Sequence of a Complete Chicken BG Haplotype Shows Dynamic Expansion and Contraction of Two Gene Lineages with Particular Expression Patterns

1. DoxiadisGGM, OttingN, de GrootNG, NoortR, BontropRE (2000) Unprecedented polymorphism of Mhc-DRB region configurations in rhesus macaques. J Immunol 164: 3193–3199.

2. DoxiadisGGM, de GrootN, OttingN, BlokhuisJH, BontropRE (2011) Genomic plasticity of the MHC class I A region in rhesus macaques: extensive haplotype diversity at the population level as revealed by microsatellites. Immunogenetics 63: 73–83.

3. JiangW, JohnsonC, JayaramanJ, SimecekN, NobleJ, et al. (2012) Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res 22: 1845–1854.

4. LanierLL (2005) NK cell recognition. Annu Rev Immunol 23: 225–274.

5. SturtevantAH (1925) The effects of unequal crossing over at the bar locus in Drosophila. Genetics 10: 117–147.

6. HaldaneJBS (1933) The part played by recurrent mutation in evolution. Am Nat 67: 5–19.

7. MüllerHJ (1935) The origination of chromatin deficiencies as minute deletions subject to insertion elsewhere. Genetica 17: 237–252.

8. Huxley J (1942) Evolution: the modern synthesis. London: Allen and Unwin.

9. WalshJB (1987) Persistence of tandem arrays: implications for satellite and simple-sequence DNAs. Genetics 115: 553–567.

10. OtaT, NeiM (1994) Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol Biol Evol 11: 469–482.

11. NeiM, GuX, SitnikovaT (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S A 94: 7799–7806.

12. FreemanJL, PerryGH, FeukL, RedonR, McCarrollSA, et al. (2006) Copy number variation: new insights in genome diversity. Genome Res 16: 949–961.

13. ForceA, LynchM, PickettFB, AmoresA, YanYL, PostlethwaitJ (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545.

14. LynchM, ConeryJS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155.

15. LynchM, O'HelyM, WalshB, ForceA (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159: 1789–1804.

16. RooneyAP, PiontkivskaH, NeiM (2002) Molecular evolution of the nontandemly repeated genes of the histone 3 multigene family. Mol Biol Evol 19: 68–75.

17. NeiM, RooneyAP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121–152.

18. FreemanJL, PerryGH, FeukL, RedonR, McCarrollSA, et al. (2006) Copy number variation: new insights in genome diversity. Genome Res 16: 949–961.

19. HughesT, LiberlesDA (2007) The pattern of evolution of smaller-scale gene duplicates in mammalian genomes is more consistent with neo- than subfunctionalisation. J Mol Evol 65: 574–588.

20. TraherneJA, MartinM, WardR, OhashiM, PellettF, et al. (2010) Mechanisms of copy number variation and hybrid gene formation in the KIR immune gene complex. Hum Mol Genet 19: 737–751.

21. Eirín-LópezJM, RebordinosL, RooneyAP, RozasJ (2012) The birth-and-death evolution of multigene families revisited. Genome Dyn 7: 170–196.

22. KatjuV, BergthorssonU (2013) Copy-number changes in evolution: rates, fitness effects and adaptive significance. Front Genet 4: 273.

23. HenryJ, MillerMM, PontarottiP (1999) Structure and evolution of the extended B7 family. Immunol Today 20: 285–288.

24. AfracheH, GouretP, AinoucheS, PontarottiP, OliveD (2012) The butyrophilin (BTN) gene family: from milk fat to the regulation of the immune response. Immunogenetics 64: 781–794.

25. Abeler-DörnerL, SwamyM, WilliamsG, HaydayAC, BasA (2012) Butyrophilins: an emerging family of immune regulators. Trends Immunol 33: 34–41.

26. ArnettHA, EscobarSS, VineyJL (2009) Regulation of costimulation in the era of butyrophilins. Cytokine 46: 370–375.

27. NguyenT, LiuXK, ZhangY, DongC (2006) BTNL2, a butyrophilin-like molecule that functions to inhibit T cell activation. J Immunol 176: 7354–7360.

28. ArnettHA, EscobarSS, Gonzalez-SuarezE, BudelskyAL, SteffenLA, et al. (2007) BTNL2, a butyrophilin/B7-like molecule, is a negative costimulatory molecule modulated in intestinal inflammation. J Immunol 178: 1523–1533.

29. SmithIA, KnezevicBR, AmmannJU, RhodesDA, AwD, et al. (2010) BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T cell activation. J Immunol 184: 3514–3525.

