Conservation of Mhc Class III Region Synteny Between Zebrafish and Human as Determined by Radiation Hybrid Mapping1

In the HLA, H2, and other mammalian Mhc, the class I and II loci are separated by the so-called class III region comprised of ∼60 genes that are functionally and evolutionarily unrelated to the class I/II genes. To explore the origin of this island of unrelated loci in the middle of the Mhc 19 homologues of HLA class III genes, we identified 19 homologues of HLA class III genes as well as 21 additional non-class I/II HLA homologues in the zebrafish and mapped them by testing a panel of 94 zebrafish-hamster radiation hybrid cell lines. Six of the HLA class III and eight of the flanking homologues were found to be linked to the zebrafish class I (but not class II) loci in linkage group 19. The remaining homologous loci were found to be scattered over 14 zebrafish linkage groups. The linkage group 19 contains at least 25 genes (not counting the class I loci) that are also syntenic on human chromosome 6. This gene assembly presumably represents the pre-Mhc that existed before the class I/II genes arose. The pre-Mhc may not have contained the complement and other class III genes involved in immune response.

[1]  E. Fisher,et al.  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. , 1996, Genomics.

[2]  J. Klein,et al.  Major histocompatibility complex class II genes of zebrafish. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[3]  J. Strominger,et al.  A new cluster of genes within the human major histocompatibility complex. , 1989, Science.

[4]  Gongora,et al.  Independent Duplications of Bf and C3 Complement Genes in the Zebrafish , 1998, Scandinavian journal of immunology.

[5]  H. Baier,et al.  A radiation hybrid map of the zebrafish genome , 1999, Nature Genetics.

[6]  J. Klein,et al.  Linkage of LMP, TAP, and RING3 with Mhc class I rather than class II genes in the zebrafish. , 1997, Journal of immunology.

[7]  E. Stewart,et al.  An STS-based radiation hybrid map of the human genome. , 1997, Genome research.

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

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

[10]  P. Pontarotti,et al.  The MHC Big Bang , 1999, Immunological reviews.

[11]  S Beck,et al.  Gene organisation, sequence variation and isochore structure at the centromeric boundary of the human MHC. , 1999, Journal of molecular biology.

[12]  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.

[13]  J. Klein,et al.  Ancient allelism at the cytosolic chaperonin-alpha-encoding gene of the zebrafish. , 2000, Genetics.

[14]  K. Schmitt,et al.  Construction and characterization of zebrafish whole genome radiation hybrids. , 1999, Methods in cell biology.

[15]  M. Bienz Xenopus hsp 70 genes are constitutively expressed in injected oocytes. , 1984, The EMBO journal.

[16]  J. Klein,et al.  Jaws and AIS , 2000 .

[17]  Margaret R. Thomson,et al.  Vertebrate genome evolution and the zebrafish gene map , 1998, Nature Genetics.

[18]  M. Reith,et al.  Winter Flounder Expressed Sequence Tags: Establishment of an EST Database and Identification of Novel Fish Genes , 1999, Marine Biotechnology.

[19]  J. Postlethwait,et al.  Centromere-linkage analysis and consolidation of the zebrafish genetic map. , 1996, Genetics.

[20]  H. Sültmann,et al.  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. , 1999, Journal of immunology.

[21]  A. Sato,et al.  Birth of the Major Histocompatibility Complex , 1998, Scandinavian journal of immunology.

[22]  B. Paw,et al.  Characterization of whole genome radiation hybrid mapping resources for non-mammalian vertebrates. , 1998, Nucleic acids research.

[23]  H. Lehrach,et al.  Linkage of TATA-binding protein and proteasome subunit C5 genes in mice and humans reveals synteny conserved between mammals and invertebrates. , 1997, Genomics.

[24]  J. Postlethwait,et al.  Radiation hybrid mapping of the zebrafish genome. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  C. Y. Yu,et al.  Human helicase gene SKI2W in the HLA class III region exhibits striking structural similarities to the yeast antiviral gene SKI2 and to the human gene KIAA0052: emergence of a new gene family. , 1995, Nucleic acids research.

[26]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[27]  Peter Parham,et al.  Virtual reality in the MHC , 1999, Immunological reviews.

