Gene duplication and fragmentation in the zebra finch major histocompatibility complex

BMC Biology

Volumn 8, Issue , 2010, Pages

  Balakrishnan, Christopher N ^a,h   Ekblom, Robert ^b,c   Völker, Martin ^d   Westerdahl, Helena ^e   Godinez, Ricardo ^a   Kotkiewicz, Holly ^f   Burt, David W ^g   Graves, Tina ^f   Griffin, Darren K ^d   Warren, Wesley C ^f   Edwards, Scott V ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UPPSALA UNIVERSITY   (Sweden)

^d UNIVERSITY OF KENT   (United Kingdom)

^e LUND UNIVERSITY   (Sweden)

^f WASHINGTON UNIVERSITY   (United States)

^g UNIVERSITY OF EDINBURGH   (United Kingdom)

^h UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVES; BACTERIA (MICROORGANISMS); GALLUS GALLUS; MAMMALIA; PASSERIFORMES; TAENIOPYGIA GUTTATA; VERTEBRATA;

ANIMAL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIOLOGICAL MODEL; DNA FRAGMENTATION; DNA SEQUENCE; FINCH; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DUPLICATION; GENETICS; GENOME; GENOMICS; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SOUTHERN BLOTTING; STATISTICAL MODEL;

ANIMALS; BASE SEQUENCE; BLOTTING, SOUTHERN; CHROMOSOMES, ARTIFICIAL, BACTERIAL; DNA FRAGMENTATION; FINCHES; GENE DUPLICATION; GENOME; GENOMICS; IN SITU HYBRIDIZATION, FLUORESCENCE; LIKELIHOOD FUNCTIONS; MAJOR HISTOCOMPATIBILITY COMPLEX; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; SEQUENCE ANALYSIS, DNA;

EID: 77950522488     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-8-29     Document Type: Article

References (83)