30. YamazakiT, GoyaI, GrafD, CraigS, Martin-OrozcoN, et al. (2010) A butyrophilin family member critically inhibits T cell activation. J Immunol 185: 5907–5914.

31. BasA, SwamyM, Abeler-DörnerL, WilliamsG, PangDJ, et al. (2011) Butyrophilin-like 1 encodes an enterocyte protein that selectively regulates functional interactions with T lymphocytes. Proc Natl Acad Sci U S A 108: 4376–4381.

32. HarlyC, GuillaumeY, NedellecS, PeignéC-M, MönkkönenH, et al. (2012) Key implication of CD277/butyrophilin-3 (BTN3A) in cellular stress sensing by a major human γδ T-cell subset. Blood 120: 2269–2279.

33. PalakodetiA, SandstromA, SundaresanL, HarlyC, NedellecS, et al. (2012) The molecular basis for modulation of human Vγ9Vδ2 T cell responses by CD277/butyrophilin-3 (BTN3A)-specific antibodies. J Biol Chem 287: 32780–32790.

34. VavassoriS, KumarA, WanGS, RamanjaneyuluGS, CavallariM, et al. (2013) Butyrophilin 3A1 binds phosphorylated antigens and stimulates human γδ T cells. Nat Immunol 14: 908–916.

35. ValentonyteR, HampeJ, HuseK, RosenstielP, AlbrechtM, et al. (2005) Sarcoidosis is associated with a truncating splice site mutation in BTNL2. Nat Genet 37: 357–364.

36. SzyldP, JagielloP, CsernokE, GrossWL, EpplenJT (2006) On the Wegener granulomatosis associated region on chromosome 6p21.3. BMC medical genetics 7: 21.

37. SpagnoloP, SatoH, GruttersJC, RenzoniEA, MarshallSE, et al. (2007) Analysis of BTNL2 genetic polymorphisms in British and Dutch patients with sarcoidosis. Tissue Antigens 70: 219–227.

38. SatoH, SpagnoloP, SilveiraL, WelshKI, du BoisRM, et al. (2007) BTNL2 allele associations with chronic beryllium disease in HLA-DPB1*Glu69-negative individuals. Tissue Antigens 70: 480–486.

39. KonnoS, TakahashiD, HizawaN, HattoriT, TakahashiA, et al. (2009) Genetic impact of a butyrophilin-like 2 (BTNL2) gene variation on specific IgE responsiveness to Dermatophagoides farinae (Der f) in Japanese. Allergol Int 58: 29–35.

40. VikenMK, BlomhoffA, OlssonM, AkselsenHE, PociotF, et al. (2009) Reproducible association with type 1 diabetes in the extended class I region of the major histocompatibility complex. Genes Immun 10: 323–333.

41. PathanS, GowdyRE, CooneyR, BecklyJB, HancockL, et al. (2009) Confirmation of the novel association at the BTNL2 locus with ulcerative colitis. Tissue Antigens 74: 322–329.

42. HsuehK-C, LinY-J, ChangJ-S, WanL, TsaiF-J (2010) BTNL2 gene polymorphisms may be associated with susceptibility to Kawasaki disease and formation of coronary artery lesions in Taiwanese children. Eur J Pediatr 169: 713–719.

43. LianY, YueJ, HanM, LiuJ, LiuL (2010) Analysis of the association between BTNL2 polymorphism and tuberculosis in Chinese Han population. Infect Genet Evol 10: 517–521.

44. YamadaY, NishidaT, IchiharaS, SawabeM, FukuN, et al. (2011) Association of a polymorphism of BTN2A1 with myocardial infarction in East Asian populations. Atherosclerosis 215: 145–152.

45. OrozcoG, BartonA, EyreS, DingB, WorthingtonJ, et al. (2011) HLA-DPB1-COL11A2 and three additional xMHC loci are independently associated with RA in a UK cohort. Genes Immun 12: 169–175.

46. HoribeH, KatoK, OguriM, YoshidaT, FujimakiT, et al. (2011) Association of a polymorphism of BTN2A1 with hypertension in Japanese individuals. Am J Hypertens 24: 924–929.

47. YoshidaT, KatoK, HoribeH, OguriM, FukudaM, et al. (2011) Association of a genetic variant of BTN2A1 with chronic kidney disease in Japanese individuals. Nephrology 16: 642–648.

48. HiramatsuM, OguriM, KatoK, YoshidaT, FujimakiT, et al. (2011) Association of a polymorphism of BTN2A1 with type 2 diabetes mellitus in Japanese individuals. Diabet Med 28: 1381–1387.

