Natural selection on marine carnivores elaborated a diverse family of classical MHC class I genes exhibiting haplotypic gene content variation and allelic polymorphism

Immunogenetics

Volumn 64, Issue 12, 2012, Pages 915-933

  Hammond, John A ^a,b   Guethlein, Lisbeth A ^a   Norman, Paul J ^a   Parham, Peter ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

Evolution; MHC class I; Pinniped; Polymorphism

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ALLELE; ANIMAL TISSUE; ARTICLE; CARNIVORE; DNA POLYMORPHISM; GENE SEQUENCE; GENETIC VARIABILITY; HAPLOTYPE; MARINE MAMMAL; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANDALIDAE; PRIORITY JOURNAL; PSEUDOGENE; SEAL; SPECIES; TERRESTRIAL SPECIES;

ANIMALS; BASE SEQUENCE; DOGS; FEMALE; GENES, MHC CLASS I; HAPLOTYPES; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; SEALS, EARLESS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; URSIDAE;

AILUROPODA MELANOLEUCA; CANIS FAMILIARIS; HALICHOERUS; PHOCA; PINNIPEDIA;

EID: 84872055583     PISSN: 00937711     EISSN: 14321211     Source Type: Journal    
DOI: 10.1007/s00251-012-0651-z     Document Type: Article

References (82)

