Skip to main content
SpringerLink
Log in

Characterisation of a cluster of TRIM-B30.2 genes in the chicken MHC B locus

  • Original Paper
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

We have identified and characterised a cluster of six TRIM-B30.2 genes flanking the chicken BF/BL region of the B complex. The TRIM-B30.2 proteins are a subgroup of the TRIM protein family containing the tripartite motif (TRIM), consisting of a RING domain, a B-box and a coiled coil region, and a B30.2-like domain. In humans, a cluster of seven TRIM-B30.2 genes has been characterised within the MHC on Chromosome 6p21.33. Among the six chicken TRIM-B30.2 genes two are orthologous to those of the human MHC, and two (TRIM41 and TRIM7) are orthologous to human genes located on Chromosome 5. In humans, these last two genes are adjacent to GNB2L1, a guanine nucleotide-binding protein gene, the ortholog of the chicken c12.3 gene situated in the vicinity of the TRIM-B30.2 genes. This suggests that breakpoints specific to mammals have occurred and led to the remodelling of their MHC structure. In terms of structure, like their mammalian counterparts, each chicken gene consists of five coding exons; exon 1 encodes the RING domain and the B-box, exons 2, 3 and 4 form the coiled-coil region, and the last exon represents the B30.2-like domain. Phylogenetic analysis led us to assume that this extended BF/BL region may be similar to the human extended class I region, because it contains a cluster of BG genes sharing an Ig-V like domain with the BTN genes (Henry et al. 1997a) and six TRIM-B30.2 genes containing the B30.2-like domain, shared with the TRIM-B30.2 members and the BTN genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abi Rached L, McDermott MF, Pontarotti P (1999) The MHC big bang. Immunol Rev 167:33–45

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Avela K, Lipsanen-Nyman M, Idanheimo N, Seemanova E, Rosengren S, Makela TP, Perheentupa J, Chapelle A, Lehesjoki AE (2000) Gene encoding a new RING–B-box–coiled-coil protein is mutated in mulibrey nanism. Nat Genet 25:298–301

    Article  Google Scholar 

  • Bacon LD, Witter RL (1992) Influence of turkey herpesvirus vaccination on the B-haplotype effect on Marek’s disease resistance in 15.B-congenic chickens. Avian Dis 36:378–385

    Google Scholar 

  • Bacon LD, Ismael N, Motta JV (1987) Allograft and antibody responses of 15I5-B congenic chickens. Prog Clin Biol Res 238:219−233

    Google Scholar 

  • Bernot A, Auffray C (1991) Primary structure and ontogeny of an avian CD3 transcript. Proc Natl Acad Sci USA 88:2550–2554

    Google Scholar 

  • Bonilla WV, Pinschewer DD, Klenerman P, Rousson V, Gaboli M, Pandolfi PP, Zinkernagel RM, Salvato MS, Hengartner H (2002) Effects of promyelocytic leukaemia protein on virus-host balance. J Virol 76:3810–3818

    Article  Google Scholar 

  • Borden KL (1998) RING fingers and B-boxes: zinc-binding protein-protein interaction domains. Biochem Cell Biol 76:351–358

    Article  Google Scholar 

  • Briles WE, McGibbon H (1948) Heterozygosity of inbred lines of chickens at two loci affecting cellular antigens. Genetics 33:605

    Google Scholar 

  • Briles WE, Stone HA, Cole RK (1977) Marek’s disease: effects of B histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195:193–195

    CAS  PubMed  Google Scholar 

  • Briles WE, Briles RW, Pollock DL, Pattison M (1982) Marek’s disease resistance of B (MHC) heterozygotes in a cross of purebred Leghorn lines. Poult Sci 61:205–211

    Google Scholar 

  • Briles WE, Goto RM, Auffray C, Miller MM (1993) A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 37:408–414

    CAS  PubMed  Google Scholar 

  • Chee AV, Lopez P, Pandolfi PP, Roizman B (2003) Promyelocytic leukaemia protein mediates interferon-based anti-herpes simplex virus 1 effects. J Virol 77:7101–7105

    Article  Google Scholar 

  • Dausset J (1981) The major histocompatibility complex in man. Science 213:1469–1474

    Google Scholar 

  • Fillon V, Zoorob R, Yerle M, Auffray C, Vignal A (1996) Mapping of the genetically independent chicken major histocompatibility complexes B and Rfp-Y to the same microchromosome by two-color fluorescent in situ hybridization. Cytogenet Cell Genet 75:7–9

