Abstract
In order to determine the genomic organization of the major histocompatibility complex (MHC) of the domestic cat (Felis catus), DNA probes for 61 markers were designed from human MHC reference sequences and used to construct feline MHC BAC contig map spanning ARE1 in the class II region to the olfactory receptor complex in the extended class I region. Selected BAC clones were then used to identify feline-specific probes for the three regions of the mammalian MHC (class II–class III–class I) for radiation hybrid mapping and fluorescent in situ hybridization to refine the organization of the domestic cat MHC. The results not only confirmed that the p-arm of domestic cat B2 is inverted relative to human Chromosome 6, but also demonstrated that one inversion breakpoint localized to the distal segment of the MHC class I between TRIM39 and TRIM26. The inversion thus disjoined the ~2.85 Mb of MHC containing class II–class III–class I (proximal region) from the ~0.50 Mb of MHC class I/extended class I region, such that TRIM39 is adjacent to the Chromosome B2 centromere and TRIM26 is adjacent to the B2 telomere in the domestic cat.
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References
Amadou C (1999) Evolution of the Mhc class I region: the framework hypothesis. Immunogenetics 49:362–367
Anzai T, Shiina T, Kimura N et al (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
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
Band MR, Larson JH, Rebeiz M, Green CA, Heyen DW, Donovan J, Windish R, Steining C, Mahyuddin P, Womack JE, Lewin HA (2000) An ordered comparative map of the cattle and human genomes. Genome Res 10:1359–1368
Beck TW, Menninger J, Voigt G, Newmann K, Nishigaki Y, Nash WG, Stephens RM, Wang Y, de Jong PJ, O’Brien SJ, Yuhki N (2001) Comparative feline genomics: a BAC/PAC contig map of the major histocompatibility complex class II region. Genomics 71:282–295
Boehnke M, Lange K, Cox DR (1991) Statistical methods for multipoint radiation hybrid mapping. Am J Hum Genet 49:1174–1188
Chardon P, Rogel-Gaillard C, Peelman L, Yerle M, Velten FW, Renard C, Vaiman M (1999a) Physical organization of the pig major histocompatibility complex class II region. Immunogenetics 50:344–348
Chardon P, Renard C, Vaiman M (1999b) The major histocompatibility complex of swine. Immunol Rev 167:179–192
Chardon P, Rogel-Gaillard C, Cattolico L, Duprat S, Vaiman M, Renard C (2001) Sequence of the swine major histocompatibility complex region containing all non-classical class I genes. Tissue Antigens 57:55–65
Chowdhary BP, Raudsepp T, Kata SR, Goh G, Millon LV, Allan V, Piumi F, Guerin G, Swinburne J, Binns M, Lear TL, Mickelson J, Murray J, Antczak DF, Womack JE, Skow LC (2003) The first-generation whole-genome radiation hybrid map in the horse identifies conserved segments in human and mouse genomes. Genome Res 13:742–751
Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14:1501–1515
Di Palma F, Archibald SD, Young JR, Ellis SA (2002) A BAC contig of approximately 400 kb contains the classical class I major histocompatiblity complex (MHC) genes of cattle. Eur J Immunogenet 29:65–68
Everts Wind A van der, Kata SR, Band MR, Rebeiz M, Larkin DM, Everts RE, Green CA, Liu L, Natarajan S, Goldammer T, Lee JH, McKay S, Womack JE, Lewin HA (2004) A 1463 gene cattle–human comparative map with anchor points defined by human genome sequence coordinates. Genome Res 14:1424–1437
Fanning TG (1987) Origin and evolution of a major feline satellite DNA. J Mol Biol 197:627–634
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
Hess M, Goldammer T, Gelhaus A, Ried K, Rappold G, Eggen A, Bishop MD, Schwerin M, Horstmann RD (1999) Physical assignment of the bovine MHC class IIa and class IIb genes. Cytogenet Cell Genet 85:244–247
Horvath JE, Gulden CL, Bailey JA, Yohn C, McPherson JD, Prescott A, Roe BA, De Jong PJ, Ventura M, Misceo D, Archidiacono N, Zhao S, Schwartz S, Rocchi M, Eichler EE (2003) Using a pericentromeric interspersed repeat to recapitulate the phylogeny and expansion of human centromeric segmental duplications. Mol Biol Evol 20:1463–1479
