Molecular analysis of the channel-forming protein P13 and its paralogue family 48 from different Lyme disease Borrelia species

Microbiology

Volumn 150, Issue 3, 2004, Pages 549-559

  Pinne, Marija ^a   Östberg, Yngve ^a   Comstedt, Pär ^a   Bergström, Sven ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EPITOPE; PROTEIN P13; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM CULTURE; BORRELIA; BORRELIA BURGDORFERI; BORRELIA INFECTION; CHANNEL GATING; CONTROLLED STUDY; GENETIC HETEROGENEITY; GENETIC TRANSCRIPTION; IN VITRO STUDY; LYME DISEASE; MAMMAL; MOLECULAR BIOLOGY; MOLECULAR MODEL; MOUSE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PARALOGY; PLASMID; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SPECIES; SPECIES CULTIVATION;

ACARI; BORRELIA; BORRELIA BURGDORFERI; MAMMALIA;

EID: 1642268055     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.26728-0     Document Type: Review

References (68)

1. Akins, D. R., Caimano, M. J., Yang, X., Cerna, F., Norgard, M. V. & Radolf, J. D. (1999). Molecular and evolutionary analysis of Borrelia burgdorferi 297 circular plasmid-encoded lipoproteins with OspE- and OspF-like leader peptides. Infect Immun 67, 1526-1532.
2. Appel, R. D., Bairoch, A. & Hochstrasser, D. F. (1994). A new generation of information retrieval tools for biologists: the example of the ExPASy WWW server. Trends Biochem Sci 19, 258-260.
3. Aron, L., Alekshun, M., Perlee, L., Schwartz, I., Godfrey, H. P. & Cabello, F. C. (1994). Cloning and DNA sequence analysis of bmpC, a gene encoding a potential membrane lipoprotein of Borrelia burgdorferi. FEMS Microbiol Lett 123, 75-82.
4. Åsbrink, E., Hederstedt, B. & Hovmark, A. (1984). The spirochetal etiology of erythema chronicum migrans Afzelius. Acta Derm Venereol 64, 291-295.
5. Baranton, G., Marti Ras, N. & Postic, D. (1998). Molecular epidemiology of the aetiological agents of Lyme borreliosis. Wien Klin Wochenschr 110, 850-855.
6. Barbour, A. G. (1984). Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57, 521-525.
7. Barbour, A. G. (1988). Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent. J Clin Microbiol 26, 475-478.
8. Barbour, A. G. (1989). The molecular biology of Borrelia. Rev Infect Dis 11, Suppl 6, S1470-S1474.
9. Barthold, S. W., Moody, K. D., Terwilliger, G. A., Duray, P. H., Jacoby, R. O. & Steere, A. C. (1988). Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J Infect Dis 157, 842-846.
10. Bergström, S., Olsen, B., Burman, N., Gothefors, L., Jaenson, T. G., Jonsson, M. & Mejlon, H. A. (1992). Molecular characterization of Borrelia burgdorferi isolated from Ixodes ricinus in northern Sweden. Scand J Infect Dis 24, 181-188.
11. Bono, J. L., Elias, A. F., Kupko, J. J., 3rd, Stevenson, B., Tilly, K. & Rosa, P. (2000). Efficient targeted mutagenesis in Borrelia burgdorferi. J Bacteriol 182, 2445-2452.
12. Bunikis, J., Noppa, L., & Bergström, S. (1995). Molecular analysis of a 66-kDa protein associated with the outer membrane of Lyme disease Borrelia. FEMS Microbiol Lett 131, 139-145.
13. Bunikis, J., Olsen, B., Fingerle, V., Bonnedahl, J., Wilske, B. & Bergström, S. (1996). Molecular polymorphism of the Lyme disease agent Borrelia garinii in northern Europe is influenced by a novel enzootic Borrelia focus in the North Atlantic. J Clin Microbiol 34, 364-368.
14. Busch, U., Will, G., Hizo-Teufel, C., Wilske, B. & Preac-Mursic, V. (1997). Long-term in vitro cultivation of Borrelia burgdorferi sensu lato strains: influence on plasmid patterns, genome stability and expression of proteins. Res Microbiol 148, 109-118.
