Stepwise threshold clustering: A new method for genotyping MHC loci using next-generation sequencing technology

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Stutz, William E ^a   Bolnick, Daniel I ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ARTIFACT; CLONING; CONTROLLED STUDY; GASTEROSTEUS ACULEATUS; GENE; GENE AMPLIFICATION; GENE FREQUENCY; GENE LIBRARY; GENE LOCUS; GENETIC ALGORITHM; GENETIC SIMILARITY; GENOME; GENOTYPE; HIGH THROUGHPUT SEQUENCING; MEASUREMENT ACCURACY; MHC GENE; NEXT GENERATION SEQUENCING; NONHUMAN; RELIABILITY; SEQUENCE HOMOLOGY; STEPWISE THRESHOLD CLUSTERING; ALLELE; ANIMAL; CLUSTER ANALYSIS; GENETICS; GENOTYPING TECHNIQUE; MAJOR HISTOCOMPATIBILITY COMPLEX; PROCEDURES; SMEGMAMORPHA;

ALLELES; ANIMALS; CLUSTER ANALYSIS; GENE LIBRARY; GENETIC LOCI; GENOTYPING TECHNIQUES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MAJOR HISTOCOMPATIBILITY COMPLEX; SMEGMAMORPHA;

EID: 84904556760     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100587     Document Type: Article

References (86)

