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Identification and expression analysis of interferon gamma genes in channel catfish

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Abstract

Multiple species of type I interferon (IFN) were recently identified in catfish (CF) (Ictalurus punctatus). Herein we extend these studies and report the existence of two distinct type II IFN genes in channel CF. As with zebrafish and the green spotted pufferfish, the two CF IFN-γ genes are dissimilar in sequence but closely linked on the same chromosome. One of the genes (IFN-γ2) encodes two distinct messages that likely arose via alternative splicing at two closely spaced splice donor sites within the first intron. Sequence analysis indicates that CF IFN-γ genes contain the hallmarks of authentic IFN-γ including: (1) a conserved nuclear localization site at the C terminus (CF IFN-γ2 only), (2) an IFN-γ signature sequence, (3) six putative helical regions within the mature protein, (4) one or more potential glycosylation sites, and (5) multiple mRNA instability motifs within the 3′ untranslated region. Moreover, well-characterized CF T and NK cell clones were shown to synthesize IFN-γ transcripts. This is the first unequivocal demonstration in any lower vertebrate species that NK and T cells synthesize IFN-γ and is consistent with results in mammalian systems where T cells and NK cells are the major sources of type II IFN production. Collectively, these studies indicate that Siluriformes possess two evolutionarily conserved IFN-γ genes and demonstrate that CF possess three key elements of the innate immune response: NK cells and types I and II IFN.

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References

  • Altmann SM, Mellon MT, Distel DL, Kim CH (2003) Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77:1992–2002

    Article  PubMed  CAS  Google Scholar 

  • Altschul S, Maden T, Schaffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bartlett NW, Buttigieg K, Kotenko SV, Smith GL (2005) Murine interferon lambdas (type III interferons) exhibit potent antiviral activity in vivo in a poxvirus infection model. J Gen Virol 86:1589–1596

    Article  PubMed  CAS  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunails S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  PubMed  CAS  Google Scholar 

  • Biron CA, Sen GC (2001) Interferons and other cytokines. In: DM Knipe, PM Howley (eds) Fundamental Virology, 4th edn. Lippincott, Philadelphia, pp 321–351

    Google Scholar 

  • Bowser P, Plumb J (1980) Growth rates of a new cell line from the channel catfish ovary and channel catfish virus replication and different temperatures. Can J Fish Aquat Sci 37:871–873

    Google Scholar 

  • Chen W-J, Orti G, Meyer A (2004) Novel evolutionary relationships among four fish model systems. Trends Genet 20:424–431

    Article  PubMed  CAS  Google Scholar 

  • Hedges SB, Kumar S (2002) Vertebrates genomes compared. Science 297:1283–1285

    Article  PubMed  CAS  Google Scholar 

  • Hogan RJ, Waldbieser G, Goudie CA, Antao A, Godwin UB, Wilson MR, Miller NW, Clem LW, McConnel TJ, Wolters WR, Chinchar VG (1999) Molecular and immunological characterization of gynogenetic channel catfish (Ictalurus punctatus). Mar Biotechnol 1:317–327

    Article  PubMed  CAS  Google Scholar 

  • Igawa D, Sakai M, Savan R (2006) An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol Immunol 43:999–1009

    Article  PubMed  CAS  Google Scholar 

  • Inoue JG, Miya M, Venkatesh B, Nishida M (2005) The mitochondrial genome of the Indonesian coelacanth Latimeria menadoenis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349:227–235

    Article  PubMed  CAS  Google Scholar 

  • Koonin EV (1991) The phylogeny of RNA polymerases of positive-strand RNA viruses. J Gen Virol 72:2197–2206

    Article  PubMed  Google Scholar 

  • Kotenko SV, Gallagher VV, Baurin A, Lewis-Antes M, Shen NK, Shah JA, Langer F, Sheikh F, Dickensheets H, Donnelly RP (2003) IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4:69–77

    Article  PubMed  CAS  Google Scholar 

  • Kountikov E, Wilson M, Miller N, Clem W, Bengten E (2004) Organization and expression of thirteen alternatively spliced exons in catfish CD45 homologs. Dev Comp Immunol 28:1023–1035

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA 3: integrated software for molecular evolutionary genetic analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Long S, Wilson M, Bengten E, Bryan L, Clem LW, Miller NW, Chinchar VG (2004) Identification of a cDNA encoding channel catfish interferon. Dev Comp Immunol 28:97–111

    Article  PubMed  CAS  Google Scholar 

  • Long S, Milev-Milovanovic I, Wilson M, Bengten E, Clem LW, Miller NW, Chinchar VG (2006) Identification and expression analysis of cDNAs encoding channel catfish type I interferons. Fish Shellfish Immunol (in press)

  • Lutfalla G, Crollius HR, Stange-Thomann N, Jaillon O, Mogensen K, Monneron D (2003) Comparative genomic analysis reveals independent expansion of a lineage-specific gene family in vertebrates: the class II cytokine receptors and their ligands in mammals and fish. BMC Genomics 4:29

    Article  PubMed  Google Scholar 

  • McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16:404–405

    Article  PubMed  CAS  Google Scholar 

  • Miller NW, Chinchar VG, Clem LW (1994a) Development of leukocyte cell lines from the channel catfish (Ictalurus punctatus). J Tissue Cult Methods 16:117–123

