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Analysis of a marsupial MHC region containing two recently duplicated class I loci

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Abstract

A 37-kb cosmid containing two complete major histocompatibility complex (MHC) class I α chain loci from the opossum Monodelphis domestica was isolated, fully sequenced, and characterized. This sequence represents the largest contiguous genomic sequence reported for the MHC region of a nonplacental mammal. Based on particular conserved amino acid residues, and limited expression analyses, the two MHC-I loci, designated ModoUB and ModoUC, appear to encode functional MHC-I molecules. The two coding regions are 98% identical at the nucleotide level; however, their promoter regions differ significantly. Two CpG islands present in the cosmid sequence correspond to the two coding regions. Twelve microsatellites and six retroelements were also present in the cosmid. The retroelements share highest sequence homology to the CORE–SINE family of retroelements. Due to high sequence identity, it is very likely that ModoUB and ModoUC loci are products of recent gene duplication that occurred less than 4 million years ago.

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References

  • SF Altschul W Gish W Miller EW Myers DJ Lipman (1990) ArticleTitleBasic local alignment search tool J Mol Biol 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999 Occurrence Handle1:CAS:528:DyaK3MXitVGmsA%3D%3D Occurrence Handle2231712

    Article  CAS  PubMed  Google Scholar 

  • J Bingulac–Popovic F Figueroa A Sato WS Talbot SL Johnson et al. (1997) ArticleTitleMapping of mhc class I and class II regions to different linkage groups in the zebrafish, Danio rerio Immunogenetics 46 129–134 Occurrence Handle10.1007/s002510050251 Occurrence Handle1:CAS:528:DyaK2sXkslaiurw%3D Occurrence Handle9162099

    Article  CAS  PubMed  Google Scholar 

  • TW Burke JT Kadonga (1996) ArticleTitle Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-deficient promoters Genes Dev 10 711–724 Occurrence Handle1:CAS:528:DyaK28XhvVCrt7o%3D Occurrence Handle8598298

    CAS  PubMed  Google Scholar 

  • C Dennis (2003) ArticleTitleOpossum hops over kangaroo to top genome list Nature 425 753 Occurrence Handle10.1038/425758a Occurrence Handle1:CAS:528:DC%2BD3sXotlWru7o%3D

    Article  CAS  Google Scholar 

  • J Felsenstein (1981) ArticleTitleEvolutionary trees from DNA sequences: a maximum likelihood approach J Mol Evol 17 368–376 Occurrence Handle1:CAS:528:DyaL3MXls1Cisr8%3D Occurrence Handle7288891

    CAS  PubMed  Google Scholar 

  • WM Fitch (1971) ArticleTitleToward defining the course of evolution: Minimum change for a specific tree topology Syst Zool 20 406–416

    Google Scholar 

  • N Gilbert D Labuda (1999) ArticleTitleCORE–SINEs: Eukaryotic short interspersed retroposing elements with common sequence motifs Proc Natl Acad Sci USA 96 2869–2874 Occurrence Handle10.1073/pnas.96.6.2869 Occurrence Handle1:CAS:528:DyaK1MXhvFyks74%3D Occurrence Handle10077603

    Article  CAS  PubMed  Google Scholar 

  • N Gilbert D Labuda (2000) ArticleTitleEvolutionary inventions and continuity of CORE–SINEs in mammals J Mol Biol 298 365–377 Occurrence Handle10.1006/jmbi.2000.3695 Occurrence Handle1:CAS:528:DC%2BD3cXisFeksL8%3D Occurrence Handle10772856

    Article  CAS  PubMed  Google Scholar 

  • PA Gorer (1937) ArticleTitleThe genetic and antigenic basis of tumour transplantation J Pathol Bacteriol 44 691–697

    Google Scholar 

  • PA Gorer S Lyman GD Snell (1948) ArticleTitleStudies on the genetic and antigenic basis of tumour transplantation, linkage between a histocompatibility gene and ‘fused’ in mice Proc R Soc London B Biol Sci 135 499–505

    Google Scholar 

  • BC Guild JL Strominger (1984) ArticleTitleHuman and murine class I MHC antigens conserved serine 335, the site of HLA phosphorylation in vivo J Biol Chem 259 9235–9240 Occurrence Handle1:CAS:528:DyaL2cXkvVymt7w%3D Occurrence Handle6430898