1. Klein J (1986) Natural History of the Major Histocompatability Complex. New York: Wiley. 798 p.
2. Flajnik MF, Kasahara M (2001) Comparative genomics of the MHC: glimpses into the evolution of the adaptive immune system. Immunity 15: 351-362. (Pubitemid 32907383)
3. Edwards SV, Hedrick PW (1998) Evolution and ecology of MHC molecules: from genomics to sexual selection. Trends Ecol Evol 13: 305-311. (Pubitemid 28368430)
4. Meyer D, Thomson G (2001) How selection shapes variation of the human major histocompatibility complex: a review. Ann Hum Genet 65: 1-26. (Pubitemid 32390186)
5. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? J Evol Biol 16: 363-377. (Pubitemid 36567968)
6. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B 277: 979-988.
7. Clarke B, Kirby DRS (1966) Maintenance of histocompatibility polymorphisms. Nature 211: 999-1000.
8. Snell GD (1968) The H-2 locus of the mouse: observations and speculations concerning its comparative genetics and its polymorphism. Folia Biol (Praha) 14: 335-358.
9. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
10. Hughes AL, Nei M (1989) Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A 86: 958-962. (Pubitemid 19056271)
11. Potts WK, Wakeland EK (1990) Evolution of diversity at the major histocompatibility complex. Trends Ecol Evol 5: 181-187. (Pubitemid 120036285)
12. Takahata N, Nei M (1990) Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124: 967-978. (Pubitemid 20146073)
13. Slade RW, McCallum HI (1992) Overdominant vs. frequency-dependent selection at MHC loci. Genetics 132: 861-862.
14. Hedrick PW (2002) Pathogen resistance and genetic variation at MHC loci. Evolution 56: 1902-1908.
15. Siddle HV, Kreiss A, Eldridge MDB, Noonan E, Clarke CJ, et al. (2007) Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci U S A 104: 16221-16226. (Pubitemid 350099388)
16. Siddle HV, Marzec J, Cheng Y, Jones M, Belov K (2010) MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer. Proc R Soc B 277: 2001-2006.
17. Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci U S A 108: 16705-16710.
18. Hedrick PW, Parker KM, Gutierrez-Espeleta GA, Rattink A, Lievers K (2000) Major histocompatibility complex variation in the Arabian oryx. Evolution 54: 2145-2151. (Pubitemid 32113840)
19. Altizer S, Pedersen AB (2008) Host-pathogen evolution, biodiversity and disease risks for natural populations. In: Carroll SP, Fox CW, editors. Conservation biology: Evolution in Action. pp. 259-278.
20. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153: 145-164. (Pubitemid 29139433)
21. Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37: 159-186.
22. Erlich RL, Jia X, Anderson S, Banks E, Gao X, et al. (2011) Next-generation sequencing for HLA typing of class I loci. BMC Genomics 12: 42.
23. Wang C, Krishnakumar S, Wilhelmy J, Babrzadeh F, Stepanyan L, et al. (2012) High-throughput, high-fidelity HLA genotyping with deep sequencing. Proc Natl Acad Sci U S A 109: 8676-8681.
24. Babik W (2010) Methods for MHC genotyping in non-model vertebrates. Mol Ecol Resour 10: 237-251.
25. Hess CM, Edwards SV (2002) The evolution of the major histocompatibility complex in birds. Bioscience 52: 423-431. (Pubitemid 34458435)
26. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA, et al. (2004) Gene map of the extended human MHC. Nat Rev Genet 5: 889-899. (Pubitemid 39564252)
27. Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56: 683-695. (Pubitemid 40174963)
28. McGinnis MD, Conrad MP, Bouwens AGM, Tilanus MGJ, Kronick MN (1995) Automated, solid-phase sequencing of DRB region genes using T7 sequencing chemistry and dye-labeled primers. Tissue Antigens 46: 173-179.
29. Livant EJ, Ewald SJ (2005) High-resolution typing for chicken BF2 (MHC class I) alleles by automated sequencing. Anim Genet 36: 432-434. (Pubitemid 43960960)
30. Bos DH, Gopurenko D, Williams RN, DeWoody JA (2008) Inferring population history and demography using microsatellites, mitochondrial DNA, and major histocompatibility complex (MHC) genes. Evolution 62: 1458-1468. (Pubitemid 351754593)
31. Klein J, Sato A, Nagl S, O'hUigin C (1998) Molecular trans-species polymorphism. Annu Rev Ecol Syst 29: 1-21. (Pubitemid 29033024)
32. Malaga-Trillo E, Zaleska-Rutczynska Z, McAndrew B, Vincek V, Figueroa F, et al. (1998) Linkage relationships and haplotype polymorphism among cichlid MHC class II B loci. Genetics 149: 1527-1537. (Pubitemid 28334542)
33. Lenz TL, Eizaguirre C, Kalbe M, Milinski M (2013) Evaluating patterns of convergent evolution and trans-species polymorphism at MHC immunogenes in two sympatric stickleback species. Evolution 67: 2400-2412.
34. Parham P, Ohta T (1996) Population biology of antigen presentation by MHC class I molecules. Science 272: 67-74. (Pubitemid 26110756)
35. Ohta T (1999) Effect of gene conversion on polymorphic patterns at major histocompatibility complex loci. Immunol Rev 167: 319-325.
36. Reusch T, Langefors Å (2005) Inter- and intralocus recombination drive MHC class IIB gene diversification in a teleost, the three-spined stickleback Gasterosteus aculeatus. J Mol Evol 61: 531-541. (Pubitemid 41416896)
37. Reusch TBH, Schaschl H, Wegner KM (2004) Recent duplication and interlocus gene conversion in major histocompatibility class II genes in a teleost, the three-spined stickleback. Immunogenetics 56: 427-437. (Pubitemid 39349884)
38. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proc Natl Acad Sci U S A 86: 2766-2770. (Pubitemid 19112622)
39. Muyzer G, Waal EC de, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59: 695-700. (Pubitemid 23072343)
40. Argüello JR, Little A-M, Bohan E, Goldman JM, Marsh SG., et al. (1998) High resolution HLA class I typing by reference strand mediated conformation analysis (RSCA). Tissue Antigens 52: 57-66. (Pubitemid 28327726)
41. Bryja J, Galan M, Charbonnel N, Cosson J-F (2005) Analysis of major histocompatibility complex class II gene in water voles using capillary electrophoresis-single stranded conformation polymorphism. Mol Ecol Notes 5: 173-176. (Pubitemid 40350915)
42. Lenz TL, Eizaguirre C, Becker S, Reusch TB (2009) RSCA genotyping of MHC for high-throughput evolutionary studies in the model organism three-spined stickleback Gasterosteus aculeatus. BMC Evol Biol 9: 57.
43. Longeri M, Zanotti M, Damiani G (2002) Recombinant DRB sequences produced by mismatch repair of heteroduplexes during cloning in Escherichia coli. Eur J Immunogenet 29: 517-523. (Pubitemid 35365662)
