Evolution of the mammalian MHC: natural selection, recombination, and convergent evolution

Summary: The genes that encode molecules involved in antigen presentation within the class I and class II regions of the mammalian major histocompatibility complex (MHC) include several that are highly polymorphic. There is evidence that this polymorphism is maintained by positive selection, most likely overdominant selection, relating to their role in presenting foreign peptides to T cells. This selection can maintain allelic lineages for much longer periods of time than neutral polymorphisms are expected to last, but sharing of polymorphic amino acid motifs among species of different mammalian orders is due to independent (or convergent) evolution rather than common ancestry. It has been suggested that interallelic recombination (gene conversion) plays a role in enhancing polymorphism, but there is evidence of striking differences among loci with respect to the rate at which such recombination has contributed to current polymorphism. Recent attempts to interpret linkage relationships in the MHC region as evidence of ancient genomic duplications are not supported by phylogenetic analysis. Rather, natural selection may have played a role in the linkage of other genes to those of the MHC.

[1]  A. Hughes,et al.  Evolution of the MHC class I genes of a New World primate from ancestral homologues of human non-classical genes , 1990, Nature.

[2]  M. Nei,et al.  Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. , 1990, Genetics.

[3]  J. Klein,et al.  Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans‐species mode of evolution. , 1988, The EMBO journal.

[4]  W. Klitz,et al.  Polymorphism, recombination, and linkage disequilibrium within the HLA class II region. , 1992, Journal of immunology.

[5]  H. Geuze,et al.  Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments , 1991, Nature.

[6]  J. Davey,et al.  Cytotoxic T cells recognize fragments of the influenza nucleoprotein , 1985, Cell.

[7]  A. Hughes,et al.  Phylogenetic tests of the hypothesis of block duplication of homologous genes on human chromosomes 6, 9, and 1. , 1998, Molecular biology and evolution.

[8]  A. F. Williams,et al.  The immunoglobulin superfamily--domains for cell surface recognition. , 1988, Annual review of immunology.

[9]  H. Mcdevitt,et al.  Evolution of major histocompatibility complex class II allelic diversity: direct descent in mice and humans. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Klein,et al.  Different modes of Mhc evolution in primates. , 1993, Molecular biology and evolution.

[11]  T. Ikemura,et al.  Chromosomal localization of the proteasome Z subunit gene reveals an ancient chromosomal duplication involving the major histocompatibility complex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Berke The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. , 1994, Annual review of immunology.

[13]  N. Armes,et al.  Fugu genome is not a good mammalian model , 1997, Nature.

[14]  J. Klein Natural history of the major histocompatibility complex , 1986 .

[15]  Norman Arnheim,et al.  New HLA–DPB1 alleles generated by interallelic gene conversion detected by analysis of sperm , 1995, Nature Genetics.

[16]  A. Hughes,et al.  Sequence convergence in the peptide-binding region of primate and rodent MHC class Ib molecules. , 1997, Molecular biology and evolution.

[17]  J. Monaco,et al.  A molecular model of MHC class-I-restricted antigen processing. , 1992, Immunology today.

[18]  R F Doolittle,et al.  Convergent evolution: the need to be explicit. , 1994, Trends in biochemical sciences.

[19]  P. Parham,et al.  Diversity and diversification of HLA-A,B,C alleles. , 1989, Journal of immunology.

[20]  M. Taylor,et al.  Endosomal aspartic proteinases are required for invariant-chain processing. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[21]  A. Goldberg,et al.  Proteolysis, proteasomes and antigen presentation , 1992, Nature.

[22]  M. A. Saper,et al.  Structure of the human class I histocompatibility antigen, HLA-A2 , 1987, Nature.

[23]  D. Wiley,et al.  Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. , 1991, Journal of molecular biology.

[24]  P. Cresswell,et al.  HLA-DM Interactions with Intermediates in HLA-DR Maturation and a Role for HLA-DM in Stabilizing Empty HLA-DR Molecules , 1996, The Journal of experimental medicine.

[25]  A. Hughes,et al.  Natural selection at major histocompatibility complex loci of vertebrates. , 1998, Annual review of genetics.

[26]  P. Cresswell,et al.  HLA-DM induces clip dissociation from MHC class II αβ dimers and facilitates peptide loading , 1995, Cell.

[27]  H. Orr,et al.  Structure of crossreactive human histocompatibility antigens HLA-A28 and HLA-A2: possible implications for the generation of HLA polymorphism. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[28]  M. Kasahara,et al.  Chromosomal duplication and the emergence of the adaptive immune system. , 1997, Trends in genetics : TIG.

[29]  J. Forman,et al.  Peptide binding to the class Ib molecule, Qa-1b. , 1997, Journal of immunology.

[30]  Partho Ghosh,et al.  Structure of the complex between human T-cell receptor, viral peptide and HLA-A2 , 1996, Nature.

[31]  L. Jin,et al.  Variances of the average numbers of nucleotide substitutions within and between populations. , 1989, Molecular biology and evolution.

