Sequence variability analysis on major histocompatibility complex class II DRB alleles in three felines

Abstract

The variation of the exon 2 of the major histocompatibility complex (MHC) class II gene DRB locus in three feline species were examined on clouded leopard (Neofelis nebulosa), leopard (Panthera pardus) and Amur tiger (Panthera tigris altaica). A pair of degenerated primers was used to amplify DRB locus covering almost the whole exon 2. Exon 2 encodes the ?1 domain which is the most variable fragments of the MHC class II molecule. Single-strand conformational polymorphism (SSCP) analysis was applied to detect different MHC class II DRB haplotypes. Fifteen recombinant plasmids for each individual were screened out, isolated, purified and sequenced finally. Totally eight distinct haplotypes of exon 2 were obtained in four individuals. Within 237 bp nucleotide sequences from four samples, 30 variable positions were found, and 21 putative peptide-binding positions were disclosed in 79 amino acid residues. The ratio of nonsynonymous substitutions (d_N) was much higher than that of synonymous substitutions (d_S), which indicated that balancing selection probably maintain the variation of exon 2. MEGA neighbor joining (NJ) and PAUP maximum parsimony (MP) methods were used to reconstruct phylogenetic trees among species, respectively. Results displayed a more close relationship between leopard and tiger; however, clouded leopard has a comparatively distant relationship form the other two.

References

1. Abbas A K Lichtman A H Pober J S 1991 Cellular and Molecular ImmunologyNew YorkSaundersW B and Co
2. Aguilar A Roemer G Debenham S Binns M Garcelon D Wayne R K 2004 High MHC diversity maintained by balancing selection inan otherwise genetically monomorphic mammalPNAS10134903494. doi:10.1073/pnas.0306582101
3. Bernatchz L Landry C 2003 MHC studiesin nonmodel vertebrates: What have we learned about natural selectionin 15 yearsJ Evol Biol16363377. doi:10.1046/j.1420‐9101.2003.00531.x
4. Brown J H Jardetzky T S Gorga J C Stern L J Urban R G Strominger J L Wiley D C 1993 Three-dimensionalstructure of the human class II histocompatibility antigen HLA–DR1Nature643339. doi:10.1038/364033a0
5. Crespi B J Fulton M J 2004 Molecularsystematics of Salmonidae: Combined nuclear data yields a robust phylogenyPhylogenet Evol31658679. doi:10.1016/j.ympev.2003.08.012
6. Drake G C Kennedy L J Auty H K 2004 The use of reference strand-mediated conformationalanalysis for the study of cheetah (Acinonyxjubatus) feline leucocytes antigen class II DRB polymorphismsMol Ecol13221229. doi:10.1046/j.1365‐294X.2003.02027.x
7. Elizabeth J G Oliver R A Russell G C 2000 Duplicated DQ haplotypes increase thecomplexity of restriction element usage in CattleJ Immunol165134138
8. Graser R O'hUigin C Vineek V Meyer A Klein J 1996 Trans-species polymorphismof class II MHC loci in danio fishesImmunogenetics443648. doi:10.1007/BF02602655
9. Hedrick P W Gutierrez-Espeleta G A Lee R N 2001 Founder effect in an islandpopulation of bighorn sheepMol Ecol10851857. doi:10.1046/j.1365‐294X.2001.01243.x
10. Hedrick P W Lee R N Garrigan D 2002 Major histocompatibility complex variationin red wolves: Evidence for common ancestry with coyotes and balancingselectionMol Ecol1119051913. doi:10.1046/j.1365‐294X.2002.01579.x
