Elimination of channel-forming activity by insertional inactivation of the p13 gene in Borrelia burgdorferi

Journal of Bacteriology

Volumn 184, Issue 24, 2002, Pages 6811-6819

  Östberg, Yngve ^a   Pinne, Marija ^a   Benz, Roland ^b   Rosa, Patricia ^c   Bergström, Sven ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; OUTER MEMBRANE PROTEIN; PORIN; PROTEIN P13; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BORRELIA BURGDORFERI; CATION TRANSPORT; CHANNEL GATING; GENE INACTIVATION; GENE INSERTION; GENE TARGETING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID BILAYER; MEMBRANE CONDUCTANCE; MEMBRANE POTENTIAL; MUTAGENESIS; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PURIFICATION; WILD TYPE;

BACTERIA (MICROORGANISMS); BORRELIA; BORRELIA BURGDORFERI; INSERTION SEQUENCES;

EID: 0036947229     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.184.24.6811-6819.2002     Document Type: Article

References (65)

1. Achouak, W., T. Heulin, and J. M. Pages. 2001. Multiple facets of bacterial porins. FEMS Microbiol. Lett. 199:1-7.
2. Alberti, S., G. Marques, S. Hernandez-Alles, X. Rubires, J. M. Tomas, F. Vivanco, and V. J. Benedi. 1996. Interaction between complement subcomponent Clq and the Klebsiella pneumoniae porin OmpK36. Infect. Immun. 64:4719-4725.
3. Bacon, D. J., W. M. Johnson, and F. G. Rodgers. 1999. Identification and characterisation of a cytotoxic porin-lipopolysaccharide complex from Campylobacter jejuni. J. Med. Microbiol. 48:139-148.
4. Barbour, A. G. 1984. Isolation and cultivation of Lyme disease spirochetes. Yale J. Biol. Med. 57:521-525.
5. Barbour, A. G., and S. F. Hayes. 1986. Biology of Borrelia species. Microbiol. Rev. 50:381-400.
6. Barthold, S. W., D. S. Beck, G. M. Hansen, G. A. Terwilliger, and K. D. Moody. 1990. Lyme borreliosis in selected strains and ages of laboratory mice. J. Infect. Dis. 162:133-138.
7. Barthold, S. W., K. D. Moody, G. A. Terwilliger, P. H. Duray, R. O. Jacoby, and A. C. Steere. 1988. Experimental Lyme arthritis in rats infected with Borrelia burgdorferi. J. Infect. Dis. 157:842-846.
8. Belisle, J. T., M. E. Brandt, J. D. Radolf, and M. V. Norgard. 1994. Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J. Bacteriol. 176:2151-2157.
9. Benz, R. 2001. Porins - structure and function, p. 227-246. In G. Winkelmann (ed.), Microbial transport systems. Wiley-VCH Verlag GmbH, Weinheim, Germany.
10. Benz, R. 1994. Solute uptake through bacterial outer membranes, p. 397-423. In R. Hackenbek and J.-M. Ghuysen (ed.), Bacterial cell wall. Elsevier, Amsterdam, The Netherlands.
11. Benz, R., K. Janko, W. Boos, and P. Lauger. 1978. Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli. Biochim. Biophys. Acta 511:305-319.
12. Benz, R., K. Janko, and P. Lauger. 1979. Ionic selectivity of pores formed by the matrix protein (porin) of Escherichia coli. Biochim. Biophys. Acta 551:238-247.
13. Benz, R., A. Schmid, C. Maier, and E. Bremer. 1988. Characterization of the nucleosid-specific binding site inside the Tsx channel of Escherichia coli outer membrane: reconstitution experiments with lipid bilayer membranes. Eur. J. Biochem, 176:699-705.
14. Berg, S., Y. Östberg, S. Bergström, and Å. Wieslander. 2001. Functional analysis of a lipid galactosyltransferase from Lyme disease Borrelia spirochetes, p. 161-186. In The glucolipid pathway in Acholeplasma laidlawii, VMC-KBC. Umeå, Sweden.