[28]  M. Kasahara Major histocompatibility complex : evolution, structure, and function , 2000 .

[29]  W. Thomson,et al.  Localization of eight additional genes in the human major histocompatibility complex, including the gene encoding the casein kinase II beta subunit (CSNK2B). , 1996, Genomics.

[30]  Q. Ju,et al.  REB1, a yeast DNA-binding protein with many targets, is essential for growth and bears some resemblance to the oncogene myb , 1990, Molecular and cellular biology.

[31]  H. Sültmann,et al.  Nonlinkage of major histocompatibility complex class I and class II loci in bony fishes , 2000, Immunogenetics.

[32]  G. Litman,et al.  Cloning of a cDNA encoding a Pim1 homologue in zebrafish, Danio rerio , 1999, Immunogenetics.

[33]  I. Dunham,et al.  Identification of multiple HTF‐island associated genes in the human major histocompatibility complex class III region. , 1989, The EMBO journal.

[34]  R. Campbell,et al.  Evidence that gene G7a in the human major histocompatibility complex encodes valyl-tRNA synthetase. , 1991, The Biochemical journal.

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

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

[37]  M. Kasahara Major Histocompatibility Complex , 2000, Springer Japan.

[38]  S. Beck,et al.  TAPASIN, DAXX, RGL2, HKE2 and four new genes (BING 1, 3 to 5) form a dense cluster at the centromeric end of the MHC. , 1998, Journal of molecular biology.

[39]  S. Beck,et al.  Gene organisation determines evolution of function in the chicken MHC , 1999, Immunological reviews.

[40]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[41]  M. Flajnik,et al.  Insight into the primordial MHC from studies in ectothermic vertebrates , 1999, Immunological reviews.

[42]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[43]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[44]  Julie Dawn Thompson,et al.  Improved sensitivity of profile searches through the use of sequence weights and gap excision , 1994, Comput. Appl. Biosci..

[45]  S. Hofmann,et al.  Structure of the human palmitoyl-protein thioesterase-2 gene (PPT2) in the major histocompatibility complex on chromosome 6p21.3. , 1999, Genomics.

[46]  Eugene W. Myers,et al.  Basic local alignment search tool. Journal of Molecular Biology , 1990 .

[47]  Thomas L. Madden,et al.  PowerBLAST: a new network BLAST application for interactive or automated sequence analysis and annotation. , 1997, Genome research.

[48]  L. Lundin,et al.  Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. , 1993, Genomics.

[49]  M. Boffa,et al.  New retinoid X receptor subtypes in zebra fish (Danio rerio) differentially modulate transcription and do not bind 9-cis retinoic acid , 1995, Molecular and cellular biology.

[50]  H. Sültmann,et al.  A Contig Map of the Mhc Class I Genomic Region in the Zebrafish Reveals Ancient Synteny , 2000, The Journal of Immunology.

[51]  M. Flajnik,et al.  Evolution of the major histocompatibility complex: a current overview. , 1995, Transplant immunology.

[52]  J. Klein,et al.  A complement factor B-like cDNA clone from the zebrafish (Brachydanio rerio). , 1996, Molecular immunology.

[53]  C. Watts,et al.  Pathways of antigen processing and presentation. , 1999, Reviews in immunogenetics.

[54]  J. Strominger,et al.  Human major histocompatibility complex contains a minimum of 19 genes between the complement cluster and HLA-B. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Stephen L. Johnson,et al.  Mapping of Mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio , 1997, Immunogenetics.

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

[57]  H. Sültmann,et al.  Organization of Mhc class II B genes in the zebrafish (Brachydanio rerio). , 1994, Genomics.

[58]  N. Kuroda,et al.  Molecular genetics of the complement C3 convertases in lower vertebrates , 1998, Immunological reviews.

[59]  M. Kasahara Genome dynamics of the major histocompatibility complex: insights from genome paralogy , 1999, Immunogenetics.

[60]  J. Klein,et al.  Composite origin of major histocompatibility complex genes. , 1993, Current opinion in genetics & development.

[61]  Margaret R. Thomson,et al.  Vertebrate genome evolution and the zebrafish gene map , 1998, Nature Genetics.

[62]  J. Klein,et al.  Origin of gene overlap: the case of TCP1 and ACAT2. , 1999, Genetics.