11. Hedrick P W Lee R N Parker K M 2000 Major histocompatibility complex (MHC)variation in the endangered Mexican wolf and related canidsHeredity85617624. doi:10.1046/j.1365‐2540.2000.00805.x
12. Hedrick P W Whittam T S Parham P 1991 Heteozygosity at individual amino acidsites: Extremely high levels for HLA-A and -B genesPNAS8858975901. doi:10.1073/pnas.88.13.5897
13. Herrington S J 1986 Phylogenetic relationships of the wild cats of the worldPhD Dissertation. University of Kansas
14. Hess C M Edwards S V 2002 The evolutionof the major histocompatibility complex in birdsBioscience22423431. doi:10.1641/0006‐3568(2002)052[0423:TEOTMH]2.0.CO;2
15. Hoelzel A R Stephens J C O'Brien S J 1999 Molecular genetic diversity and evolutionat the MHC DQB locus in four species of PinnipedesMol Biol Evol16(5)611618
16. Hughes A L Yeager M 1998 Natural selectionat major histocompatibility complex loci of vertebratesAnnu Rev Genet32415435. doi:10.1146/annurev.genet.32.1.415
17. Janczewski D N Modi W S Stephens J C O'Brien S J 1995 Molecular evolution of mitochondrial 12SrRNA and cytochrome b sequences in the Pantherine lineage ofFelidaeMol Biol Evol12(4)690707
18. Jeanmougin F Thompson D Gouy M G.Higgins D Gibson T J 1998 Multiple sequencealignment with Clustal XTrends BiochemSci23403405. doi:10.1016/S0968‐0004(98)01285‐7
19. Johnson W E O'Brien S J 1997 Phylogeneticreconstruction of the Felidae using 16S rRNA and NADH-5 mitochondrialgenesMol Evol4498116. doi:10.1007/PL00000060
20. Jukes T H Cantor C R 1969 Evolutionof protein moleculesIn: Munro H NMammalian Protein MetabolismAcademic,New York 21132
21. Kennedy L J Ryvar R Gaskell R M Addie D A Willoughby K Carter S D Thompson W Ollier W E Radford A D 2002 Sequence analysis of MHC DRB alleles in domestic cats from the UnitedKingdomImmunogenetics54348352. doi:10.1007/s00251‐002‐0465‐5
22. Klein J 1980 Generation of diversity at MHC Loci: Implications for T-cellreceptor repertoiresFougereau MDausset JImmunology80LondonAcademic Press239253
23. Klein J Figueroa F 1986 Evolutionof the major histocompatibility complexImmunogenetics6295386
24. Klein J Satta Y Takahata N 1993 Trans-specific MHC polymorphism and theorigin of species in primatesJ Med Primatol225764
25. Kumar S Tamura K Jakobsen I B Nei M 2001 MAGE2: Molecular evolutionary genetics analysis softwareBioinformatics1712441245. doi:10.1093/bioinformatics/17.12.1244
26. Kuwahara Y Kitoh K Kobayashi R Iwata J Ohne R Hosokawakana T Matsumoto Y Kitagawa H Sasaki Y 2000 Genotyping of feline MHC (FLA) class II DRB by PCR-RFLP Method usingGroup-Specific PrimersJ Vet Med Sci6212831289. doi:10.1292/jvms.62.1283
27. Masuda R Lopez J V Slattery J P Yuhki N O'Brien S J 1996 Molecular phylogeny ofmitochondrial cytochrome b and12S rRNA sequences in the Felidae: Ocelot and domestic cat lineagesMol Phylogenet Evol6(3)351365. doi:10.1006/mpev.1996.0085
28. Mikko S Andersson L 1995 Low majorhistocompatibility complex class II diversity in European and NorthAmerican moosePNAS9242594263. doi:10.1073/pnas.92.10.4259
29. Murray B W Malik S White B N 1995 Sequence variation at the major histocompatibilitycomplex locus DQB in beluga whales (Delphinapterusleucas)Mol Biol Evol12(4)582593
30. Nei M Gojobori T 1986 Simple methodsfor estimating the numbers of synonymous and nonsynonymous nucleotidesubstitutionsMol Biol Evol3418426
