The major histocompatibility complex in Old World camelids and low polymorphism of its class II genes
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
P 24706
Austrian Science Fund FWF - Austria
PubMed
26931144
PubMed Central
PMC4774177
DOI
10.1186/s12864-016-2500-1
PII: 10.1186/s12864-016-2500-1
Knihovny.cz E-zdroje
- MeSH
- alely MeSH
- exony MeSH
- fylogeneze MeSH
- fyzikální mapování chromozomů MeSH
- geny MHC třídy II * MeSH
- haplotypy MeSH
- molekulární sekvence - údaje MeSH
- polymorfismus genetický * MeSH
- sekvence nukleotidů MeSH
- velbloudi genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
BACKGROUND: The Major Histocompatibility Complex (MHC) is a genomic region containing genes with crucial roles in immune responses. MHC class I and class II genes encode antigen-presenting molecules expressed on the cell surface. To counteract the high variability of pathogens, the MHC evolved into a region of considerable heterogeneity in its organization, number and extent of polymorphism. Studies of MHCs in different model species contribute to our understanding of mechanisms of immunity, diseases and their evolution. Camels are economically important domestic animals and interesting biomodels. Three species of Old World camels have been recognized: the dromedary (Camelus dromedarius), Bactrian camel (Camelus bactrianus) and the wild camel (Camelus ferus). Despite their importance, little is known about the MHC genomic region, its organization and diversity in camels. The objectives of this study were to identify, map and characterize the MHC region of Old World camelids, with special attention to genetic variation at selected class MHC II loci. RESULTS: Physical mapping located the MHC region to the chromosome 20 in Camelus dromedarius. Cytogenetic and comparative analyses of whole genome sequences showed that the order of the three major sub-regions is "Centromere - Class II - Class III - Class I". DRA, DRB, DQA and DQB exon 2 sequences encoding the antigen binding site of the corresponding class II antigen presenting molecules showed high degree of sequence similarity and extensive allele sharing across the three species. Unexpectedly low extent of polymorphism with low numbers of alleles and haplotypes was observed in all species, despite different geographic origins of the camels analyzed. The DRA locus was found to be polymorphic, with three alleles shared by all three species. DRA and DQA sequences retrieved from ancient DNA samples of Camelus dromedarius suggested that additional polymorphism might exist. CONCLUSIONS: This study provided evidence that camels possess an MHC comparable to other mammalian species in terms of its genomic localization, organization and sequence similarity. We described ancient variation at the DRA locus, monomorphic in most species. The extent of molecular diversity of MHC class II genes seems to be substantially lower in Old World camels than in other mammalian species.
Ceitec VFU RG Animal Immunogenomics Brno Czech Republic
Department of Animal Genetics Veterinary and Pharmaceutical University Brno Czech Republic
Department of Biology Duke University Durham NC USA
Department of Genetics and Reproduction Veterinary Research Institute Brno Czech Republic
Institute of Population Genetics Vetmeduni Vienna Vienna Austria
Research Institute of Wildlife Ecology Vetmeduni Vienna Vienna Austria
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Janeway CA, Travers P, Walport M, Shlomchik MJ. Immunobiology: The Immune System in Health and Disease. 5. New York: Garland Science; 2001.
Meyer D, Thomson G. How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet. 2001;65:1–26. doi: 10.1046/j.1469-1809.2001.6510001.x. PubMed DOI
Hedrick PW. Evolutionary genetics of the major histocompatibility complex. American Naturalist. 1994;143:945–964.