1. Zinkernagel RM, Doherty PC. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function and responsiveness. Adv Immunol 1979, 27:52-277.
2. Hughes AL, Nei M. Nucleotide substitution at major histocompatibility complex class-II loci - evidence for overdominant selection. Proc Nat Acad Sci USA 1989, 86:958-962. 10.1073/pnas.86.3.958, 286598, 2492668.
3. Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class-I loci reveals overdominant selection. Nature 1988, 335:167-170. 10.1038/335167a0, 3412472.
4. Bernatchez L, Landry C. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?. J Evol Biol 2003, 16:363-377. 10.1046/j.1420-9101.2003.00531.x, 14635837.
5. Roberts SC. Complexity and context of MHC-correlated mating preferences in wild populations. Mol Ecol 2009, 18:3121-3123. 10.1111/j.1365-294X.2009.04244.x, 19682244.
6. Ekblom R, Saether SA, Jacobsson P, Fiske P, Sahlman T, Grahn M, Kalas JA, Hoglund J. Spatial pattern of MHC class II variation in the great snipe (Gallinago media). Mol Ecol 2007, 16:1439-1451. 10.1111/j.1365-294X.2007.03281.x, 17391268.
7. Westerdahl H. Passerine MHC: genetic variation and disease resistance in the wild. J Ornith 2007, 148:S469-S477.
8. Hale ML, Verduijn MH, Moller AP, Wolff K, Petrie M. Is the peacock's train an honest signal of genetic quality at the major histocompatibility complex?. J Evol Biol 2009, 22:1284-1294. 10.1111/j.1420-9101.2009.01746.x, 19453370.
9. Von Schantz T, Wittzell H, Goransson G, Grahn M. Mate choice, male condition-dependent ornamentation and MHC in the pheasant. Hereditas 1997, 127:133-140.
10. Kulski JK, Shiina T, Anzai T, Kohara S, Inoko H. Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man. Immunol Rev 2002, 190:95-122. 10.1034/j.1600-065X.2002.19008.x, 12493009.
11. Ohta Y, Goetz W, Hossain MZ, Nonaka M, Flajnik MF. Ancestral organization of the MHC revealed in the amphibian Xenopus. J Immunol 2006, 176:3674-3685.
12. Lukacs MF, Harstad H, Grimholt U, Beetz-Sargent M, Cooper GA, Reid L, Bakke HG, Phillips RB, Miller KM, Davidson WS, Koop BF. Genomic organization of duplicated major histocompatibility complex class I regions in Atlantic salmon (Salmo salar). BMC Genomics 2007, 8:16. 10.1186/1471-2164-8-251, 1781436, 17222329.
13. Brigl M, Brenner MB. CD1: Antigen presentation and T cell function. Ann Rev Immunol 2004, 22:817-890.
14. Martin LH, Calabi F, Milstein C. Isolation of CD1 genes - a family of major histocompatibility complex-related differentiation antigens. Proc Nat Acad Sci USA 1986, 83:9154-9158. 10.1073/pnas.83.23.9154, 387093, 3097645.
15. Miller MM, Wang C, Parisini E, Coletta RD, Goto RM, Lee SY, Barral DC, Townes M, Roura-Mir C, Ford HL, Brenner MB, Dascher CC. Characterization of two avian MHC-like genes reveals an ancient origin of the CD1 family. Proc Nat Acad Sci USA 2005, 102:8674-8679. 10.1073/pnas.0500105102, 1150814, 15939884.
16. Salomonsen J, Sorensen MR, Marston DA, Rogers SL, Collen T, van Hateren A, Smith AL, Beal RK, Skjodt K, Kaufman J. Two CD1 genes map to the chicken MHC, indicating that CD1 genes are ancient and likely to have been present in the primordial MHC. Proc Nat Acad Sci USA 2005, 102:8668-8673. 10.1073/pnas.0409213102, 1150808, 15939887.
17. Trowsdale J, Hanson I, Mockridge I, Beck S, Townsend A, Kelley A. Sequences encoded ni the class II region of the MHC related to the 'ABC' superfamily of transporters. Nature 1990, 348:741-744. 10.1038/348741a0, 2259383.
18. Bahram S, Arnold D, Bresnahan M, Strominger JL, Spies T. Two putative subunits of a peptide pump encoded in the human major histocompatibility complex class II region. Proc Nat Acad Sci USA 1991, 88:10094-10098. 10.1073/pnas.88.22.10094, 52874, 1946428.
19. Kaufman J, Milne S, Gobel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S. The chicken B locus is a minimal essential major histocompatibility complex. Nature 1999, 401:923-925. 10.1038/44856, 10553909.
