Major histocompatibility complex variation at class II DQA locus in the brown hare (Lepus europaeus)

Molecular Ecology

Volumn 18, Issue 22, 2009, Pages 4631-4649

  Koutsogiannouli, E A ^a   Moutou, K A ^a   Sarafidou, T ^a   Stamatis, C ^a   Spyrou, V ^b   Mamuris, Z ^a  

^a UNIVERSITY OF THESSALY   (Greece)

^b Technological Educational Institute   (Greece)

Author keywords

DQA gene; Lepus europaeus; Major histocompatability complex; Peptide binding region; Population genetics; Positive selection

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ALLELE; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DNA SEQUENCE; EUROPE; EXON; GENE; GENE FREQUENCY; GENETIC SELECTION; GENETICS; GEOGRAPHY; HARE; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION GENETICS; SEQUENCE ALIGNMENT; SINGLE STRAND CONFORMATION POLYMORPHISM;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DNA, MITOCHONDRIAL; EUROPE; EVOLUTION, MOLECULAR; EXONS; GENE FREQUENCY; GENES, MHC CLASS II; GENETICS, POPULATION; GEOGRAPHY; HARES; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, SINGLE-STRANDED CONFORMATIONAL; SELECTION, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

LEPUS CAPENSIS; LEPUS EUROPAEUS;

EID: 70350761851     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2009.04394.x     Document Type: Article

References (74)