Hurt P, Walter L, Sudbrak R, Klages S, Muller I, Shiina T, Inoko H, Lehrach H, Gunther E, Reinhardt R, Himmelbauer H (2004) The genomic sequence and comparative analysis of the rat major histocompatibility complex. Genome Res 14:631–639
Jackson MS, Rocchi M, Thompson G, Hearn T, Crosier M, Guy J, Kirk D, Mulligan L, Ricco A, Piccininni S, Marzella R, Viggiano L, Archidiacono N (1999) Sequences flanking the centromere of human chromosome 10 are a complex patchwork of arm-specific sequences, stable duplications and unstable sequences with homologies to telomeric and other centromeric locations. Hum Mol Genet 8:205–215
James MR, Richard CW 3rd, Schott JJ, Yousry C, Clark K, Bell J, Terwilliger JD, Hazan J, Dubay C, Vignal A et al (1994) A radiation hybrid map of 506 STS markers spanning human chromosome 11. Nat Genet 8:70-76
Kaufman J, Milne S, Gobel TW, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401:923–925
Kumanovics A, Takada T, Fischer Lindahl K (2003) Genomic organization of the mammalian MHC. Annu Rev Immunol 21:629–665
Lewin HA, Russell GC, Glass EJ (1999) Comparative organization and function of the major histocompatibility complex of domesticated cattle. Immunol Rev 167:145–158
Marra MA, Kucaba TA, Dietrich NL, Green ED, Brownstein B, Wilson RK, McDonald KM, Hillier LW, McPherson JD, Waterston RH (1997) High throughput fingerprint analysis of large-insert clones. Genome Res 7:1072–1084
McShane RD, Gallagher DS Jr, Newkirk H, Taylor JF, Burzlaff JD, Davis SK, Skow LC (2001) Physical localization and order of genes in the class I region of the bovine. MHC Anim Genet 32:235–239
Menotti-Raymond M, David VA, Chen ZQ, Menotti KA, Sun S, Schaffer AA, Agarwala R, Tomlin JF, O’Brien SJ, Murphy WJ (2003) Second-generation integrated genetic linkage/radiation hybrid maps of the domestic cat (Felis catus). J Hered 94:95–106
MHC Sequencing Consortium (1999) Complete sequence and gene map of a human major histocompatibility complex. Nature 401:921–923
Miska KB, 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
Modi WS, Fanning TG, Wayne RK, O’Brien SJ (1988) Chromosomal localization of satellite DNA sequences among 22 species of felids and canids (Carnivora). Cytogenet Cell Genet 48:208–213
Modi WS, Nash WG, Ferrari AC, O’Brien SJ (1987) Cytogenetic methodologies for gene mapping and comparative analyses in mammalian cell culture systems. Gene Anal Tech 4:75–85
Murphy WJ, Menotti-Raymond M, Lyons LA, Thompson MA, O’Brien SJ (1999a) Development of a feline whole genome radiation hybrid panel and comparative mapping of human chromosome 12 and 22 loci. Genomics 57:1–8
Murphy WJ, Sun S, Chen ZQ, Pecon-Slattery J, O’Brien SJ (1999b) Extensive conservation of sex chromosome organization between cat and human revealed by parallel radiation hybrid mapping. Genome Res 9:1223–1230
Murphy WJ, Sun S, Chen Z, Yuhki N, Hirschmann D, Menotti-Raymond M, O’Brien SJ (2000) A radiation hybrid map of the cat genome: implications for comparative mapping. Genome Res 10:691–702
Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351
Nash WG, Wienberg J, Ferguson-Smith MA, Menninger JC, O’Brien SJ (1998) Comparative genomics: tracking chromosome evolution in the family Ursidae using reciprocal chromosome painting. Cytogenet Cell Genet 83:182–192
Nash WG, Menninger JC, Wienberg J, Padilla-Nash HM, O’Brien SJ (2001) The pattern of phylogenomic evolution of the Canidae. Cytogenet Cell Genet 95:210–224
O’Brien SJ, Cevario SJ, Martenson JS, Thompson MA, Nash WG, Chang E, Graves JA, Spencer JA, Cho KW, Tsujimoto H, Lyons LA (1997a) Comparative gene mapping in the domestic cat (Felis catus). J Hered 88:408–414
O’Brien SJ, Wienberg J, Lyons LA (1997b) Comparative genomics: lessons from cats. Trends Genet 13:393–399
O’Brien SJ, Yuhki N (1999) Comparative genome organization of the major histocompatibility complex: lessons from the Felidae. Immunol Rev 167:133–144
