Mosaic VSGs and the Scale of Trypanosoma brucei Antigenic Variation

PLoS Pathogens

Volumn 9, Issue 7, 2013, Pages

  Hall, James P J ^a   Wang, Huanhuan ^a   David Barry, J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; VARIANT SURFACE GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGENIC VARIATION; ARTICLE; CONTROLLED STUDY; DISEASE TRANSMISSION; DNA SEQUENCE; FEMALE; GENE CONVERSION; IMMUNOFLUORESCENCE; MASS SPECTROMETRY; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TRYPANOSOMA BRUCEI; TRYPANOSOMIASIS;

EID: 84884800658     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003502     Document Type: Article

References (58)

1. Deitsch KW, Lukehart S, Stringer J, (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7: 493-503 doi:10.1038/nrmicro2145.
2. Ueti MW, Tan Y, Broschat SL, Ortiz EJC, Camacho-Nuez M, et al. (2012) Expansion of Variant Diversity Associated with a High Prevalence of Pathogen Strain Superinfection under Conditions of Natural Transmission. Infect Immun 80: 2354-2360 doi:10.1128/IAI.00341-12.
3. Morrison LJ, Marcello L, McCulloch R, (2009) Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cell Microbiol 11: 1724-1734 doi:10.1111/j.1462-5822.2009.01383.x.
4. Schwede A, Carrington M, (2010) Bloodstream form Trypanosome plasma membrane proteins: antigenic variation and invariant antigens. Parasitology 137: 2029-2039 doi:10.1017/S0031182009992034.
5. Schwede A, Jones N, Engstler M, Carrington M, (2011) The VSG C-terminal domain is inaccessible to antibodies on live trypanosomes. Mol Biochem Parasitol 175: 201-204 doi:10.1016/j.molbiopara.2010.11.004.
6. Hsia R, Beals TP, Boothroyd JC, (1996) Use of chimeric recombinant polypeptides to analyse conformational, surface epitopes on trypanosome variant surface glycoproteins. Mol Microbiol 19: 53-63.
7. Robinson NP, Burman N, Melville SE, Barry JD, (1999) Predominance of duplicative VSG gene conversion in antigenic variation in African trypanosomes. Mol Cell Biol 19: 5839-5846.
8. Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, et al. (2005) The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422 doi:10.1126/science.1112642.
9. Wickstead B, Ersfeld K, Gull K, (2004) The small chromosomes of Trypanosoma brucei involved in antigenic variation are constructed around repetitive palindromes. Genome Res 14: 1014-1024 doi:10.1101/gr.2227704.
10. Gjini E, Haydon DT, Barry JD, Cobbold CA, (2010) Critical interplay between parasite differentiation, host immunity, and antigenic variation in trypanosome infections. Am Nat 176: 424-439 doi:10.1086/656276.
11. Marcello L, Barry JD, (2007) Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure. Genome Res 17: 1344-1352 doi:10.1101/gr.6421207.
12. MacGregor P, Savill NJ, Hall D, Matthews KR, (2011) Transmission Stages Dominate Trypanosome Within-Host Dynamics during Chronic Infections. Cell Host Microbe 9: 310-318 doi:10.1016/j.chom.2011.03.013.
13. Futse JE, Brayton KA, Dark MJ, Knowles DP, Palmer GH, (2008) Superinfection as a driver of genomic diversification in antigenically variant pathogens. Proc Natl Acad Sci USA 105: 2123-2127 doi:10.1073/pnas.0710333105.
14. 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 Pathog 5: e1000293 doi:10.1371/journal.ppat.1000293.
15. Criss AK, Kline KA, Seifert HS, (2005) The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 58: 510-519 doi:10.1111/j.1365-2958.2005.04838.x.
16. Giacani L, Molini BJ, Kim EY, Godornes BC, Leader BT, et al. (2010) Antigenic Variation in Treponema pallidum: TprK Sequence Diversity Accumulates in Response to Immune Pressure during Experimental Syphilis. J Immunol 184: 3822-3829 doi:10.4049/jimmunol.0902788.
17. 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 doi:10.1111/j.1365-2958.2007.05898.x.
