the puffer fish, fugu rubripes. Immunogenetics 55, 325-335 https://doi.org/10.1007/s00251-003-0580-y
  28. Zdanov, A. (2004) Structural features of the interleukin-10 family of cytokines. Curr. Pharm. Des. 10, 3873-3884 https://doi.org/10.2174/1381612043382602

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