49. OguriM, KatoK, YoshidaT, FujimakiT, HoribeH, et al. (2011) Association of a genetic variant of BTN2A1 with metabolic syndrome in East Asian populations. J Med Genet 48: 787–792.

50. HeidHW, WinterS, BruderG, KeenanTW, JaraschED (1983) Butyrophilin, an apical plasma membrane-associated glycoprotein characteristic of lactating mammary glands of diverse species. Biochim Biophys Acta 728: 228–238.

51. StammersM, RowenL, RhodesD, TrowsdaleJ, BeckS (2000) BTL-II: a polymorphic locus with homology to the butyrophilin gene family, located at the border of the major histocompatibility complex class II and class III regions in human and mouse. Immunogenetics 51: 373–382.

52. RhodesDA, StammersM, MalcherekG, BeckS, TrowsdaleJ (2001) The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71: 351–362.

53. BoydenLM, LewisJM, BarbeeSD, BasA, GirardiM, et al. (2008) Skint1, the prototype of a newly identified immunoglobulin superfamily gene cluster, positively selects epidermal gammadelta T cells. Nat Genet 40: 656–662.

54. BarbeeSD, WoodwardMJ, TurchinovichG, MentionJJ, LewisJM, et al. (2011) Skint-1 is a highly specific, unique selecting component for epidermal T cells. Proc Natl Acad Sci U S A 108: 3330–3335.

55. TurchinovichG, HaydayAC (2011) Skint-1 identifies a common molecular mechanism for the development of interferon-γ-secreting versus interleukin-17-secreting γδ T cells. Immunity 35: 59–68.

56. BrilesWE, McGibbonWH, IrwinMR (1950) On multiple alleles effecting cellular antigens in the chicken. Genetics 35: 633–652.

57. SchiermanLW, NordskogAW (1961) Relationship of blood type to histocompatibility in chickens. Science 134: 1008–1009.

58. VilhelmováM, MiggianoVC, PinkJR, HálaK, HartmanováJ (1977) Analysis of the alloimmune properties of a recombinant genotype in the major histocompatibility complex of the chicken. Eur J Immunol 7: 674–679.

59. KaufmanJ, SkjødtK, SalomonsenJ (1991) The B-G multigene family of the chicken major histocompatibility complex. Crit Rev Immunol 11: 113–143.

60. SalomonsenJ, SkjødtK, CroneM, SimonsenM (1987) The chicken erythrocyte-specific MHC antigen. Characterization and purification of the B-G antigen by monoclonal antibodies. Immunogenetics 25: 373–382.

61. GotoR, MiyadaCG, YoungS, WallaceRB, AbplanalpH, et al. (1988) Isolation of a cDNA clone from the B-G subregion of the chicken histocompatibility (B) complex. Immunogenetics 27: 102–109.

62. MillerMM, AbplanalpH, GotoR (1988) Genotyping chickens for the B-G subregion of the major histocompatibility complex using restriction fragment length polymorphisms. Immunogenetics 28: 374–379.

63. MillerMM, GotoR, YoungS, LiuJ, HardyJ (1990) Antigens similar to major histocompatibility complex B-G are expressed in the intestinal epithelium in the chicken. Immunogenetics 32: 45–50.

64. KaufmanJ, SalomonsenJ, SkjødtK, ThorpeD (1990) Size polymorphism of chicken major histocompatibility complex-encoded B-G molecules is due to length variation in the cytoplasmic heptad repeat region. Proc Natl Acad Sci U S A 87: 8277–8281.

65. SalomonsenJ, DunonD, SkjødtK, ThorpeD, VainioO, et al. (1991) Chicken major histocompatibility complex-encoded B-G antigens are found on many cell types that are important for the immune system. Proc Natl Acad Sci U S A 88: 1359–1363.

66. SalomonsenJ, ErikssonH, SkjødtK, LundgreenT, SimonsenM, et al. (1991) The “adjuvant effect” of the polymorphic B-G antigens of the chicken major histocompatibility complex analyzed using purified molecules incorporated in liposomes. Eur J Immunol 21: 649–658.

67. Miller MM (1991) The Major Histocompatibility Complex of the Chicken. Phylogenesis of Immune Functions. Boca Raton FL: CRC Press. pp. 151–169.

68. Döhring C, Riegert P, Salomonsen J, Skjødt K, Kaufman J (1993) The extracellular Ig V-like regions of the polymorphic B-G antigens of the chicken Mhc lack structural features expected for antibody variable regions. Avian Immunology in Progress: Institut National de la Recherche Agronomique. pp. 145–152.