15. Bernardini, M. L., M. G. Sanna, A. Fontaine, and P. J. Sansonetti. 1993. OmpC is involved in invasion of epithelial cells by Shigella flexneri. Infect, Immun, 61:3625-3635.
16. Blanco, D. R., C. I. Champion, M. M. Exner, H. Erdjument-Bromage, R. E. Hancock, P. Tempst, J. N. Miller, and M. A. Lovett. 1995, Porin activity and sequence analysis of a 31-kilodalton Treponema pallidum subsp. pallidum rare outer membrane protein (Trompl). J. Bacteriol. 177:3556-3562.
17. Bono, J. L., A. F. Elias, J. J. Kupko III, B. Stevenson, K. Tilly, and P. Rosa. 2000. Efficient targeted mutagenesis in Borrelia burgdorferi. J. Bacteriol. 182:2445-2452.
18. Bunikis, J., L. Noppa, and S. Bergström. 1995. Molecular analysis of a 66-kDa protein associated with the outer membrane of Lyme disease Borrelia. FEMS Microbiol. Lett. 131:139-145.
19. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease - a tick-borne spirochetosis? Science 216:1317-1319.
20. Calladine, C. R., A. Sharff, and B. Luisi. 2001. How to untwist an alpha-helix: structural principles of an alpha-helical barrel. J. Mol. Biol. 305:603-618.
21. Casjens, S., N. Palmer, R. van Vugt, W. M. Huang, B. Stevenson, P. Rosa, R. Lathigra, G. Sutton, J. Peterson, R. J. Dodson, D. Haft, E. Hickey, M. Gwinn, O. White, and C. M. Fraser. 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.
22. Castellan, G. W. 1983. The ionic current in aqueous solutions, p. 769-780. In G. W. Castellan (ed.), Physical chemistry. Addison-Wesley, Reading, Mass.
23. Coburn, J., W. Chege, L. Magoun, S. C. Bodary, and J.M. Leong. 1999. Characterization of a candidate Borrelia burgdorferi β3-chain integrin ligand identified using a phage display library. Mol. Microbiol. 34:926-940.
24. Cox, D. L., D. R. Akins, K. W. Bourell, P. Lahdenne, M. V. Norgard, and J. D. Radolf 1996. Limited surface exposure of Borrelia burgdorferi outer surface lipoproteins. Proc. Natl. Acad. Sci. USA 93:7973-7978.
25. Cox, D. L., and J. D. Radolf. 2001. Insertion of fluorescent fatty acid probes into the outer membranes of the pathogenic spirochaetes Treponema pallidum and Borrelia burgdorferi. Microbiology 147:1161-1169.
26. Defoe, G., and J. Coburn. 2001. Delineation of Borrelia burgdorferi p66 sequences required for integrin a(IIb)β(3) recognition. Infect. Immun. 69:3455-3459.
27. Dutzler, R., Y. F. Wang, P. Rizkallah, J. P. Rosenbusch, and T. Schirmer. 1996. Crystal structures of various maltooligosaccharides bound to maltoporin reveal a specific sugar translocation pathway. Structure 4:127-134.
28. Egli, C., W. K. Leung, K. H. Muller, R. E. Hancock, and B. C. McBride. 1993. Pore-forming properties of the major 53-kilodalton surface antigen from the outer sheath of Treponema denticola. Infect. Immun. 61:1694-1699.
29. Elias, A. F., P. E. Stewart, D. Grimm, M. J. Caimano, C. H. Eggers, K. Tilly, J. L. Bono, D. R. Akins, J. D. Radolf, T. G. Schwan, and P. Rosa. 2002. Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect. Immun. 70:2139-2150.
30. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, et al. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
31. Garavito, R. M., and J. P. Rosenbusch. 1980. Three-dimensional crystals of an integral membrane protein: an initial x-ray analysis. J. Cell Biol. 86:327-329.
32. Haines, K. A., L. Yeh, M. S. Blake, P. Cristello, H. Korchak, and G. Weissmann. 1988. Protein I, a translocatable ion channel from Neisseria gonorrhoeae, selectively inhibits exocytosis from human neutrophils without inhibiting O2- generation. J. Biol. Chem. 263:945-951.