44. Babik W, Taberlet P, Ejsmond MJ, Radwan J (2009) New generation sequencers as a tool for genotyping of highly polymorphic multilocus MHC system. Mol Ecol Resour 9: 713-719.
45. Galan M, Guivier E, Caraux G, Charbonnel N, Cosson J-F (2010) A 454 multiplex sequencing method for rapid and reliable genotyping of highly polymorphic genes in large-scale studies. BMC Genomics 11: 296.
46. Zagalska-Neubauer M, Babik W, Stuglik M, Gustafsson L, Cichoń M, et al. (2010) 454 sequencing reveals extreme complexity of the class II Major Histocompatibility Complex in the collared flycatcher. BMC Evol Biol 10: 395.
47. Stuglik MT, Radwan J, Babik W (2011) jMHC: software assistant for multilocus genotyping of gene families using next-generation amplicon sequencing. Mol Ecol Resour 11: 739-742.
48. Nadachowska-Brzyska K, Zieliński P, Radwan J, Babik W (2012) Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol Ecol 21: 887-906.
49. Promerová M, Babik W, Bryja J, Albrecht T, Stuglik MT, et al. (2012) Evaluation of two approaches to genotyping major histocompatibility complex class I in a passerine - CE-SSCP and 454 pyrosequencing. Mol Ecol Resour 12: 285-292.
50. Radwan J, Zagalska-Neubauer M, Cichoń M, Sendecka J, Kulma K, et al. (2012) MHC diversity, malaria and lifetime reproductive success in collared flycatchers. Mol Ecol 21: 2469-2479.
51. Strandh M, Westerdahl H, Pontarp M, Canbäck B, Dubois M-P, et al. (2012) Major histocompatibility complex class II compatibility, but not class I, predicts mate choice in a bird with highly developed olfaction. Proc R Soc B 279: 4457-4463.
52. Dunn PO, Bollmer JL, Freeman-Gallant CR, Whittingham LA (2013) MHC variation is related to a sexually selected ornament, survival, and parasite resistance in common yellowthroats. Evolution 67: 679-687.
53. Sommer S, Courtiol A, Mazzoni CJ (2013) MHC genotyping of non-model organisms using next-generation sequencing: a new methodology to deal with artefacts and allelic dropout. BMC Genomics 14: 1-17.
54. Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, et al. (2007) The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE 2: e197.
55. Meyer M, Stenzel U, Hofreiter M (2008) Parallel tagged sequencing on the 454 platform. Nat Protocols 3: 267-278. (Pubitemid 351266511)
56. Huse SM, Huber JA, Morrison HG, Sogin ML, Welch DM (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8: R143.
57. Dohm JC, Lottaz C, Borodina T, Himmelbauer H (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucl Acids Res 36: e105-e105.
58. Bradley RD, Hillis DM (1997) Recombinant DNA sequences generated by PCR amplification. Mol Biol Evol 14: 592.
59. Sato A, Felipe Figueroa, Colm O'hUigin, Nicole Steck, Jan Klein (1998) Cloning of major histocompatibility complex (MHC) genes from threespine stickleback, Gasterosteus aculeatus. Mol Mar Biol Biotechnol 7: 221-231.
60. Dijkstra JM, Grimholt U, Leong J, Koop BF, Hashimoto K (2013) Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol Biol 13: 260.
61. Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E, et al. (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484: 55-61.
62. Kurtz J, Kalbe M, Aeschlimann PB, Häberli MA, Wegner KM, et al. (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc B 271: 197-204. (Pubitemid 38121766)
63. Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci - Implications for evolutionary analysis. Gene 427: 117-123.
64. Prosperi MCF, De Luca A, Di Giambenedetto S, Bracciale L, Fabbiani M, et al. (2010) The threshold bootstrap clustering: a new approach to find families or transmission clusters within molecular quasispecies. PLoS One 5: e13619.
65. Kanagawa T (2003) Bias and artifacts in multitemplate polymerase chain reactions (PCR). J Biosci Bioeng 96: 317-323.
66. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20: 2317-2319. (Pubitemid 39341624)
67. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
68. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21: 494-504.
69. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289-290. (Pubitemid 38195693)
70. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685-695.
71. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
72. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Meth Ecol Evol 3: 89-101.
73. Wang Y, Naumann U, Wright ST, Warton DI (2012) mvabund- an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3: 471-474.
74. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
75. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
76. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Methodol: 289-300.
77. Reusch TBH, Haberli M, Aeschlimann PB, Milinski M (2001) Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature 414: 300-302. (Pubitemid 33097804)
78. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16: 224-232. (Pubitemid 36261053)
79. Berner D, Grandchamp A, Hendry AP (2009) Variable progress toward ecological speciation in parapatry: stickleback across eight lake-stream transitions. Evolution 63: 1740-1753.
80. Promerová M, Králová T, Bryjová A, Albrecht T, Bryja J (2013) MHC class IIB exon 2 polymorphism in the grey partridge (perdix perdix) is shaped by selection, recombination and gene conversion. PLoS ONE 8: e69135.
81. Hermel E, Yuan J, Monaco JJ (1995) Characterization of polymorphism within the H2-M MHC class II loci. Immunogenetics 42: 136.
82. Richman AD, Herrera FA, Nash D, Schierup MH (2003) Relative roles of mutation and recombination in generating allelic polymorphism at an MHC class II locus in Peromyscus maniculatus. Genet Res 82: 89-99. (Pubitemid 37527160)
83. Spurgin LG, Van Oosterhout C, Illera JC, Bridgett S, Gharbi K, et al. (2011) Gene conversion rapidly generates major histocompatibility complex diversity in recently founded bird populations. Mol Ecol 20: 5213-5225.
84. Zagordi O, Geyrhofer L, Roth V, Beerenwinkel N (2010) Deep sequencing of a genetically heterogeneous sample: local haplotype reconstruction and read error correction. J Comput Biol 17: 417-428.
85. Zagordi O, Klein R, Däumer M, Beerenwinkel N (2010) Error correction of next-generation sequencing data and reliable estimation of HIV quasispecies. Nucl Acids Res 38: 7400-7409.
86. Pavey SA, Sevellec M, Adam W, Normandeau E, Lamaze FC, et al. (2013) Nonparallelism in MHCIIb diversity accompanies nonparallelism in pathogen infection of lake whitefish (Coregonus clupeaformis) species pairs as revealed by next-generation sequencing. Mol Ecol 22: 3833-3849.