Skip to main content
Log in

Comparative genomics of major histocompatibility complexes

  • Review
  • Published:
Immunogenetics Aims and scope Submit manuscript

Abstract

The major histocompatibility complex (MHC) is a gene dense region found in all jawed vertebrates examined to date. The MHC contains a high percentage of immune genes, in particular genes involved in antigen presentation, which are generally highly polymorphic. The region plays an important role in disease resistance. The clustering of MHC genes could be advantageous for co-evolution or regulation, and its study in many species is desirable. Even though some linkage of MHC genes is apparent in all gnathostomes, the genomic organization can differ greatly by species, suggesting rapid evolution of MHC genes after divergence from a common ancestor. Previous reviews of comparative MHC organization have been written when relatively fragmentary sequence and mapping data were available on many species. This review compares maps of MHC gene orders in commonly studied species, where extensive sequencing has been performed.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Notes

  1. The adaptive immune is traditionally thought to be possessed by only jawed vertebrates, due to, among other factors, the emergence of rearranging immunoglobulin segments (Kaufman 2002). However, a recent study has shown that a jawless vertebrate rearranges leucine-rich repeat (LRR) modules to create varying lymphocyte receptors useful in an adaptive response (Pancer et al. 2004). Therefore, given the presence of a type of adaptive immune system in lampreys (Flajnik 2004), the definition of adaptive immune system and the accepted evolutionary date of its emergence will likely be a topic of discussion in the immediate future.

  2. In mice and rats, the centromeric H2-K and RT1-A genes are still closely linked to TAP genes.

References

  • Abi-Rached L, Gilles A, Shiina T, Pontarotti P, Inoko H (2002) Evidence of en bloc duplication in vertebrate genomes. Nat Genet 31:100–105

    Article  CAS  PubMed  Google Scholar 

  • Adams EJ, Parham P (2001a) Genomic analysis of common chimpanzee major histocompatibility complex class I genes. Immunogenetics 53:200–208

    Article  CAS  PubMed  Google Scholar 

  • Adams EJ, Parham P (2001b) Species-specific evolution of MHC class I genes in the higher primates. Immunol Rev 183:41–64

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Adams EJ, Cooper S, Parham P (2001) A novel, nonclassical MHC class I molecule specific to the common chimpanzee. J Immunol 167:3858–3869

    CAS  PubMed  Google Scholar 

  • Aguado B, Milner CM, Campbell RD (1996) Genes of the MHC class III region and the functions of the proteins they encode. In: Browning M, McMichael A (eds) HLA and MHC: genes, molecules, and functions. Bios, Oxford, pp 39–76

    Google Scholar 

  • Amadou C (1999) Evolution of the MHC class I region: the framework hypothesis. Immunogenetics 49:362–367

    Article  CAS  PubMed  Google Scholar 

  • Amills M, Ramiya V, Norimine J, Lewin HA (1998) The major histocompatibility of ruminants. Rev Sci Tech 17:108–120

    CAS  PubMed  Google Scholar 

  • Anzai T, Shiina T, Kimura N, Yanagiya K, Kohara S, Shigenari A, Yamagata T, Kulski JK, Naruse TK, Fujimori Y, Fukuzumi Y, Yamazaki M, Tashiro H, Iwamoto C, Umehara Y, Imanishi T, Meyer A, Ikeo K, Gojobori T, Bahram S, Inoko H (2003) Comparative sequencing of human and chimpanzee MHC class I regions unveils insertions/deletions as the major path to genomic divergence. Proc Natl Acad Sci USA 100:7708–7713

    Article  CAS  PubMed  Google Scholar 

  • Ballingall KT, Ellis SA, MacHugh ND, Archibald SD, McKeever DJ (2004) The DY genes of the cattle MHC: expression and comparative analysis of an unusual class II MHC gene pair. Immunogenetics 55:748–755

    Article  CAS  PubMed  Google Scholar 

  • Band M, Larson JH, Womack JE, Lewin HA (1998) A radiation hybrid map of BTA23: identification of a chromosomal rearrangement leading to separation of the cattle MHC class II subregions. Genomics 53:269–275

    Article  CAS  PubMed  Google Scholar 

  • Bartl S, Weissman IL (1994) Isolation and characterization of major histocompatibility complex class IIB genes from the nurse shark. Proc Natl Acad Sci USA 91:262–266

    Google Scholar 

  • Bartl S, Baish MA, Flajnik MF, Ohta Y (1997) Identification of class I genes in cartilaginous fish, the most ancient group of vertebrates displaying an adaptive immune response. J Immunol 159:6097–6104

    CAS  PubMed  Google Scholar 

  • Beck S, Trowsdale J (2000) The human major histocompatibility complex: lessons from the DNA sequence. Annu Rev Genomics Hum Genet 1:117–137

    Article  Google Scholar 

  • Beck S, Kelly A, Radley E, Khurshid F, Alderton RP, Trowsdale J (1992) DNA sequence analysis of 66 kb of the human MHC class II region encoding a cluster of genes for antigen processing. J Mol Biol 228:433–441

    CAS  PubMed  Google Scholar 

  • Belov K, Lam MKP, Hellman L, Colgan DJ (2003) Evolution of the major histocompatibility complex: isolation of class II beta cDNAs from two monotremes, the platypus and the short-beaked echidna. Immunogenetics 55:402–411

    Article  CAS  PubMed  Google Scholar 

  • Benacerraf B (1981) Role of MHC gene products in immune regulation. Science 212:1229–1238