    CAS  PubMed  Google Scholar 

  • Guillemot F, Billault A, Pourquié O, Béhar G, Chaussé, AM, Zoorob R, Kreibich G, Auffray C (1988) A molecular map of the chicken major histocompatibility complex: the class II β genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7:2775–2785

    CAS  PubMed  Google Scholar 

  • Guillemot F, Billault A, Auffray C (1989) Physical linkage of a guanine nucleotide-binding protein-related gene to the chicken major histocompatibility complex. Proc Natl Acad Sci USA 86:4594–4598

    Google Scholar 

  • Hala K, Boyd R, Wick G (1981) Chicken major histocompatibility complex and disease. Scand J Immunol 14:607–616

    CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Henry J, Ribouchon MT, Offer C, Pontarotti P (1997a) B30.2-like domain proteins: a growing family. Biochem Biophys Res Commun 235:162–165

    Article  Google Scholar 

  • Henry J, Ribouchon MT, Depetris D, Mattéi MG, Offer C, Tazi-Ahnini R, Pontarotti P (1997b) Cloning, structural analysis, and mapping of the B30 and B7 multigenic families to the major histocompatibility complex (MHC) and other chromosomal regions. Immunogenetics 46:383–395

    Article  CAS  PubMed  Google Scholar 

  • Henry J, Mather IH, McDermott MF, Pontarotti P (1998) B30.2-like domain proteins: update and new insights into a rapidly expanding family of proteins. Mol Biol Evol 15:1696–1705

    Google Scholar 

  • Jarvi SI, Goto RM, Gee GF, Briles WE, Miller MM (1999) Identification, inheritance, and linkage of BG-like and MHC class I genes in cranes. J Hered 90:152–159

    Article  Google Scholar 

  • Kaufman J, Volk H, Wallny HJ (1995) A “minimal essential Mhc” and an “unrecognized Mhc”: two extremes in selection for polymorphism. Immunol Rev 143:63–88

    CAS  PubMed  Google Scholar 

  • Kaufman J, Milne S, Göbel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  CAS  PubMed  Google Scholar 

  • Meyer M, Gauderi S, Rhodes DA, Trowsdale J (2002) Cluster of TRIM genes in the human MHC class I region sharing the B30.2 domain. Tissue Antigens 61:63–71

    Article  Google Scholar 

  • Miller MM, Goto R, Young S, Liu J, Hardy J (1990) Antigens similar to major histocompatibility complex B-G are expressed in the intestinal epithelium in the chicken. Immunogenetics 32:45–50

    Google Scholar 

  • Miller MM, Goto R, Young S, Chirivella J, Hawke D, Miyada CG (1991) Immunoglobulin variable-region-like domains of diverse sequence within the major histocompatibility complex of the chicken. Proc Natl Acad Sci USA 88:4377–4381

    CAS  PubMed  Google Scholar 

  • Miller MM, Goto RM, Taylor RL Jr, Zoorob R, Auffray C, Briles RW, Briles WE, Bloom SE (1996) Assignment of Rfp-Y to the chicken major histocompatibility comple/NOR microchromosome and evidence for high-frequency recombination associated with the nucleolar organizer region. Proc Natl Acad Sci USA 93:3958–3962

    Article  CAS  PubMed  Google Scholar 

  • Mungall AJ, Palmer SA, Sims SK, Edwards CA, Ashurst JL, Wilming L, Jones MC, Horton R, Hunt SE, Scott CE et al (2003) The DNA sequence and analysis of human chromosome 6. Nature 425:805–811

    Article  Google Scholar 

  • Ogawa S, Goto W, Orimo A, Hosoi T, Ouchi Y, Muramatsu M, Inoue S (1998) Molecular cloning of a novel RING finger-B box-coiled coil (RBCC) protein, terf, expressed in the testis. Biochem Biophys Res Commun 251:515–519

    Article  Google Scholar 

  • Orimo A, Yamagishi T, Tominaga N, Yamauchi Y, Hishinuma T, Okada, K, Suzuki M, Sato M, Nogi Y, Suzuki H, Inoue S, Yoshimura K, Shimizu Y, Muramatsu M (2000) Molecular cloning of testis-abundant finger protein/Ring finger protein 23 (RNF23), a novel RING-B box-coiled coil-B30.2 protein on the class I region of the human MHC. Biochem Biophys Res Commun 276:45–51

    Article  Google Scholar 

  • Pearson WR, Lipman DJ (1988) Improved tools for biological sequence analysis. Proc Natl Acad Sci USA 85:2444–2448