18. Al-Khedery B, Allred DR, (2006) Antigenic variation in Babesia bovis occurs through segmental gene conversion of the ves multigene family, within a bidirectional locus of active transcription. Mol Microbiol 59: 402-414 doi:10.1111/j.1365-2958.2005.04993.x.
19. Zhuang Y, Futse JE, Brown WC, Brayton KA, Palmer GH, (2007) Maintenance of antibody to pathogen epitopes generated by segmental gene conversion is highly dynamic during long-term persistent infection. Infect Immun 75: 5185-5190 Available: http://eutils.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&id=17785476&retmode=ref&cmd=prlinks.
20. Michels PA, Liu AY, Bernards A, Sloof P, Van der Bijl MM, et al. (1983) Activation of the genes for variant surface glycoproteins 117 and 118 in Trypanosoma brucei. J Mol Biol 166: 537-556.
21. Aline RF, Myler PJ, Gobright E, Stuart KD, (1994) Early expression of a Trypanosoma brucei VSG gene duplicated from an incomplete basic copy. J Eukaryot Microbiol 41: 71-78.
22. Roth CW, Bringaud F, Layden RE, Baltz T, Eisen H, (1989) Active late-appearing variable surface antigen genes in Trypanosoma equiperdum are constructed entirely from pseudogenes. Proc Natl Acad Sci USA 86: 9375-9379.
23. Thon G, Baltz T, Giroud C, Eisen H, (1990) Trypanosome variable surface glycoproteins: composite genes and order of expression. Genes Dev 4: 1374-1383.
24. Kamper SM, Barbet AF, (1992) Surface epitope variation via mosaic gene formation is potential key to long-term survival of Trypanosoma brucei. Mol Biochem Parasitol 53: 33-44.
25. Marcello L, Barry JD, (2007) From silent genes to noisy populations-dialogue between the genotype and phenotypes of antigenic variation. J Eukaryot Microbiol 54: 14-17 doi:10.1111/j.1550-7408.2006.00227.x.
26. Barry JD, Marcello L, Morrison LJ, Read AF, Lythgoe K, et al. (2005) What the genome sequence is revealing about trypanosome antigenic variation. Biochem Soc Trans 33: 986-989 doi:10.1042/BST20050986.
27. Marcello L, Menon S, Ward P, Wilkes JM, Jones NG, et al. (2007) VSGdb: a database for trypanosome variant surface glycoproteins, a large and diverse family of coiled coil proteins. BMC Bioinformatics 8: 143 doi:10.1186/1471-2105-8-143.
28. Zhang Z, Schwartz S, Wagner L, Miller W, (2000) A Greedy Algorithm for Aligning DNA Sequences. Journal of Computational Biology 7: 203-214 doi:10.1089/10665270050081478.
29. Pays E, Houard S, Pays A, Van Assel S, Dupont F, et al. (1985) Trypanosoma brucei: the extent of conversion in antigen genes may be related to the DNA coding specificity. Cell 42: 821-829.
30. Aline RF, Stuart K, (1989) Trypanosoma brucei: conserved sequence organization 3′ to telomeric variant surface glycoprotein genes. Exp Parasitol 68: 57-66.
31. Leinster T, Cobbold CA, (2012) Measuring diversity: the importance of species similarity. Ecology 93: 477-489.
32. Chao A, (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783-791.
33. Morrison LJ, Majiwa P, Read AF, Barry JD, (2005) Probabilistic order in antigenic variation of Trypanosoma brucei. Int J Parasitol 35: 961-972 doi:10.1016/j.ijpara.2005.05.004.
34. Turner C, Barry J, (1989) High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology 99: 67-75.
35. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9: 40 doi:10.1186/1471-2105-9-40.
36. Kelley LA, Sternberg MJE, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371 doi:10.1038/nprot.2009.2.
37. Barry JD, (1986) Antigenic variation during Trypanosoma vivax infections of different host species. Parasitology 92 (Pt 1) (): 51-65.
38. Morrison WI, Black SJ, Paris J, Hinson CA, Wells PW, (1982) Protective immunity and specificity of antibody responses elicited in cattle by irradiated Trypanosoma brucei. Parasite Immunol 4: 395-407.
39. MacGregor P, Szöo{double acute}r B, Savill NJ, Matthews KR, (2012) Trypanosomal immune evasion, chronicity and transmission: an elegant balancing act. Nat Rev Microbiol 10: 431-8 doi:10.1038/nrmicro2779.