Reche PA, Reinherz EL. Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol. 2003;331:623–641. doi: 10.1016/S0022-2836(03)00750-2. PubMed DOI
Cho S, Attaya M, Monaco JJ. New class ll-like genes in the murine MHC. Nature. 1991;353:573–576. doi: 10.1038/353573a0. PubMed DOI
Bontrop RE, Otting N, Groot NG, Doxiadis GG. Major histocompatibility complex class II polymorphisms in primates. Immunol Rev. 1999;167:339–350. doi: 10.1111/j.1600-065X.1999.tb01403.x. PubMed DOI
Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SGE. IPD—the Immuno Polymorphism Database. Nucleic Acids Res. 2013;41:D1234–D1240. doi: 10.1093/nar/gks1140. PubMed DOI PMC
He Y, Xi D, Leng J, Qian T, Jin D, Chen T, et al. Genetic variability of MHC class II DQB exon 2 alleles in yak (Bos grunniens) Mol Biol Rep. 2014;41:2199–2206. doi: 10.1007/s11033-014-3071-3. PubMed DOI
Alcaide M, Munoz J, Martínez‐de la Puente J, Soriguer R, Figuerola J. Extraordinary MHC class II B diversity in a non‐passerine, wild bird: the Eurasian Coot Fulica atra (Aves: Rallidae) Ecol Evol. 2014;4:688–698. doi: 10.1002/ece3.974. PubMed DOI PMC
Wegner KM, Reusch TBH, Kalbe M. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol. 2003;16:224–232. doi: 10.1046/j.1420-9101.2003.00519.x. PubMed DOI
Bulliet RW. The Camel and the Wheel. Cambridge, MA: Harvard University Press; 1975. p. 340.
Burger PA. Genetic Traces of Domestication in Old World Camelids. In: Knoll EM, Burger PA, editors. Camels in Asia and North Africa: Interdisciplinary Perspectives on Their Past and Present Significance. Vienna: Austrian Academy of Science Press; 2012. pp. 17–28.
Wu H, Guang X, Al-Fageeh MB, Cao J, Pan S, Zhou H, et al. Camelid genomes reveal evolution and adaptation to desert environments. Nat Commun. 2014;5:1–9. PubMed
Ji R, Cui P, Ding F, Geng J, Gao H, Zhang H, et al. Monophyletic origin of domestic bactrian camel (Camelus bactrianus) and its evolutionary relationship with the extant wild camel (Camelus bactrianus ferus) Anim Genet. 2009;40:377–382. doi: 10.1111/j.1365-2052.2008.01848.x. PubMed DOI PMC
Silbermayr K, Orozco-terWengel P, Charruau P, Enkhbileg D, Walzer C, Vogl C, et al. High mitochondrial differentiation levels between wild and domestic Bactrian camels: a basis for rapid detection of maternal hybridization. Anim Genet. 2010;41:315–318. doi: 10.1111/j.1365-2052.2009.01993.x. PubMed DOI
Jirimutu, Wang Z, Ding G, Chen G, Sun Y, Sun Z, Zhang H, Wang L, Hasi S, Zhang Y, Li J, Shi Y, Xu Z, He C, Yu S, Li S, Zhang W, Batmunkh M, Ts B, Narenbatu, Unierhu, Bat-Ireedui S, Gao H, Baysgalan B, Li Q, Jia Z, Turigenbayila, Subudenggerile, Narenmanduhu, Wang Z, et al. Genome sequences of wild and domestic bactrian camels. Nat Commun. 2012; 3:1202. PubMed PMC
Wernery U, Kaaden OR. Foot-and-mouth disease in camelids: a review. Vet J. 2004;168:134–142. doi: 10.1016/j.tvjl.2003.10.005. PubMed DOI
Dirie MF, Abdurahman O. Observations on little known diseases of camels (Camelus dromedarius) in the Horn of Africa. Revue scientifique et technique-Office international des épizooties. 2003;22:1043–1050. PubMed
Azhar EI, El-Kafrawy SA, Farraj SA, Hassan AM, Al-Saeed MS, Hashem AM, et al. Evidence for Camel-to-Human Transmission of MERS Coronavirus. N Engl J Med. 2014;370(26):2499–2505. doi: 10.1056/NEJMoa1401505. PubMed DOI
Hemida MG, Elmoslemany A, Al‐Hizab F, Alnaeem A, Almathen F, Faye B, et al. Dromedary Camels and the Transmission of Middle East Respiratory Syndrome Coronavirus (MERS‐CoV) Transbound Emerg Dis. 2015 PubMed PMC
Muyldermans S, Baral TN, Retamozzo VC, De Baetselier P, De Genst E, Kinne J, et al. Camelid immunoglobulins and nanobody technology. Vet Immunol Immunopathol. 2009;128:178–183. doi: 10.1016/j.vetimm.2008.10.299. PubMed DOI
Tillib SV, Vyatchanin AS, Muyldermans S. Molecular analysis of heavy chain-only antibodies of Camelus bactrianus. Biochem Mosc. 2014;79:1382–1390. doi: 10.1134/S000629791412013X. PubMed DOI
Antczak D. Major Histocompatibility Complex Genes Of The Dromedary Camel. In: Qatar Foundation Annual Research Conference. Doha, Qatar: BIOP 015;2013.