Renard C, Vaiman M, Chiannilkulchai N, Cattolico L, Robert C, Chardon P (2001) Sequence of the pig major histocompatibility region containing the classical class I genes. Immunogenetics 53:490–500
Riethman H, Ambrosini A, Castaneda C, Finklestein J, Hu XL, Mudunuri U, Paul S, Wei J (2004) Mapping and initial analysis of human subtelomeric sequence assemblies. Genome Res 14:18–28
Rink A, Santschi EM, Eyer KM, Roelofs B, Hess M, Godfrey M, Karajusuf EK, Yerle M, Milan D, Beattie CW (2002) A first-generation EST RH comparative map of the porcine and human genome. Mamm Genome 13:578–587
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-386
Shigenari A, Ando A, Renard C, Chardon P, Shiina T, Kulski JK, Yasue H, Inoko H (2004) Nucleotide sequencing analysis of the swine 433-kb genomic segment located between the non-classical and classical SLA class I gene clusters. Immunogenetics 55:695–705
Shiina T, Tamiya G, Oka A, Takishima N, Inoko H (1999) Genome sequencing analysis of the 1.8 Mb entire human MHC class I region. Immunol Rev 167:193–199
Skow LC, Snaples SN, Davis SK, Taylor JF, Huang B, Gallagher DH (1996) Localization of bovine lymphocyte antigen (BoLA) DYA and class I loci to different regions of chromosome 23. Mammal Genome 7:388–389
Smith TP, Rohrer GA, Alexander LJ, Troyer DL, Kirby-Dobbels KR, Janzen MA, Cornwell DL, Louis CF, Schook LB, Beattie CW (1995) Directed integration of the physical and genetic linkage maps of swine chromosome 7 reveals that the SLA spans the centromere. Genome Res 5:259–271
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
Soderlund C, Longden I, Mott R (1997) FPC: a system for building contigs from restriction fingerprinted clones. Comput Appl Biosci 13:523–535
Stewart EA, McKusick KB, Aggarwal A et al (1997) An STS-based radiation hybrid map of the human genome. Genome Res 7:422-433
Takada T, Kumanovics A, Amadou C, Yoshino M, Jones EP, Athanasiou M, Evans GA, Fischer Lindahl K (2003) Species-specific class I gene expansions formed the telomeric 1 Mb of the mouse major histocompatibility complex. Genome Res 13:589–600
Thomas JW, Lee-Lin SQ, Green ED (1999) Human–mouse comparative mapping of the genomic region containing CDK6: localization of an evolutionary breakpoint. Mamm Genome 10:764–767
Thomas JW, Schueler MG, Summers TJ, Blakesley RW, McDowell JC, Thomas PJ, Idol JR, Maduro VV, Lee-Lin SQ, Touchman JW, Bouffard GG, Beckstrom-Sternberg SM, Green ED (2003) Pericentromeric duplications in the laboratory mouse. Genome Res 13:55–63
Trowsdale J (1995) “Both man & bird & beast”: comparative organization of MHC genes. Immunogenetics 41:1–17
Velten F, Rogel-Gaillard C, Renard C, Pontarotti P, Tazi-Ahnini R, Vaiman M, Chardon P (1998) A first map of the porcine major histocompatibility complex class I region. Tissue Antigens 51:183–194
Velten FW, Renard C, Rogel-Gaillard C, Vaiman M, Chardon P (1999) Spatial arrangement of pig MHC class I sequences. Immunogenetics 49:919–930
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
Acknowledgements
The authors gratefully acknowledge to the technical assistance of H. Banh, M. Clotter, N. Crumpler, C. Jones, M. Kessler, and S. Selway. In addition, the authors are indebted to Drs. Pat Martin and Colm O’hUigin for critical reading of this manuscript and R. Stephens (Advanced Biomedical Computing Center, National Cancer Institute at Frederick). This publication has been funded in whole or part with F
federal funds from the National Cancer Institute, National Institutes of Health, under contract no. N01-C0-12400. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government.
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Beck, T.W., Menninger, J., Murphy, W.J. et al. The feline major histocompatibility complex is rearranged by an inversion with a breakpoint in the distal class I region. Immunogenetics 56, 702–709 (2005). https://doi.org/10.1007/s00251-004-0742-6
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DOI: https://doi.org/10.1007/s00251-004-0742-6