Detailed analysis of sequence changes occurring during vlsE antigenic variation in the mouse model of Borrelia burgdorferi infection

PLoS Pathogens

Volumn 5, Issue 2, 2009, Pages

  Coutte, Loïc ^a,b   Botkin, Douglas J ^a   Gao, Lihui ^a   Norris, Steven J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b INSTITUT DE BIOLOGIE DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEIN; LIPOPROTEIN VLSE; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; VLSE PROTEIN, BORRELIA BURGDORFERI;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGENIC VARIATION; ARTICLE; BLADDER; CODON; CONTROLLED STUDY; EAR; FEMALE; GENE CASSETTE; GENE LOCUS; HEART; IN VIVO STUDY; JOINT; LYME DISEASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; SCID MOUSE; SEQUENCE ANALYSIS; SKIN; STOP CODON; UNINDEXED SEQUENCE; ANIMAL; BORRELIA BURGDORFERI; C3H MOUSE; CHEMISTRY; DISEASE MODEL; DNA SEQUENCE; GENE EXPRESSION; GENETIC RECOMBINATION; GENETICS; IMMUNOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE MUTANT; STATISTICAL ANALYSIS;

ANIMALIA; BORRELIA; BORRELIA BURGDORFERI; MAMMALIA; MUS;

ANIMALS; ANTIGENIC VARIATION; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; DATA INTERPRETATION, STATISTICAL; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; LIPOPROTEINS; LYME DISEASE; MICE; MICE, INBRED C3H; MICE, SCID; MOLECULAR SEQUENCE DATA; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN;

EID: 61449110987     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000293     Document Type: Article

References (54)