    CAS  PubMed  Google Scholar 

  • Quaderi NA, Schweiger S, Gaudenz K, Franco B, Rugarli EI, Berger W, Feldman GJ, Volta M, Andolfi G, Gilgenkrantz S, Marion RW, Hennekam RC, Opitz JM, Muenke M, Ropers HH, Ballabio A (1997) Opitz G/BBB syndrome, a defect of midline development, is due to mutations in a new RING finger gene on Xp22. Nat Genet 17:285–291

    Google Scholar 

  • Reddy BA, Etkin LD, Freemont PS (1992) A novel zinc finger coiled-coil domain in a family of nuclear proteins. Trends Biochem Sci 17:344–345

    Article  Google Scholar 

  • Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D, Zanaria E, Messali S, Cainarca S, Guffanti A, Minucci S, Pelicci PG, Ballabio A (2001) The tripartite motif family identifies cell compartments. EMBO J 20:2140–2151

    Article  Google Scholar 

  • Rhodes DA, Stammers M, Malcherek G, Beck S, Trowsdale J (2001) The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71:351–362

    Article  Google Scholar 

  • Salomonsen J, Dunond D, Skjoedt K, Thorpe D, Vainio O, Kaufman J (1991) Chicken major histocompatibility complex-encoded B-G antigens are found on many cell types that are important for the immune system. Proc Natl Acad Sci USA 88:1359–1363

    Google Scholar 

  • Stammers M, Rowen L, Rhodes D, Trowsdale J, Beck S (2000) BTL-II: a polymorphic locus with homology to the butyrophilin gene family, located at the border of the major histocompatibility complex class II and class III regions in human and mouse. Immunogenetics 51:373–382

    Article  Google Scholar 

  • Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J (2004) The cytoplasmic component TRIM5α restricts HIV-1 infection in Old World monkeys. Nature 427:848–853

    Article  Google Scholar 

  • Takahashi M, Inaguma Y, Hiai H, Hirose F (1988) Developmentally regulated expression of a human ‘finger’-containing gene encoded by the 5′ half of the ret transforming gene. Mol Cell Biol 8:1853–1856

    Google Scholar 

  • Venturini L, You J, Stadler M, Galien R, Lallemand V, Koken MH, Mattei MG, Ganser A, Chambon P, Losson R, de The H (1999) TIF1γ, a novel member of the transcriptional intermediary factor 1 family. Oncogene 18:1209–1217

    Article  Google Scholar 

  • Vernet C, Boretto J, Mattéi MG, Takahashi M, Jack LJW, Mather IH, Rouquier S, Pontarotti P (1993) Evolutionary study of multigenic families mapping close to the human MHC class I region. J Mol Evol 37:600–612

    CAS  PubMed  Google Scholar 

  • Vitale N, Moss J, Vaughan M (1996) ARD1, a 64-kDa bifunctional protein containing an 18-kDa GTP-binding ADP-ribosylation factor domain and a 46-kDa GTPase-activating domain. Proc Natl Acad Sci USA 93:1941–1944

    Article  Google Scholar 

  • Zoorob R, Billault A, Severac V, Fillon V, Vignal A, Aufray C (1996) Two chicken genomic libraries in the PAC and BAC cloning systems: organization and characterization. Anim Genet 27:69

    Google Scholar 

Download references

Acknowledgements

We thank Dr. J.M. El Hage Chahine for discussion and advice and Dr. F. Dautry for useful comments. This research was supported by grants from the European Commission to R.Z. (KA5-QLRT-CT99-1591 Chicken IMAGE).

Author information

Authors and Affiliations

  1. UPR 1983, CNRS, 7 rue Guy Môquet, 94801, Villejuif Cedex, France

    Thomas Ruby, Véronique Morin, Anne Oudin & Rima Zoorob

  2. LABOGENA, Domaine de Vilvert, 78352, Jouy en Josas Cedex, France

    Bertrand Bed’Hom

  3. Botanical museum (LD), Lund University, Ostra Vallgatan 18, 22361, Lund, Sweden

    Hakan Wittzell

Authors
  1. Thomas Ruby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bertrand Bed’Hom
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hakan Wittzell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Véronique Morin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anne Oudin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rima Zoorob
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rima Zoorob.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruby, T., Bed’Hom, B., Wittzell, H. et al. Characterisation of a cluster of TRIM-B30.2 genes in the chicken MHC B locus. Immunogenetics 57, 116–128 (2005). https://doi.org/10.1007/s00251-005-0770-x

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-005-0770-x

Keywords

Search

Navigation