Comparative genomic structure of human, dog, and cat MHC: HLA, DLA, and FLA.

Comparisons of the genomic structure of 3 mammalian major histocompatibility complexes (MHCs), human HLA, canine DLA, and feline FLA revealed remarkable structural differences between HLA and the other 2 MHCs. The 4.6-Mb HLA sequence was compared with the 3.9-Mb DLA sequence from 2 supercontigs generated by 7x whole-genome shotgun assembly and 3.3-Mb FLA draft sequence. For FLA, we confirm that 1) feline FLA was split into 2 pieces within the TRIM (member of the tripartite motif) gene family found in human HLA, 2) class II, III, and I regions were placed in the pericentromeric region of the long arm of chromosome B2, and 3) the remaining FLA was located in subtelomeric region of the short arm of chromosome B2. The exact same chromosome break was found in canine DLA structure, where class II, III, and I regions were placed in a pericentromeric region of chromosome 12 whereas the remaining region was located in a subtelomeric region of chromosome 35, suggesting that this chromosome break occurred once before the split of felid and canid more than 55 million years ago. However, significant differences were found in the content of genes in both pericentromeric and subtelomeric regions in DLA and FLA, the gene number, and amplicon structure of class I genes plus 2 other class I genes found on 2 additional chromosomes; canine chromosomes 7 and 18 suggest the dynamic nature in the evolution of MHC class I genes.

[1]  E Soeda,et al.  Molecular dynamics of MHC genesis unraveled by sequence analysis of the 1,796,938-bp HLA class I region. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C. Desmarais,et al.  Automated finishing with autofinish. , 2001, Genome research.

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

[4]  P. Parham Immunogenetics of killer cell immunoglobulin-like receptors. , 2003, Molecular immunology.

[5]  Toyoyuki Takada,et al.  Genomic organization of the mammalian MHC. , 2003, Annual review of immunology.

[6]  K. Benirschke,et al.  An Atlas of Mammalian Chromosomes , 2020, Springer New York.

[7]  P. A. Peterson,et al.  The role of H2‐O and HLA‐DO in major histocompatibility complex class Il‐restricted antigen processing and presentation , 1999, Immunological reviews.

[8]  S. O’Brien,et al.  Molecular phylogenetics and the origins of placental mammals , 2001, Nature.

[9]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[10]  J. Faraco,et al.  Sequence of the canine major histocompatibility complex region containing non-classical class I genes. , 2005, Tissue antigens.

[11]  C. Arrecubieta,et al.  Sequence and transcriptional analysis of a DNA region involved in the production of capsular polysaccharide in Streptococcus pneumoniae type 3. , 1995, Gene.

[12]  S. Bromley,et al.  The immunological synapse: a molecular machine controlling T cell activation. , 1999, Science.

[13]  M. Crumpton,et al.  MAJOR HISTOCOMPATIBILITY ANTIGENS , 1981 .

[14]  Jean L. Chang,et al.  Initial sequence and comparative analysis of the cat genome. , 2007, Genome research.

[15]  B. Arp,et al.  HLA-DMA and -DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells , 1994, Nature.

[16]  Jeffrey A. Shaman,et al.  An essential role for HLA–DM in antigen presentation by class II major histocompatibility molecules , 1994, Nature.

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

[18]  Stephen J O'Brien,et al.  Comparative genome organization of human, murine, and feline MHC class II region. , 2003, Genome research.

[19]  Donald C. Miller,et al.  An ordered BAC contig map of the equine major histocompatibility complex , 2003, Cytogenetic and Genome Research.

[20]  H. Lewin,et al.  Comparative organization and function of the major histocompatibility complex of domesticated cattle , 1999, Immunological reviews.

[21]  J. Trowsdale,et al.  DNA sequence analysis of 66 kb of the human MHC class II region encoding a cluster of genes for antigen processing. , 1992, Journal of molecular biology.

[22]  J. Strominger,et al.  Molecular analyses of the interactions between human NK receptors and their HLA ligands. , 2000, Human immunology.

[23]  C. Auffray,et al.  The chicken B locus is a minimal essential major histocompatibility complex , 1999, Nature.

[24]  Gustavo Glusman,et al.  Genetic divergence of the rhesus macaque major histocompatibility complex. , 2004, Genome research.