1. Steere AC, Coburn J, Glickstein L (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
2. Craft JE, Grodzicki RL, ShresthaM, Fischer DK, Garcia-Blanco M, et al. (1984) The antibody response in Lyme disease. Yale J Biol Med 57: 561-565.
3. Craft JE, Grodzicki RL, Steere AC (1984) Antibody response in Lyme disease: evaluation of diagnostic tests. J Infect Dis 149: 789-795.
4. Dressler F, Whalen JA, Reinhardt BN, Steere AC (1993) Western blotting in the serodiagnosis of Lyme disease. J Infect Dis 167: 392-400.
5. Feder HM Jr, Gerber MA, Luger SW, Ryan RW (1992) Persistence of serum antibodies to Borrelia burgdorferi in patients treated for Lyme disease. Clin Infect Dis 15: 788-793.
6. Hilton E, Tramontano A, DeVoti J, Sood SK (1997) Temporal study of immunoglobin M seroreactivity to Borrelia burgdorferi in patients treated for Lyme borreliosis. J Clin Micro 35: 774-776.
7. van der Woude MW, Bäumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581-611.
8. Gitelman AK, Kaverin NV, Kharitonenkov IG, Rudneva IA, Zhdanov VM (1984) Changes in the antigenic specificity of influenza hemagglutinin in the course of adaptation to mice. Virology 134: 230-232.
9. Johnson WE, Desrosiers RC (2002) Viral persistence: HIV's strategies of immune system evasion. Annual Review of Medicine 53: 499-518.
10. Zhang QY, DeRyckere D, Lauer P, Koomey M (1992) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Nat Acad Sci USA 89: 5366-5370.
11. Noormohammadi AH, Markham PF, Kanci A, Whithear KG, Browning GF (2000) A novel mechanism for control of antigenic variation in the haemagglutinin gene family of Mycoplasma synoviae. Mol Microbiol 35: 911-923.
12. Denison AM, Clapper B, Dybvig K (2005) Avoidance of the host immune system through phase variation in Mycoplasma pulmonis. Infect Immun 73: 2033-2039.
13. Brayton KA, Palmer GH, Lundgren A, Yi J, Barbet AF (2002) Antigenic variation of Anaplasma marginale msp2 occurs by combinatorial gene conversion. Mol Microbiol 43: 1151-1159.
14. Zhang JR, Norris SJ (1998) Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun 66: 3698-3704.
15. Restrepo BI, Barbour AG (1994) Antigen diversity in the bacterium B. hermsii through "somatic" mutations in rearranged vmp genes. Cell 78: 867-876.
16. Dai Q, Restrepo BI, Porcella SF, Raffel SJ, Schwan TG, et al. (2006) Antigenic variation by Borrelia hermsii occurs through recombination between extragenic repetitive elements on linear plasmids. Mol Microbiol 60: 1329-1343.
17. 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.
18. Harrington CS, Thomson-Carter FM, Carter PE (1997) Evidence for recombination in the flagellin locus of Campylobacter jejuni: implications for the flagellin gene typing scheme. J Clin Microbiol 35: 2386-2392.
19. De Las Penas A, Pan S-J, Castano I, Alder J, Cregg R, et al. (2003) Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev 17: 2245-2258.
20. Dzikowski R, Templeton TJ, Deitsch K (2006) Variant antigen gene expression in malaria. Cellular Microbiology 8: 1371-1381.
21. Taylor JE, Rudenko G (2006) Switching trypanosome coats: what's in the wardrobe? Trends in Genetics 22: 614-620.
22. 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.
23. 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. Mol Microbiol 65: 1547-1558.
24. Lawrenz MB, Wooten RM, Norris SJ (2004) Effects of vlsE complementation on the infectivity of Borrelia burgdorferi lacking the linear plasmid lp28-1. Infect Immun 72: 6577-6585.
25. Zhang JR, Norris SJ (1998) Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun 66: 3689-3697.
26. Labandeira-Rey M, Baker E, Skare J (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69: 446-455.
27. Purser JE, Norris SJ (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97: 13865-13870.
28. Embers ME, Liang FT, Howell JK, Jacobs MB, Purcell JE, et al. (2007) Antigenicity and recombination of VlsE, the antigenic variation protein of Borrelia burgdorferi, in rabbits, a host putatively resistant to long-term infection with this spirochete. FEMS Immunol Med Microbiol 50: 421-429.
29. Indest KJ, Howell JK, Jacobs MB, Scholl-Meeker D, Norris SJ, et al. (2001) Analysis of Borrelia burgdorferi vlsE gene expression and recombination in the tick vector. Infect Immun 69: 7083-7090.
30. Ohnishi J, Schneider B, Messer WB, Piesman J, de Silva AM (2003) Genetic variation at the vlsE locus of Borrelia burgdorferi within ticks and mice over the course of a single transmission cycle. J Bacteriol 185: 4432-4441.
31. 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. J Biol Chem 277: 21691-21696.
32. 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. Infect Immun 70: 4196-4203.
33. Labandeira-Rey M, Seshu J, Skare JT (2003) The absence of linear plasmid 25 or 28-1 of Borrelia burgdorferi dramatically alters the kinetics of experimental infection via distinct mechanisms. Infect Immun 71: 4608-4613.
34. Knight SW, Kimmel BJ, Eggers CH, Samuels DS (2000) Disruption of the Borrelia burgdorferi gac gene, encoding the naturally synthesized GyrA C-terminal domain. J Bacteriol 182: 2048-2051.
35. Sung SY, McDowell JV, Marconi RT (2001) Evidence for the contribution of point mutations to vlsE variation and for apparent constraints on the net accumulation of sequence changes in vlsE during infection with Lyme disease spirochetes. J Bacteriol 183: 5855-5861.
36. Anguita J, Thomas V, Samanta S, Persinski R, Hernanz C, et al. (2001) Borrelia burgdorferi-induced inflammation facilitates spirochete adaptation and variable major protein-like sequence locus recombination. J Immunol 167: 3383-3390.
37. Denis M, Campbell D, Gregg EO (1991) Interleukin-2 and granulocyte-macrophage colony-stimulating factor stimulate growth of a virulent strain of Escherichia coli. Infect Immun 59: 1853-1856.
38. Bermudez LE, Petrofsky M, Shelton K (1996) Epidermal growth factor-binding protein in Mycobacterium avium and Mycobacterium tuberculosis: a possible role in the mechanism of infection. Infect Immun 64: 2917-2922.
39. Hall BS, Pereira MA (2000) Dual role for transforming growth factor beta - dependent signaling in Trypanosoma cruzi infection of mammalian cells. Infect Immun 68: 2077-2081.
40. Purser JE, Lawrenz MB, Caimano MJ, Howell JK, Radolf JD, et al. (2003) A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48: 753-764.
41. Xu Q, Seemanapalli SV, Lomax L, McShan K, Li X, et al. (2005) Association of linear plasmid 28-1 with an arthritic phenotype of Borrelia burgdorferi. Infect Immun 73: 7208-7215.
42. Cadavid D, Pachner AR, Estanislao L, Patalapati R, Barbour AG (2001) Isogenic serotypes of Borrelia turicatae show different localization in the brain and skin of mice. Infect Immun 69: 3389-3397.
43. Pennington PM, Cadavid D, Barbour AG (1999) Characterization of VspB of Borrelia turicatae, a major outer membrane protein expressed in blood and tissues of mice. Infect Immun 67: 4637-4645.
44. Criss AK, Kline KA, Seifert HS (2005) The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Molec Microbiol 58: 510-519.
45. Allred DR, Al-Khedery B (2004) Antigenic variation and cytoadhesion in Babesia bovis and Plasmodium falciparum: different logics achieve the same goal. Mol Biochem Parasitol 134: 27-35.
46. Hagblom P, Segal E, Billyard E, So M (1985) Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315: 156-158.
47. Haas R, Meyer TF (1986) The repertoire of silent pilus genes in Neisseria gonorrhoeae: evidence for gene conversion. Cell 44: 107-115.
48. Serkin CD, Seifert HS (1998) Frequency of pilin antigenic variation in Neisseria gonorrhoeae. J Bacteriol 180: 1955-1958.
49. Howell-Adams B, Seifert HS (2000) Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37: 1146-1158.
50. Alugupalli KR, Gerstein RM, Chen J, Szomolanyi-Tsuda E, Woodland RT, et al. (2003) The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J Immunol 170: 3819-3827.
51. Liang FT, Yan J, Mbow ML, Sviat SL, Gilmore RD, et al. (2004) Borrelia burgdorferi changes its surface antigenic expression in response to host immune responses. Infect Immun 72: 5759-5767.
52. Barbour AG (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
53. 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. Infect Immun 63: 2206-2212.
54. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.