Evolution of Major Histocompatibility Complex Polymorphisms and T‐Cell Receptor Diversity in Primates

The major histocompatibility complexes (Mhc) of chimpanzees and rhesus monkeys were discovered about two decades ago (Balner et al. 1971. 1974). Because of its relevance for transplantation, a detailed description of polymorphism of some chimpanzee and rhesus macaque Mhc class I and II loci was achieved by serological techniques (Table I). In those days, it was already apparent that the Mhc\ of humans and nonhuman primates shared many similar features. For example, cross-reactions of typing sera suggested that humans and chimpanzees possessed highly related alleles belonging to the HLA-AI/A3/AU lineage (Balner 1977). The self-sustaining nonhuman primate colonies at our institute have been pedigreed based on Mhc genetics and their outbred character has been carefully maintained for more than 20 years. This pioneering work of Hans Balner and colleagues has been fundamental to our current research program focusing on the biological role o[Mhc and Ttr gene products in relation to health and disease. The introduction of molecular and cellular techniques has extended our knowledge on the co-evolution of primate Mhc and Tcr systems as well as their complex array of interactions. The next paragraphs arc devoted to a review of the results that we and our colleagues have obtained in recent years.

[1]  J. Lanchbury,et al.  Healthy human T-cell receptor β-chain repertoire , 1995 .

[2]  R. Bontrop,et al.  Evolution of the major histocompatibility complex DPA1 locus in primates. , 1995, Human immunology.

[3]  J. Klein,et al.  Intensity of natural selection at the major histocompatibility complex loci. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[4]  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.

[5]  J. Klein,et al.  The origin of the primate Mhc-DRB genes and allelic lineages as deduced from the study of prosimians. , 1994, Journal of immunology.

[6]  R. Bontrop,et al.  Gel electrophoretic analysis of rhesus macaque major histocompatibility complex class II DR molecules. , 1994, Human immunology.

[7]  L. Hood,et al.  Nucleotide sequence analysis of 77.7 kb of the human V beta T-cell receptor gene locus: direct primer-walking using cosmid template DNAs. , 1994, Genomics.

[8]  R. Bontrop,et al.  Characterization of a novel human T cell receptor β chain variable region family by transspecies DNA hybridization , 1994, European journal of immunology.

[9]  R. Bontrop,et al.  Expansion and contraction of rhesus macaque DRB regions by duplication and deletion. , 1994, Journal of immunology.

[10]  R. Bontrop,et al.  DRB, DQA, DQB AND DPB NUCLEOTIDE SEQUENCES OF SANGUINUS OEDIPUS B95‐8 , 1994, European journal of immunogenetics : official journal of the British Society for Histocompatibility and Immunogenetics.

[11]  F J Ayala,et al.  MHC polymorphism and human origins. , 1993, Scientific American.

[12]  J. Klein,et al.  Resolution of the HLA-DRB6 puzzle: a case of grafting a de novo-generated exon on an existing gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Bontrop,et al.  Nucleotide sequences, polymorphism and gene deletion of T cell receptor beta-chain constant regions of Pan troglodytes and Macaca mulatta. , 1993, Journal of immunology.

[14]  R. Bontrop,et al.  The biologic importance of conserved major histocompatibility complex class II motifs in primates. , 1993, Human immunology.

[15]  N. Letvin,et al.  Conserved T-cell receptor repertoire in simian immunodeficiency virus-infected rhesus monkeys. , 1993, Journal of immunology.

[16]  R. Bontrop,et al.  Major hstocompatibility haplotypes in a breeding colony of chimpanzees (Pan troglodytes) , 1993 .

[17]  R. Bontrop,et al.  Major histocompatibility complex class II haplotypes in a breeding colony of chimpanzees (Pan troglodytes). , 1993, Tissue antigens.

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

[19]  F. Koning,et al.  HLA‐DRβ chain residue 86 controls DRαβ dimer stability , 1993 .

[20]  C. Schönbach,et al.  Conservative evolution of the Mbc-DP region in anthropoid primates. , 1993, Human immunology.

[21]  J. Bell,et al.  Characterization of the human T cell receptor α‐chain repertoire and demonstration of a genetic influence on Vα usage , 1993, European journal of immunology.

[22]  R. Bontrop,et al.  Evolutionary conservation of major histocompatibility complex- DR/peptide/T cell interactions in primates , 1993, The Journal of experimental medicine.

