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Identification and regulatory analysis of rainbow trout tapasin and tapasin-related genes

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Abstract

Tapasin (TAPBP) is a key member of MHC class Ia antigen-loading complexes, bridging the class Ia molecule to the transporter associated with antigen presentation (TAP). As part of an ongoing study of MHC genomics in rainbow trout, we have identified two rainbow trout TAPBP genes (Onmy-TAPBP.a and .b) and a similar but distinct TAPBP-related gene (Onmy-TAPBP-R) that had previously only been described in mammals. Physical and genetic mapping indicate that Onmy-TAPBP.a is on chromosome 18 in the MHC class Ia region and that Onmy-TAPBP.b resides on chromosome 14 in the MHC class Ib region. There are also at least two copies of TAPBP-R, Onmy-TAPBP-R.a and Onmy-TAPBP-R.b, located on chromosomes 2 and 3, respectively. Due to the central role of TAPBP expression during acute viral infection, we have characterized the transcriptional profile and regulatory regions for both Onmy-TAPBP and Onmy-TAPBP-R. Transcription of both genes increased during acute infection with infectious hematapoeitic necrosis virus (IHNV) in a fashion indicative of interferon-mediated regulation. Promoter–reporter assays in STE-137 cells demonstrate that the trout TAPBP and TAPBP-R promoters respond to interferon regulatory factors, Onmy-IRF1 and Onmy-IRF2. Overall, TAPBP is expressed at higher levels than TAPBP-R in naïve tissues and TAPBP transcription is more responsive to viral infection and IRF1 and 2 binding.

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References

  • Abarca-Heidemann K, Friederichs S, Klamp T, Boehm U, Guethlein LA, Ortmann B (2002) Regulation of the expression of mouse TAP-associated glycoprotein (tapasin) by cytokines. Immunol Lett 83:197–207

    Article  PubMed  CAS  Google Scholar 

  • Altmann S, 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 

  • August A, Dupont B (1994) CD28 of T lymphocytes associates with phosphatidylinositol 3-kinase. Int Immunol 6:769–774

    Article  PubMed  CAS  Google Scholar 

  • Bangia N, Cresswell P (2005) Stoichiometric tapasin interactions in the catalysis of major histocompatibility complex class I molecule assembly. Immunology 114:346–353

    Article  PubMed  CAS  Google Scholar 

  • Bangia N, Lehner PJ, Hughes EA, Surman M, Cresswell P (1999) The N-terminal region of tapasin is required to stabilize the MHC class I loading complex. Eur J Immunol 29:1858–1870

    Article  PubMed  CAS  Google Scholar 

  • Bingulac-Popovic J, Figueroa F, Sato A, Talbot WS, Johnson SL, Gates M, Postlethwait JH, Klein J (1997) Mapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio. Immunogenetics 46:129–134

    Article  PubMed  CAS  Google Scholar 

  • Chun T, Grandea AG 3rd, Lybarger L, Forman J, Van Kaer L, Wang CR (2001) Functional roles of TAP and tapasin in the assembly of M3-N-formylated peptide complexes. J Immunol 167:1507–1514

    PubMed  CAS  Google Scholar 

  • Collet B, McDonald C, Secombes CJ (2003a) The promoter for the interferon regulatory factor (IRF)-2 in the rainbow trout Oncorhynchus mykiss: cloning and reporter gene activity. Fish Shellfish Immunol 15:473–477

    Article  PubMed  CAS  Google Scholar 

  • Collet B, Hovens GC, Mazzoni D, Hirono I, Aoki T, Secombes CJ (2003b) Cloning and expression analysis of rainbow trout Oncorhynchus mykiss interferon regulatory factor 1 and 2 (IRF-1 and IRF-2). Dev Comp Immunol 27:111–126

