Skip to main content
SpringerLink
Log in

Bovine T cell receptor gamma variable and constant genes: combinatorial usage by circulating γδ T cells

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

Abstract

Studies here describe expression and sequence of several new bovine T cell receptor gamma (TRG) genes to yield a total of 11 TRG variable (TRGV) genes (in eight subgroups) and six TRG constant (TRGC) genes. Publicly available genomic sequences were annotated to show their placement. Homologous TRG genes in cattle and sheep were assigned, using four accepted criteria. New genes described here include the bovine TRGC6, TRGV2, and TRGV4, homologues of ovine TRGC4, TRGV2, and TRGV4, respectively. The bovine Vγ7 and BTGV1 clones (previously TRGV4 and TRGV2, respectively) were reassigned to new subgroups TRGV7 and TRGV8, respectively, with approval by the IMGT Nomenclature Committee. Three TRGV subgroups (TRGV5, TRGV6, and TRGV8) were further designated as TRGV5-1 and TRGV5-2, TRGV6-1 and TRGV6-2, and TRGV8-1 and TRGV8-2 because each subgroup is comprised of two mapped genes. The complete sequence of bovine TRGC5 is also reported, for which a limited number of nucleotides was previously available, and shown to be most closely related to ovine TRGC5. Analysis of circulating γδ T cells revealed that rearrangement of TRGV genes with TRGC genes is largely dictated by their proximity within one of the six genomic V-J-C cassettes, with all TRG genes expressed by bovine peripheral blood γδ T cells. Cattle are useful models for γδ T cell biology because they have γδ T cells that respond to isopentenylpyrophosphate (IPP) antigens, while mice do not, and some bovine TRGV genes cluster closely with human 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

  • Bosc N, Lefranc MP (2003) The mouse (Mus musculus) T cell receptor alpha (TRA) and delta (TRD) variable genes. Dev Comp Immunol 27:465–497

    Article  PubMed  CAS  Google Scholar 

  • Buresi C, Ghanem N, Huck S, Lefranc G, Lefranc MP (1989) Exon duplication and triplication in the human T-cell receptor gamma constant region genes and RFLP in French, Lebanese, Tunisian, and black African populations. Immunogenetics 29:161–172

    Article  PubMed  CAS  Google Scholar 

  • Chen ZW (2002) Comparative biology of γδ T cells. Sci Prog 85:347–358

    Article  PubMed  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500

    Article  PubMed  CAS  Google Scholar 

  • Clark SP, Arden B, Kabelitz D, Mak TW (1995) Comparison of human and mouse T-cell receptor variable gene segment subfamilies. Immunogenetics 42:531–540

    Article  PubMed  CAS  Google Scholar 

  • Conrad ML, Pettman R, Whitehead J, McKinnel L, Davis SK, Koop BF (2002) Genomic sequencing of the bovine T cell receptor beta locus. Vet Immunol Immunopathol 87:439–441

    Article  PubMed  CAS  Google Scholar 

  • Cooper MD, Chen CL, Bucy RP, Thompson CB (1991) Avian T cell ontogeny. Adv Immunol 50:87–117

    PubMed  CAS  Google Scholar 

  • Daubenberger CA, Taracha EL, Gaidulis L, Davis WC, McKeever DJ (1999) Bovine γδ T-cell responses to the intracellular protozoan parasite Theileria parva. Infect Immun 67:2241–2249

    PubMed  CAS  Google Scholar 

  • Ghanem N, Soua Z, Zhang XG, Zijun M, Zhiwei Y, Lefranc G, Lefranc MP (1991) Polymorphism of the T-cell receptor gamma variable and constant region genes in a Chinese population. Hum Genet 86:450–456

    Article  PubMed  CAS  Google Scholar 

  • Glusman G, Rowen L, Lee I, Boysen C, Roach JC, Smit AF, Wang K, Koop BF, Hood L (2001) Comparative genomics of the human and mouse T cell receptor loci. Immunity 15:337–349

    Article  PubMed  CAS  Google Scholar 

  • Groh V, Steinle A, Bauer S, Spies T (1998) Recognition of stress-induced MHC molecules by intestinal epithelial γδ T cells. Science 279:1737–1740

    Article  PubMed  ADS  CAS  Google Scholar 

  • Hayday AC (2000) γδ cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18:975–1026

    Article  PubMed  CAS  Google Scholar 

  • Hein WR, Dudler L (1993) Divergent evolution of T cell repertoires: extensive diversity and developmentally regulated expression of the sheep γδ T cell receptor. EMBO J 12:715–724