    CAS  PubMed  Google Scholar 

  • BC Guild RL Erikson JL Strominger (1983) ArticleTitleHLA-A2 and HLA-B7 antigens are phosphorylated in vitro by Rous sarcoma virus kinase (pp60V-src) at a tyrosine residue encoded in a highly conserved exon of the intracellular domain Proc Natl Acad Sci USA 91 2894–2898

    Google Scholar 

  • E Günther L Walter (2001) ArticleTitleThe major histocompatibility complex of the rat (Rattus norvegicus) Immunogenetics 53 520–542 Occurrence Handle10.1007/s002510100361 Occurrence Handle11685465

    Article  PubMed  Google Scholar 

  • JD Hansen P Strassburger GH Thorgaard WP Young L Du Pasquier (1999) ArticleTitleExpression, linkage, and polymorphism of MHC-related genes in rainbow trout, Oncorhynchus mykiss J Immunol 163 774–786 Occurrence Handle1:CAS:528:DyaK1MXksVeguro%3D Occurrence Handle10395670

    CAS  PubMed  Google Scholar 

  • AL Hughes M Nei (1988) ArticleTitlePattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection Nature 335 167–170 Occurrence Handle10.1038/335167a0 Occurrence Handle1:CAS:528:DyaL1cXlvVCktrY%3D Occurrence Handle3412472

    Article  CAS  PubMed  Google Scholar 

  • A Janke X Xu U Arnason (1997) ArticleTitleThe complete mitochondrial genome of the wallaroo (Macropus robustus) and the phylogenetic relationship among Monotremata, Marsupiala, and Eutheria Proc Natl Acad Sci USA 94 1276–1281 Occurrence Handle10.1073/pnas.94.4.1276 Occurrence Handle1:CAS:528:DyaK2sXhtlGlu7o%3D Occurrence Handle9037043

    Article  CAS  PubMed  Google Scholar 

  • J Kaufman J Salomonsen M Flajnik (1994) ArticleTitleEvolutionary conservation of Mhc class I and II molecules: different yet the same Semin Immunol 6 411–424 Occurrence Handle10.1006/smim.1994.1050 Occurrence Handle1:CAS:528:DyaK2MXltlagtbg%3D Occurrence Handle7654997

    Article  CAS  PubMed  Google Scholar 

  • J Kaufman S Milne TW Gobel BA Walker JP Jacob et al. (1999) ArticleTitleThe chicken B locus is a minimal essential major histocompatibility complex Nature 401 923–925 Occurrence Handle10.1038/44856 Occurrence Handle1:CAS:528:DyaK1MXntFyksrg%3D Occurrence Handle10553909

    Article  CAS  PubMed  Google Scholar 

  • JAW Kirsch GC Mayer (1998) ArticleTitleThe platypus is not a rodent: DNA hybridization, amniote phylogeny and the palimpsest theory Philos Trans R Soc Lond B Biol Sci 353 1221–1237 Occurrence Handle10.1098/rstb.1998.0278 Occurrence Handle1:CAS:528:DyaK1cXlsVWhtrg%3D Occurrence Handle9720117

    Article  CAS  PubMed  Google Scholar 

  • JAW Kirsch FJ Lapointe MS Springer (1997) ArticleTitleDNA studies of marsupials and their implications for metatherian classification Aust J Zool 45 211–280 Occurrence Handle10.1071/ZO96030 Occurrence Handle1:CAS:528:DyaK2sXmt1Oqtbg%3D

    Article  CAS  Google Scholar 

  • J Klein RE Bontrop RL Dawkins HA Erlich UB Gyllensten et al. (1990) ArticleTitleNomenclature for the major histocompatibility complexes of different species: a proposal Immunogenetics 31 217–219 Occurrence Handle1:CAS:528:DyaK3cXlsFSiu7c%3D Occurrence Handle2329006

    CAS  PubMed  Google Scholar 

  • JK Kulski S Gaudieri M Bellgard L Balmer K Giles et al. (1997) ArticleTitleThe evolution of MHC diversity by segmental duplication and transposition of retroelements J Mol Evol 45 599–609 Occurrence Handle1:CAS:528:DyaK1cXkt1ei Occurrence Handle9419237