Burger PA, Palmieri N. Estimating the Population Mutation Rate from a de novo Assembled Bactrian Camel Genome and Cross-Species Comparison with Dromedary ESTs. J Hered. 2013;105(6):839–846. PubMed PMC
Fitak RR, Mohandesan E, Corander J, Burger PA. The de novo genome assembly and annotation of a female domestic dromedary of North African origin. Mol Ecol Resour. 2015 PubMed PMC
Green ED, Guyer MS, Institute NHGR Charting a course for genomic medicine from base pairs to bedside. Nature. 2011;470:204–213. doi: 10.1038/nature09764. PubMed DOI
Lighten J, van Oosterhout C, Bentzen P. Critical review of NGS analyses for de novo genotyping multigene families. Mol Ecol. 2014;23:3957–3972. doi: 10.1111/mec.12843. PubMed DOI
Green MR, Sambrook J. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press; 2012.
Knapp M, Clarke AC, Horsburgh KA, Matisoo-Smith EA. Setting the stage–building and working in an ancient DNA laboratory. Annals of Anatomy-Anatomischer Anzeiger. 2012;194:3–6. doi: 10.1016/j.aanat.2011.03.008. PubMed DOI
Rohland N, Hofreiter M. Comparison and optimization of ancient DNA extraction. Biotechniques. 2007;42:343. doi: 10.2144/000112383. PubMed DOI
Rohland N, Siedel H, Hofreiter M. A rapid column‐based ancient DNA extraction method for increased sample throughput. Mol Ecol Resour. 2010;10:677–683. doi: 10.1111/j.1755-0998.2009.02824.x. PubMed DOI
Avila F, Das PJ, Kutzler M, Owens E, Perelman P, Rubes J, et al. Development and application of camelid molecular cytogenetic tools. J Hered. 2014;201(105):858–869. PubMed PMC
Basic Local Alignment Search Tool. http://blast.ncbi.nlm.nih.gov/Blast.cgi. Accessed 15 Oct 2015.
Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics methods and protocols. New York, NY. USA: Springer; 1999. 365–386. PubMed
Sigurdardóttir S, Borsch C, Gustafsson K, Andersson L. Gene duplications and sequence polymorphism of bovine class II DQB genes. Immunogenetics. 1992;35:205–213. doi: 10.1007/BF00185115. PubMed DOI
Gyllensten UB, Lashkari D, Erlich HA. Allelic diversification at the class II DQB locus of the mammalian major histocompatibility complex. Proc Natl Acad Sci. 1990;87:1835–1839. doi: 10.1073/pnas.87.5.1835. PubMed DOI PMC
Sff_extract. http://bioinf.comav.upv.es/sff_extract/index.html. Accessed 9 July 2014.
GS de novo Assembler. http://www.454.com/products/analysis-software/. Accessed 9 July 2014
FastQC. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. Accessed 10 July 2014.
