Natural Selection Promotes Antigenic Evolvability

PLoS Pathogens

Volumn 9, Issue 11, 2013, Pages

  Graves, Christopher J ^a   Ros, Vera I D ^a   Stevenson, Brian ^b   Sniegowski, Paul D ^a   Brisson, Dustin ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; MEMBRANE ANTIGEN;

ANTIGENICITY; ARTICLE; BACTERIAL STRAIN; BORRELIA BURGDORFERI; GENE CASSETTE; GENE CONVERSION; GENETIC ANALYSIS; GENETIC VARIABILITY; IMMUNE RESPONSE; LYME DISEASE; MAXIMUM LIKELIHOOD METHOD; MOUSE; MUTATION RATE; NATURAL SELECTION; NEIGHBOR JOINING METHOD; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; TANDEM REPEAT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIGENS, BACTERIAL; BORRELIA BURGDORFERI; EVOLUTION, MOLECULAR; HUMANS; LYME DISEASE; SELECTION, GENETIC;

EID: 84888232449     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003766     Document Type: Article

References (61)

1. Sniegowski PD, Murphy HA, (2006) Evolvability. Current Biology 16: R831-R834.
2. Lynch M, (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. Proceedings of the National Academy of Sciences, USA 104 Suppl 1: 8597-8604.
3. Brookfield JF, (2001) Evolution: the evolvability enigma. Current Biology 11: R106-108.
4. Williams GC (1966) Adaptation and Natural Selection. Princeton, NJ: Princeton University Press.
5. Draghi J, Wagner GP, (2008) Evolution of evolvability in a developmental model. Evolution 62: 301-315.
6. Moxon ER, Rainey PB, Nowak MA, Lenski RE, (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24-33.
7. Plotkin JB, Dushoff J, (2003) Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc Natl Acad Sci U S A 100: 7152-7157.
8. Masel J, (2005) Evolutionary capacitance may be favored by natural selection. Genetics 170: 1359-1371.
9. Verstrepen KJ, Jansen A, Lewitter F, Fink GR, (2005) Intragenic tandem repeats generate functional variability. Nat Genet 37: 986-990.
10. Frank SA, (1996) Models of parasite virulence. Quarterly review of Biology 71: 37-78.
11. Frank SA, (1994) Kin selection and virulence in the evolution of protocells and parasites. Proc Biol Sci 258: 153-161.
12. Levin BR, Bull JJ, (1994) Short-sighted evolution and the virulence of pathogenic microorganisms. Trends in Microbiology 2: 76-81.
13. Ewald PW (1994) Evolution of infectious disease. Oxford University Press.
14. Frank SA, Schmid-Hempel P, (2008) Mechanisms of pathogenesis and the evolution of parasite virulence. Journal of Evolutionary Biology 21: 396-404.
15. Mrazek J, Guo X, Shah A, (2007) Simple sequence repeats in prokaryotic genomes. Proc Natl Acad Sci U S A 104: 8472-8477.
16. Bankhead T, Chaconas G, (2007) The role of VlsE antigenic variation in the Lyme disease spirochete: persistence through a mechanism that differs from other pathogens. Molecular Microbiology 65: 1547-1558.
17. Zhang JR, Norris SJ, (1998) Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infection and Immunity 66: 3689-3697.
18. Zhang JR, Hardham JM, Barbour AG, Norris SJ, (1997) Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89: 275-285.
19. Purser JE, Norris SJ, (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proceedings of the National Academy of Sciences of the United States of America U S A 97: 13865-13870.
20. Norris SJ, Howell JK, Garza SA, Ferdows MS, Barbour AG, (1995) High- and low-infectivity phenotypes of clonal populations of in vitro-cultured Borrelia burgdorferi. Infection and Immunity 63: 2206-2212.
21. Coutte L, Botkin DJ, Gao L, Norris SJ, (2009) Detailed analysis of sequence changes occurring during vlsE antigenic variation in the mouse model of Borrelia burgdorferi infection. PLoS Pathogens 5: e1000293.
22. Wang D, Botkin DJ, Norris SJ, (2003) Characterization of the vls antigenic variation loci of the Lyme disease spirochaetes Borrelia garinii Ip90 and Borrelia afzelii ACAI. Molecular Microbiology 47: 1407-1417.
23. Eicken C, Sharma V, Klabunde T, Lawrenz MB, Hardham JM, et al. (2002) Crystal structure of Lyme disease variable surface antigen VlsE of Borrelia burgdorferi. Journal of Biological Chemistry 277: 21691-21696.
24. McDowell JV, Sung SY, Hu LT, Marconi RT, (2002) Evidence that the variable regions of the central domain of VlsE are antigenic during infection with Lyme disease spirochetes. Infection and Immunity 70: 4196-4203.
25. Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu WG, Dunn JJ, et al. (2011) Whole-genome sequences of thirteen isolates of Borrelia burgdorferi. Journal of Bacteriology 193: 1018-1020.
26. Swanson WJ, Nielsen R, Yang Q, (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20: 18-20.
27. Yang Z, Nielsen R, Goldman N, Pedersen AM, (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431-449.
28. Santoyo G, Romero D, (2005) Gene conversion and concerted evolution in bacterial genomes. FEMS Microbiol Rev 29: 169-183.