1. Abbott KM, Wickings EJ, Knapp LA (2006) High levels of diversity characterize mandrill (Mandrillus sphinx) Mhc-DRB sequences. Immunogenetics, 58, 628 640.
2. Andersson L, Mikko S (1995) Generation of MHC class II diversity by intra- and intergenic recombination. Immunological Reviews, 143, 5 12.
3. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK (1997) The nature of selection on the major histocompatibility complex. Critical Reviews in Immunology, 17, 179 224.
4. Belkhir K (1999) genetix, logiciel sous Windows pour la génétique des populations, Laboratoire Génome et Populations, CNRS UPR 9060. Université de Montpellier II, Montpellier (France).
5. de Bellocq JG, Suchentrunk F, Baird SJE, Schaschl H (2009) Evolutionary history of an MHC gene in two leporid species: characterisation of Mhc-DQA in the European brown hare and comparison with the European rabbit. Immunogenetics, 61, 131 144.
6. Ben Slimen H, Suchentrunk F, Stamatis C et al. (2008) Population genetics of cape and brown hares (Lepus capensis and L. europaeus): a test of Petter's hypothesis of conspecificity. Biochemical Systematics and Ecology, 36, 22 39.
7. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology, 16, 363 377.
8. Bernatchez L, Savard L, Dodson J, Pallota D (1988) Mitochondrial DNA sequence heterogeinity among James-Hudson Bay anadromous coregonines. Finnish Fish Research, 9, 17 26.
9. Bondinas GP, Moustakas AK, Papadopoulos GK (2007) The spectrum of HLA-DQ and HLA-DR alleles, 2006: a listing correlating sequence and structure with function. Immunogenetics, 59, 539 553.
10. Brown JH, Jardetzky TS, Gorga JC et al. (1993) Three-dimensional structure of the human class II histocompatability antigen HLA-DR1. Nature, 364, 33 39.
11. Cárdenas C, Ortiz M, Balbín A, Villaveces JL, Patarroyo ME (2005) Allele effects in MHC-peptide interactions: a theoretical analysis of HLA-DRβ1*0101-HA and HLA-DRβ1*0401-HA complexes. Biochemical and Biophysical Research Communications, 330, 1162 1167.
12. Cárdenas C, Obregón M, Balbín A, Villaveces JL, Patarroyo ME (2007) Wave function analysis of MHC-peptide interactions. Journal of Molecular Graphics and Modelling, 25, 605 615.
13. Cheylan G (1991) Patterns of Pleistocene turnover, current distribution and speciation among Mediterranean mammals. In : Biogeography of Mediterranean Invasion (eds Groves RH, Di Castri F pp. 227 262. Cambridge University Press, Cambridge.
14. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends in Ecology and Evolution, 13, 305 311.
15. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial-DNA restriction data. Genetics, 131, 479 491.
16. Fain MA, Zhao T, Kindt TJ (2001) Improved typing procedure for the polymorphic single-copy RLA-DQA gene of the rabbit reveals a new allele. Tissue Antigens, 57, 332 338.
17. Fickel J, Lieckfeldt D, Pitra C (1999) Analysis of genetic diversity and structure in neighboring populations of the European brown hare (Lepus europaeus, Pallas 1778). Zeitschrift für Jagdwissenschaft, 45, 230 237.
18. Fickel J, Schmidt A, Putze M et al. (2005) Genetic structure of populations of European brown hare: implications for management. The Journal of Wildlife Management, 69, 760 771.
19. Fickel J, Hauffe CH, Pecchioli E et al. (2008) Cladogenesis of the European brown hare (Lepus europaeus Pallas, 1778). European Journal of Wildlife Research, 54, 495 510.
20. Figueroa F, Gunther E, Klein J (1988) MHC polymorphism pre-dating speciation. Nature, 355, 265 267.
21. Flux ECJ (2007) Notes on New Zealand mammals 3. Brown hare signals to cat. New Zealand Journal of Zoology, 34, 159 160.
22. Gökaşan E, Demirbà E, Oktay FY et al. (1997) On the origin of the Bosphorus. Marine Geology, 140, 183 199.
23. Goudet J (2001) fstat, A Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3). Available at: http://www2.unil.ch/popgen/ softwares/fstat.html. Updated from Goudet 1995.
24. Hedrick PW (1994) Evolutionary genetics at the major histocompatibility complex. American Naturalist, 143, 945 964.
25. Hedrick PW, Lee RN, Parker KM (2000a) Major histocompatibility complex (MHC) variation in the endangered Mexican wolf and related canids. Heredity, 85, 617 624.
26. Hedrick PW, Parker KM, Gutierrez-Espeleta GA, Rattink A, Lievers K (2000b) Major histocompatibility complex variation in the Arabian oryx. Evolution, 54, 2145 2151.
27. Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature, 405, 907 913.
28. Hill AVS, Allsopp EM, Dwiatkowski D et al. (1991) Common West African HLA antigens are associated with protection from severe malaria. Nature, 352, 595 600.
29. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature, 335, 167 170.
30. Hughes A, Yeager M, Carrington M (1996) Peptide binding function and the paradox of HLA disease associations. Immunology and Cell Biology, 74, 444 448.
31. Janeway CA, Travers P, Walport M, Shlomchik MJ (2005) Immunobiology, 6th edn. Garland Science, London, pp 183 201.
32. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In : Mammalian Protein Metabolis (ed. Munro HN pp. 21 123. Academic Press, New York.
33. Kasapidis P, Suchentrunk F, Magoulas A, Kotoulas G (2005) The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations. Molecular Phylogenetic Evolution, 34, 55 66.
34. Kjøglum S, Larsen S, Bakke HG, Grimholt U (2006) How specific MHC class I and class II combinations affect disease resistance against infectious salmon anaemia in Atlantic salmon (Salmo salar). Fish and Shellfish Immunology, 21, 431 441.
35. Klein J, Takahata N (1990) The major histocompatibility complex and the quest for origins. Immunological Reviews, 113, 5 25. (Pubitemid 20076533)
36. Klein J, Sato A, Nagl S, O'hUigin C (1998) Molecular trans-species polymorphism. Annual Review of Ecology and Systematics, 29, 1 21.