31. Nei M Hughes A L 1991 Polymorphismand evolution of the major histocompatibility complex Loci in mammalsIn: Selander RClarkAWhittam TEvolution at the Molecular LevelSunderlandSinauer Associates222247
32. Nei M Kumar S 2000 MolecularEvolution and PhylogeneticsLondonOxford University Press
33. Nino-Vasquez J J Vogel D Rodriguez R 2000 Sequence and diversity of DRB genes of Aotus nancymaae, a primate model for humanmalaria parasitesImmunogenetics51219230. doi:10.1007/s002510050035
34. Nowak R M 1991 Walker's Mammals of the World5th ed BaltimoreJohns Hopkins UniversityPress
35. Nowell K Jackson P 1996 Wild Cats-StatusSurvey and Conservation Action PlanSwitzlandIUCN/SSC Cat Specialist Group, IUCN, Gland5565
36. O'Brien S J Evermann J F 1988 Interactiveinfluence of infectious disease and genetic diversity in natural populationsTrends Ecol Evol3254259. doi:10.1016/0169‐5347(88)90058‐4
37. O'Brien S J Wildt D E Goldman D Merril C R Bush M 1983 The cheetah is depauperatein genetic variationScience221459462. doi:10.1126/science.221.4609.459
38. Packer C Pusey A E Rowley H 1991 Case study of a population bottleneck-lionsof the Ngorongoro CraterCons Biol5219230. doi:10.1111/j.1523‐1739.1991.tb00127.x
39. Rozas J Sánchez-DelBarrio J C Messeguer X Rozas R 2003 DnaSP, DNA polymorphism analyses by thecoalescent and other methodsBioinformatics1924962497. doi:10.1093/bioinformatics/btg359
40. Russello A M Gladyshev E Miquelle D Caccone A 2004 Potential genetic consequences of a recent bottleneck in the Amurtiger of the Russian Far EastCons Genet5707713. doi:10.1007/s10592‐004‐1860‐2
41. Salles L 1992 Felid phylogenetics: Extant taxa and skull morphologyAmerican Museum Novitates3047167
42. Sambrook J Russell D W 2001 MolecularCloning: A Laboratory Manual3rd ed NewYorkCold Spring Harbor LaboratoryPress
43. Schaschl H Goodman S J Suchentrunk F 2004 Sequence analysis of the MHC class IIDRB alleles in Alpine chamois (Rupicapra r. rupicapra).Dev Comp Immunol28265277. doi:10.1016/j.dci.2003.08.003
44. Shia Y C Bradshaw M Rutherford M S Lewin H A Schook L B 1995 PCR-based genotyping forcharacterization of SLA-DQB and SLADRB alleles in domestic pigAnim Genet269199
45. Slattery J P O'Brien S J 1998 Patterns ofY and X chromosome DNA sequence divergence during the Felidae radiationGenetics14812451255
46. Swofford D L 1998 PAUP*. Phylogenetic Analysis Using Parsimony (*and othermethods), Version 4Sunderland, MassachusettsSinauer Associates
47. Wang S 1998 China red data book of endangered animalsBeijingScience Press(in Chinese)
48. Wayne R K Valkenburgh B V O'Brien S J 1991 Molecular distance and divergence timein carnivores and primatesMol Biol Evol8297319
49. Westerdahl H Wittzell H Schantz T V 2000 MHC diversity in two passerine birds:No evidence for a minimal essential MHCImmunogenetics5292100. doi:10.1007/s002510000256
50. Yuhki N Eizirik E Johnson W E O'Brien S J 2000 Sequencediversity of major histocompatibility complex class II DRB Exon2 regionof two sister species of the Felidae, Ocelot (Leopardus pardalis)and Margay (Leopardus wiedii) (Unpublished) [DB/OL]: http://www.ncbi.nlm.nih.gov/
51. Yuhki N O'Brien S J 1997 Nature andorigin of polymorphism in feline MHC class II DRA and DRB genesJ Immuol1582,8222,833
52. Zheng T Fei R M Wu X B 2005 Phylogeney of 13 Felidae species fromChina based on partial 12S rRNA and Cyt b genes sequencesActa Zool Sin51(4)630639(in Chinese)