    Article  Google Scholar 

  • Miller NW, Rycyzyn MA, Wilson MR, Warr GW, Naftel JP, Clem LW (1994b) Development and characterization of channel catfish long term B cell lines. J Immunol 152:2180–2189

    PubMed  CAS  Google Scholar 

  • Nelson JS (1994) Fishes of the world, 3rd edn. Wiley, New York

    Google Scholar 

  • Panopoulou G, Poustka AJ (2005) Timing and mechanism of ancient vertebrate genome duplications—the adventure of a hypothesis. Trends Genet 21:559–567

    Article  PubMed  CAS  Google Scholar 

  • Perussia B, Mangoni L, Engers HD, Trinchieri G (1980) Interferon production by human and murine lymphocytes in response to alloantigens. J Immunol 125:1589–1595

    PubMed  CAS  Google Scholar 

  • Pestka S, Krause CD, Walter MR (2004) Interferons, interferon-like cytokines, and their receptors. Immunol Rev 202:8–32

    Article  PubMed  CAS  Google Scholar 

  • Robertsen B (2006) The interferon system of teleost fish. Fish Shellfish Immunol 20:172–191

    Article  PubMed  CAS  Google Scholar 

  • Robertsen B, Bergen V, Rokenes T, Larsen R, Albuquerque A (2003) Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 23:601–612

    Article  PubMed  CAS  Google Scholar 

  • Savant-Bhonsale S, Cleveland DW (1992) Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a >20S degradation complex. Genes Dev 6:1927–1939

    Article  PubMed  CAS  Google Scholar 

  • Schroeder K, Hertzog PJ, Ravasi T, Hume DA (2004) Interferon-γ: an overview of signals, mechanisms, and functions. J Leukoc Biol 75:163–189

    Article  CAS  Google Scholar 

  • Schultz U, Kaspers B, Staeheli P (2004) The interferon system of non-mammalian vertebrates. Dev Comp Immunol 28:499–508

    Article  PubMed  CAS  Google Scholar 

  • Shen L, Stuge TB, Bengten E, Wilson M, Chinchar VG, Naftel JP, Bernanke JM, Clem LW, Miller NW (2004) Identification and characterization of clonal NK-like cells from channel catfish (Ictalurus punctatus). Dev Comp Immunol 28:139–152

    Article  PubMed  CAS  Google Scholar 

  • Stuge TB, Yoshida SH, Chinchar VG, Miller NW, Clem LW (1997) Cytotoxic activity generated from channel catfish peripheral blood leukocytes in mixed leukocyte cultures. Cell Immunol 177:154–161

    Article  PubMed  CAS  Google Scholar 

  • Van der Meer A, Wissink WM, Schattenberg AVMB, Joosten I (1999) Interferon-γ based mixed lymphocyte culture as a selection tool for allogeneic bone marrow donors other than identical siblings. Br J Haematol 105:340–348

    Article  PubMed  Google Scholar 

  • Vilcek J, Sen GC (1996) Interferons and other cytokines. In: Fields BN, Knipe DM, Howley PM et al (eds) Fundamental virology, 3rd edn. Lippincott-Raven, Philadelphia, pp 341–365

    Google Scholar 

  • Wilson M, Bengten M, Miller NW, Clem LW, DuPasquier L, Warr GW (1997) A novel chimeric Ig heavy chain from a teleost fish shares similarities to IgD. Proc Natl Acad Sci U S A 94:4593–4597

    Article  PubMed  CAS  Google Scholar 

  • Wilson MR, Zhou H, Bengten E, Clem LW, Stuge TB, Warr GW, Miller NW (1998) T-cell receptors in channel catfish: structure and expression of TCR alpha and beta genes. Mol Immunol 35:545–557

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Yoshiura Y, Dijkstra JM, Sakai M, Ototake M, Secombes C (2004) Identification of an interferon gamma homologue in fugu, Takifugu rubripes. Fish Shellfish Immunol 17:403–409

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Carrington A, Collet B, Dijkstra JM, Yoshiura Y, Bols N, Secombes C (2005) Identification and bioactivities of IFN-γ in rainbow trout Oncorhynchus mykiss: the first Th1-type cytokine characterized functionally in fish. J Immunol 175:2484–2494

    PubMed  CAS  Google Scholar 

  • Zubiaga AM, Belasco JG, Greenberg ME (1995) The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol Cell Biol 15:2219–2230

    PubMed  CAS  Google Scholar 

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Acknowledgements

The work was partially supported by grants from the United States Department of Agriculture NRI/CGP (award number 2002-35204-12211) and the National Institutes of Health (award number R01-AI-19530). We thank S. Quinou and G. Waldbieser (USDA/ARS, Stoneville, MS) for initial sequencing of the CF IFN-γ clones. The experiments described herein comply with current laws of the United States of America.

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Correspondence to V. G. Chinchar.

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Milev-Milovanovic, I., Long, S., Wilson, M. et al. Identification and expression analysis of interferon gamma genes in channel catfish. Immunogenetics 58, 70–80 (2006). https://doi.org/10.1007/s00251-006-0081-x

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  • DOI: https://doi.org/10.1007/s00251-006-0081-x

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