37. Kwok WW, Kovats S, Thurtle P, Nepom GT (1993) HLA-DQ allelic polymorphisms constrain patterns of class II heterdimer formation. Journal of Immunology, 150, 2263 2272.
38. LeGuern C, Marche PN, Kindt TJ (1985) Molecular evidence for five distinct MHC class II alpha genes in the rabbit. Immunogenetics, 22, 141 148.
39. Mamuris Z, Sfougaris AI, Stamatis C (2001) Genetic structure of Greek brown hare (Lepus europaeus) populations as revealed by mtDNA RFLP-PCR analysis: implications for conserving genetic diversity. Biological Conservation, 101, 187 196.
40. Mamuris Z, Sfougaris AI, Stamatis C, Suchentrunk F (2002) Assessment of genetic structure of Greek brown hare (Lepus europaeus) populations based on variation in random amplified polymorphic DNA (RAPD). Biochemical Genetics, 40, 323 338.
41. McFarland BJ, Beeson C (2002) Binding interactions between peptides and proteins of the class II major histocompatability complex. Medicinal Research Reviews, 22, 168 203.
42. Musolf K, Meyer-Lucht Y, Sommer S (2004) Evolution of MHC-DRB class II polymorphism in the genus Apodemus and a comparison of DRB sequences within the family Muridae (Mammalia: Rodentia). Immunogenetics, 56, 420 426.
43. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution, 3, 418 426.
44. Otting N, de Groot NG, Doxiadis GGM, Bontrop RE (2002) Extensive Mhc-DQB variation in humans and non-human primate species. Immunogenetics, 54, 230 239.
45. Ottova E, Simkova A, Martin JF et al. (2005) Evolution and trans-species polymorphism of MHC class IIβ genes in cyprinid fish. Fish & Shellfish Immunology, 18, 199 222.
46. Paterson S, Wilson K, Pemberton JM (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proceedings of the National Academy of Sciences, USA, 95, 3714 3719.
47. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. The American Naturalist, 153, 145 164.
48. Piertney SB, Oliver MK (2006) The evolutionary ecology of the major histocompatability complex. Heredity, 96, 7 21.
49. Potts WK, Slev PR (1995) Pathogen-based models favoring MHC genetic diversity. Immunological Reviews, 143, 181 197.
50. Potts WK, Wakeland EK (1993) Evolution of MHC genetic diversity: a tale of incest, pestilence and sexual preference. Trends in Genetics, 9, 408 412.
51. Rammensee HG, Friede T, Stevanovic S (1995) MHC ligands and peptide motifs: first listing. Immunogenetics, 41, 178 228.
52. Reche PA, Reinherz EL (2003) Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphism. Journal of Molecular Biology, 331, 623 641.
53. Richman AD, Herrera LG, Nash D, Schierup HM (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genetical Research, 82, 89 99.
54. Roberts N, Kuzucuoglu C, Karabiyikoglu M (1999) The Late Quaternary in the Eastern Mediterranean region: an introduction. Quaternary Science Reviews, 18, 497 499.
55. Sawyer S (1989) Statistical tests for detecting gene conversion. Molecular Biology and Evolution, 6, 526 538.
56. Seddon JM, Baverstock PR (2000) Evolutionary lineages of RT1.Ba in the Australian Rattus. Molecular Biology and Evolution, 17, 768 772.
57. Seddon JM, Ellegren H (2002) MHC class II genes in European wolves: a comparison with dogs. Immunogenetics, 54, 490 500.
58. Sert H, Suchentrunk F, Erdogan A (2005) Genetic diversity in brown hares (Lepus europaeus Pallas, 1778) from Anatolia and differentiation among Anatolian and European populations. Mammalian Biology, 70, 171 186.
59. Siebold C, Hansen BE, Wyer JR et al. (2004) Crystal structure of HLA-DQ0602 that protects against type I diabetes and confers strong susceptibility to narcolepsy. Proceedings of National Academy of Sciences, USA, 93, 5380 5383.
60. Sittisombut N, Knight KL (1986) Rabbit major histocompatibility complex. I. Isolation and characterization of three subregions of class II genes. Journal of Immunology, 136, 1871 1875.
61. Smith GR (2001) Homologous recombination near and far from DNA breaks: alternative roles and contrasting views. Annual Review of Genetics, 35, 243 274.
62. Sommer S (2005) The importance of immune gene variability (MHC) in evolutionary ecology and conservation. Frontiers in Zoology, 2, 16.
63. SPSS Inc. (2004) spss 13.0 for Windows User's Guide. SPSS Inc., Chicago, IL.
64. Stamatis C, Suchentrunk F, Sert H et al. (2007) Genetic evidence for survival of released captive-bred brown hares Lepus europaeus during restocking operations in Greece. Oryx, 41, 548 551.
65. Stamatis C, Suchentrunk F, Moutou KA et al. (2009) Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia? Journal of Biogeography, 36, 515 528.
66. Suchentrunk F, Michailov C, Markov G, Haiden A (2000) Population genetics of Bulgarian brown hares Lepus europaeus: Allozymic diversity at zoogeographical crossroads. Acta Theriologica, 45, 1 12.
67. Suchentrunk F, Mamuris Z, Sfougaris AI, Stamatis C (2003) Biochemical genetic variability in brown hares (Lepus europaeus) from Greece. Biochemical Genetics, 41, 127 140.
68. Surridge AK, van der Loo W, Abrentes J et al. (2008) Diversity and evolutionary history of the MHC DQA gene in leporids. Immunogenetics, 60, 515 525.
69. Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7, 453 464.
70. Takahata N, Nei M (1990) Allelic genealogy under overdominance and frequency-dependent selection and polymorphism of major histocompatability complex loci. Genetics, 124, 967 978.
71. Tamura K, Dudley J, Nei M, Kumar S (2007) mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596 1599.
72. Thompson JD, Higgins DG, Gibson TJ (1994) clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673 4680.
73. Van Eijk MJT, Stewart-Haynes JA, Beever JE, Fernando RL, Lewin HA (1992) Development of persistent lymphocytosis in cattle in closely associated with DRB2. Immunogenetics, 37, 64 68.
74. Xu A, Van Eijk MJT, Park C, Lewin HA (1993) Polymorphism in BoLA-DRB3 Exon 2 Correlates with Resistance to Persistent Lymphocytosis Caused by Bovine Leukaemia Virus. Journal of Immunology, 151, 6977 6985.