Central role of the holliday junction helicase RuvAB in vlsE recombination and infectivity of Borrelia burgdorferi

PLoS Pathogens

Volumn 5, Issue 12, 2009, Pages

  Lin, Tao ^a   Gao, Lihui ^a   Edmondson, Diane G ^a   Jacobs, Mary B ^b   Philipp, Mario T ^b   Norris, Steven J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE RUVA; HELICASE RUVB; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN VLSE; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; HELICASE; LIPOPROTEIN; RUVB PROTEIN, BACTERIA; VLSE PROTEIN, BORRELIA BURGDORFERI;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGENIC VARIATION; ARTICLE; BACTERIAL GENETICS; BACTERIAL SURVIVAL; BORRELIA BURGDORFERI; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; DNA SEQUENCE; FEMALE; GENE MUTATION; GENETIC COMPLEMENTATION; HOLLIDAY JUNCTION; IMMUNE RESPONSE; IMMUNOCOMPETENCE; INOCULATION; LYME DISEASE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SCREENING; TICK; TRANSPOSON; ANIMAL; CLUSTER ANALYSIS; DNA DAMAGE; ENZYMOLOGY; GENETIC RECOMBINATION; GENETICS; IXODES; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; MUTATION; PATHOGENICITY; PHYSIOLOGY;

BORRELIA BURGDORFERI; MAMMALIA; MUS; PROTOZOA;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CLUSTER ANALYSIS; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA TRANSPOSABLE ELEMENTS; GENETIC COMPLEMENTATION TEST; IXODES; LIPOPROTEINS; MICE; MICE, SCID; MUTATION; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RECOMBINATION, GENETIC;

EID: 74549129395     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000679     Document Type: Article

References (63)