    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  CAS  PubMed  Google Scholar 

  • Boyson JE, Shufflebotham C, Cadavid LF, Urvater JA, Knapp LA, Hughes AL, Watkins DL (1996) The MHC class I genes of the Rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 156:4656–4665

    CAS  PubMed  Google Scholar 

  • Browning TL, Belov K, Miller RD, Eldridge MDB (2004) Molecular cloning and characterization of the polymorphic MHC class II DBB from the tammar wallaby (Macropus eugenii). Immunogenetics 55:791–795

    Article  CAS  PubMed  Google Scholar 

  • Cadavid LF, Shufflebotham C, Ruiz FJ, Yeager M, Hughes AL, Watkins DL (1997) Evolutionary instability of the major histocompatibility complex class I loci in new world primates. Proc Natl Acad Sci USA 94:14536–14541

    Google Scholar 

  • Cadavid LF, Mejia BE, Watkins DL (1999) MHC class I genes in a new world primate, the cotton-top tamarin (Saguinus oedipus), have evolved by an active process of loci turnover. Immunogenetics 49:196–205

    Article  CAS  PubMed  Google Scholar 

  • Carrington M, Bontrop RE (2002) Effects of MHC class I on HIV/SIV disease in primates. AIDS 16:S105–S114

    CAS  PubMed  Google Scholar 

  • Castro LFC, Furlong RF, Holland PWH (2004) An antecedent of the MHC-linked genomic region in Amphioxus. Immunogenetics 55:782–784

    Article  CAS  PubMed  Google Scholar 

  • Cattley SK, Longman N, Dawkins RL, Gaudieri S, Kulski JK, Leelayuwat C (1999) Phylogenetic analysis of primate MIC (PERB11) sequences suggests that the representation of the gene family differs in different primates: comparison of MIC (PERB11) and C4. Eur J Immunogenet 26:233–238

    Article  CAS  PubMed  Google Scholar 

  • Chardon P, Renard C, Gaillard CR, Vaiman M (2000) The porcine major histocompatibility complex and paralagous regions: a review. Genet Sel Evol 32:109–128

    Article  CAS  PubMed  Google Scholar 

  • Clark MS, Pontarotti P, Gilles A, Kelly A, Elgar G (2000) Identification and characterization of a β proteasome subunit cluster in the Japanese pufferfish (Fugu rubripes). J Immunol 165:4446–4452

    Google Scholar 

  • Clark MS, Shaw L, Kelly A, Snell P, Elgar G (2001) Characterization of the MHC class I region of the Japanese pufferfish (Fugu rubripes). Immunogenetics 52:174–185

    Google Scholar 

  • Courtet M, Flajnik MF, Du Pasquier L (2001) Major histocompatibility complex and immunoglobulin loci visualized by in situ hybridization on Xenopus chromosomes. Dev Comp Immunol 25:149–157

    Article  CAS  PubMed  Google Scholar 

  • Danchin EGJ, Abi-Rached L, Gilles A, Pontarotti P (2003) Conservation of the MHC-like region throughout evolution. Immunogenetics 55:141–148

    Google Scholar 

  • Danchin EGJ, Vitiello V, Vienne A, Richard O, Gouret P, McDermott MF, Pontarotti P (2004) The major histocompatibility complex origin. Immunol Rev 198:216–232

    Article  CAS  PubMed  Google Scholar 

  • Dausset J (1959) Iso-leuco-anticorps. Acta Haematol 20:156

    Google Scholar 

  • Delarbre C, Jaulin C, Kourilsky P, Gachelin G (1992) Evolution of the major histocompatibility complex: a hundred-fold amplification of MHC class I genes in the African pigmy mouse Nannomys setulosus. Immunogenetics 37:29–38

    Google Scholar 

  • De Tomaso AW, Weissman IL (2003) Initial characterization of a protochordate histocompatibility locus. Immunogenetics 55:480–490

    Google Scholar 

  • De Tomaso AW, Weissman IL (2004) Evolution of a protochordate allorecognition locus. Science 303:977

    Google Scholar 

  • Edwards SV, Grahn M, Potts WK (1995a) Dynamics of MHC evolution in birds and crocodilians: amplification of class II genes with degenerate primers. Mol Ecol 4:719–729

    CAS  PubMed  Google Scholar 

  • Edwards SV, Wakeland EK, Potts WK (1995b) Contrasting histories of avian and mammalian MHC genes revealed by class II B sequences from songbirds. Proc Natl Acad Sci USA 92:12200–12204

    Google Scholar 

  • Edwards SV, Gasper J, Garrigan D, Martindale D, Koop BF (2000) A 39-kb sequence around a blackbird MHC class II gene: ghost of selection past and songbird genome architecture. Mol Biol Evol 17:1384–1395

    CAS  PubMed  Google Scholar 

  • Ellis SA, Ballingall KT (1999) Cattle MHC: evolution in action? Immunol Rev 167:159–168

    Google Scholar 

  • Escriva H, Manzon L, Youson J, Laudet V (2002) Analysis of lamprey and hagfish genes reveals a complex history of gene duplications during early vertebrate evolution. Mol Biol Evol 19:1440–1450

    CAS  PubMed  Google Scholar 

  • Fagan MB, Weissman IL (1998) Linkage analysis of HSP70 genes and historecognition locus in Botryllus schlosseri. Immunogenetics 47:468–476

    Google Scholar 

  • Fernández-Busquets X, Burger MM (1999) Cell adhesion and histocompatibility in sponges. Microsc Res Tech 44:204–218