1. Adams EJ, Parham P (2001) Species-specific evolution of MHC class I genes in the higher primates. Immunol Rev 183:41-64 (Pubitemid 34015437)
2. Aldridge BM, Bowen L, Smith BR, Antonelis GA, Gulland F, Stott JL (2006) Paucity of class I MHC gene heterogeneity between individuals in the endangered Hawaiian monk seal population. Immunogenetics 58:203-215
3. Arnason A, Gullberg A, Janke A, Kullberg M, Lehman N, Petrov EA, Vainola R (2006) Pinniped phylogeny and a new hypothesis for their origin and dispersal. Mol Phylogenet Evol 46:345-354 (Pubitemid 44462747)
4. Ballingall KT, Miltiadou D, Chai ZW, McLean K, Rocchi M, Yaga R, McKeever DJ (2008) Genetic and proteomic analysis of the MHC class I repertoire from four ovine haplotypes. Immunogenetics 60:177-184
5. Bashirova AA, Thomas R, Carrington M (2011) HLA/KIR restraint of HIV: surviving the fittest. Annu Rev Immunol 29:295-317
6. Beck TW, Menninger J, Murphy WJ, Nash WG, O'Brien SJ, Yuhki N (2005) The feline major histocompatibility complex is rearranged by an inversion with a breakpoint in the distal class I region. Immunogenetics 56:702-709 (Pubitemid 40174965)
7. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC (1987) Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329:506-512 (Pubitemid 17131093)
8. Bowen L, Aldridge BM, Gulland F, Woo J, Van Bonn W, DeLong R, Stott JL, Johnson ML (2002) Molecular characterization of expressed DQA and DQB genes in the California sea lion (Zalophus californianus). Immunogenetics 54:332-347 (Pubitemid 34983951)
9. Bowen L, Aldridge BM, Gulland F, Van Bonn W, DeLong R, Melin S, Lowenstine LJ, Stott JL, Johnson ML (2004) Class II multiformity generated by variable MHC-DRB region configurations in the California sea lion (Zalophus californianus). Immunogenetics 56:12-27 (Pubitemid 38626418)
10. Bowen L, Aldridge BM, Delong R, Melin S, Godinez C, Zavala A, Gulland F, Lowenstine L, Stott JL, Johnson ML (2006) MHC gene configuration variation in geographically disparate populations of California sea lions (Zalophus californianus). Mol Ecol 15:529-533
11. Boyington JC, Sun PD (2002) A structural perspective on MHC class I recognition by killer cell immunoglobulin-like receptors. Mol Immunol 38:1007-1021 (Pubitemid 34310440)
12. Boyington JC, Motyka SA, Schuck P, Brooks AG, Sun PD (2000) Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405:537-543 (Pubitemid 30367719)
13. Boyson JE, Shufflebotham C, Cadavid LF, Urvater JA, Knapp LA, Hughes AL, Watkins DI (1996) The MHC class I genes of the rhesus monkey. Different evolutionary histories of MHC class I and II genes in primates. J Immunol 156:4656-4665 (Pubitemid 26174447)
14. Breen M, Thomas R, Binns MM, Carter NP, Langford CF (1999) Reciprocal chromosome painting reveals detailed regions of conserved synteny between the karyotypes of the domestic dog (Canis familiaris) and human. Genomics 61:145-155 (Pubitemid 29514138)
15. Burnett RC, Geraghty DE (1995) Structure and expression of a divergent canine class I gene. J Immunol 155:4278-4285
16. Burnett RC, DeRose SA, Wagner JL, Storb R (1997) Molecular analysis of six dog leukocyte antigen class I sequences including three complete genes, two truncated genes and one full-length processed gene. Tissue Antigens 49:484-495 (Pubitemid 27207754)
17. Cammen K, Hoffman JI, Knapp LA, Harwood J, Amos W (2011) Geographic variation of the major histocompatibility complex in Eastern Atlantic grey seals (Halichoerus grypus). Mol Ecol 20:740-752
18. Cao Y, Fujiwara M, Nikaido M, Okada N, Hasegawa M (2000) Interordinal relationships and timescale of eutherian evolution as inferred from mitochondrial genome data. Gene 259:149-158 (Pubitemid 32119246)
19. Carlyle JR, Mesci A, Fine JH, Chen P, Belanger S, Tai LH, Makrigiannis AP (2008) Evolution of the Ly49 and Nkrp1 recognition systems. Semin Immunol 20:321-330
20. Chatterjee HJ, Ho SY, Barnes I, Groves C (2009) Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evol Biol 9:259
21. Cheent K, Khakoo SI (2009) Natural killer cells: integrating diversity with function. Immunology 126:449-457
22. Codner GF, Birch J, Hammond JA, Ellis SA (2012) Constraints on haplotype structure and variable gene frequencies suggest a functional hierarchy within cattle MHC class I. Immunogenetics 64:435-445
23. Decker DJ, Stewart BS, Lehman N (2002) Major histocompatibility complex class II DOA sequences from three Antarctic seal species verify stabilizing selection on the DO locus. Tissue Antigens 60:534-538 (Pubitemid 36177277)
24. Dietz R, Heide-Jørgensen MP, Harkonen T (1989) Mass deaths of harbor seals (Phoca vitulina) in Europe. Ambio 18:258-264 (Pubitemid 20421191)
25. Doxiadis GG, de Groot N, Otting N, Blokhuis JH, Bontrop RE (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