15. Carlyon, J. F., Roberts, D. M. & Marconi, R. T. (2000). Evolutionary and molecular analyses of the Borrelia bdr super gene family: delineation of distinct sub-families and demonstration of the genus wide conservation of putative functional domains, structural properties and repeat motifs. Microb Pathog 28, 89-105.
16. Carroll, J. A., El-Hage, N., Miller, J. C., Babb, K. & Stevenson, B. (2001). Borrelia burgdorferi RevA antigen is a surface-exposed outer membrane protein whose expression is regulated in response to environmental temperature and pH. Infect Immun 69, 5286-5293.
17. Casjens, S., Palmer, N., van Vugt, R. & 12 other authors (2000). A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35, 490-516.
18. Feng, S., Das, S., Barthold, S. W. & Fikrig, E. (1996). Characterization of two genes, p11 and p5, on the Borrelia burgdorferi 49-kilobase linear plasmid. Biochim Biophys Acta 1307, 270-272.
19. Fraser, C. M., Casjens, S., Huang, W. M. & 35 other authors (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586.
20. Fukunaga, M., Hamase, A., Okada, K. & Nakao, M. (1996). Borrelia tanukii sp. nov. and Borrelia turdae sp. nov. found from ixodid ticks in Japan: rapid species identification by 16S rRNA gene-targeted PCR analysis. Microbiol Immunol 40, 877-881.
21. Gorbacheva, V. Y., Godfrey, H. P. & Cabello, F. C. (2000). Analysis of the bmp gene family in Borrelia burgdorferi sensu lato. J Bacteriol 182, 2037-2042.
22. Grimm, D., Elias, A. F., Tilly, K. & Rosa, P. A. (2003). Plasmid stability during in vitro propagation of Borrelia burgdorferi assessed at a clonal level. Infect Immun 71, 3138-3145.
23. Hefty, P. S., Jolliff, S. E., Caimano, M. J., Wikel, S. K., Radolf, J. D. & Akins, D. R. (2001). Regulation of OspE-related, OspF-related, and Elp lipoproteins of Borrelia burgdorferi strain 297 by mammalian host-specific signals. Infect Immun 69, 3618-3627.
24. Hefty, P. S., Brooks, C. S., Jett, A. M., White, G. L., Wikel, S. K., Kennedy, R. C. & Akins, D. R. (2002). OspE-related, OspF-related, and Elp lipoproteins are immunogenic in baboons experimentally infected with Borrelia burgdorferi and in human Lyme disease patients. J Clin Microbiol 40, 4256-4265.
25. Kawabata, H., Masuzawa, T. & Yanagihara, Y. (1993). Genomic analysis of Borrelia japonica sp. nov. isolated from Ixodes ovatus in Japan. Microbiol Immunol 37, 843-848.
26. Kriuchechnikov, V. N., Korenberg, E. I., Shcherbakov, S. V., Kovalevskii lu, V. & Levin, M. L. (1988). Identification of Borrelia isolated in the USSR from Ixodes persulcatus Schulze ticks. Zh Mikrobiol Epidemiol Immunobiol 12, 41-44.
27. Labandeira-Rey, M. & Skare, J. T. (2001). Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69, 446-455.
28. Labandeira-Rey, M., Baker, E. A. & Skare, J. T. (2001). VraA (BBI16) protein of Borrelia burgdorferi is a surface-exposed antigen with a repetitive motif that confers partial protection against experimental Lyme borreliosis. Infect Immun 69, 1409-1419.
29. Le Fleche, A., Postic, D., Girardet, K., Peter, O. & Baranton, G. (1997). Characterization of Borrelia lusitaniae sp. nov. by 16S ribosomal DNA sequence analysis. Int J Syst Bacteriol 47, 921-925.
30. Magnarelli, L. A., Anderson, J. F. & Barbour, A. G. (1989). Enzyme-linked immunosorbent assays for Lyme disease: reactivity of subunits of Borrelia burgdorferi. J Infect Dis 159, 43-49.
31. McDowell, J. V., Sung, S. Y., Labandeira-Rey, M., Skare, J. T. & Marconi, R. T. (2001). Analysis of mechanisms associated with loss of infectivity of clonal populations of Borrelia burgdorferi B31MI. Infect Immun 69, 3670-3677.