    CAS  PubMed  Google Scholar 

  • S Kumar SB Hedges (1998) ArticleTitleA molecular timescale for vertebrate evolution Nature 392 917–920 Occurrence Handle10.1038/31927 Occurrence Handle1:CAS:528:DyaK1cXjtV2jur8%3D Occurrence Handle9582070

    Article  CAS  PubMed  Google Scholar 

  • F Larsen G Gundersen R Lopez H Prydz (1992) ArticleTitleCpG islands as gene markers in the human genome Genomics 13 1095–1107 Occurrence Handle10.1016/0888-7543(92)90024-M Occurrence Handle1:CAS:528:DyaK3sXhs1aitL0%3D Occurrence Handle1505946

    Article  CAS  PubMed  Google Scholar 

  • MHC Sequencing Consortium (1999) ArticleTitleComplete sequence and gene map of a human major histocompatibility complex Nature 401 921–923 Occurrence Handle10.1038/44853 Occurrence Handle10553908

    Article  PubMed  Google Scholar 

  • KB Miska RD Miller (1999) ArticleTitleMarsupial Mhc class I: classical sequences from the opossum, Monodelphis domestica Immunogenetics 50 89–93 Occurrence Handle10.1007/s002510050692 Occurrence Handle1:CAS:528:DyaK1MXmt12it70%3D Occurrence Handle10541813

    Article  CAS  PubMed  Google Scholar 

  • KB Miska GH Harrison L Hellman RD Miller (2002) ArticleTitleThe major histocompatibility complex in monotremes: An analysis of the evolution of Mhc class I genes across all three mammalian subclasses Immunogenetics 54 381–393 Occurrence Handle10.1007/s00251-002-0484-2 Occurrence Handle1:CAS:528:DC%2BD38XntFems70%3D Occurrence Handle12242589

    Article  CAS  PubMed  Google Scholar 

  • M Nei X Gu T Sitnikova (1997) ArticleTitleEvolution by the birth-and-death process in multigene families of the vertebrate immune system Proc Natl Acad Sci USA 94 7799–7806 Occurrence Handle10.1073/pnas.94.15.7799 Occurrence Handle1:CAS:528:DyaK2sXksl2nsbg%3D Occurrence Handle9223266

    Article  CAS  PubMed  Google Scholar 

  • Y Ohta K Okamura EC McKinney S Bartl K Hashimoto et al. (2000) ArticleTitlePrimitive synteny of vertebrate major histocompatibility complex class I and class II genes Proc Natl Acad Sci USA 97 4712–4717 Occurrence Handle10.1073/pnas.97.9.4712 Occurrence Handle1:CAS:528:DC%2BD3cXivFKjtLg%3D Occurrence Handle10781076

    Article  CAS  PubMed  Google Scholar 

  • P Parham DA Lawlor CE Lomen PD Ennis (1989) ArticleTitleDiversity and diversification of HLA-A, B, C alleles J Immunol 142 3937–3950 Occurrence Handle1:CAS:528:DyaL1MXlt1yhs7g%3D Occurrence Handle2715640

    CAS  PubMed  Google Scholar 

  • JL Patton SF dos Reis MNF da Silva (1996) ArticleTitleRelationships among didelphid marsupials based on sequence variation in the mitochondrial cytochrome B gene J Mamm Evol 3 3–29

    Google Scholar 

  • D Posada KA Crandall (1998) ArticleTitleMODELTEST: testing the model of DNA substitution Bioinformatics 14 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953

    Article  CAS  PubMed  Google Scholar 

  • C Renard M Vaiman N Chiannilkulchai L Cattolico C Robert et al. (2001) ArticleTitleSequence of the pig major histocompatibility region containing the classical class I genes Immunogenetics 53 490–500 Occurrence Handle10.1007/s002510100348 Occurrence Handle1:CAS:528:DC%2BD3MXosFShurY%3D Occurrence Handle11685460

    Article  CAS  PubMed  Google Scholar 

  • JD Retief C Krajewski M Westerman RJ Winkfein GH Dixon (1995) ArticleTitleMolecular phylogeny and evolution of marsupial protamine PI genes Proc R Soc Lond B Biol Sci 259 7–14 Occurrence Handle1:CAS:528:DyaK2MXosFCjtrs%3D Occurrence Handle7700877