33. Hossain, H., H. Wellensiek, R. Geyer, and G. Lochnit. 2001. Structural analysis of glycolipids from Borrelia burgdorferi. Biochimie 83:683-692.
34. Jelfs, J., R. Munro, E. Wedege, and D. A. Caugant. 2000. Sequence variation in the porA gene of a clone of Neisseria meningitidis during epidemic spread. Clin. Diagn. Lab. Immunol. 7:390-395.
35. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239-253.
36. Koronakis, V., A. Sharff, E. Koronakis, B. Luisi, and C. Hughes. 2000. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914-919.
37. Ludwig, O., V. De Pinto, F. Palmieri, and R. Benz. 1986. Pore formation by the mitochondrial porin of rat brain in lipid bilayer membranes., Biochim. Biophys. Acta 860:268-276.
38. Magnarelli, L. A., J. F. Anderson, and A. G. Barbour. 1989. Enzyme-linked immunosorbent assays for Lyme disease: reactivity of subunits of Borrelia burgdorferi. J. Infect. Dis. 159:43-49.
39. Maier, E., G. Polleichtner, B. Boeck, R. Schinzel, and R. Benz. 2001. Identification of the outer membrane porin of Thermus thermophilus HB8: the channel-forming complex has an unusually high molecular mass and an extremely large single-channel conductance. J. Bacteriol. 183:800-803.
40. Mathers, D. A., W. K. Leung, J. C. Fenno, Y. Hong, and B. C. McBride. 1996. The major surface protein complex of Treponema denticola depolarizes and induces ion channels in HeLa cell membranes. Infect. Immun. 64:2904-2910.
41. Merino, S., M. M. Nogueras, A. Aguilar, X. Rubires, S. Alberti, V. J. Benedi, and J. M. Tomas. 1998. Activation of the complement classical pathway (Clq binding) by mesophilic Aeromonas hydrophila outer membrane protein. Infect. Immun. 66:3825-3831.
42. Nikaido, H. 1992. Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6:435-442.
43. Nilsson, C., H. J. Cooper, K. Hfikansson, A. G. Marshall, Y. Östberg, M. Lavrinovicha, and S. Bergström. 2002. Characterization of the P13 membrane protein of Borrelia burgdorferi by mass spectrometry. J. Am. Soc. Mass. Spectrom. 13:295-299.
44. Noppa, L., Y. Östberg, M. Lavrinovicha, and S. Bergström. 2001. P13, an integral membrane protein of Borrelia burgdorferi, is C-terminally processed and contains surface-exposed domains. Infect. Immun. 69:3323-3334.
45. Pautsch, A., and G. E. Schulz. 1998. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5:1013-1017.
46. Probert, W. S., K. M. Allsup, and R. B. LeFebvre. 1995. Identification and characterization of a surface-exposed, 66-kilodalton protein from Borrelia burgdorferi. Infect. Immun. 63:1933-1939.
47. Radolf, J. D., K. W. Bourell, D. R. Akins, J. S. Brusca, and M. V. Norgard. 1994. Analysis of Borrelia burgdorferi membrane architecture by freeze-fracture electron microscopy. J. Bacteriol. 176:21-31.
48. Radolf, J. D., M. S. Goldberg, K. Bourell, S. I. Baker, J. D. Jones, and M. V. Norgard. 1995. Characterization of outer membranes isolated from Borrelia burgdorferi, the Lyme disease spirochete. Infect. Immun. 63:2154-2163.
49. Regelink, A. G., D. Dahan, L. V. Moller, J. W. Coulton, P. Eijk, P. Van Ulsen, J. Dankert, and L. Van Alphen. 1999. Variation in the composition and pore function of major outer membrane pore protein P2 of Haemophilus influenzae from cystic fibrosis patients. Antimicrob. Agents Chemother. 43:226-232.