20. Shiina T, Briles WE, Goto RM, Hosomichi K, Yanagiya K, Shimizu S, Inoko H, Miller MM. Extended gene map reveals tripartite motif, C-type lectin, and Ig superfamily type genes within a subregion of the chicken MHC-B affecting infectious disease. J Immunol 2007, 178:7162-7172.
21. Briles WE, Goto RM, Auffray C, Miller MM. A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 1993, 37:408-414. 10.1007/BF00222464, 8436415.
22. Miller MM, Golo R, Bernot A, Zoorob R, Auffray C, Bumstead N, Briles WE. 2 MHC Class-II genes map to the chicken RFP-Y system outside the B-complex. Proc Nat Acad Sci USA 1994, 91:4397-4401. 10.1073/pnas.91.10.4397, 43792, 7910407.
23. Kaufman J, Volk H, Wallny HJ. A Minimal-Essential-Mhc and an Unrecognized-Mhc - 2 Extremes in Selection for Polymorphism. Immunol Rev 1995, 143:63-88. 10.1111/j.1600-065X.1995.tb00670.x, 7558083.
24. Kaufman J. Co-evolving genes in MHC haplotypes: the "rule" for nonmammalian vertebrates?. Immunogenetics 1999, 50:228-236. 10.1007/s002510050597, 10602883.
25. Delany ME, Robinson CM, Goto RM, Miller MM. Architecture and organization of chicken microchromosome 16: order of the NOR, MHC-Y, and MHC-B subregions. J Hered 2009, 100:507-514. 10.1093/jhered/esp044, 19617522.
26. Kaufman J, Jacob J, Shaw I, Walker B, Milne S, Beck S, Salomonsen J. Gene organisation determines evolution of function in the chicken MHC. Immunol Rev 1999, 167:101-117. 10.1111/j.1600-065X.1999.tb01385.x, 10319254.
27. Jacob JP, Milne S, Beck S, Kaufman J. The major and a minor class II beta-chain (B-LB) gene flank the Tapasin gene in the B-F/B-L region of the chicken major histocompatibility complex. Immunogenetics 2000, 51:138-147. 10.1007/s002510050022, 10663576.
28. Dawkins R, Leelayuwat C, Gauderi S, Tay G, Hui J, Cattley S, Martinez P, Kulski J. Genomics of the major histocompatibility complex: haplotypes, duplication, retroviruses and disease. Immunol Rev 1999, 167:275-304. 10.1111/j.1600-065X.1999.tb01399.x, 10319268.
29. Cole RK. Studies on the genetic resistance to Marek's disease. Avian Diseases 1968, 12:9-28. 10.2307/1588081, 5643702.
30. Plachy J, Pink JRL, Hala K. Biology of the chicken MHC (B complex). Crit Rev Immunol 1992, 12:47-49.
31. Gregory TR. A bird's-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class aves. Evolution 2002, 56:121-130.
32. Organ CL, Shedlock AM, Meade A, Pagel M, Edwards SV. Origin of avian genome size and structure in non-avian dinosaurs. Nature 2007, 446:180-184. 10.1038/nature05621, 17344851.
33. Brown JW, Rest JS, Garcia-Moreno J, Sorenson MD, Mindell DP. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biology 2008, 6:6. 2267772, 18226223.
34. Shiina T, Shimizu S, Hosomichi K, Kohara S, Watanabe S, Hanzawa K, Beck S, Kulski JK, Inoko H. Comparative genomic analysis of two avian (quail and chicken) MHC regions. J Immunol 2004, 172:6751-6763.
35. Hosomichi K, Shiina T, Suzuki S, Tanaka M, Shimizu S, Iwamoto S, Hara H, Yoshida Y, Kulski JK, Inoko H, Hanzawa K. The major histocompatibility complex (Mhc) class IIB region has greater genomic structural flexibility and diversity in the quail than the chicken. BMC Genomics 2006, 7. 10.1186/1471-2164-7-322, 1769493, 17184537.
36. Chaves LD, Krueth SB, Reed KM. Defining the Turkey MHC: Sequence and Genes of the B Locus. J Immunol 2009, 183:6530-6537. 10.4049/jimmunol.0901310, 19864609.
37. Chaves LD, Krueth SB, Reed KM. Characterization of the Turkey MHC chromosome through genetic and physical mapping. Cytogenet Gen Res 2007, 117:213-220.
38. Edwards SV, Wakeland EK, Potts WK. Contrasting histories of avian and mammalian Mhc genes revealed by class II B sequences from songbirds. Proc Nat Acad Sci USA 1995, 92:12200-12204. 10.1073/pnas.92.26.12200, 40324, 8618869.
39. Wittzell H, Madsen T, Westerdahl H, Shine R, von Schantz T. MHC variation in birds and reptiles. Genetica 1998, 104:301-309. 10.1023/A:1026421607089, 10386396.