    CAS  PubMed  Google Scholar 

  • N Saitou M Nei (1987) ArticleTitleThe neighbor joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406–425 Occurrence Handle1:STN:280:BieC1cbgtVY%3D Occurrence Handle3447015

    CAS  PubMed  Google Scholar 

  • R Salter R Benjamin P Wesley S Buxton T Garret et al. (1990) ArticleTitleA binding site for the T cell co-receptor CD8 on the α3 domain of HLA-A2 Nature 345 41–46 Occurrence Handle10.1038/345041a0 Occurrence Handle1:CAS:528:DyaK3cXktlyms7c%3D Occurrence Handle2109837

    Article  CAS  PubMed  Google Scholar 

  • PB Samollow JA Marshall–Graves (1998) ArticleTitleGene maps of marsupials ILAR J 39 203–224 Occurrence Handle11528080

    PubMed  Google Scholar 

  • MA Saper PJ Bjorkman DC Wiley (1991) ArticleTitleRefined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution J Mol Biol 219 277–319 Occurrence Handle1:CAS:528:DyaK3MXkvFSgtbw%3D Occurrence Handle2038058

    CAS  PubMed  Google Scholar 

  • T Shiina G Tamiya A Oka N Takishima T Yamagata et al. (1999) ArticleTitleMolecular dynamics of MHC genesis unraveled by sequence analysis of the 1,796,938-bp HLA class I region Proc Natl Acad Sci USA 96 13282–13287 Occurrence Handle10.1073/pnas.96.23.13282 Occurrence Handle1:CAS:528:DyaK1MXns1Gmt78%3D Occurrence Handle10557312

    Article  CAS  PubMed  Google Scholar 

  • C Solier V Mallet F Lenfant A Bertrand A Huchenq et al. (2001) ArticleTitleHLA-G unique promoter region: functional implications Immunogenetics 53 617–625 Occurrence Handle10.1007/s00251-001-0373-0 Occurrence Handle1:CAS:528:DC%2BD3MXovVWgs7o%3D Occurrence Handle11797094

    Article  CAS  PubMed  Google Scholar 

  • ELL Sonnhammer R Durbin (1995) ArticleTitleA dot-matrix program with dynamic threshold control suited for genomic DNA and protein sequence analysis Gene 167 GC1–10 Occurrence Handle10.1016/0378-1119(95)00714-8 Occurrence Handle1:STN:280:BymC2cvjtVA%3D Occurrence Handle8566757

    Article  CAS  PubMed  Google Scholar 

  • DL Swofford (1998) PAUP*: Phylogenetic analysis using parsimony (* and other methods), Ver. 4.0 beta : Sinauer) (Sunderland, MA: Sinauer)

    Google Scholar 

  • JD Thompson DG Higgins TJ Gibson (1994) ArticleTitleCLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice Nucleic Acids Res 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • AN Vallejo LR Pease (1995) ArticleTitleEvolution of class I promoter sequences: relationship to function and diversity Immunol Rev 143 249–262 Occurrence Handle1:CAS:528:DyaK2MXlsVCntbg%3D Occurrence Handle7558079

    CAS  PubMed  Google Scholar 

  • H Westerdahl H Wittzell T Schantz Particlevon (2000) ArticleTitleMhc diversity in two passerine birds: no evidence for a minimal essential Mhc Immunogenetics 52 92–100 Occurrence Handle10.1007/s002510000256 Occurrence Handle1:CAS:528:DC%2BD3cXot1yltLk%3D Occurrence Handle11132162

    Article  CAS  PubMed  Google Scholar 

  • Y Xu EC Uberbacher (1997) ArticleTitleAutomated gene identification in large-scale genomic sequences J Comput Biol 4 325–338 Occurrence Handle1:CAS:528:DyaK2sXls1Whur4%3D Occurrence Handle9278063

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank G.H. Rosenberg for his assistance in cosmid sequencing strategies, and J. Salazar and D. Burke for valuable technical assistance. This material is based upon work supported by the National Science Foundation under Grant No. 9981960.

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Correspondence to Robert D. Miller.

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Miska, K.B., Wright, A.M., Lundgren, R. et al. Analysis of a marsupial MHC region containing two recently duplicated class I loci. Mamm Genome 15, 851–864 (2004). https://doi.org/10.1007/s00335-004-2224-4

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