Shrestha R, Lubinsky B, Bansode V, Moinz M, McCormack G, Travers S. QTrim: a novel tool for the quality trimming of sequence reads generated using the Roche/454 sequencing platform. BMC Bioinformatics. 2014;15:33. doi: 10.1186/1471-2105-15-33. PubMed DOI PMC
Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10–12. doi: 10.14806/ej.17.1.200. DOI
Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:13033997 2013.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC
Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24–26. doi: 10.1038/nbt.1754. PubMed DOI PMC
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297–1303. doi: 10.1101/gr.107524.110. PubMed DOI PMC
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011;43:491–498. doi: 10.1038/ng.806. PubMed DOI PMC
Hall TA. Nucleic acids symposium series. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT; pp. 95–98.
Auwera GA, Carneiro MO, Hartl C, Poplin R, del Angel G, Levy‐Moonshine A, et al. From FastQ data to high‐confidence variant calls: the genome analysis toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;11(1110):11.10.1–11.10.33. PubMed PMC
Jukes TH, Cantor CR. Evolution of protein molecules. Mamm Protein Metab. 1969;3:21–132. doi: 10.1016/B978-1-4832-3211-9.50009-7. DOI
Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–120. doi: 10.1007/BF01731581. PubMed DOI
Akaike H. A new look at the statistical model identification. Automatic Control, IEEE Transactions on. 1974;19:716–723. doi: 10.1109/TAC.1974.1100705. DOI
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–425. PubMed
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–2729. doi: 10.1093/molbev/mst197. PubMed DOI PMC
Klein J, Bontrop RE, Dawkins RL, Erlich HA, Gyllensten UB, Heise ER, Jones PP, Parham P, Wakeland EK, Watkins DI. Nomenclature for the major histocompatibility complexes of different species: a proposal. In: Solheim BG, Ferrone S, Möller E. editors. The HLA System in Clinical Transplantation. Berlin, Heidelberg, Germany: Springer. 1993; 407–411.
Balmus G, Trifonov VA, Biltueva LS, O’Brien PC, Alkalaeva ES, Fu B, et al. Cross-species chromosome painting among camel, cattle, pig and human: further insights into the putative Cetartiodactyla ancestral karyotype. Chromosom Res. 2007;15:499–514. doi: 10.1007/s10577-007-1154-x. PubMed DOI
Kumánovics A, Takada T, Lindahl KF. Genomic organization of the mammalian MHC. Annu Rev Immunol. 2003;21:629–657. doi: 10.1146/annurev.immunol.21.090501.080116. PubMed DOI
Avila F, Baily MP, Perelman P, Das PJ, Pontius J, Chowdhary R, et al. A Comprehensive Whole-Genome Integrated Cytogenetic Map for the Alpaca (Lama pacos) Cytogenet Genome Res. 2014;144:196–207. doi: 10.1159/000370329. PubMed DOI
Klein J, Figueroa F. Evolution of the major histocompatibility complex. Crit Rev Immunol. 1985;6:295–386. PubMed
Parham P. Virtual reality in the MHC. Immunol Rev. 1999;167:5–15. doi: 10.1111/j.1600-065X.1999.tb01378.x. PubMed DOI
Mikko S, Røed K, Schmutz S, Andersson L. Monomorphism and polymorphism at Mhc DRB loci in domestic and wild ruminants. Immunol Rev. 1999;167:169–178. doi: 10.1111/j.1600-065X.1999.tb01390.x. PubMed DOI
Andersson L, Rask L. Characterization of the MHC class II region in cattle. The number of DQ genes varies between haplotypes. Immunogenetics. 1988;27:110–120. doi: 10.1007/BF00351084. PubMed DOI
Bollmer JL, Vargas FH, Parker PG. Low MHC variation in the endangered Galapagos penguin (Spheniscus mendiculus) Immunogenetics. 2007;59:593–602. doi: 10.1007/s00251-007-0221-y. PubMed DOI