    PubMed  CAS  Google Scholar 

  • Hein WR, Dudler L (1997) TCR γδ+ cells are prominent in normal bovine skin and express a diverse repertoire of antigen receptors. Immunology 91:58–64

    Article  PubMed  CAS  Google Scholar 

  • Hein WR, Mackay CR (1991) Prominence of γδ T cells in the ruminant immune system. Immunol Today 12:30–34

    Article  PubMed  CAS  Google Scholar 

  • Hein WR, Dudler L, Marcuz A, Grossberger D (1990) Molecular cloning of sheep T cell receptor γ and δ chain constant regions: unusual primary structure of γ chain hinge segments. Eur J Immunol 20:1795–1804

    PubMed  CAS  Google Scholar 

  • Ishiguro N, Aida Y, Shinagawa T, Shinagawa M (1993) Molecular structures of cattle T-cell receptor γ and δ chains predominantly expressed on peripheral blood lymphocytes. Immunogenetics 38:437–443

    Article  PubMed  CAS  Google Scholar 

  • Lahmers KK, Norimine J, Abrahamsen MS, Palmer GH, Brown WC (2005) The CD4+ T cell immunodominant Anaplasma marginale major surface protein 2 stimulates γδ T cell clones that express unique T cell receptors. J Leukoc Biol 77:199–208

    Article  PubMed  CAS  Google Scholar 

  • Lefranc MP, Lefranc G (2001) The T cell receptor facts book. Academic, London, UK, p 398

    Google Scholar 

  • Lefranc MP, Rabbitts TH (1989) The human T-cell receptor gamma (TRG) genes. Trends Biochem Sci 14:214–218

    Article  PubMed  CAS  Google Scholar 

  • Lefranc MP, Forster A, Baer R, Stinson MA, Rabbitts TH (1986a) Diversity and rearrangement of the human T cell rearranging gamma genes: nine germ-line variable genes belonging to two subgroups. Cell 45:237–246

    Article  PubMed  CAS  Google Scholar 

  • Lefranc MP, Forster A, Rabbitts TH (1986b) Genetic polymorphism and exon changes of the constant regions of the human T-cell rearranging gene gamma. Proc Natl Acad Sci U S A 83:9596–9600

    PubMed  ADS  CAS  Google Scholar 

  • Lefranc MP, Pommie C, Ruiz M, Giudicelli V, Foulquier E, Truong L, Thouvenin-Contet V, Lefranc G (2003) IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev Comp Immunol 27:55–77

    Article  PubMed  CAS  Google Scholar 

  • Lefranc MP, Giudicelli V, Kaas Q, Duprat E, Jabado-Michaloud J, Scaviner D, Ginestoux C, Clement O, Chaume D, Lefranc G (2005) IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res 33:D593–D597

    Article  PubMed  CAS  Google Scholar 

  • Machugh ND, Mburu JK, Carol MJ, Wyatt CR, Orden JA, Davis WC (1997) Identification of two distinct subsets of bovine γδ T cells with unique cell surface phenotype and tissue distribution. Immunology 92:340–345

    Article  PubMed  CAS  Google Scholar 

  • Meyer-Olson D, Brady KW, Blackard JT, Allen TM, Islam S, Shoukry NH, Hartman K, Walker CM, Kalams SA (2003) Analysis of the TCR β variable gene repertoire in chimpanzees: identification of functional homologs to human pseudogenes. J Immunol 170:4161–4169

    PubMed  CAS  Google Scholar 

  • Miccoli MC, Lipsi MR, Massari S, Lanave C, Ciccarese S (2001) Exon–intron organization of TRGC genes in sheep. Immunogenetics 53:416–422

    Article  PubMed  CAS  Google Scholar 

  • Miccoli MC, Antonacci R, Vaccarelli G, Lanave C, Massari S, Cribiu EP, Ciccarese S (2003) Evolution of TRG clusters in cattle and sheep genomes as drawn from the structural analysis of the ovine TRG2@ locus. J Mol Evol 57:52–62

    Article  PubMed  CAS  Google Scholar 

  • Morita CT, Parker CM, Brenner MB, Band H (1994) TCR usage and functional capabilities of human γδ T cells at birth. J Immunol 153:3979–3988

    PubMed  CAS  Google Scholar 

  • Naiman BM, Alt D, Bolin CA, Zuerner R, Baldwin CL (2001) Protective killed Leptospira borgpetersenii vaccine induces potent Th1 immunity comprising responses by CD4 and γδ T lymphocytes. Infect Immun 69:7550–7558