    Article  PubMed  CAS  Google Scholar 

  • Darnell JE Jr, Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415–1421

    Article  PubMed  CAS  Google Scholar 

  • de Kinkelin P, Dorson M (1973) Interferon production in rainbow trout (Salmo gairdneri) experimentally infected with Egtved virus. J Gen Virol 19:125–127

    Article  PubMed  Google Scholar 

  • Dick TP, Bangia N, Peaper DR, Cresswell P (2002) Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 16:87–98

    Article  PubMed  CAS  Google Scholar 

  • Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15:351–362

    Article  PubMed  CAS  Google Scholar 

  • Garbi N, Tan P, Diehl AD, Chambers BJ, Ljunggren HG, Momburg F, Hammerling GJ (2000) Impaired immune responses and altered peptide repertoire in tapasin-deficient mice. Nat Immunol 1:234–238

    Article  PubMed  CAS  Google Scholar 

  • Garbi N, Tiwari N, Momburg F, Hammerling GJ (2003) A major role for tapasin as a stabilizer of the TAP peptide transporter and consequences for MHC class I expression. Eur J Immunol 33:264–273

    Article  PubMed  CAS  Google Scholar 

  • Gobin SJ, van Zutphen M, Woltman AM, van den Elsen PJ (1999) Transactivation of classical and nonclassical HLA class I genes through the IFN-stimulated response element. J Immunol 163:1428–1434

    PubMed  CAS  Google Scholar 

  • Goodbourn S, Didcock L, Randall RE (2000) Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341–2364

    PubMed  CAS  Google Scholar 

  • Hansen JD, La Patra S (2002) Induction of the rainbow trout MHC class I pathway during acute IHNV infection. Immunogenetics 54:654–661

    Article  PubMed  CAS  Google Scholar 

  • Hansen JD, Strassburger P, Thorgaard GH, Young WP, Du Pasquier L (1999) Expression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss. J Immunol 163:774–786

    PubMed  CAS  Google Scholar 

  • Harada Y, Ohgai D, Watanabe R, Okano K, Koiwai O, Tanabe K, Toma H, Altman A, Abe R (2003) A single amino acid alteration in cytoplasmic domain determines IL-2 promoter activation by ligation of CD28 but not inducible costimulator (ICOS). J Exp Med 197:257–262

    Article  PubMed  Google Scholar 

  • Herrmann F, Trowsdale J, Huber C, Seliger B (2003) Cloning and functional analyses of the mouse tapasin promoter. Immunogenetics 55:379–388

    Article  PubMed  CAS  Google Scholar 

  • Ioerger TR, Du C, Linthicum DS (1999) Conservation of cys–cys trp structural triads and their geometry in the protein domains of immunoglobulin superfamily members. Mol Immunol 36:373–386

    Article  PubMed  CAS  Google Scholar 

  • Johnson KR, Wright JE Jr, May B (1987) Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics 116:579–591

    PubMed  CAS  Google Scholar 

  • Kasahara M (1999) Genome dynamics of the major histocompatibility complex: insights from genome paralogy. Immunogenetics 50:134–145

    Article  PubMed  CAS  Google Scholar 

  • Kuroda N, Naruse K, Shima A, Nonaka M, Sasaki M (2000) Molecular cloning and linkage analysis of complement C3 and C4 genes of the Japanese medaka fish. Immunogenetics 51:117–128

    Article  PubMed  CAS  Google Scholar 

  • Landis ED, Hansen JD (2004) Annotation of two tapasin promoters from rainbow trout. Mar Biotechnol 6:S118–S122

    Google Scholar 

  • Levy DE, Kessler DS, Pine R, Reich N, JEJ Darnell (1988) Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev 2:383

    Article  PubMed  CAS  Google Scholar 

  • Long S, Wilson M, Bengten E, Locke B, LW Clem, NW Miller, VG Chinchar (2003) Identification of a cDNA encoding channel catfish interferon. Dev Comp Immunol 28:97–111

    Article  CAS  Google Scholar 

  • Momburg F, Tan P (2002) Tapasin—the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol Immunol 39:217–233

