Skip to main content
SpringerLink
Log in

Evolution of major histocompatibility complex class I genes in Cetartiodactyls

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

Abstract.

Previous studies of cattle MHC have suggested the presence of at least four classical class I loci. Analysis of haplotypes showed that any combination of one, two or three genes may be expressed, although no gene is expressed consistently. The aim of this study was to examine the evolutionary relationships among these genes and to study their phylogenetic history in Cetartiodactyl species, including cattle and their close relatives. A secondary aim was to determine whether recombination had occurred between any of the genes. MHC class I data sets were generated from published sequences or by polymerase chain reaction from cDNA. Phylogenetic analysis revealed that MHC class I sequences from Cetartiodactyl species closely related to cattle were distributed among the main cattle gene "groups", while those from more distantly related species were either scattered (sheep, deer) or clustered in a species-specific manner (sitatunga, giraffe). A comparison between gene and species trees showed a poor match, indicating that divergence of the MHC sequences had occurred independently from that of the hosts from which they were obtained. We also found two clear instances of interlocus recombination among the cattle MHC sequences. Finally, positive natural selection was documented at positions throughout the alpha 1 and 2 domains, primarily on those amino acids directly involved in peptide binding, although two positions in the alpha 3 domain, a region generally conserved in other species, were also shown to be undergoing adaptive evolution.

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.

Similar content being viewed by others

References

  • Adams EJ, Thomson G, Parham P (1999) Evidence for an HLA-C-like locus in the orangutan Pongo pygmaeus. Immunogenetics 49:865–871

    Article  CAS  PubMed  Google Scholar 

  • Bensaid A, Kaushal A, Baldwin CL, Clevers H, Young JR, Kemp Sj, MacHugh ND, Toye PG, Teale AJ (1991) Identification of expressed bovine class I MHC genes at 2 loci and demonstration of physical linkage. Immunogenetics 33:247–254

    CAS  PubMed  Google Scholar 

  • Boyson JE, Shufflebotham C, Cadavid LF, Urvater JA, Knapp LA, Hughes AL, Watkins DI (1996) The MHC class I genes of the rhesus monkey. J Immunol 156:4656–4665

    CAS  PubMed  Google Scholar 

  • Cadavid LF, Mejia B, Watkins DI (1999) MHC class I genes in a New World primate, the cotton-top tamarin, have evolved by an active process of loci turnover. Immunogenetics 49:196–205

    Article  CAS  PubMed  Google Scholar 

  • Di Palma F, Archibald SD, Young JR, Ellis SA (2002) A BAC contig of approximately 400 kb contains the classical class I MHC genes of cattle. Eur J Immunogenet 29:65–68

    Article  PubMed  Google Scholar 

  • Ellis SA, Martin AJ, Holmes EC, Morrison WI (1995) At least 4 MHC class I genes are transcribed in the horse. Eur J Immunogenet 22:249–260

    CAS  PubMed  Google Scholar 

  • Ellis SA, Staines KA Morrison WI (1996) cDNA sequence of cattle MHC class I genes transcribed in serologically defined haplotypes A18 and A31. Immunogenetics 43:156–159

    CAS  PubMed  Google Scholar 

  • Ellis SA, Holmes EC, Staines KA, Smith KB, Stear MJ, McKeever DJ, MacHugh ND, Morrison WI (1999) Variation in the number of expressed MHC genes in different cattle class I haplotypes. Immunogenetics 50:319–328

    Article  CAS  PubMed  Google Scholar 

  • Figueroa F, Mayer WE, Sato A, Zaleska-Rutczynska Z, Hess B, Tichy H, Klein J (2001) Mhc class I genes of swordtail fishes, Xiphophorus: Variation in the number of loci and existence of ancient gene families. Immunogenetics 53:695–708

    Article  CAS  PubMed  Google Scholar 

  • Fremont DH, Matsumura M, Stura EA, Peterson PA, Wilson IA (1992) Crystal structures of 2 viral peptides in complex with murine MHC class I H-2Kb. Science 257:919–926

    CAS  PubMed  Google Scholar 

  • Gaddum RM, Cook RS, Furze JM, Ellis SA, Taylor G (2003) Recognition of bovine respiratory syncytial virus proteins by bovine CD8+ T lymphocytes. Immunology 108:220–229

    Article  CAS  PubMed  Google Scholar 

  • Garrigan D, Hedrick PW (2001) Class I MHC polymorphism and evolution in endangered California Chinook and other Pacific salmon. Immunogenetics 53:483–489

    Article  CAS  PubMed  Google Scholar 

  • Geller R, Adams EJ, Guethlein LA, Little A-M, Madrigal JA, Parham P (2002) Linkage of Patr-AL to Patr-A and -B in the MHC of the common chimpanzee. Immunogenetics 54:212–215

    Article  CAS  PubMed  Google Scholar 

  • Hassanin A, Douzery EJP (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 13:227–243

    CAS  PubMed  Google Scholar 

  • Hegde NR, Ellis SA, Gaddum RM, Tregaskes CA, Sarath G, Srikumaran S (1995) Peptide motif of the cattle MHC class I antigen BoLA-A11. Immunogenetics 42:302–303