    Article  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

    Google Scholar 

  • Flajnik MF (2004) Immunology: another manifestation of GOD. Nature 430:157–158

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Flajnik MF, Kasahara M, Shum BP, Salter-Cid L, Taylor E, Du Pasquier L (1993) A novel type of class I gene organization in vertebrates: a large family of non-MHC-linked class I genes is expressed at the RNA level in the amphibian Xenopus. EMBO J 12:4385–4396

    CAS  PubMed  Google Scholar 

  • Flajnik MF, Ohta Y, Namikawa-Yamada C, Nonaka M (1999) Insight into the primordial MHC from studies in ectothermic vertebrates. Immunol Rev 167:59–67

    Google Scholar 

  • Flügge P, Zimmermann E, Hughes AL, Gunther E, Walter L (2002) Characterization and phylogenetic relationship of prosimian MHC class I genes. J Mol Evol 55:768–775

    Article  PubMed  Google Scholar 

  • Frangoulis B, Park I, Guillemot F, Severac V, Auffray C, Zoorob R (1999) Identification of the tapasin gene in the chicken major histocompatibility complex. Immunogenetics 49:328–337

    Google Scholar 

  • Freeman-Gallant CR, Johnson EM, Saponara F, Stanger M (2002) Variation at the major histocompatibility complex in savannah sparrows. Mol Ecol 11:1125–1130

    Google Scholar 

  • Gebe JA, Swanson E, Kwok WW (2002) HLA class II peptide-binding and autoimmunity. Tissue Antigens 59:78–87

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Geraghty DE, Daza R, Williams LM, Vu Q, Ishitani A (2002) Genetics of the immune response: identifying immune variation within the MHC and throughout the genome. Immunol Rev 190:69–85

    Google Scholar 

  • Glynne R, Powis SH, Beck S, Kelly A, Kerr L-A, Trowsdale J (1991) A proteasome-related gene between the two ABC transporter loci in the class II region of the human MHC. Nature 353:357–360

    Article  CAS  PubMed  Google Scholar 

  • Go Y, Satta Y, Kawamoto Y, Rakotoarisoa G, Randrianjafy A, Koyama N, Hirai H (2003) Frequent segmental sequence exchanges and rapid gene duplication characterize the MHC class I genes in lemurs. Immunogenetics 55:450–461

    Google Scholar 

  • Gorer PA, Lyman S, Snell GD (1948) Studies on the genetic and antigenic basis of tumour transplantation: linkage between a histocompatibility gene and “Fused” in mice. Proc R Soc Lond 135:499–505

    Google Scholar 

  • Grossberger D, Parham P (1992) Reptilian class I major histocompatibility complex genes reveal conserved elements in class I structure. Immunogenetics 36:166–174

    Google Scholar 

  • Gruen JR, Weissman SM (1997) Evolving views of the major histocompatability complex. Blood 90:4252–4265

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gustafson AL, Tallmadge RL, Ramlachan N, Miller D, Bird H, Antczak DF, Raudsepp T, Chowdhary BP, Skow LC (2003) An ordered BAC contig map of the equine major histocompatibility complex. Cytogenet Genome Res 102:189–195

    Article  CAS  PubMed  Google Scholar 

  • Hansen JD, Strassburger P, Du Pasquier L (1996) Conservation of an alpha 2 domain within the teleostean world, MHC class I from the rainbow trout Oncorhynchus mykiss. Dev Comp Immunol 20:417–425

    Article  CAS  PubMed  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

    Google Scholar 

  • Herberg JA, Beck S, Trowsdale J (1998) TAPASIN, DAXX, RGL2, HKE2 and four new genes (BING1, 3 to 5) form a dense cluster at the centromeric end of the MHC. J Mol Biol 277:839–857

    Article  CAS  PubMed  Google Scholar 

  • Holling T, Schooten E, van Den Elsen PJ (2004) Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men. Hum Immunol 65:282–290

    Article  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 

  • Horton R, Wilming LG, Rand V, Lovering RC, Bruford EA, Khodiyar VK, Talbot CC, Wright MW, Wain HM, Trowsdale J, Ziegler A, Beck S (2004) Gene map of the extended human major histocompatibility complex. Nat Genet Rev (in press)

  • Houlden BA, Greville WD, Sherwin WB (1996) Evolution of MHC class I loci in marsupials: characterization of sequences from koala (Phascolarctos cinereus). Mol Biol Evol 13:1119–1127

    CAS  PubMed  Google Scholar 

  • Hughes AL (1995) Origin and evolution of HLA class I pseudogenes. Mol Biol Evol 12:247–258

    CAS  PubMed  Google Scholar 

  • Hughes AL, Nei M (1989) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579

    CAS  PubMed  Google Scholar 

  • Hurt P, Walter L, Sudbrak R, Klages S, Muller I, Shiina T, Inoko H, Lehrach H, Günther E, Reinhardt R, Himmelbauer H (2004) The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res 14:631–639

    Article  CAS  PubMed  Google Scholar 

  • Ishii T, Hirota J, Mombaerts P (2003) Combinatorial coexpression of neural and immune multigene families in mouse vomeronasal sensory neurons. Curr Biol 13:394–400

    Article  CAS  PubMed  Google Scholar 

  • Joly E, Le Rolle A-F, Gonzalez AL, Mehling B, Stevens J, Coadwell WJ, Hunig T, Howard JC, Butcher GW (1998) Co-evolution of rat TAP transporters and MHC class I RT1-A molecules. Curr Biol 8:169–172