[23]  R. Bontrop,et al.  Mhc-DRB and -DQA1 nucleotide sequences of three lowland gorillas. Implications for the evolution of primate Mhc class II haplotypes. , 1993, Human immunology.

[24]  Antonio Lanzavecchia,et al.  The set of naturally processed peptides displayed by DR molecules is tuned by polymorphism of residue 86 , 1993, European journal of immunology.

[25]  J. Bodmer,et al.  Nomenclature for Factors of the HLA System, 1991 , 1992, Immunobiology.

[26]  R. Bontrop,et al.  Major histocompatibility complex class II polymorphisms in humans and chimpanzees. , 1993, Journal of medical primatology.

[27]  J. Bodmer,et al.  HLA Class II nucleotide sequences, 1992. , 1993, Immunobiology.

[28]  F. Koning,et al.  HLA-DR beta chain residue 86 controls DR alpha beta dimer stability. , 1993, European journal of immunology.

[29]  M. Aidoo,et al.  Molecular analysis of the association of HLA-B53 and resistance to severe malaria , 1992, Nature.

[30]  M. Cohn,et al.  What is the selective pressure that maintains the gene loci encoding the antigen receptors of T and B cells? A hypothesis , 1992, Immunology and cell biology.

[31]  J. Klein,et al.  Comparative anatomy of the primate major histocompatibility complex DR subregion: evidence for combinations of DRB genes conserved across species. , 1992, Genomics.

[32]  M. Robinson Usage of human T-cell receptor Vβ, Jβ, Cβ, and Vα gene segments is not proportional to gene number , 1992 .

[33]  R. Bontrop,et al.  Evolutionary stability of transspecies major histocompatibility complex class II DRB lineages in humans and rhesus monkeys. , 1992, Human immunology.

[34]  L. Hood,et al.  Organization, structure, and function of 95 kb of DNA spanning the murine T-cell receptor CαCδ region , 1992 .

[35]  J. Klein,et al.  Shared polymorphism between gorilla and human major histocompatibility complex DRB loci. , 1992, Human immunology.

[36]  R. Bontrop,et al.  Mhc-DQB repertoire variation in hominoid and Old World primate species. , 1992, Journal of immunology.

[37]  D. Watkins,et al.  Predominant use of a T-cell receptor V beta gene family in simian immunodeficiency virus Gag-specific cytotoxic T lymphocytes in a rhesus monkey , 1992, Journal of virology.

[38]  A. Hughes,et al.  New recombinant HLA-B alleles in a tribe of South American Amerindians indicate rapid evolution of MHC class I loci , 1992, Nature.

[39]  M. Petzl-Erler,et al.  Unusual HLA-B alleles in two tribes of Brazilian Indians , 1992, Nature.

[40]  A. Hughes,et al.  Molecular cloning of orangutan and gibbon MHC class I cDNA. The HLA-A and -B loci diverged over 30 million years ago. , 1992, Journal of immunology.

[41]  J. Bell,et al.  Variation in human T cell receptor Vβ and Jβ repertoire: analysis using anchor polymerase chain reaction , 1992 .

[42]  G. Nepom,et al.  Conservation of the HLA-DQB2 locus in nonhuman primates. , 1992, Journal of immunology.

[43]  L. Andersson,et al.  Exon encoding the antigen-binding site of MHC class II beta-chains is divided into two subregions with different evolutionary histories. , 1992, Journal of immunology.

[44]  Ursula Esser,et al.  Mapping T-cell receptor–peptide contacts by variant peptide immunization of single-chain transgenics , 1992, Nature.

[45]  T. Ottenhoff,et al.  Binding of a major T cell epitope of mycobacteria to a specific pocket within HLA‐DRw17(DR3) molecules , 1992, European journal of immunology.

[46]  A. Hughes,et al.  Sequence and diversity of rhesus monkey T-cell receptor beta chain genes. , 1992, Immunogenetics.

[47]  L. Hood,et al.  Organization, structure, and function of 95 kb of DNA spanning the murine T-cell receptor C alpha/C delta region. , 1992, Genomics.

[48]  M. Ott,et al.  The T-cell-receptor repertoire in the synovial fluid of a patient with rheumatoid arthritis is polyclonal. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Andrew J. McMichael,et al.  Common West African HLA antigens are associated with protection from severe malaria , 1991, Nature.