[32]  M. Nei,et al.  Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. , 1989, Molecular biology and evolution.

[33]  H. Mcdevitt,et al.  Genetics and expression of mouse Ia antigens. , 1985, Annual review of immunology.

[34]  A. McMichael,et al.  The human major histocompatibility complex class Ib molecule HLA‐E binds signal sequence‐derived peptides with primary anchor residues at positions 2 and 9 , 1997, European journal of immunology.

[35]  S. Yokoyama,et al.  Convergent evolution of the red- and green-like visual pigment genes in fish, Astyanax fasciatus, and human. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[36]  N. M. Brooke,et al.  A molecular timescale for vertebrate evolution , 1998, Nature.

[37]  G. Chelvanayagam A roadmap for HLA-A, HLA-B, and HLA-C peptide binding specificities , 1996, Immunogenetics.

[38]  A. Bourke,et al.  The Ecology of Communal Breeding: The Case of Multiple-Queen Leptothoracine Ants , 1994 .

[39]  K.,et al.  Contrasting roles of interallelic recombination at the HLA-A and HLA-B loci. , 1993, Genetics.

[40]  A. Wilson,et al.  Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin. , 1994, Molecular biology and evolution.

[41]  Peter Parham,et al.  HLA-A and B polymorphisms predate the divergence of humans and chimpanzees , 1988, Nature.

[42]  Don C. Wiley,et al.  Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide , 1994, Nature.

[43]  M. Nei,et al.  Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection , 1988, Nature.

[44]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[45]  R Mehr,et al.  Regulatory feedback pathways in the thymus. , 1997, Immunology today.

[46]  H. Erlich,et al.  Genetic diversity at class II DRB loci of the primate MHC. , 1991, Journal of immunology.

[47]  J. Klein,et al.  The conundrum of nonclassical major histocompatibility complex genes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Allan C. Wilson,et al.  Adaptive evolution in the stomach lysozymes of foregut fermenters , 1987, Nature.

[49]  M. Nei,et al.  MEGA: Molecular Evolutionary Genetics Analysis, Version 1.02. , 1995 .

[50]  A. Hughes,et al.  Locus-specific conservation of the HLA class I introns by intra-locus homogenization , 1997, Immunogenetics.

[51]  T Gojobori,et al.  Evolutionary significance of intra-genome duplications on human chromosomes. , 1997, Gene.

[52]  O. Bakke,et al.  MHC class II-associated invariant chain contains a sorting signal for endosomal compartments , 1990, Cell.

[53]  J. Klein,et al.  Linkage of RXRB-like genes to class I and not to class II Mhc genes in the zebrafish , 1998, Immunogenetics.

[54]  R. Demars,et al.  A gene in the human major histocompatibility complex class II region controlling the class I antigen presentation pathway , 1990, Nature.

[55]  J. Stephens,et al.  Statistical methods of DNA sequence analysis: detection of intragenic recombination or gene conversion. , 1985, Molecular biology and evolution.

[56]  C. Meyer,et al.  HLA-DP--part of the concert. , 1997, Immunology today.

[57]  B. Evavold,et al.  Enhanced Dissociation of HLA-DR-Bound Peptides in the Presence of HLA-DM , 1996, Science.

[58]  D. Zaller,et al.  Mediation by HLA-DM of dissociation of peptides from HLA-DR , 1995, Nature.

[59]  M. Nei,et al.  Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[60]  P. Cresswell,et al.  Role for intracellular proteases in the processing and transport of class II HLA antigens. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[61]  D. Wiley,et al.  Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1 , 1993, Nature.

[62]  A. Hughes,et al.  A uniquely high level of recombination at the HLA-B locus. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[63]  J. Klein,et al.  Evolution of the major histocompatibility complex. , 1986, Critical reviews in immunology.

[64]  R. Zinkernagel,et al.  Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex , 1975, Nature.

[65]  A. Hughes,et al.  Interallelic recombination has not played a major role in the history of the HLA-C locus , 1996, Immunogenetics.

[66]  F. Bonhomme,et al.  Amplification of major histocompatibility complex class II gene diversity by intraexonic recombination. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[67]  S. Tonegawa,et al.  TAP1-dependent peptide translocation in vitro is ATP dependent and peptide selective , 1993, Cell.

[68]  A. Sidow Gen(om)e duplications in the evolution of early vertebrates. , 1996, Current opinion in genetics & development.

[69]  P. Travers,et al.  A cDNA clone encoding the mouse Qa-1a histocompatibility antigen and proposed structure of the putative peptide binding site. , 1993, Journal of immunology.

[70]  D. Pilbeam Genetic and morphological records of the Hominoidea and hominid origins: a synthesis. , 1996, Molecular phylogenetics and evolution.

[71]  Hiroshi Akashi,et al.  Molecular Evidence for Natural Selection , 1995 .

[72]  M. A. Saper,et al.  The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens , 1987, Nature.

[73]  M. Nei,et al.  Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. , 1990, Molecular biology and evolution.

[74]  J. Neefjes,et al.  Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter. , 1993, Science.