26. Flajnik MF, Kasahara M (2010) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11:47-59
27. Gonzalez-Galarza FF, Christmas S, Middleton D, Jones AR (2011) Allele frequency net: a database and online repository for immune gene frequencies in worldwide populations. Nucleic Acids Res 39:D913-D919
28. Goodman SJ (1998) Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol Biol Evol 15:104-118 (Pubitemid 28078410)
29. Graumann MB, DeRose SA, Ostrander EA, Storb R (1998) Polymorphism analysis of four canine MHC class I genes. Tissue Antigens 51:374-381
30. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95-98
31. Hall AJ, Jepson PD, Goodman SJ, Harkonen T (2006) Phocine distemper virus in the North and European Seas-data and models, nature and nurture. Biol Conserv 131:221-229 (Pubitemid 43849644)
32. Hammond JA, Pomeroy PP, Hall AJ, Smith VJ (2005) Identification and real-time PCR quantification of Phocine distemper virus from two colonies of Scottish grey seals in 2002. J Gen Virol 86:2563-2567 (Pubitemid 41167605)
33. Hammond JA, Guethlein LA, Abi-Rached L, Moesta AK, Parham P (2009) Evolution and survival of marine carnivores did not require a diversity of killer cell Ig-like receptors or Ly49 NK cell receptors. J Immunol 182:3618-3627
34. Harkonen T, Dietz R, Reijnders P, Teilmann J, Harding K, Hall A, Brasseur S, Siebert U, Goodman SJ, Jepson PD, Dau Rasmussen T, Thompson P (2006) The 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis Aquat Organ 68:115-130
35. Harkonen T, Harding K, Rasmussen TD, Teilmann J, Dietz R (2007) Age-and sex-specific mortality patterns in an emerging wildlife epidemic: the phocine distemper in European harbour seals. PLoS One 2:e887
36. Harris CM, Travis JM, Harwood J (2008) Evaluating the influence of epidemiological parameters and host ecology on the spread of phocine distemper virus through populations of harbour seals. PLoS One 3:e2710
37. Higdon JW, Bininda-Emonds OR, Beck RM, Ferguson SH (2007) Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset. BMC Evol Biol 7:216
38. Hoelzel AR, Stephens JC, O'Brien SJ (1999) Molecular genetic diversity and evolution at the MHC DQB locus in four species of pinnipeds. Mol Biol Evol 16:611-618 (Pubitemid 29215373)
39. Hofstetter AR, Sullivan LC, Lukacher AE, Brooks AG (2011) Diverse roles of non-diverse molecules: MHC class Ib molecules in host defense and control of autoimmunity. Curr Opin Immunol 23:104-110
40. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683-695 (Pubitemid 40174963)
41. Kennedy LJ, Ollier WER, Marti E, Wagner JL, Storb R (2012) Caninine immunogenetics. In: Ostrander EA, Ruvinsky A (eds) The genetics of the dog, 2nd edn. CAB International, Oxon
42. Kulski JK, Anzai T, Shiina T, Inoko H (2004) Rhesus macaque class I duplicon structures, organization, and evolution within the alpha block of the major histocompatibility complex. Mol Biol Evol 21:2079-2091 (Pubitemid 39391984)
43. Marrack P, Scott-Browne JP, Dai S, Gapin L, Kappler JW (2008) Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu Rev Immunol 26:171-203 (Pubitemid 351600374)
44. Marsh SG, Albert ED, Bodmer WF, Bontrop RE, Dupont B, Erlich HA, Fernandez-Vina M, Geraghty DE, Holdsworth R, Hurley CK, Lau M, Lee KW, Mach B, Maiers M, Mayr WR, Muller CR, Parham P, Petersdorf EW, Sasazuki T, Strominger JL, Svejgaard A, Terasaki PI, Tiercy JM, Trowsdale J (2010) Nomenclature for factors of the HLA system, 2010. Tissue Antigens 75:291-455
45. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463
46. Mellersh CS, Hitte C, Richman M, Vignaux F, Priat C, Jouquand S, Werner P, Andre C, DeRose S, Patterson DF, Ostrander EA, Galibert F (2000) An integrated linkage-radiation hybrid map of the canine genome. Mamm Genome 11:120-130 (Pubitemid 30054414)
47. Moffett A, Loke C (2006) Immunology of placentation in eutherian mammals. Nat Rev Immunol 6:584-594 (Pubitemid 44134091)
48. Neefjes J, Jongsma ML, Paul P, Bakke O (2011) Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 11:823-836
49. Nery MF, Gonzalez DJ, Hoffmann FG, Opazo JC (2012) Resolution of the laurasiatherian phylogeny: evidence from genomic data. Mol Phylogenet Evol 64:685-689
50. Orange JS, Ballas ZK (2006) Natural killer cells in human health and disease. Clin Immunol 118:1-10 (Pubitemid 43012040)
51. Pan H-J, Wan Q-H, Fang S-G (2008) Molecular characterization of major histocompatibility complex class I genes from the giant panda (Ailuropoda melanoleuca). Immunogenetics 60:185-193
52. Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272:67-74 (Pubitemid 26110756)