    CAS  PubMed  Google Scholar 

  • Holmes EC, Ellis SA (1999) Evolutionary history of MHC class I genes in the mammalian order Perissodactyla. J Mol Evol 49:316–324

    CAS  PubMed  Google Scholar 

  • Holmes EC, Worobey M, Rambaut A (1999) Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 16:405–409

    CAS  PubMed  Google Scholar 

  • Joly E, Leong L, Coadwell J, Clarkson C, Butcher GW (1996) The rat MHC haplotype RT1 c expresses 2 classical class I molecules. J Immunol 157:1551–1558

    CAS  PubMed  Google Scholar 

  • Klein J, Ono H, Klein D, O'hUigan C (1993) The accordion model of MHC evolution. In: Gergely J (ed) Progress in Immunology VIII. Springer, Heidelberg Berlin New York, pp 137–146

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920

    CAS  PubMed  Google Scholar 

  • Matthee CA, Robinson TJ (1999) Cytochrome b phylogeny of the family Bovidae: resolution within the Alcelaphini, Antilopini, Neotragini, and Tragelaphini. Mol Phylogenet Evol 12:31–46

    Article  CAS  PubMed  Google Scholar 

  • Miyamoto MW, Kraus F, Laipis PJ, Tanhauser SM, Webb SD (1993) Mitochondrial DNA phylogenies within artiodactyla. In: Szalay FS, Novacek MJ, McKenna MC (eds) Mammalian phylogeny (vol. 2 Placentals). Springer, New York Berlin Heidelberg, pp 268–281

  • Paquet ME, Williams DB (2002) Mutant MHC molecules define interactions between components of the peptide-loading complex. Int Immunol 14:347–358

    Article  PubMed  Google Scholar 

  • Parham P, Adams EJ, Arnett K (1995) The origins of HLA-A, B, C polymorphism. Immunol Rev 143:140–180

    Google Scholar 

  • Pichowski JS, Ellis SA, Morrison WI (1996) Sequence of 2 cattle MHC class I cDNAs associated with BoLA specificity. Immunogenetics 43:253–254

    Article  CAS  PubMed  Google Scholar 

  • Rambaut A, Grassly NC (1997) Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. CABIOS 13:235–238

    CAS  PubMed  Google Scholar 

  • Renard C, Vaiman M, Chiannilkulchai N, Cattolico L, Robert C, Chardon P (2001) Sequence of the pig MHC region containing the classical class I genes. Immunogenetics 53:490–500

    CAS  PubMed  Google Scholar 

  • Salter RD, Norment AM, Chen BP, Clayberger C, Krensky AM, Littman DR, Parham P (1989) Polymorphism in the alpha 3 domain of HLA-A molecules affects binding to CD8. Nature 338:345–347

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5469

    CAS  PubMed  Google Scholar 

  • Shilling HG, Guethlein LA, Cheng NW, Gardiner CM, Rodriguez R, Tyan D, Parham P (2002) Allelic polymorphism synergizes with variable gene content to individualize human KIR genotype. J Immunol 168:2307–2315

    CAS  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer, Sunderland, Mass., USA

  • Taracha ELN, Goddeeris BM, Teale AJ, Kemp SJ, Morrison WI (1995) Parasite strain specificity of bovine CTL responses to Theileria parva is determined primarily by immunodominance. J Immunol 155:4854–4860

    CAS  PubMed  Google Scholar 

  • Trowsdale J (2001) Genetic and functional relationships between MHC and NK receptor genes. Immunity 15:363–374

    PubMed  Google Scholar 

  • Wagner JL, Sarmiento UM, Storb R (2002) Cellular, serological, and molecular polymorphism of the class I and class II loci of the canine MHC. Tissue Antigens 59:205–210

    Article  CAS  PubMed  Google Scholar 

  • Wroblewski JM, Kaminsky SG, Nakamura I (1994) Bat-1 genes and the origin of multiple class I loci in the H-2D region. Immunogenetics 39:276–280

    CAS  PubMed  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13:555–556

    CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements.

This work was supported by the Biological Sciences and Biotechnology Research Council, UK, and the Wellcome Trust. We would like to thank Edmund Flach at Whipsnade Wild Animal Park, and Dr. Niall MacHugh, Moredun Research Institute, for providing blood samples, and Mike Charleston for assisting with the TreeMap analysis. Experiments carried out in this study comply with UK law.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    Edward C. Holmes

  2. Institute for Animal Health, Compton, Newbury, RG20 7NN, UK

    Karen A. Staines & Shirley A. Ellis

  3. Medical Research Council, Harwell, Oxfordshire, OX11 0RD, UK

    Ann F. C. Roberts

Authors
  1. Edward C. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ann F. C. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen A. Staines
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shirley A. Ellis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shirley A. Ellis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Holmes, E.C., Roberts, A.F.C., Staines, K.A. et al. Evolution of major histocompatibility complex class I genes in Cetartiodactyls. Immunogenetics 55, 193–202 (2003). https://doi.org/10.1007/s00251-003-0560-2

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-003-0560-2

Keywords

Search

Navigation