29. Liao D, (2000) Gene conversion drives within genic sequences: concerted evolution of ribosomal RNA genes in bacteria and archaea. J Mol Evol 51: 305-317.
30. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW, (1983) The double-strand-break repair model for recombination. Cell 33: 25-35.
31. Wyman C, Ristic D, Kanaar R, (2004) Homologous recombination-mediated double-strand break repair. DNA Repair (Amst) 3: 827-833.
32. Lin T, Gao L, Edmondson DG, Jacobs MB, Philipp MT, et al. (2009) Central role of the Holliday junction helicase RuvAB in vlsE recombination and infectivity of Borrelia burgdorferi. PLoS Pathog 5: e1000679.
33. Zhang J-R, Norris SJ, (1998) Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infection and Immunity 66: 3698-3704.
34. Stevenson B, Bockenstedt LK, Barthold SW, (1994) Expression and gene sequence of outer surface protein C of Borrelia burgdorferi reisolated from chronically infected mice. Infection and Immunity 62: 3568-3571.
35. El Hage N, Lieto LD, Stevenson B, (1999) Stability of erp loci during Borrelia burgdorferi infection: recombination is not required for chronic infection of immunocompetent mice. Infect Immun 67: 3146-3150.
36. Bykowski T, Woodman ME, Cooley AE, Brissette CA, Wallich R, et al. (2008) Borrelia burgdorferi complement regulator-acquiring surface proteins (BbCRASPs): Expression patterns during the mammal-tick infection cycle. Int J Med Microbiol 298 Suppl 1: 249-256.
37. Hovius JW, van Dam AP, Fikrig E, (2007) Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol 23: 434-438.
38. Stevenson B, von Lackum K, Riley SP, Cooley AE, Woodman ME, et al. (2006) Evolving models of Lyme disease spirochete gene regulation. Wien Klin Wochenschr 118: 643-652.
39. Schwan TG, (2003) Temporal regulation of outer surface proteins of the Lyme-disease spirochaete Borrelia burgdorferi. Biochem Soc Trans 31: 108-112.
40. Kryazhimskiy S, Plotkin JB, (2008) The population genetics of dN/dS. PLoS Genet 4: e1000304.
41. Stern A, Doron-Faigenboim A, Erez E, Martz E, Bacharach E, et al. (2007) Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res 35: W506-511.
42. Bichara M, Wagner J, Lambert IB, (2006) Mechanisms of tandem repeat instability in bacteria. Mutat Res 598: 144-163.
43. Moxon R, Bayliss C, Hood D, (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40: 307-333.
44. Sniegowski PD, Gerrish PJ, Johnson T, Shaver A, (2000) The evolution of mutation rates: separating causes from consequences. Bioessays 22: 1057-1066.
45. Brunham RC, Plummer FA, Stephens RS, (1993) Bacterial antigenic variation, host immune response, and pathogen-host coevolution. Infection and Immunity 61: 2273-2276.
46. Deitsch KW, Moxon ER, Wellems TE, (1997) Shared themes of antigenic variation and virulence in bacterial, protozoal, and fungal infections. Microbiol Mol Biol Rev 61: 281-293.
47. Deitsch KW, Lukehart SA, Stringer JR, (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nature Reviews Microbiology 7: 493-503.
48. Kitten T, Barbour AG, (1990) Juxtaposition of expressed variable antigen genes with a conserved telomere in the bacterium Borrelia hermsii. Proc Natl Acad Sci U S A 87: 6077-6081.
49. Haas R, Meyer TF, (1986) The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44: 107-115.
50. Centurion-Lara A, LaFond RE, Hevner K, Godornes C, Molini BJ, et al. (2004) Gene conversion: a mechanism for generation of heterogeneity in the tprK gene of Treponema pallidum during infection. Mol Microbiol 52: 1579-1596.
51. Iverson-Cabral SL, Astete SG, Cohen CR, Totten PA, (2007) mgpB and mgpC sequence diversity in Mycoplasma genitalium is generated by segmental reciprocal recombination with repetitive chromosomal sequences. Mol Microbiol 66: 55-73.
52. Katoh K, Kuma K, Toh H, Miyata T, (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518.
53. Suyama M, Torrents D, Bork P, (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34: W609-612.
54. Nei M, Gojobori T, (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418-426.
55. Nei M, Kumar S (2000) Molecular Evolution and Phylogenetics. New York: Oxford University Press.
56. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731-9 doi: 10.1093/molbev/msr121.
57. Kolpakov R, Bana G, Kucherov G, (2003) mreps: Efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res 31: 3672-3678.
58. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
59. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, et al. (2010) Geneious v5.3 Available: http://www.geneious.com.
60. Barthold SW, Moody KD, Terwilliger GA, Duray PH, Jacoby RO, et al. (1988) Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J Infect Dis 157: 842-846.
61. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, et al. (2004) Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150: 1741-1755.