53. Parham P, Abi-Rached L, Matevosyan L, Moesta AK, Norman PJ, Older Aguilar AM, Guethlein LA (2010) Primate-specific regulation of natural killer cells. J Med Primatol 39:194-212
54. Rada C, Lorenzi R, Powis SJ, van den Bogaerde J, Parham P, Howard JC (1990) Concerted evolution of class I genes in the major histocompatibility complex of murine rodents. Proc Natl Acad Sci U S A 87:2167-2171
55. Rajalingam R (2012) Overview of the killer cell immunoglobulin-like receptor system. Methods Mol Biol 882:391-414
56. Robinson J, Mistry K, McWilliam H, Lopez R, Marsh SG (2010) IPD - the Immuno Polymorphism Database. Nucleic Acids Res 38:D863-D869
57. Robinson J, Mistry K, McWilliam H, Lopez R, Parham P, Marsh SG (2011) The IMGT/HLA database. Nucleic Acids Res 39:D1171-D1176
58. Rodgers JR, Cook RG (2005) MHC class Ib molecules bridge innate and acquired immunity. Nat Rev Immunol 5:459-471 (Pubitemid 40835034)
59. Ross P, Buntzman AS, Vincent BG, Grover EN, Gojanovich GS, Collins EJ, Frelinger JA, Hess PR (2012) Allelic diversity at the DLA-88 locus in Golden Retriever and Boxer breeds is limited. Tissue Antigens 80(2):175-183
60. Saito Y, Naruse TK, Akari H, Matano T, Kimura A (2012) Diversity of MHC class I haplotypes in cynomolgus macaques. Immunogenetics 64:131-141
61. Saper MA, Bjorkman PJ, Wiley DC (1991) Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J Mol Biol 219:277-319
62. Slade RW (1992) Limited MHC polymorphism in the southern elephant seal: implications for MHC evolution and marine mammal population biology. Proc Biol Sci 249:163-171 (Pubitemid 23403207)
63. Staden R, Beal KF, Bonfield JK (2000) The Staden package, 1998. Methods Mol Biol 132:115-130
64. Tallmadge RL, Campbell JA, Miller DC, Antczak DF (2010) Analysis of MHC class I genes across horse MHC haplotypes. Immunogenetics 62:159-172
65. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596-1599 (Pubitemid 47236692)
66. Tanaka-Matsuda M, Ando A, Rogel-Gaillard C, Chardon P, Uenishi H (2009) Difference in number of loci of swine leukocyte antigen classical class I genes among haplotypes. Genomics 93:261-273
67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876-4882 (Pubitemid 28022245)
68. Trowsdale J (2011) The MHC, disease and selection. Immunol Lett 137:1-8
69. Vivian JP, Duncan RC, Berry R, O'Connor GM, Reid HH, Beddoe T, Gras S, Saunders PM, Olshina MA, Widjaja JM, Harpur CM, Lin J, Maloveste SM, Price DA, Lafont BA, McVicar DW, Clements CS, Brooks AG, Rossjohn J (2011) Killer cell immunoglobulinlike receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature 479:401-405
70. Wagner JL (2003) Molecular organization of the canine major histocompatibility complex. J Hered 94:23-26 (Pubitemid 37553177)
71. Wagner JL, Palti Y, DiDario D, Faraco J (2005) Sequence of the canine major histocompatibility complex region containing non-classical class I genes. Tissue Antigens 65:549-555 (Pubitemid 40776304)
72. Wang J, Whitman MC, Natarajan K, Tormo J, Mariuzza RA, Margulies DH (2002) Binding of the natural killer cell inhibitory receptor Ly49A to its major histocompatibility complex class I ligand. J Biol Chem 277:1433-1442
73. Weber DS, Stewart BS, Schienman J, Lehman N (2004) Major histocompatibility complex variation at three class II loci in the northern elephant seal. Mol Ecol 13:711-718 (Pubitemid 38260951)
74. Welch AY, Kasahara M, Spain LM (2003) Identification of the mouse killer immunoglobulin-like receptor (Kir1) gene family mapping to chromosome X. Immunogenetics 54:782-790 (Pubitemid 36384473)
75. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555-556 (Pubitemid 27480216)
76. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107-1118 (Pubitemid 40471423)
77. Yuhki N, O'Brien SJ (1988) Molecular characterization and genetic mapping of class I and class II MHC genes of the domestic cat. Immunogenetics 27:414-425
78. Yuhki N, O'Brien SJ (1994) Exchanges of short polymorphic DNA segments predating speciation in feline major histocompatibility complex class I genes. J Mol Evol 39:22-33 (Pubitemid 24181121)
79. Yuhki N, Heidecker GF, O'Brien SJ (1989) Characterization of MHC cDNA clones in the domestic cat. Diversity and evolution of class I genes. J Immunol 142:3676-3682 (Pubitemid 19137506)
80. Yuhki N, Beck T, Stephens R, Neelam B, O'Brien SJ (2007) Comparative genomic structure of human, dog, and cat MHC: HLA, DLA, and FLA. J Hered 98:390-399 (Pubitemid 47357595)
81. Yuhki N, Mullikin JC, Beck T, Stephens R, O'Brien SJ (2008) Sequences, annotation and single nucleotide polymorphism of the major histocompatibility complex in the domestic cat. PLoS One 3:e2674
82. Zhong JF, Harvey JT, Boothby JT (1998) Characterization of a harbor seal class I major histocompatability complex cDNA clone. Immunogenetics 48:422-424 (Pubitemid 28482590)