    Article  PubMed  CAS  Google Scholar 

  • Ota Y, Kobata T, Seki M, Yagita H, Shimada S, Huang YY, Takagaki Y, Okumura K (1992) Extrathymic origin of Vγ1/Vδ6 T cells in the skin. Eur J Immunol 22:595–598

    PubMed  CAS  Google Scholar 

  • Parker CM, Groh V, Band H, Porcelli SA, Morita C, Fabbi M, Glass D, Strominger JL, Brenner MB (1990) Evidence for extrathymic changes in the T cell receptor γ/δ repertoire. J Exp Med 171:1597–1612

    Article  PubMed  CAS  Google Scholar 

  • Rogers AN, Vanburen DG, Hedblom EE, Tilahun ME, Telfer JC, Baldwin CL (2005) γδ T cell function varies with the expressed WC1 co-receptor. J Immunol 174:3386–3393

    PubMed  CAS  Google Scholar 

  • Sathiyaseelan T, Naiman B, Welte S, Machugh N, Black SJ, Baldwin CL (2002a) Immunological characterization of a γδ T-cell stimulatory ligand on autologous monocytes. Immunology 105:181–189

    Article  PubMed  CAS  Google Scholar 

  • Sathiyaseelan T, Rogers A, Baldwin CL (2002b) Response of bovine γδ T cells to activation through CD3. Vet Immunol Immunopathol 90:155–168

    Article  PubMed  CAS  Google Scholar 

  • Steele CR, Oppenheim DE, Hayday AC (2000) γδ T cells: non-classical ligands for non-classical cells. Curr Biol 10:R282–R285

    Article  PubMed  CAS  Google Scholar 

  • Su C, Jakobsen I, Gu X, Nei M (1999) Diversity and evolution of T-cell receptor variable region genes in mammals and birds. Immunogenetics 50:301–308

    Article  PubMed  CAS  Google Scholar 

  • Takeuchi N, Ishiguro N, Shinagawa M (1992) Molecular cloning and sequence analysis of bovine T-cell receptor γ and δ chain genes. Immunogenetics 35:89–96

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Sano S, Nieves E, De Libero G, Rosa D, Modlin RL, Brenner MB, Bloom BR, Morita CT (1994) Nonpeptide ligands for human γδ T cells. Proc Natl Acad Sci U S A 91:8175–8179

    PubMed  ADS  CAS  Google Scholar 

  • Welsh MD, Kennedy HE, Smyth AJ, Girvin RM, Andersen P, Pollock JM (2002) Responses of bovine WC1+ γδ T cells to protein and nonprotein antigens of Mycobacterium bovis. Infect Immun 70:6114–6120

    Article  PubMed  CAS  Google Scholar 

  • Wijngaard PL, Machugh ND, Metzelaar MJ, Romberg S, Bensaid A, Pepin L, Davis WC, Clevers HC (1994) Members of the novel WC1 gene family are differentially expressed on subsets of bovine CD4–CD8–γδ T lymphocytes. J Immunol 152:3476–3482

    PubMed  CAS  Google Scholar 

  • Zhang XM, Cathala G, Soua Z, Lefranc MP, Huck S (1996) The human T-cell receptor gamma variable pseudogene V10 is a distinctive marker of human speciation. Immunogenetics 43:196–203

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Research Initiative of the USDA CSREES, grant #2002-02038 and 2004-01157 and the Massachusetts Agricultural Experiment Station Project No. MAS00851. We thank Drs Wendy Brown and Kevin Lahmers for access to prepublication data.

Author information

Authors and Affiliations

  1. Paige Laboratory, Department of Veterinary and Animal Sciences and Program in Molecular and Cellular Biology, University of Massachusetts, Amherst,, MA, 01003, USA

    Carolyn Herzig, Seth Blumerman & Cynthia Baldwin

  2. Laboratoire d’ImmunoGénétique Moléculaire and Institut de Génétique Humaine, Université Montpellier II, Montpellier, 34396, France

    Marie-Paule Lefranc

Authors
  1. Carolyn Herzig
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Seth Blumerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marie-Paule Lefranc
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cynthia Baldwin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cynthia Baldwin.

Additional information

Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank database under the accession numbers DQ179591, DQ179592, DQ179593, and DQ179594.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Herzig, C., Blumerman, S., Lefranc, MP. et al. Bovine T cell receptor gamma variable and constant genes: combinatorial usage by circulating γδ T cells. Immunogenetics 58, 138–151 (2006). https://doi.org/10.1007/s00251-006-0097-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-006-0097-2

Keywords

Search

Navigation