Weber DS, Van Coeverden De Groot PJ, Peacock E, Schrenzel MD, Perez DA, Thomas S, et al. Low MHC variation in the polar bear: implications in the face of Arctic warming? Anim Conserv. 2013;16:671–683. doi: 10.1111/acv.12045. DOI
Sommer S, Tichy H. Major histocompatibility complex (MHC) class II polymorphism and paternity in the monogamous Hypogeomys antimena, the endangered, largest endemic Malagasy rodent. Mol Ecol. 1999;8:1259–1272. doi: 10.1046/j.1365-294X.1999.00687.x. PubMed DOI
Ellegren H, Mikk S, Wallin K, Andersson L. Limited polymorphism at major histocompatibility complex (MHC) loci in the Swedish moose A. alces. Mol Ecol. 1996;5:3–9. doi: 10.1111/j.1365-294X.1996.tb00286.x. PubMed DOI PMC
Zhou H, Hickford JGH, Fang Q, Byun SO. Short Communication: Identification of Allelic Variation at the Bovine DRA Locus by Polymerase Chain Reaction-Single Strand Conformational Polymorphism. J Dairy Sci. 2007;90:1943–1946. doi: 10.3168/jds.2006-578. PubMed DOI
Takada T, Kikkawa Y, Yonekawa H, Amano T. Analysis of goat MHC class II DRA and DRB genes: identification of the expressed gene and new DRB alleles. Immunogenetics. 1998;48:408–412. doi: 10.1007/s002510050452. PubMed DOI
Takeshima S, Saitou N, Morita M, Inoko H, Aida Y. The diversity of bovine MHC class II DRB3 genes in Japanese Black, Japanese Shorthorn, Jersey and Holstein cattle in Japan. Gene. 2003;316:111–118. doi: 10.1016/S0378-1119(03)00744-3. PubMed DOI
Yadamsuren, A, Dulamtseren E, Reading RP. The conservation status and management of wild camels in Mongolia. In: Knoll EM, Burgr PA, editors. Camels in Asia and North Africa. Interdisciplinary perspectives on their significance in past and present.Vienna. Austrian Academy of Sciences Press. 2012; p 45–54.
Ballingall KT, Steele P, Lantier I, Cotelli M, Todd H, Lopez G, et al. An ancient interlocus recombination increases class II MHC DQA diversity in sheep and other Bovidae. Anim Genet. 2015;46:333–336. doi: 10.1111/age.12290. PubMed DOI
Ballingall KT, Luyai A, McKeever DJ. Analysis of genetic diversity at the DQA loci in African cattle: evidence for a BoLA-DQA3 locus. Immunogenetics. 1997;46:237–244. doi: 10.1007/s002510050268. PubMed DOI
Moutou K, Koutsogiannouli E, Stamatis C, Billinis C, Kalbe C, Scandura M, et al. Domestication does not narrow MHC diversity in Sus scrofa. Immunogenetics. 2013;65:195–209. doi: 10.1007/s00251-012-0671-8. PubMed DOI
Behl JD, Verma NK, Tyagi N, Mishra P, Behl R, Joshi BK. The Major Histocompatibility Complex in Bovines: A Review. ISRN Vet Sci. 2012;2012:1–12. doi: 10.5402/2012/872710. PubMed DOI PMC
Hořín P, Matiašovic J. A second locus and new alleles in the major histocompatibility complex class II (ELA-DQB) region in the horse. Anim Genet. 2002;33:196–200. doi: 10.1046/j.1365-2052.2002.00839.x. PubMed DOI
Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K, Gragert L, et al. The shaping of modern human immune systems by multiregional admixture with archaic humans. Science. 2011;334:89–94. doi: 10.1126/science.1209202. PubMed DOI PMC
Hofreiter M, Paijmans JL, Goodchild H, Speller CF, Barlow A, Fortes GG, et al. The future of ancient DNA: Technical advances and conceptual shifts. BioEssays. 2015;37:284–293. doi: 10.1002/bies.201400160. PubMed DOI
Briggs AW, Stenzel U, Meyer M, Krause J, Kircher M, Pääbo S. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 2010;38:87. doi: 10.1093/nar/gkp1163. PubMed DOI PMC