40. Westerdahl H, Wittzell H, von Schantz T. Mhc diversity in two passerine birds: no evidence far a minimal essential Mhc. Immunogenetics 2000, 52:92-100. 10.1007/s002510000256, 11132162.
41. Hess CM, Gasper J, Hoekstra HE, Hill CE, Edwards SV. MHC class II pseudogene and genomic signature of a 32-kb cosmid in the house finch (Carpodacus mexicanus). Genome Research 2000, 10:613-623. 10.1101/gr.10.5.613, 310861, 10810083.
42. Edwards SV, Gasper J, March M. Genomics and polymorphism of Agph-DAB1, an Mhc class II B gene in red-winged blackbirds (Agelaius phoeniceus). Mol Biol Evol 1998, 15:236-250.
43. Edwards SV, Gasper J, Garrigan D, Martindale D, Koop BF. A 39-kb sequence around a blackbird Mhc class II gene: Ghost of selection past and songbird genome architecture. Mol Biol Evol 2000, 17:1384-1395.
44. Westerdahl H, Wittzell H, von Schantz T. Polymorphism and transcription of Mhc class I genes in a passerine bird, the great reed warbler. Immunogenetics 1999, 49:158-170. 10.1007/s002510050477, 9914330.
45. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunster A, Searle S, White S, Vilella AJ, Fairly S, Heger A, Kong L, Ponting CP, Jarvis ED, Mello CV, Minx P, Lovell P, Velho TAF, Ferris M, Balakrishnan CN, Sinha S, Blatti C, London SE, Li Y, Lin Y, George J, Sweedler J, Southey B, Gunaratne P, Watson M, Nam K, Backstrom N, Smeds L, Nabholz B, Itoh Y, Whitney O, Pfenning AR, Howard J, Volker M, Skinner BM, Griffin DK, Ye L, McLaren WM, Flicek P, Quesada V, Velasco G, Lopez-Otin C, Puente XS, Olender T, Lancet D, Smit AFA, Hubley R, Konkel MK, Walker JA, Batzer MA, Gu W, Pollock DD, Chen L, Cheng Z, Eichler EE, Stapley J, Slate J, Ekblom R, Birkhead T, Burke T, Burt D, Scharff C, Adam I, Hughes R, Sultan M, Soldatov A, Lehrach H, Edwards SV, Yang S, Li X, Graves T, Fulton L, Nelson J, Chinwalla A, Hou S, Mardis ER, Wilson RK. The genome of a songbird. Nature
46. Ekblom R, Balakrishnan CN, Burke T, Slate J. Digital gene expression analysis of the zebra finch genome. BMCGenomics
47. Ovcharenko I, Loots GG, Hardison RC, Miller W, Stubbs L. zPicture: Dynamic alignment and visualization tool for analyzing conservation profiles. Genome Res 2004, 14:472-477. 10.1101/gr.2129504, 353235, 14993211.
48. Gasper JS, Shiina T, Inoko H, Edwards SV. Songbird genomics: Analysis of 45 kb upstream of a polymorphic Mhc class II gene in red-winged blackbirds (Agelaius phoeniceus). Genomics 2001, 75:26-34. 10.1006/geno.2001.6596, 11472064.
49. Yang ZH. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591. 10.1093/molbev/msm088, 17483113.
50. Yang ZH. PAML: a program package for phylogenetic analysis by maximum likelihood. Comp App Biosci 1997, 13:555-556.
51. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, Strominger JL, Wiley DC. 3-Dimensional structure of the human class-II histocompatibility antigen HLA-DR1. Nature 1993, 364:33-39. 10.1038/364033a0, 8316295.
52. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 1987, 329:593-602.
53. Alcaide M, Edwards SV, Cadahia L, Negro JJ. MHC class I genes of bird of prey: isolation, polymorphism, and diversifying selection. Cons Genet
54. Alcaide M, Edwards SV, Negro JJ. Characterization, polymorphism, and evolution of MHC class IIB genes in birds of prey. J Mol Evol 2007, 65:541-554. 10.1007/s00239-007-9033-9, 17925996.
55. Deakin JE, Siddle HV, Cross JG, Belov K, Graves JA. Class I genes have split from the MHC in the tammar wallaby. Cytogenet Genome Res 2007, 116:205-211. 10.1159/000098188, 17317961.
56. Siddle HV, Deakin JE, Coggill P, Hart E, Cheng YY, Wong ESW, Harrow J, Beck S, Belov K. MHC-linked and un-linked class I genes in the wallaby. BMC Genomics 2009, 10:310. 10.1186/1471-2164-10-310, 2719672, 19602235.
57. Kaufman J. The simple chicken major histocompatibility complex: life and death in the face of pathogens and vaccines. Phil Trans Roy Soc Lond B 2000, 355:1077-1084.
58. Aguilar A, Smith TB, Wayne RK. A comparison of variation between a MHC pseudogene and microsatellite loci of the little greenbul (Andropadus virens). BMC Evol Biol 2005, 5:47. 10.1186/1471-2148-5-47, 1249561, 16159389.