69. EllederD, StepanetsV, MelderDC, SeniglF, GerykJ, et al. (2005) The receptor for the subgroup C avian sarcoma and leukosis viruses, Tvc, is related to mammalian butyrophilins, members of the immunoglobulin superfamily. J Virol 79: 10408–10419.

70. BikleDD, MunsonS, KomuvesL (1996) Zipper protein, a B-G protein with the ability to regulate actin/myosin 1 interactions in the intestinal brush border. J Biol Chem 271: 9075–9083.

71. GotoRM, WangY, TaylorRL, WakenellPS, HosomichiK, et al. (2009) BG1 has a major role in MHC-linked resistance to malignant lymphoma in the chicken. Proc Natl Acad Sci U S A 106: 16740–16745.

72. GuillemotF, BillaultA, PourquiéO, BéharG, ChausséAM, et al. (1988) A molecular map of the chicken major histocompatibility complex: the class II beta genes are closely linked to the class I genes and the nucleolar organizer. The EMBO journal 7: 2775–2785.

73. KaufmanJ, MilneS, GöbelTW, WalkerBA, JacobJP, et al. (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401: 923–925.

74. MillerMM, GotoR, BernotA, ZoorobR, AuffrayC, BumsteadN, BrilesWE (1994) Two Mhc class I and two Mhc class II genes map to the chicken Rfp-Y system outside the B complex. Proc Natl Acad Sci USA 91: 4397–4401.

75. RubyT, Bed'HomB, WittzellH, MorinV, OudinA, et al. (2005) Characterisation of a cluster of TRIM-B30.2 genes in the chicken MHC B locus. Immunogenetics 57: 116–128.

76. WallnyH-J, AvilaD, HuntLG, PowellTJ, RiegertP, et al. (2006) Peptide motifs of the single dominantly expressed class I molecule explain the striking MHC-determined response to Rous sarcoma virus in chickens. Proc Natl Acad Sci U S A 103: 1434–1439.

77. ShawI, PowellTJ, MarstonDA, BakerK, van HaterenA, et al. (2007) Different evolutionary histories of the two classical class I genes BF1 and BF2 illustrate drift and selection within the stable MHC haplotypes of chickens. J Immunol 178: 5744–5752.

78. KaufmanJ, SalomonsenJ, SkjødtK (1989) B-G cDNA clones have multiple small repeats and hybridize to both chicken MHC regions. Immunogenetics 30: 440–451.

79. International Chicken Genome SequencingConsortium (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716.

80. MillerMM, GotoR, AbplanalpH (1984) Analysis of the B-G antigens of the chicken MHC by two-dimensional gel electrophoresis. Immunogenetics 20: 373–385.

81. ShiinaT, BrilesWE, GotoRM, HosomichiK, YanagiyaK, et al. (2007) 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 178: 7162–7172.

82. MillerMM, GotoR, YoungS, ChirivellaJ, HawkeD, et al. (1991) Immunoglobulin variable-region-like domains of diverse sequence within the major histocompatibility complex of the chicken. Proc Natl Acad Sci U S A 88: 4377–4381.

83. HosomichiK, MillerMM, GotoRM, WangY, SuzukiS, et al. (2008) Contribution of mutation, recombination, and gene conversion to chicken MHC-B haplotype diversity. J Immunol 181: 3393–3399.

84. ShiinaT, OtaM, ShimizuS, KatsuyamaY, HashimotoN, et al. (2006) Rapid evolution of majorhistocompatibility complex class I genes in primates generates new disease alleles in humans via hitchhiking diversity. Genetics 173: 1555–1570.

85. van Oosterhout (2009) A new theory of MHC evolution: beyond selection on the immune genes.Proc Biol Sci. 276: 657–665.

86. AmadouC (1999) Evolution of the Mhc class I region: the framework hypothesis. Immunogenetics 49: 362–367.

87. MillerMM, GotoR, BrilesWE (1988) Biochemical confirmation of recombination within the B-G subregion of the chicken major histocompatibility complex. Immunogenetics 27: 127–132.

88. WilsonMJ, TorkarM, HaudeA, MilneS, JonesT, et al. (2000) Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci U S A 97: 4778–4783.

89. CanavezF, YoungNT, GuethleinLA, RajalingamR, KhakooSI, et al. (2001) Comparison of chimpanzee and human leukocyte Ig-like receptor genes reveals framework and rapidly evolving genes. J Immunol 167: 5786–5794.

90. Abi-RachedL, ParhamP (2005) Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J Exp Med 201: 1319–1332.

91. Maniatis T, Fritsch E, Sambrook J (1982) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.

92. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: Vol-3: A Laboratory Manual: Appendixes: CSH Laboratory Press.