50. Rosa, P., D. S. Samuels, D. Hogan, B. Stevenson, S. Casjens, and K. Tilly. 1996. Directed insertion of a selectable marker into a circular plasmid of Borrelia burgdorferi. J. Bacteriol. 178:5946-5953.
51. Rudel, T., A. Schmid, R. Benz, H.-A. Kolb, L. F., and T. F. Meyer. 1996. Modulation of translocatable pathogenic Neisseria porin (PorB) by cytosolic ATP/GTP of target cells: parallels between intracellular pathogen accomodation and mitochondrial endosymbiosis. Cell 85:391-402.
52. Sadziene, A., D. D. Thomas, and A. G. Barbour. 1995. Borrelia burgdorferi mutant lacking Osp: biological and immunological characterization. Infect. Immun. 63:1573-1580.
53. Sallmann, F. R., S. Baveye-Descamps, F. Pattus, V. Salmon, N. Branza, G. Spik, and D. Legrand. 1999. Porins OmpC and PhoE of Escherichia coli as specific cell-surface targets of human lactoferrin. Binding characteristics and biological effects. J. Biol. Chem. 274:16107-16114.
54. Shang, E. S., M. M. Exner, T. A. Summers, C. Martinich, C. I. Champion, R. E. Hancock, and D. A. Haake. 1995. The rare outer membrane protein, OmpL1, of pathogenic Leptospira species is a heat-modifiable porin. Infect. Immun. 63:3174-3181.
55. Shang, E. S., J. T. Skare, M. M. Exner, D. R. Blanco, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1998. Isolation and characterization of the outer membrane of Borrelia hermsii. Infect. Immun. 66:1082-1091.
56. Skare, J. T., B. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
57. Skare, J. T., C. I. Champion, T. A. Mirzabekov, E. S. Shang, D. R. Blanco, H. Erdjument-Bromage, P. Tempst, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1996. Porin activity of the native and recombinant outer membrane protein Oms28 of Borrelia burgdorferi. J. Bacteriol. 178:4909-4918.
58. Skare, J. T., T. A. Mirzabekov, E. S. Shang, D. R. Blanco, H. Erdjument-Bromage, J. Bunikis, S. Bergström, P. Tempst, B. L. Kagan, J. N. Miller, and M. A. Lovett. 1997. The Oms66 (p66) protein is a Borrelia burgdorferi porin. Infect. Immun. 65:3654-3661.
59. Steere, A. C., R. L. Grodzicki, A. N. Kornblatt, J. E. Craft, A. G. Barbour, W. Burgdorfer, G. P. Schmid, E. Johnson, and S. E. Malawista. 1983. The spirochetal etiology of Lyme disease. N. Engl. J. Med. 308:733-740.
60. Takayama, K., R. J. Rothenberg, and A. G. Barbour. 1987. Absence of lipopolysaccharide in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 55:2311-2313.
61. Tilly, K., A. F. Elias, J. L. Bono, P. Stewart, and P. Rosa. 2000. DNA exchange and insertional inactivation in spirochetes. J. Mol. Microbiol. Biotechnol. 2:433-442.
62. Trias, J., and R. Benz. 1993. Characterization of the channel formed by. the mycobacterial porin in lipid bilayer membranes. Demonstration of voltage gating and of negative point charges at the channel mouth. J. Biol. Chem. 268:6234-6240.
63. Vieira, J., and J. Messing. 1991. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194.
64. Walker, E. M., L. A. Borenstein, D. R. Blanco, J. N. Miller, and M. A. Lovett. 1991. Analysis of outer membrane ultrastructure of pathogenic Treponema and Borrelia species by freeze-fracture electron microscopy. J. Bacteriol. 173:5585-5588.
65. Yu, S., H. Ding, J. Seah, K. Wu, Y. Chang, K. S. Chang, M. F. Tam, and W. Syu. 1998. Characterization of a phage specific to hemorrhagic Escherichia coli O157:H7 and disclosure of variations in host outer membrane protein OmpC. J. Biomed. Sci. 5:370-382.