    Article  PubMed  CAS  Google Scholar 

  • Nichols KM, Young WP, Danzmann RG, Robison BD, Rexroad C, Noakes M, Phillips RB, Bentzen P, Spies I, Knudsen K, Allendorf FW, Cunningham BM, Brunelli J, Zhang H, Ristow S, Drew R, Brown KH, Wheeler PA, Thorgaard GH (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Anim Genet 34:102–115

    Article  PubMed  CAS  Google Scholar 

  • Ortmann B, Copeman J, Lehner PJ, Sadasivan B, Herberg JA, Grandea AG, Riddell SR, Tampe R, Spies T, Trowsdale J, Cresswell P (1997) A critical role for tapasin in the assembly and function of multimeric MHC class I–TAP complexes. Science 277:1306–1309

    Article  PubMed  CAS  Google Scholar 

  • Palti Y, Gahr SA, Hansen JD, Rexroad CE 3rd (2004) Characterization of a new BAC library for rainbow trout: evidence for multi-locus duplication. Anim Genet 35:130–133

    Article  PubMed  CAS  Google Scholar 

  • Park B, Ahn K (2003) An essential function of tapasin in quality control of HLA-G molecules. J Biol Chem 278:14337–14345

    Article  PubMed  CAS  Google Scholar 

  • Parrington J, Rogers NC, Gewert DR, Pine R, Veals SA, Levy DE, Stark GR, Kerr IM (1993) The interferon-stimulable response elements of two human genes detect overlapping sets of transcription factors. Eur J Biochem 214:617–626

    Article  PubMed  CAS  Google Scholar 

  • Petersen JL, Hickman-Miller HD, McIlhaney MM, Vargas SE, Purcell AW, Hildebrand WH, Solheim JC (2005) A charged amino acid residue in the transmembrane/cytoplasmic region of tapasin influences MHC class I assembly and maturation. J Immunol 174:962–969

    PubMed  CAS  Google Scholar 

  • Phillips RB, Zimmerman A, Noakes MA, Palti Y, Morasch MR, Eiben L, Ristow SS, Thorgaard GH, Hansen, JD (2003) Physical and genetic mapping of the rainbow trout major histocompatibility regions: evidence for duplication of the class I region. Immunogenetics 55:561–569

    Article  PubMed  CAS  Google Scholar 

  • 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 23:4878–4884

    Article  PubMed  CAS  Google Scholar 

  • Robertsen B, Bergan V, Rokenes T, Larsen R, Albuquerque A (2003) Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 10:601–612

    Article  CAS  Google Scholar 

  • Sadasivan B, Lehner PJ, Ortmann B, Spies T, Cresswell P (1996) Roles for calreticulin and a novel glycoprotein, tapasin, in the interaction of MHC class I molecules with TAP. Immunity 5:103–114

    Article  PubMed  CAS  Google Scholar 

  • Sambrook JG, Russell R, Umrania Y, Edwards YJ, Campbell RD, Elgar G, Clark MS (2002) Fugu orthologues of human major histocompatibility complex genes: a genome survey. Immunogenetics 54:367–380

    Article  PubMed  CAS  Google Scholar 

  • Shiina T, Dijkstra JM, Shimizu S, Watanabe A, Yanagiya K, Kiryu I, Fujiwara A, Nishida-Umehara C, Kaba Y, Hirono I, Yoshiura Y, Aoki T, Inoko H, Kulski JK, Ototake M (2005) Interchromosomal duplication of major histocompatibility complex class I regions in rainbow trout (Oncorhynchus mykiss), a species with a presumably recent tetraploid ancestry. Immunogenetics 56:878–893

    Article  PubMed  CAS  Google Scholar 

  • Shultz U, Kaspers B, Staeheli P (2003) The interferon system of non-mammalian vertebrates. Dev Comp Immunol 28:499–508