[25]  S. O’Brien,et al.  Atlas of mammalian chromosomes , 2006 .

[26]  D. Wiley,et al.  A hypothetical model of the foreign antigen binding site of Class II histocompatibility molecules , 1988, Nature.

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

[28]  P Green,et al.  Base-calling of automated sequencer traces using phred. II. Error probabilities. , 1998, Genome research.

[29]  S. O’Brien,et al.  The feline major histocompatibility complex is rearranged by an inversion with a breakpoint in the distal class I region , 2004, Immunogenetics.

[30]  N. Yuhki,et al.  Comparative genome organization of the major histocompatibility complex: lessons from the Felidae , 1999, Immunological reviews.

[31]  S. Karlin,et al.  Prediction of complete gene structures in human genomic DNA. , 1997, Journal of molecular biology.

[32]  Gen Tamiya,et al.  Complete sequence and gene map of a human major histocompatibility complex , 1999 .

[33]  Elena S. Babaylova,et al.  Complete sequence and gene map of a human major histocompatibility complex , 1999, Nature.

[34]  H. Lewin,et al.  A radiation hybrid map of BTA23: identification of a chromosomal rearrangement leading to separation of the cattle MHC class II subregions. , 1998, Genomics.

[35]  S. O’Brien,et al.  Chromosomal localization of satellite DNA sequences among 22 species of felids and canids (Carnivora). , 1988, Cytogenetics and cell genetics.

[36]  J. Klein,et al.  The molecular descent of the major histocompatibility complex. , 1993, Annual review of immunology.

[37]  S Beck,et al.  The genomic sequence and analysis of the swine major histocompatibility complex. , 2006, Genomics.

[38]  Robert P. Erickson,et al.  Natural history of the major histocompatibility complex , 1987 .

[39]  S. O’Brien,et al.  DNA recombination and natural selection pressure sustain genetic sequence diversity of the feline MHC class I genes , 1990, The Journal of experimental medicine.

[40]  P. Green,et al.  Base-calling of automated sequencer traces using phred. I. Accuracy assessment. , 1998, Genome research.

[41]  R. Durbin,et al.  A dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis. , 1995, Gene.

[42]  R. Gibbs,et al.  PipMaker--a web server for aligning two genomic DNA sequences. , 2000, Genome research.

[43]  Mouse Genome Sequencing Consortium Initial sequencing and comparative analysis of the mouse genome , 2002, Nature.

[44]  H. Himmelbauer,et al.  The genomic sequence and comparative analysis of the rat major histocompatibility complex. , 2004, Genome research.

[45]  P. Green,et al.  Consed: a graphical tool for sequence finishing. , 1998, Genome research.

[46]  B. Wilhelm,et al.  Ly49 and CD94/NKG2: developmentally regulated expression and evolution , 2001, Immunological reviews.

[47]  C. Dulac,et al.  Functional Expression of Murine V2R Pheromone Receptors Involves Selective Association with the M10 and M1 Families of MHC Class Ib Molecules , 2003, Cell.

[48]  S. O’Brien,et al.  The pattern of phylogenomic evolution of the Canidae , 2002, Cytogenetic and Genome Research.

[49]  Tadashi Imanishi,et al.  Comparative sequencing of human and chimpanzee MHC class I regions unveils insertions/deletions as the major path to genomic divergence , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Michael A Quail,et al.  Genomic sequence of the class II region of the canine MHC: comparison with the MHC of other mammalian species. , 2005, Genomics.

[51]  S. O’Brien,et al.  Cytogenetic methodologies for gene mapping and comparative analyses in mammalian cell culture systems. , 1987, Gene analysis techniques.

[52]  J. Wagner Molecular organization of the canine major histocompatibility complex. , 2003, The Journal of heredity.

[53]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[54]  James A. Cuff,et al.  Genome sequence, comparative analysis and haplotype structure of the domestic dog , 2005, Nature.

[55]  Sophie Palmer,et al.  Complete MHC haplotype sequencing for common disease gene mapping. , 2004, Genome research.

[56]  P. Bouteiller,et al.  The functionality of HLA‐G is emerging , 1999, Immunological reviews.

[57]  R. Tampé,et al.  A critical role for tapasin in the assembly and function of multimeric MHC class I-TAP complexes. , 1997, Science.