[50]  G. Gutman,et al.  Organization and nucleotide sequence of the rat T cell receptor beta-chain complex. , 1991, Journal of immunology.

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

[52]  M. Robinson The human T cell receptor beta-chain gene complex contains at least 57 variable gene segments. Identification of six V beta genes in four new gene families. , 1991, Journal of immunology.

[53]  F. Christiansen,et al.  Major histocompatibility complex ancestral haplotypes in the chimpanzee: identification using C4 allotyping. , 1991, Human immunology.

[54]  C. Schönbach,et al.  Gorilla major histocompatibility complex-DRB pseudogene orthologous to HLA-DRBVIII. , 1991, Human immunology.

[55]  R. Bontrop,et al.  RFLP analysis of the rhesus monkey MHC class II DR subregion. , 1991, Human immunology.

[56]  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.

[57]  R. Bontrop,et al.  Major histocompatibility complex class II-restricted antigen presentation across a species barrier: conservation of restriction determinants in evolution , 1990, The Journal of experimental medicine.

[58]  A. Begovich,et al.  Limited heterogeneity of rearranged T-cell receptor Vα transcripts in brains of multiple sclerosis patients , 1990, Nature.

[59]  D. Lashkari,et al.  Allelic diversification at the class II DQB locus of the mammalian major histocompatibility complex. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[60]  H. Erlich,et al.  Ancient roots for polymorphism at the HLA-DQ alpha locus in primates. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[61]  P. Marrack,et al.  Interaction of Staphylococcus aureus toxin "superantigens" with human T cells. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[62]  J. Klein,et al.  Shared class II MHC polymorphisms between humans and chimpanzees. , 1989, Human immunology.

[63]  M. Nei,et al.  Positive darwinian selection observed at the variable-region genes of immunoglobulins. , 1989, Molecular biology and evolution.

[64]  J. Gorski The HLA-DRw8 lineage was generated by a deletion in the DR B region followed by first domain diversification. , 1989, Journal of immunology.

[65]  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.

[66]  L. Lanier,et al.  Polymerase chain reaction with single-sided specificity: analysis of T cell receptor delta chain. , 1989, Science.

[67]  J. Claverie,et al.  Implications of a Fab-like structure for the T-cell receptor. , 1989, Immunology today.

[68]  A. Lesk,et al.  The outline structure of the T‐cell alpha beta receptor. , 1988, The EMBO journal.

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

[70]  Mark M. Davis,et al.  T-cell antigen receptor genes and T-cell recognition , 1988, Nature.

[71]  L. Hood,et al.  Structure, Organization and Polymorphism of Murine and Human T‐Cell Receptor a and β Chain Gene Families , 1988, Immunological reviews.

[72]  J. Klein Origin of major histocompatibility complex polymorphism: the trans-species hypothesis. , 1987, Human immunology.

[73]  T. Mak,et al.  Genes of the T-cell antigen receptor in normal and malignant T cells. , 1987, Annual review of immunology.

[74]  S. Rudikoff,et al.  Gene correction in the evolution of the T cell receptor beta chain , 1986, The Journal of experimental medicine.

[75]  T. Kindt,et al.  A variable region gene subfamily encoding T cell receptor beta-chains is selectively conserved among mammals. , 1986, Journal of immunology.

[76]  P. A. Peterson,et al.  HLA-DR beta genes vary in number between different DR specificities, whereas the number of DQ beta genes is constant. , 1985, Journal of immunology.

[77]  C. Milstein,et al.  Sequence and evolution of the human T-cell antigen receptor beta-chain genes. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[78]  S. Ohno,et al.  Antigen-binding specificities of antibodies are primarily determined by seven residues of VH. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[79]  H. Ertl,et al.  Genetic and antigenic requirements for induction of T helper cells for anti‐Sendai virus‐specific antibody production , 1981, European journal of immunology.

[80]  H. Balner The Major Histocompatibility System of Subhuman Primate Species , 1977 .

[81]  M. Torres,et al.  Nomenclature for factors of the HLA system. , 2011, Bulletin of the World Health Organization.

[82]  J. D'Amaro,et al.  Evidence for two linked loci controlling ther serologically defined leukocyte antigens of chimpanzees (ChL-A). , 2008, Tissue antigens.

[83]  W. Bodmer,et al.  Evolutionary Significance of the HL-A System , 1972, Nature.

[84]  H. Hudson,et al.  Observations of Unresolved Galactic X-ray Sources , 1971, Nature.