    Article  CAS  Google Scholar 

  • Stet RJ, Kruiswijk CP, Dixon B (2003) Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23:441–471

    Article  PubMed  CAS  Google Scholar 

  • Sultmann H, Murray BW, Klein J (2000) Identification of seven genes in the major histocompatibility complex class I region of the zebrafish. Scand J Immunol 51:577–585

    Article  PubMed  CAS  Google Scholar 

  • Taniguchi T (1997) Transcription factors IRF-1 and IRF-2: linking the immune responses and tumor suppression. J Cell Physiol 173:128–130

    Article  PubMed  CAS  Google Scholar 

  • Tan P, Kropshofer H, Mandelboim O, Bulbuc N, Hammerling GJ, Momburg F (2002) Recruitment of MHC class I molecules by tapasin into the transporter associated with antigen processing-associated complex is essential for optimal peptide loading. J Immunol 168:1950–1960

    PubMed  CAS  Google Scholar 

  • Teng MS, Stephens R, Du Pasquier L, Freeman T, Lindquist JA, Trowsdale J (2002) A human TAPBP (TAPASIN)-related gene, TAPBP-R. Eur J Immunol 32:1059–1068

    Article  PubMed  CAS  Google Scholar 

  • Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S (1992) TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 71:1205–1214

    Article  PubMed  Google Scholar 

  • Viertlboeck BC, Habermann FA, Schmitt R, Groenen MA, Du Pasquier L, Gobel TW (2005) The chicken leukocyte receptor complex: a highly diverse multigene family encoding at least six structurally distinct receptor types. J Immunol 175:385–393

    PubMed  CAS  Google Scholar 

  • 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 28:316–319

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Song Y, Bakker AB, Bauer S, Spies T, Lanier LL, Phillips JH (1999) An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285:730–732

    Article  PubMed  CAS  Google Scholar 

  • Young WP, Wheeler PA, Coryell VH, Kelm P, Thorgaard GH (1998) A detailed linkage map of rainbow trout produced using doubled haploids. Genetics 148: 839–850

    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-{gamma} in rainbow trout Oncorhynchus mykiss: the First Th1-type cytokine characterized functionally in fish. J Immunol 175:2484–2494

    PubMed  CAS  Google Scholar 

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Acknowledgements

This project was supported by National Research Initiative Grant no. 2003-35205-15072 from the USDA Cooperative State Research, Education, and Extension Service and internal base funds provided by the Department of the Interior.

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Authors and Affiliations

  1. Molecular Medicine Program, University of Maryland Medical School, Baltimore, Maryland, USA

    Eric D. Landis & John D. Hansen

  2. Western Fisheries Research Center, Biological Resources Division USGS, Seattle, Washington, USA

    Eric D. Landis & John D. Hansen

  3. USDA-ARS-NCCCWA, 11876 Leetown Road, Kearneysville, WV 25430, USA

    Yniv Palti

  4. Department of Biological Sciences, Washington State University, Vancouver, Washington, USA

    Jenefer Dekoning & Ruth B. Phillips

  5. School of Biological Sciences, Washington State University, Pullman, Washington, USA

    Robert Drew

  6. Department of Pathobiology, University of Washington, Seattle, Washington, USA

    John D. Hansen

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  1. Eric D. Landis
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  2. Yniv Palti
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  3. Jenefer Dekoning
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  4. Robert Drew
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  5. Ruth B. Phillips
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  6. John D. Hansen
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Correspondence to John D. Hansen.

Additional information

The following sequences have been deposited in GenBank: DQ092322–330 and DQ288281.

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Landis, E.D., Palti, Y., Dekoning, J. et al. Identification and regulatory analysis of rainbow trout tapasin and tapasin-related genes. Immunogenetics 58, 56–69 (2006). https://doi.org/10.1007/s00251-005-0070-5

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  • DOI: https://doi.org/10.1007/s00251-005-0070-5

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