    Article  CAS  PubMed  Google Scholar 

  • Juul-Madsen HR, Dalgaard TS, Guldbrandtsen B, Salomonsen J (2000) A polymorphic major histocompatibility complex class II-like locus maps outside of both the chicken B-system and Rfp-Y system. Eur J Immunogenet 27:63–71

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Kasahara M (2000) Major histocompatibility complex: evolution, structure, and function. Springer, Tokyo

    Google Scholar 

  • Kasahara M, Vazquez M, Sato K, McKinney EC, Flajnik MF (1992) Evolution of the major histocompatibility complex: isolation of class II A cDNA clones from the cartilaginous fish. Proc Natl Acad Sci USA 89:6688–6692

    Google Scholar 

  • Kasahara M, Hayashi M, Tanaka K, Inoko H, Sugaya K, Ikemura T, Ishibashi T (1996) Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. Proc Natl Acad Sci USA 93:9096–9101

    Google Scholar 

  • Kasahara M, Watanabe Y, Sumasu M, Negata T (2002) A family of MHC class I-like genes located in the vicinity of the mouse leukocyte receptor complex. Proc Natl Acad Sci USA 99:13687–13692

    Google Scholar 

  • Kasahara M, Suzuki T, Du Pasquier L (2004) On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25:105–111

    Article  CAS  PubMed  Google Scholar 

  • Katsanis N, Fitzgibbon J, Fisher EMC (1996) Paralogy mapping: identification of a region in the human MHC triplicated onto human chromosomes 1 and 9 allows the prediction and isolation of novel PBX and NOTCH loci. Genomics 35:101–108

    Article  CAS  PubMed  Google Scholar 

  • Kaufman J (2002) The origins of the adaptive immune system: whatever next? Nat Immunol 3:1124–1125

    Google Scholar 

  • Kaufman J, Skjoedt K, Salomonsen J (1990) The MHC molecules of nonmammalian vertebrates. Immunol Rev 113:83–117

    CAS  PubMed  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, Gobel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999a) The chicken B locus is a minimal major histocompatibility complex. Nature 401:923–925

    Article  CAS  PubMed  Google Scholar 

  • Kaufman J, Jacob JP, Shaw I, Walker B, Milne S, Beck S, Salomonsen J (1999b) Gene organization determines evolution of function in the chicken MHC. Immunol Rev 167:101–117

    Google Scholar 

  • Kelly A, Powis SH, Glynne R, Radley E, Beck S, Trowsdale J (1991) Second proteasome-related gene in the human MHC class II region. Nature 353:667–668

    Article  CAS  PubMed  Google Scholar 

  • Khalturin K, Becker M, Rinkevich B, Bosch TCG (2003) Urochordates and the origin of natural killer cells: identification of a CD94/NKR-P1-related receptor in blood cells of Botryllus. Proc Natl Acad Sci 100:622–627

    Google Scholar 

  • Klein J (1976) Evolution and function of the major histocompatibility complex: facts and speculations. In: Gotze D (ed) The major histocompatibility system in man and animals. Springer, New York Berlin Heidelberg, pp 339–378

    Google Scholar 

  • Klein J, Sato A (1998) Birth of the major histocompatibility complex. Scand J Immunol 47:199–209

    Article  CAS  PubMed  Google Scholar 

  • Kobari F, Sato K, Shum BP, Tochinai S, Katagiri M, Ishibashi T, Du Pasquier L, Flajnik MF, Kasahara M (1995) Exon–intron organization of Xenopus class II beta chain genes. Immunogenetics 42:376–385

    Google Scholar 

  • Kulski JK, Shiina T, Anzai T, Kohara S, Inoko H (2002) Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity, and complexity from shark to man. Immunol Rev 190:95–122

    Article  CAS  PubMed  Google Scholar 

  • Kumánovics A, Takada T, Lindahl KF (2003) Genomic organization of the mammalian MHC. Annu Rev Immunol 21:629–657

    Article  PubMed  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

    Google Scholar 

  • Kuroda N, Figueroa F, O’hUigin C, Klein J (2002) Evidence that the separation of MHC class II from class I loci in the zebrafish, Danio rerio, occurred by translocation. Immunogenetics 54:418–430

    Article  CAS  PubMed  Google Scholar 

  • Laird DJ, De Tomaso AW, Cooper MD, Weissman IL (2000) 50 Million years of chordate evolution: seeking the origins of adaptive immunity. Proc Natl Acad Sci USA 97:6924–6926

    Google Scholar 

  • Lambracht-Washington D, Lindahl KF (2004) Active MHC class Ib genes in rat are pseudogenes in the mouse. Immunogenetics 56:118–121

    Google Scholar 

  • Lawlor DA, Warren E, Taylor P, Parham P (1991) Gorilla class I major histocompatibility complex alleles: comparison to human and chimpanzee class I. J Exp Med 174:1491–1509

    Article  CAS  PubMed  Google Scholar 

  • Lienert K, Parham P (1996) Evolution of MHC class I genes in higher primates. Immunol Cell Biol 74:349–356

    CAS  PubMed  Google Scholar 

  • Loconto J, Papes F, Chang E, Stowers L, Jones EP, Takada T, Kumanovics A, Lindahl KF, Dulac C (2003) Functional expression of murine V2R pheromone receptors involves selective association with the M10 and M1 families of MHC class Ib molecules. Cell 112:607–618