32. Miller, J. C. & Stevenson, B. (2003). Immunological and genetic characterization of Borrelia burgdorferi BapA and EppA proteins. Microbiology 149, 1113-1125.
33. Nilsson, C. L., Cooper, H. J., Håkansson, K., Marshall, A. G., Östberg, Y., Lavrinovicha, M. & Bergström, S. (2002). Characterization of the P13 membrane protein of Borrelia burgdorferi by mass spectrometry. J Am Soc Mass Spectrom 13, 295-299.
34. Noppa, L., Burman, N., Sadziene, A., Barbour, A. G. & Bergström, S. (1995). Expression of the flagellin gene in Borrelia is controlled by an alternative sigma factor. Microbiology 141, 85-93.
35. Noppa, L., Östberg, Y., Lavrinovicha, M. & Bergström, S. (2001). P13, an integral membrane protein of Borrelia burgdorferi, is C-terminally processed and contains surface-exposed domains. Infect Immun 69, 3323-3334.
36. Norris, S. J., Howell, J. K., Garza, S. A., Ferdows, M. S. & Barbour, A. G. (1995). High- and low-infectivity phenotypes of clonal populations of in vitro-cultured Borrelia burgdorferi. Infect Immun 63, 2206-2212.
37. Ojaimi, C., Brooks, C., Casjens, S. & 12 other authors (2003). Profiling of temperature-induced changes in Borrelia burgdorferi gene expression by using whole genome arrays. Infect Immun 71, 1689-1705.
38. Ornstein, K., Berglund, J., Nilsson, I., Norrby, R. & Bergström, S. (2001). Characterization of Lyme borreliosis isolates from patients with erythema migrans and neuroborreliosis in southern Sweden. J Clin Microbiol 39, 1294-1298.
39. Östberg, Y., Pinne, M., Benz, R., Rosa, P. & Bergström, S. (2002). Elimination of channel forming activity by insertional inactivation of the p13 gene in Borrelia burgdorferi. J Bacteriol 184, 6811-6819.
40. Peter, O. & Bretz, A. G. (1992). Polymorphism of outer surface proteins of Borrelia burgdorferi as a tool for classification. Zentbl Bakteriol 277, 28-33.
41. Pinto do, O. P., Kolterud, Å. & Carlsson, L. (1998). Expression of the LIM-homeobox gene LH2 generates immortalized steel factor-dependent multipotent hematopoietic precursors. EMBO J 17, 5744-5756.
42. Porcella, S. F., Fitzpatrick, C. A. & Bono, J. L. (2000). Expression and immunological analysis of the plasmid-borne mlp genes of Borrelia burgdorferi strain B31. Infect Immun 68, 4992-5001.
43. Postic, D., Ras, N. M., Lane, R. S., Hendson, M. & Baranton, G. (1998). Expanded diversity among Californian borrelia isolates and description of Borrelia bissettii sp. nov. (formerly Borrelia group DN127). J Clin Microbiol 36, 3497-3504.
44. Purser, J. E. & Norris, S. J. (2000). Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci U S A 97, 13865-13870.
45. Purser, J. E., Lawrenz, M. B., Caimano, M. J., Howell, J. K., Radolf, J. D. & Norris, S. J. (2003). A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48, 753-764.
46. Ramamoorthy, R., Povinelli, L. & Philipp, M. T. (1996). Molecular characterization, genomic arrangement, and expression of bmpD, a new member of the bmp class of genes encoding membrane proteins of Borrelia burgdorferi. Infect Immun 64, 1259-1264.
47. Sadziene, A., Thomas, D. D. & Barbour, A. G. (1995). Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect Immun 63, 1573-1580.
48. Schwan, T. G., Burgdorfer, W. & Garon, C. F. (1988a). Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation. Infect Immun 56, 1831-1836.