59. Miller HC, Lambert DM. Gene duplication and gene conversion in class II MHC genes of New Zealand robins (Petroicidae). Immunogenetics 2004, 56:178-191.
60. Burri R, Niculita-Hirzel H, Roulin A, Fumagalli L. Isolation and characterization of major histocompatibility complex (MHC) class IIB genes in the barn owl (Aves: Tyto alba). Immunogenetics 2008, 60:543-550. 10.1007/s00251-008-0308-0, 18548243.
61. Hosomichi K, Miller MM, Goto RM, Wang YJ, Suzuki S, Kulski JK, Nishibori M, Inoko H, Hanzawa K, Shiina T. Contribution of mutation, recombination, and gene conversion to chicken Mhc-B haplotype diversity. J Immunol 2008, 181:3393-3399. 2657362, 18714011.
62. Hughes CR, Miles S, Walbroehl JM. Support for the minimal essential MHC hypothesis: a parrot with a single, highly polymorphic MHC class IIB gene. Immunogenetics 2008, 60:219-231. 10.1007/s00251-008-0287-1, 18431567.
63. Ekblom R, Grahn M, Hoglund J. Patterns of polymorphism in the MHC class II of a non-passerine bird, the great snipe (Gallinago media). Immunogenetics 2003, 54:734-741.
64. Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T. A phylogenomic study of birds reveals their evolutionary history. Science 2008, 320:1763-1768. 10.1126/science.1157704, 18583609.
65. Moon DA, Veniamin SM, Parks-Dely JA, Magor KE. The MHC of the duck (Anas platyrhynchos) contains five differentially expressed class I genes. J Immunol 2005, 175:6702-6712.
66. Eddy S. Profile hidden Markov models. Bioinformatics 1998, 14:755-763. 10.1093/bioinformatics/14.9.755, 9918945.
67. Birney E, Clamp M, Durbin R. GeneWise and genomewise. Genome Res 2004, 14:988-995. 10.1101/gr.1865504, 479130, 15123596.
68. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL-W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nuc Acid Res 1994, 22:4673-4680.
69. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acid Symp Ser 1999, 95-98.
70. Birney E, Clamp M, Kraspcyk A, Slater G, Hubbard T, Curwen V, Stabenau A, Stupka E, Huminiecki L, Potter S. Ensembl: A multi-genome computational platform. Am J Hum Genet 2001, 69:219.
71. Edwards SV, Grahn M, Potts WK. Dynamics of Mhc evolution in birds and crocodilians: amplification of class II genes with degenerate primers. Mol Ecol 1995, 4:719-729. 10.1111/j.1365-294X.1995.tb00272.x, 8564010.
72. Shedlock AM, Janes DE, Edwards SV. Amniote phylogenomics: testing evolutionary hypotheses with BAC library scanning and targeted clone analysis of large-scale DNA sequences from reptiles. Phylogenomics 2008, Totowa, NJ: Humana Press, Murphy W.
73. Ross MT, LaBrie S, McPherson J, Stanton VP. Current Protocols in Human Genetics 1999, 561-565. New York: Wiley, Dracopoli NC.
74. de la Blastide M, McCombie WR. Assembling genomic DNA sequences with PHRAP. Current Protocols in Bioinformatics 2007, (Supp. 17). Unit 11.4..
75. Salomov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Gen Res 2000, 11:817-832.
76. Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol 1997, 268:78-94. 10.1006/jmbi.1997.0951, 9149143.
77. Smit AFA, Hubley R, Green P. RepeatMasker Open 3.0. 1996, , http://www.repeatmasker.org
78. Itoh Y, Arnold AP. Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 2005, 13:47-56. 10.1007/s10577-005-6602-x, 15791411.
79. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA, Khodiyar VK, Lush MJ, Povey S, Talbot CC, Wright MW, Wain HM, Trowsdale J, Ziegler A, Beck S. Gene map of the extended human MHC. Nat Rev Genet 2004, 5:889-899. 10.1038/nrg1489, 15573121.
80. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc Acid Res 2004, 32:1792-1797.
81. Rambaut A. Se-Al: Sequence Alignment Editor. 1996, , http://evolve.zoo.ac.uk
82. Huelsenbeck JP, Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754, 11524383.
83. Yang ZH, Wong WSW, Nielsen R. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005, 22:1107-1118. 10.1093/molbev/msi097, 15689528.