    Article  CAS  PubMed  Google Scholar 

  • Madden DR (1995) The three-dimensional structure of peptide-MHC complexes. Annu Rev Immunol 13:587–622

    Article  CAS  PubMed  Google Scholar 

  • Magor BG, De Tomaso AW, Rinkevich B, Weissman IL (1999) Allorecognition in colonial tunicates: protection against predatory cell lineages. Immunol Rev 167:69–79

    Google Scholar 

  • Malaga-Trillo E, Zaleska-Rutczynska Z, McAndrew B, Vincek V, Figueroa F, Sultmann H, Klein J (1998) Linkage relationships and haplotype polymorphism among cichlid MHC class II B loci. Genetics 149:1527–1537

    CAS  PubMed  Google Scholar 

  • Matsuo MY, Asakawa S, Shimizu N, Kimura H, Nonaka M (2002) Nucleotide sequence of the MHC class I genomic region of a teleost, the medaka (Oryzias latipes). Immunogenetics 53:930–940

    Article  CAS  PubMed  Google Scholar 

  • Mayer WE, Jonker M, Klein D, Ivanyi P, van Seventer G, Klein J (1988) Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J 7:2765–2774

    CAS  PubMed  Google Scholar 

  • McConnell TJ, Godwin UB, Cuthbertson BJ (1998a) Expressed major histocompatibility complex class II loci in fishes. Immunol Rev 166:294–300

    CAS  PubMed  Google Scholar 

  • McConnell TJ, Godwin UB, Norton SF, Nairn RS, Kazianis S, Morizot DC (1998b) Identification and mapping of two divergent, unlinked major histocompatibility complex class II B genes in Xiphophorus fishes. Genetics 149:1921–1934

    CAS  PubMed  Google Scholar 

  • MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921–923

    Google Scholar 

  • Michalova V, Murray BW, Sultmann H, Klein J (2000) A contig map of the MHC class I genomic region in the zebrafish reveals ancient synteny. J Immunol 164:5296–5305

    Google Scholar 

  • Miller KM, Withler RE (1998) The salmonid class I MHC: limited diversity in a primitive teleost. Immunol Rev 166:279–293

    Google Scholar 

  • Miller MM, Goto RM, Bernot A, Zoorob R, Auffray C, Bumstead N, Briles WE (1994) Two MHC class I and two MHC class II genes map to the chicken Rfp-Y system outside the B complex. Proc Natl Acad Sci USA 91:4397–4401

    CAS  PubMed  Google Scholar 

  • Milner CM, Campbell RD (2001) Genetic organization of the human MHC class III region. Front Biosci 6:D914–D926

    CAS  PubMed  Google Scholar 

  • Miska K, Miller RD (1999) Marsupial MHC class I: classical sequences from the opossum, Monodelphis domestica. Immunogenetics 50:89–93

    Google Scholar 

  • Miska K, Harrison GA, Hellman L, Miller RD (2002) The major histocompatibility complex in monotremes: an analysis of the evolution of MHC class I genes across all three mammalian subclasses. Immunogenetics 54:381–393

    Google Scholar 

  • Monaco JJ (1992) Major histocompatibility complex-linked transport proteins and antigen processing. Immunol Res 11:125–132

    CAS  PubMed  Google Scholar 

  • Moretta A, Vitale M, Bottino C, Orengo AM, Morelli L, Augugliaro R, Barbaresi M, Ciccone E, Moretta L (1993) p58 Molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I protected cells in NK clones displaying different specificities. J Exp Med 178:597–604

    Article  CAS  PubMed  Google Scholar 

  • Müller WE, Blumbach B, Müller IM (1999) Evolution of the innate and adaptive immune systems: relationships between potential immune molecules in the lowest metazoan phylum (Porifera) and those in vertebrates. Transplantation 68:1215–1227

    PubMed  Google Scholar 

  • Müller WE, Krasko A, Skorokhod A, Bünz C, Grebenjuk VA, Steffen R, Batel R, Schröder HC (2002) Histocompatibility reaction in tissue and cells of the marine sponge Suberites domuncula in vitro and in vivo: central role of the allograft inflammatory factor 1. Immunogenetics 54:48–58

    Google Scholar 

  • Murray BW, Sültmann H, Klein J (1999) Analysis of a 26-kb region linked to the MHC in zebrafish: genomic organization of the proteasome component beta/transporter associated with antigen processing-2 gene cluster and identification of five new proteasome beta subunit genes. J Immunol 163:2657–2666

    Google Scholar 

  • Murray BW, Nilsson P, Zaleska-Rutczynska Z, Sultmann H, Klein J (2000) Linkage relationships and haplotype variation of the major histocompatibility complex class I A genes in the cichlid fish Oreochromis niloticus. Mar Biotechnol (NY) 2:437–448

    Google Scholar 

  • Naper C, Ryan JC, Kirsch R, Butcher GW, Rolstad B, Vaage JT (1999) Genes in two major histocompatibility complex class I regions control selection, phenotype, and function of a rat Ly-49 natural killer cell subset. Eur J Immunol 29:2046–2053

    Google Scholar 

  • Nizetic D, Figueroa F, Dembic Z, Nevo E, Klein J (1987) Major histocompatibility complex gene organization in the mole rat Spalax ehrenbergi: evidence for transfer of function between class II genes. Proc Natl Acad Sci USA 84:5828–5832

    Google Scholar 

  • Nonaka M (2001) Evolution of the complement system. Curr Opin Immunol 13:69–73

    Google Scholar 

  • Nonaka M, Namikawa C, Kato Y, Sasaki M, Salter-Cid L, Flajnik MF (1997) Major histocompatibility complex gene mapping in the amphibian Xenopus implies a primordial organization. Proc Natl Acad Sci USA 94:5789–5791