49. Schwan, T. G., Burgdorfer, W., Schrumpf, M. E. & Karstens, R. H. (1988b). The urinary bladder, a consistent source of Borrelia burgdorferi in experimentally infected white-footed mice (Peromyscus leucopus). J Clin Microbiol 26, 893-895.
50. Shoberg, R. J., Jonsson, M., Sadziene, A., Bergström, S. & Thomas, D. D. (1994). Identification of a highly cross-reactive outer surface protein B epitope among diverse geographic isolates of Borrelia spp. causing Lyme disease. J Clin Microbiol 32, 489-500.
51. Simpson, W. J., Cieplak, W., Schrumpf, M. E., Barbour, A. G. & Schwan, T. G. (1994). Nucleotide sequence and analysis of the gene in Borrelia burgdorferi encoding the immunogenic P39 antigen. FEMS Microbiol Lett 119, 381-387.
52. Skare, J. T., Champion, C. I., Mirzabekov, T. A. & 7 other authors (1996). Porin activity of the native and recombinant outer membrane protein Oms28 of Borrelia burgdorferi. J Bacteriol 178, 4909-4918.
53. Steere, A. C. (1989). Lyme disease. N Engl J Med 321, 586-596.
54. Stevenson, B., Tilly, K. & Rosa, P. A. (1996). A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J Bacteriol 178, 3508-3516.
55. Stevenson, B., Bono, J. L., Schwan, T. G. & Rosa, P. (1998a). Borrelia burgdorferi Erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect Immun 66, 2648-2654.
56. Stevenson, B., Casjens, S. & Rosa, P. (1998b). Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiology 144, 1869-1879.
57. Stevenson, B., El-Hage, N., Hines, M. A., Miller, J. C. & Babb, K. (2002). Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect Immun 70, 491-497.
58. Thomas, V., Anguita, J., Samanta, S., Rosa, P. A., Stewart, P., Barthold, S. W. & Fikrig, E. (2001). Dissociation of infectivity and pathogenicity in Borrelia burgdorferi. Infect Immun 69, 3507-3509.
59. Wang, G., van Dam, A. P., Le Fleche, A., Postic, D., Peter, O., Baranton, G., de Boer, R., Spanjaard, L. & Dankert, J. (1997). Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19). Int J Syst Bacteriol 47, 926-932.
60. Wang, G., van Dam, A. P. & 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.
61. Xu, Y. & Johnson, R. C. (1995). Analysis and comparison of plasmid profiles of Borrelia burgdorferi sensu lato strains. J Clin Microbiol 33, 2679-2685.
62. Xu, Y., Kodner, C., Coleman, L. & Johnson, R. C. (1996). Correlation of plasmids with infectivity of Borrelia burgdorferi sensu stricto type strain B31. Infect Immun 64, 3870-3876.
63. Yang, X., Popova, T. G., Hagman, K. E., Wikel, S. K., Schoeler, G. B., Caimano, M. J., Radolf, J. D. & Norgard, M. V. (1999). Identification, characterization, and expression of three new members of the Borrelia burgdorferi Mlp (2.9) lipoprotein gene family. Infect Immun 67, 6008-6018.
64. Yang, X., Goldberg, M. S., Popova, T. G., Schoeler, G. B., Wikel, S. K., Hagman, K. E. & Norgard, M. V. (2000). Interdependence of environmental factors influencing reciprocal patterns of gene expression in virulent Borrelia burgdorferi. Mol Microbiol 37, 1470-1479.
65. Zhang, J. R. & Norris, S. J. (1998a). Genetic variation of the Borrelia burgdorferi gene vlsE involves cassette-specific, segmental gene conversion. Infect Immun 66, 3698-3704.
66. Zhang, J. R. & Norris, S. J. (1998b). Kinetics and in vivo induction of genetic variation of vlsE in Borrelia burgdorferi. Infect Immun 66, 3689-3697.
67. Zhang, J. R., Hardham, J. M., Barbour, A. G. & Norris, S. J. (1997). Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89, 275-285.
68. Zuckert, W. R., Meyer, J. & Barbour, A. G. (1999). Comparative analysis and immunological characterization of the Borrelia Bdr protein family. Infect Immun 67, 3257-3266.