93. RiegertP, AndersenR, BumsteadN, DöhringC, Dominguez-SteglichM, et al. (1996) The chicken beta 2-microglobulin gene is located on a non-major histocompatibility complex microchromosome: a small, G+C-rich gene with X and Y boxes in the promoter. Proc Natl Acad Sci U S A 93: 1243–1248.

94. SalomonsenJ, MarstonD, AvilaD, BumsteadN, JohanssonB, et al. (2003) The properties of the single chicken MHC classical class II alpha chain (B-LA) gene indicate an ancient origin for the DR/E-like isotype of class II molecules. Immunogenetics 55: 605–614.

95. PeckR, MurthyKK, VainioO (1982) Expression of B-L (Ia-like) antigens on macrophages from chicken lymphoid organs. J Immunol 129: 4–5.

96. MastJ, GoddeerisBM, PeetersK, VandesandeF, BerghmanLR (1998) Characterisation of chicken monocytes, macrophages and interdigitating cells by the monoclonal antibody KUL01. Vet Immunol Immunopathol 61: 343–357.

97. WeiningKC, SchultzU, MünsterU, KaspersB, StaeheliP (1996) Biological properties of recombinant chicken interferon-gamma. Eur J Immunol 26: 2440–2447.

98. DingM, ZhangM, WongJL, RogersNE, IgnarroLJ, et al. (1998) Antisense knockdown of inducible nitric oxide synthase inhibits induction of experimental autoimmune encephalomyelitis in SJL/J mice. J Immunol 160: 2560–2564.

99. WuZ, RothwellL, YoungJR, KaufmanJ, ButterC, et al. (2010) Generation and characterization of chicken bone marrow-derived dendritic cells. Immunology 129: 133–145.

100. GoodmanT, LefrançoisL (1988) Expression of the gamma-delta T-cell receptor on intestinal CD8+ intraepithelial lymphocytes. Nature 333: 855–858.

101. SalomonsenJ, SørensenMR, MarstonDA, RogersSL, CollenT, et al. (2005) 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 Natl Acad Sci U S A 102: 8668–8673.

102. LinnaTJ, FrommelD, GoodRA (1972) Effects of early cyclophosphamide treatment on the development of lymphoid organs and immunological functions in the chickens. Int Arch Allergy Appl Immunol 42: 20–39.

103. KaufmanJ, AndersenR, AvilaD, EngbergJ, LambrisJ, et al. (1992) Different features of the MHC class I heterodimer have evolved at different rates. Chicken B-F and beta 2-microglobulin sequences reveal invariant surface residues. J Immunol 148: 1532–1546.

104. RonquistF, HuelsenbeckJP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.

105. Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

106. ShimodairaH, HasegawaM (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246–1247.

107. HusonDH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14: 68–73.

108. HusonDH, BryantD (2006) Application of Phylogenetic Networks in Evolutionary Studies. Mol Biol Evol 23: 254–267.

109. BruenT, PhillipeH, BryantD (2006) A quick and robust statistical test to detect the presence of recombination. Genetics 172: 2665–2681.

110. CastresanaJ (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molec Biol Evol 17: 540–552.

111. TalaveraG, CastresanaJ (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systemat Biol 56: 564–577.

112. ZamaniN, RussellP, LantzH, HoeppnerMP, MeadowsJRS, et al. (2013) Unsupervised genome-wide recognition of local relationship patterns. BMC genomics 14: 347.

113. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

114. MarmorMD, BenatarT, RatcliffeMJ (1993) Retroviral transformation in vitro of chicken T cells expressing either alpha/beta or gamma/delta T cell receptors by reticuloendotheliosis virus strain T. J Exp Med 177: 647–656.

115. MaccubbinD, SchiermanL (1986) MHC-restricted cytotoxic response of chicken T cells: expression, augmentation, and clonal characterization. J Immunol 136: 12–16.

116. Walker BA, Hunt LG, Sowa AK, Skjødt K, Göbel TW, et al The dominantly expressed class I molecule of the chicken MHC is explained by coevolution with the polymorphic peptide transporter (TAP) genes. Proc Natl Acad Sci U S A 108: 8396–8401.

117. KorbelJO, UrbanAE, AffourtitJP, GodwinB, GrubertF, et al. (2007) Paired-End Mapping Reveals Extensive Structural Variation in the Human Genome. Science 318: 420–426.

118. PerryGH, YangF, Marques-BonetT, MurphyC, FitzgeraldT, et al. (2008) Copy number variation and evolution in humans and chimpanzees. Genome Res 18: 1698–1710.

119. YangF, MüllerS, JustR, Ferguson-SmithMA, WienbergJ (1997) Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39: 396–401.