    Google Scholar 

  • Nonaka M, Matsuo M, Naruse K, Shima A (2001) Comparative genomics of medaka: the major histocompatibility complex (MHC). Mar Biotechnol (NY) 3:141–144

    Google Scholar 

  • O’Callaghan CA, Bell JI (1998) Structure and function of the human MHC class Ib molecules HLA-E, HLA-F, and HLA-G. Immunol Rev 163:129–138

    Google Scholar 

  • Ohta Y, Kazuhiko O, McKinney EC, Bartl S, Hashimoto K, Flajnik MF (2000) Primitive synteny of vertebrate major histocompatibility complex class I and class II genes. Proc Natl Acad Sci USA 97:4712–4717

    Google Scholar 

  • Ohta Y, McKinney EC, Criscitiello MF, Flajnik MF (2002) Proteasome, transporter associated with antigen processing, and class I genes in the nurse shark Ginglymostoma cirratum: evidence for a stable class I region and MHC haplotype lineages. J Immunol 168:771–781

    Google Scholar 

  • Ohta Y, Powis SH, Lohr RL, Nonaka M, Pasquier LD, Flajnik MF (2003) Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co-evolution among MHC class I region genes. Eur J Immunol 33:3017–3027

    Google Scholar 

  • Okamura K, Ototake M, Nakanishi T, Kurosawa Y, Hashimoto K (1997) The most primitive vertebrates with jaws possess highly polymorphic MHC class I genes comparable to those of humans. Immunity 7:777–790

    Article  CAS  PubMed  Google Scholar 

  • Pancer Z, Amemiya CT, Ehrhardt GRA, Ceitlin J, Gartland GL, Cooper MD (2004) Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 430:174–180

    Article  CAS  PubMed  Google Scholar 

  • Persson A-C, Stet RJM, Pilstrom L (1999) Characterization of MHC class I and beta(2)-microglobulin sequences in Atlantic cod reveals an unusually high number of expressed class I genes. Immunogenetics 50:49–59

    Google Scholar 

  • van der Poel JJ, Groenen MA, Dijkhof RJ, Ruyter D, Giphart MJ (1990) The nucleotide sequence of the bovine MHC class II alpha genes: DRA, DOA, and DYA. Immunogenetics 31:29–36

    Google Scholar 

  • Radtkey RR, Becker B, Miller RD, Riblet R, Case TJ (1996) Variation and evolution of class I MHC in sexual and parthenogenetic geckos. Proc R Soc Lond B Biol Sci 263:1023–1032

    CAS  PubMed  Google Scholar 

  • Ritz U, Seliger B (2001) The transporter associated with antigen processing (TAP): structural integrity, expression, function, and its clinical relevance. Mol Med 7:149–158

    CAS  PubMed  Google Scholar 

  • Rolstad B, Naper C, Lovik G, Vaage JT, Ryan JC, Backman-Petersson E, Kirsch RD, Butcher GW (2002) Rat natural killer cell receptor systems and recognition of MHC class I molecules. Immunol Rev 181:149–157

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Salomonsen J, Marston D, Avila D, Bumstead N, Johansson B, Juul-Madsen H, Olesen GD, Riegert P, Skjodt K, Vainio O, Wiles MV, Kaufman J (2003) The properties of the single chicken MHC class II alpha chain (B-LA) gene indicate an ancient origin for the DR/E-like isotype of class II molecules. Immunogenetics 55:605–614

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Sambrook JG, Campbell RD, Elgar G (2003) Characterisation of a gene cluster in Fugu rubripes containing the complement component C4 gene. Gene 312:73–83

    Article  CAS  PubMed  Google Scholar 

  • Sammut B, Du Pasquier L, Ducoroy P, Laurens V, Marcuz A, Tournefier A (1999) Axolotl MHC architecture and polymorphism. Eur J Immunol 29:2897–2907

    Google Scholar 

  • Sammut B, Marcuz A, Du Pasquier L (2002) The fate of duplicated major histocompatibility complex class Ia Genes in a dodecaploid amphibian, Xenopus ruwenzoriensis. Eur J Immunol 32:2698–2709

    Google Scholar 

  • Sato K, Flajnik MF, Du Pasquier L, Katagiri M, Kasahara M (1993) Evolution of the MHC: isolation of class II beta-chain cDNA clones from the amphibian Xenopus laevis. J Immunol 150:2831–2843

    Google Scholar 

  • Sato A, Figueroa F, Murray BW, Malaga-Trillo E, Zaleska-Rutczynska Z, Sultmann H, Toyosawa S, Wedekind C, Steck N, Klein J (2000) Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes. Immunogenetics 51:108–116

    Article  CAS  PubMed  Google Scholar 

  • Scott PC, Choi CL, Brandon MR (1987) Genetic organization of the ovine MHC class II region. Immunogenetics 25:116–122

    Google Scholar 

  • Seo JW, Bontrop RE, Walter L, Günther E (1999) Major histocompatibility complex-linked MIC genes in rhesus macaques and other primates. Immunogenetics 50:358–362

    Google Scholar 

  • Seo JW, Walter L, Günther E (2001) Genomic analysis of MIC genes in rhesus macaques. Tissue Antigens 58:159–165