40. Wang CW, Hermsen CC, Sauerwein RW, Arnot DE, Theander TG, et al. (2009) The Plasmodium falciparum var gene transcription strategy at the onset of blood stage infection in a human volunteer. Parasitol Int 58: 478-480 doi:10.1016/j.parint.2009.07.004.
41. Vink C, Rudenko G, Seifert HS, (2011) Microbial antigenic variation mediated by homologous DNA recombination. FEMS Microbiol Rev [Epub ahead of print] doi:10.1111/j.1574-6976.2011.00321.x.
42. Futse JE, Brayton KA, Knowles DP, Palmer GH, (2005) Structural basis for segmental gene conversion in generation of Anaplasma marginale outer membrane protein variants. Mol Microbiol 57: 212-221 doi:10.1111/j.1365-2958.2005.04670.x.
43. Field MC, Sergeenko T, Wang Y-N, Böhm S, Carrington M, (2010) Chaperone requirements for biosynthesis of the trypanosome variant surface glycoprotein. PLoS ONE 5: e8468 doi:10.1371/journal.pone.0008468.
44. Barnes RL, McCulloch R, (2007) Trypanosoma brucei homologous recombination is dependent on substrate length and homology, though displays a differential dependence on mismatch repair as substrate length decreases. Nucleic Acids Res 35: 3478-3493 doi:10.1093/nar/gkm249.
45. Pays E, Van Assel S, Laurent M, Darville M, Vervoort T, et al. (1983) Gene conversion as a mechanism for antigenic variation in trypanosomes. Cell 34: 371-381.
46. Radwanska M, Guirnalda P, De Trez C, Ryffel B, Black S, et al. (2008) Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog 4: e1000078 doi:10.1371/journal.ppat.1000078.
47. Engstler M, Pfohl T, Herminghaus S, Boshart M, Wiegertjes G, et al. (2007) Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131: 505-515 doi:10.1016/j.cell.2007.08.046.
48. La Greca F, Magez S, (2011) Vaccination against trypanosomiasis: can it be done or is the trypanosome truly the ultimate immune destroyer and escape artist? Hum Vaccin 7: 1225-1233 doi:10.4161/hv.7.11.18203.
49. Nei M, Rooney AP, (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152 doi:10.1146/annurev.genet.39.073003.112240.
50. Gjini E, Haydon DT, Barry JD, Cobbold CA, (2012) The impact of mutation and gene conversion on the local diversification of antigen genes in African trypanosomes. Mol Biol Evol 29: 3321-31 doi:10.1093/molbev/mss166.
51. Barry JD, Ginger ML, Burton P, McCulloch R, (2003) Why are parasite contingency genes often associated with telomeres? Int J Parasitol 33: 29-45.
52. Barry JD, Hall JPJ, Plenderleith L, (2012) Genome hyperevolution and the success of a parasite. Ann N Y Acad Sci 1267: 11-17 doi:10.1111/j.1749-6632.2012.06654.x.
53. Caporale LH, (2012) Overview of the creative genome: effects of genome structure and sequence on the generation of variation and evolution. Ann N Y Acad Sci 1267: 1-10 doi:10.1111/j.1749-6632.2012.06749.x.
54. Jackson AP, Berry A, Aslett M, Allison HC, Burton P, et al. (2012) Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. Proc Natl Acad Sci USA 109: 3416 doi:10.1073/pnas.1117313109.
55. Oberle M, Balmer O, Brun R, Roditi I, (2010) Bottlenecks and the Maintenance of Minor Genotypes during the Life Cycle of Trypanosoma brucei. PLoS Pathog 6: e1001023 doi:10.1371/journal.ppat.1001023.
56. Peacock L, Cook S, Ferris V, Bailey M, Gibson W, (2012) The life cycle of Trypanosoma (Nannomonas) congolense in the tsetse fly. Parasites & vectors 5: 109 doi:10.1186/1756-3305-5-109.
57. McCulloch R, Rudenko G, Borst P, (1997) Gene conversions mediating antigenic variation in Trypanosoma brucei can occur in variant surface glycoprotein expression sites lacking 70-base-pair repeat sequences. Mol Cell Biol 17: 833-843.
58. Smith TK, Vasileva N, Gluenz E, Terry S, Portman N, et al. (2009) Blocking variant surface glycoprotein synthesis in Trypanosoma brucei triggers a general arrest in translation initiation. PLoS ONE 4: e7532 doi:10.1371/journal.pone.0007532.