1. Steere AC, Coburn J, Glickstein L (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
2. Lane RS, Piesman J, Burgdorfer W (1991) Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu Rev Entomol 36: 587-609.
3. van der Woude MW, Bäumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17: 581-611.
4. Wisniewski-Dye F, Vial L (2008) Phase and antigenic variation mediated by genome modifications. Antonie Van Leeuwenhoek 94: 493-515.
5. 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. Mol Microbiol 47: 1407-1417.
6. 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.
7. Wang G, van Dam AP, Dankert J (2001) Analysis of a VMP-like sequence (vls) locus in Borrelia garinii and Vls homologues among four Borrelia burgdorferi sensu lato species. FEMS Microbiol Lett 199: 39-45.
8. Kawabata H, Myouga F, Inagaki Y, Murai N, Watanabe H (1998) Genetic and immunological analyses of Vls (VMP-like sequences) of Borrelia burgdorferi. Microb Pathog 24: 155-166.
9. Göttner G, Schulte-Spechtel U, Wilske B (2004) Heterogeneity of the immunodominant surface protein VlsE among the three genospecies of Borrelia burgdorferi pathogenic for humans. Int J Med Microbiol 293 Suppl 37: 172-173.
10. Zhang JR, Norris SJ (1998) Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun 66: 3698-3704.
11. 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.
12. 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.
13. 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.
14. 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.
15. Purser JE, Norris SJ (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97: 13865-13870.
16. Grimm D, Eggers CH, Caimano MJ, Tilly K, Stewart PE, et al. (2004) Experimental assessment of the roles of linear plasmids lp25 and lp28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect Immun 72: 5938-5946.
17. 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.
18. 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.
19. 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.
20. 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.
21. Nosbisch LK, de Silva AM (2007) Lack of detectable variation at Borrelia burgdorferi vlsE locus in ticks. J Med Entomol 44: 168-170.
22. Zhang JR, Norris SJ (1998) Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun 66: 3689-3697.
23. Norris SJ (2006) Antigenic variation with a twist - the Borrelia story. Mol Microbiol 60: 1319-1322.
24. 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.
25. Crother TR, Champion CI, Wu XY, Blanco DR, Miller JN, et al. (2003) Antigenic composition of Borrelia burgdorferi during infection of SCID mice. Infect Immun 71: 3419-3428.
26. Crother TR, Champion CI, Whitelegge JP, Aguilera R, Wu XY, et al. (2004) Temporal analysis of the antigenic composition of Borrelia burgdorferi during infection in rabbit skin. Infect Immun 72: 5063-5072.
27. Mehr IJ, Seifert HS (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation and DNA repair. Mol Microbiol 30: 697-710.
28. Skaar EP, Lazio MP, Seifert HS (2002) Roles of the recJ and recN genes in homologous recombination and DNA repair pathways of Neisseria gonorrhoeae. J Bacteriol 184: 919-927.
29. Kline KA, Sechman EV, Skaar EP, Seifert HS (2003) Recombination, repair and replication in the pathogenic Neisseriae: the 3 R's of molecular genetics of two human-specific bacterial pathogens. Mol Microbiol 50: 3-13.
30. Sechman EV, Kline KA, Seifert HS (2006) Loss of both Holliday junction processing pathways is synthetically lethal in the presence of gonococcal pilin antigenic variation. Mol Microbiol 61: 185-193.
31. Liveris D, Mulay V, Sandigursky S, Schwartz I (2008) Borrelia burgdorferi vlsE antigenic variation is not mediated by RecA. Infect Immun 76: 4009-4018.
32. Dresser AR, Hardy P-O, Chaconas G (2009) Investigation of the role of DNA replication, recombination and repair genes on antigenic switching at the vlsE locus in Borrelia burgdorferi. PLoS Pathog 5: e1000680. doi:10.1371/journal.ppat. 1000680.
33. Kawabata H, Norris SJ, Watanabe H (2004) BBE02 disruption mutants of Borrelia burgdorferi B31 have a highly transformable, infectious phenotype. Infect Immun 72: 7147-7154.
34. Boursaux-Eude C, Margarita D, Belfaiza J, Old IG, Saints Girons I (1998) Homologues of helicase genes priA and ruvAB of Borrelia burgdorferi, the Lyme borreliosis agent. Res Microbiol 149: 235-245.
35. Frank KL, Bundle SF, Kresge ME, Eggers CH, Samuels DS (2003) aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 185: 6723-6727.
36. Iwasaki H, Takahagi M, Nakata A, Shinagawa H (1992) Escherichia coli RuvA and RuvB proteins specifically interact with Holliday junctions and promote branch migration. Genes Dev 6: 2214-2220.
37. Parsons CA, Tsaneva I, Lloyd RG, West SC (1992) Interaction of Escherichia coli RuvA and RuvB proteins with synthetic Holliday junctions. Proc Natl Acad Sci U S A 89: 5452-5456.
38. Shiba T, Iwasaki H, Nakata A, Shinagawa H (1991) SOS-inducible DNA repair proteins, RuvA and RuvB, of Escherichia coli: functional interactions between RuvA and RuvB for ATP hydrolysis and renaturation of the cruciform structure in supercoiled DNA. Proc Natl Acad Sci U S A 88: 8445-8449.
39. Connolly B, Parsons CA, Benson FE, Dunderdale HJ, Sharples GJ, et al. (1991) Resolution of Holliday junctions in vitro requires the Escherichia coli ruvC gene product. Proc Natl Acad Sci U S A 88: 6063-6067.
40. Aravind L, Makarova KS, Koonin EV (2000) Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories. Nucleic Acids Res 28: 3417-3432.
41. Lloyd RG, Benson FE, Shurvinton CE (1984) Effect of ruv mutations on recombination and DNA repair in Escherichia coli K12. Mol Gen Genet 194: 303-309.
42. Stacey KA, Lloyd RG (1976) Isolation of Rec2 mutants from an F-prime merodiploid strain of Escherichia coli K-12. Mol Gen Genet 143: 223-232.
43. Otsuji N, Iyehara H, Hideshima Y (1974) Isolation and characterization of an Escherichia coli ruv mutant which forms nonseptate filaments after low doses of ultraviolet light irradiation. J Bacteriol 117: 337-344.
44. Courcelle J, Hanawalt PC (2001) Participation of recombination proteins in rescue of arrested replication forks in UV-irradiated Escherichia coli need not involve recombination. Proc Natl Acad Sci U S A 98: 8196-8202.
45. Pavel P, Khil R, Camerini-Otero D (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microbiol 44: 89-105.
46. Goodman MF (2002) Error-prone repair DNA polymerases in prokaryotes and eukaryotes. Ann Rev Biochem 71: 17-50.
47. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
48. Liveris D, Mulay V, Schwartz I (2004) Functional properties of Borrelia burgdorferi recA. J Bacteriol 186: 2275-2280.
49. Dresser AR, Hardy P-O, Chaconas G (2009) Investigation of the role of DNA replication, recombination and repair genes in antigenic switching at the vlsE locus in Borrelia burgdorferi: an essential role for the RuvAB branch migrase. Submitted.
50. Wang TF, Chen LT, Wang AH (2008) Right or left turn? RecA family protein filaments promote homologous recombination through clockwise axial rotation. Bioessays 30: 48-56.
51. 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.
52. Palmer GH, Brayton KA (2007) Gene conversion is a convergent strategy for pathogen antigenic variation. Trends Parasitol 23: 408-413.
53. 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.
54. Barbour AG, Restrepo BI (2000) Antigenic variation in vector-borne pathogens. Emerg Infect Dis 6: 449-457.
55. Barbour AG, Dai Q, Restrepo BI, Stoenner HG, Frank SA (2006) Pathogen escape from host immunity by a genome program for antigenic variation. Proc Natl Acad Sci U S A 103: 18290-18295.
56. Futse JE, Brayton KA, Knowles DP Jr, Palmer GH (2005) Structural basis for segmental gene conversion in generation of Anaplasma marginale outer membrane protein variants. Mol Microbiol 57: 212-221.
57. 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.
58. Barbour AG (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
59. Stewart PE, Hoff J, Fischer E, Krum JG, Rosa PA (2004) Genome-wide transposon mutagenesis of Borrelia burgdorferi for identification of phenotypic mutants. Appl Environ Microbiol 70: 5973-5979.
60. Samuels DS (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
61. Lawrenz MB, Hardham JM, Owens RT, Nowakowski J, Steere AC, et al. (1999) Human antibody responses to VlsE antigenic variation protein of Borrelia burgdorferi. J Clin Microbiol 37: 3997-4004.
62. Jacobs MB, Purcell JE, Philipp MT (2003) Ixodes scapularis ticks (Acari: Ixodidae) from Louisiana are competent to transmit Borrelia burgdorferi, the agent of Lyme borreliosis. J Med Entomol 40: 964-967.
63. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-469.