    Article  CAS  PubMed  Google Scholar 

  • Shiina T, Shimizu C, Oka A, Teraoka Y, Imanishi T, Gojobori T, Hanzawa K, Watanabe S, Inoko H (1999a) Gene organization of the quail major histocompatibility complex (MhcCoja) class I gene region. Immunogenetics 49:384–394

    Article  CAS  PubMed  Google Scholar 

  • Shiina T, Tamiya G, Oka A, Takishima N, Yamagata T, Kikkawa E, Iwata K, Tomizawa M, Okuaki N, Kuwano Y, Wantanabe K, Fukuzumi Y, Itakura S, Sugawara C, Ono A, Yamazaki M, Tashiro H, Ando A, Ikemura T, Soeda E, Kimura M, Bahram S, Inoko H (1999b) Molecular dynamics of MHC genesis unraveled by sequence analysis of the 1,796,938-bp HLA class I region. Proc Natl Acad Sci USA 96:13282–13287

    Google Scholar 

  • Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S, Hanzawa K, Beck S, Kulski JK, Inoko H (2004) Comparative genomic analysis of two avian (Quail and Chicken) MHC regions. J Immunol 172:6751–6763

    CAS  PubMed  Google Scholar 

  • Shum BP, Avila D, Du Pasquier L, Kasahara M, Flajnik MF (1993) Isolation of a classical class I cDNA from an amphibian. Evidence for only one class I locus in the Xenopus MHC. J Immunol 151:5376–5386

    Google Scholar 

  • Shum BP, Guethlein L, Flodin LR, Adkison MA, Hedrick RP, Nehring RB, Stet RJM, Secombes C, Parham P (2001) Modes of salmonid MHC class I and II evolution differ from the primate paradigm. J Immunol 166:3297–3308

    CAS  PubMed  Google Scholar 

  • Sidebottom DA, Kennedy R, Hildebrand WH (2001) Class I MHC expression in the yellow baboon. J Immunol 166:3983–3993

    Google Scholar 

  • Singer DS, Mozes E, Kirshner S, Kohn LD (1997) Role of MHC class I molecules in autoimmune disease. Crit Rev Immunol 17:463–468

    CAS  PubMed  Google Scholar 

  • Snell GD (1981) Studies in histocompatibility. Science 213:172–178

    Google Scholar 

  • Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2003) Placental mammal diversification and the cretaceous-tertiary boundary. Proc Natl Acad Sci USA 100:1056–1061

    Article  CAS  PubMed  Google Scholar 

  • Steffer A, Schubart A, Storch M, Amini A, Mather I, Lassmann H, Linington C (2000) Butyrophilin, a milk protein, modulates the encephalitogenic T cell response to myelin oligodendrocyte glycoprotein in experimental autoimmune encephalomyelitis. J Immunol 165:2859–2865

    Google Scholar 

  • Stenzel A, Lu T, Koch WA, Hampe J, Guenther SM, De La Vega FM, Krawczak M, Schreiber S (2004) Patterns of linkage disequilibrium in the MHC region on human chromosome 6p. Hum Genet 114:377–385

    Article  CAS  PubMed  Google Scholar 

  • Stephens R, Horton R, Humphray S, Rowen L, Trowsdale J, Beck S (1999) Gene organisation, sequence variation and isochore structure at the centromeric boundary of the human MHC. J Mol Biol 291:789–799

    Article  CAS  PubMed  Google Scholar 

  • Stet RJM, Johnstone R, Parham P, Wiegertjes GF (1997) The unMHC of teleostean fish: segregation analyses in common carp and Atlantic salmon. Hereditas 127:169–170

    Google Scholar 

  • Stet RJM, Kruiswijk CP, Saeij JP, Wiegertjes GF (1998) Major histocompatibility genes in cyprinid fishes: theory and practice. Immunol Rev 166:301–316

    Google Scholar 

  • Stone RT, Muggli-Cockett NE (1990) Partial nucleotide sequence of a novel bovine major histocompatibility complex class II beta-chain gene, BoLA-DIB. Anim Genet 21:353–360

    CAS  PubMed  Google Scholar 

  • Sudbrak R, Reinhardt R, Hennig S, Lehrach H, Günther E, Walter L (2003) Comparative and evolutionary analysis of the rhesus macaque extended MHC class II region. Immunogenetics 54:699–704

    Google Scholar 

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

    Google Scholar 

  • Takada T, Kumanovics A, Amadou C, Yoshino M, Jones EP, Athanasiou M, Evans GA, Lindahl KF (2003) Species-specific class I gene expansions formed the telomeric 1 Mb of the mouse major histocompatibility complex. Genome Res 13:589–600

    Article  CAS  PubMed  Google Scholar 

  • Takahashi K, Rooney AP, Nei M (2000) Origins and divergence times of mammalian class II MHC gene clusters. J Hered 91:198–204

    Article  CAS  PubMed  Google Scholar 

  • Takami K, Zaleska-Rutczynska Z, Figueroa F, Klein J (1997) Linkage of LMP, TAP, and RING3 with MHC class I rather than class II genes in the zebrafish. J Immunol 159:6052–6060

    Google Scholar 

  • Terado T, Okamura K, Ohta Y, Shin D-H, Smith SL, Hashimoto K, Takemoto T, Nonaka MI, Kimura H, Flajnik MF, Nonaka M (2003) Molecular cloning of C4 gene and identification of the class III complement region in the shark MHC. J Immunol 171:2461–2466

    Google Scholar 

  • Totaro A, Rommens JM, Grifa A, Lunardi C, Carella M, Huizenga JJ, Roetto A, Camaschella C, De Sandre G, Gasparini P (1996) Hereditary hemochromatosis: generation of a transcription map within a refined and extended map of the HLA class I region. Genomics 31:319–326

    Article  CAS  PubMed  Google Scholar 

  • Trachtulec Z, Hamvas RM, Forejt J, Lehrach H, Vincek V, Klein J (1997) Linkage of TATA-binding protein and proteasome subunit C5 genes in mice and humans reveals synteny conserved between mammals and invertebrates. Genomics 44:1–7

    Article  CAS  PubMed  Google Scholar 

  • Trowsdale J (1995) “Both Man & Bird & Beast”: comparative organization of MHC genes. Immunogenetics 41:1–17

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trowsdale J (2002) The gentle art of gene arrangement: the meaning of gene clusters. Genome Biol 3:2002.1–2002.5

    Article  Google Scholar 

  • Trowsdale J, Parham P (2004) Defense strategies and immune-related genes. Eur J Immunol 34:7–17

    Google Scholar 

  • Tsuda TT, Tsuda M, Naruse T, Kawata H, Ando A, Shiina T, Fukuda M, Kurita M, LeMaho I, Kulski JK, Inoko H (2001) Phylogenetic analysis of penguin (Spheniscidae) species based on sequence variation in MHC class II genes. Immunogenetics 53:712–716

    Article  CAS  PubMed  Google Scholar 

  • Villadangos JA (2001) Presentation of antigens by MHC class II molecules: getting the most out of them. Mol Immunol 38:329–346

    Google Scholar 

  • Vogel TU, Evans DT, Urvater JA, O’Connor DH, Hughes AL, Watkins DI (1999) Major histocompatibility complex class I genes in primates: co-evolution with pathogens. Immunol Rev 167:327–337

    Google Scholar 

  • Wagner JL (2003) Molecular organization of the canine major histocompatibility complex. J Hered 94:23–26

    Article  CAS  PubMed  Google Scholar 

  • Walter L, Günther E (2000) Physical mapping and evolution of the centromeric class I gene-containing region of the rat MHC. Immunogenetics 51:829–837

    Article  CAS  PubMed  Google Scholar 

  • Walter L, Hurt P, Himmelbauer H, Sudbrak R, Günther E (2002) Physical mapping of the major histocompatibility complex class II and class III regions of the rat. Immunogenetics 54:268–275

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Perera TV, Ford HL, Dascher CC (2003) Characterization of a divergent non-classical MHC class I gene in sharks. Immunogenetics 55:57–61

    Google Scholar 

  • Watanabe Y, Maruoka T, Walter L, Kasahara M (2004) Comparative genomics of the mill family: a rapidly evolving MHC class I gene family. Eur J Immunol 34:1597–1607

    Google Scholar 

  • Watkins DI (1995) The evolution of major histocompatibility class I genes in primates. Crit Rev Immunol 15:1–29

    CAS  PubMed  Google Scholar 

  • Westerdahl H, Wittzell H, von Schantz T (1999) Polymorphism and transcription of MHC class I genes in a passerine bird, the great reed warbler. Immunogenetics 49:158–170

    Article  CAS  PubMed  Google Scholar 

  • Westerdahl H, Wittzell H, von Schantz T (2000) MHC diversity in two passerine birds: no evidence for a minimal essential MHC. Immunogenetics 52:92–100

    Article  CAS  PubMed  Google Scholar 

  • Wiegertjes GF, Egberts E, Stet RJM (1997) Segregation of MHC class I and class II genes in the common carp (Cyprinus carpio L.). Dev Comp Immunol 21:105

    Article  Google Scholar 

  • Williams A, Peh CA, Elliott T (2002) The cell biology of MHC class I antigen presentation. Tissue Antigens 59:3–17

    Article  CAS  PubMed  Google Scholar 

  • Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T (1998–1999) MHC variation in birds and reptiles. Genetica 104:301–309

    Article  CAS  Google Scholar 

  • Wright H, Ballingall KT, Redmond J (1994) The DY sub-region of the sheep MHC contains and A/B gene pair. Immunogenetics 40:230–234

    Google Scholar 

  • Xie T, Rowen L, Aguado B, Ahearn ME, Madan A, Qin S, Campbell RD, Hood L (2003) Analysis of the gene-dense major histocompatibility complex class III region and its comparison to mouse. Genome Res 13:2621–2636

    Article  CAS  PubMed  Google Scholar 

  • Yeager M, Kumar S, Hughes AL (1997) Sequence convergence in the peptide-binding region of primate and rodent MHC class Ib molecules. Mol Biol Evol 14:1035–1041

    CAS  PubMed  Google Scholar 

  • Yuhki N, Beck T, Stephens RM, Nishigaki Y, Newmann K, O’Brien SJ (2003) Comparative genome organization of human, murine, and feline MHC class II region. Genome Res 13:1169–1179

    Article  CAS  PubMed  Google Scholar 

  • Zekarias B, Ter Huurne AAHM, Landman WJM, Rebel JMJ, Pol JMA, Gruys E (2002) Immunological basis of differences in disease resistance in chicken. Vet Res 33:109–125

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Martin Flajnik and Pierre Pontarotti for useful comments regarding this review.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Trowsdale.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kelley, J., Walter, L. & Trowsdale, J. Comparative genomics of major histocompatibility complexes. Immunogenetics 56, 683–695 (2005). https://doi.org/10.1007/s00251-004-0717-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00251-004-0717-7

Keywords

Navigation