Study of the protein complex, Pore diameter, and pore-forming activity of the borrelia burgdorferi P13 Porin

Journal of Biological Chemistry

Volumn 289, Issue 27, 2014, Pages 18614-18624

  Bárcena Uribárri, Ivan ^a,b   Thein, Marcus ^a   Barbot, Mariam ^a   Sans Serramitjana, Eulalia ^a   Bonde, Mari ^c   Mentele, Reinhard ^d   Lottspeich, Friedrich ^d   Bergström, Sven ^c   Benz, Roland ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b JACOBS UNIVERSITY BREMEN   (Germany)

^c UMEÅ UNIVERSITY   (Sweden)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ANTIBIOTIC TREATMENT; BORRELIA; BORRELIA BURGDORFERI; DIFFUSION PATHWAYS; HOMO-OLIGOMERS; MOLECULAR TRANSPORT; PORE DIAMETERS; PROTEIN COMPLEXES;

PROTEINS;

PORIN; POTASSIUM CHLORIDE; PROTEIN P13; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BORRELIA BURGDORFERI; ENZYME SPECIFICITY; LIPID BILAYER; MASS SPECTROMETRY; MUTANT; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION; WESTERN BLOTTING;

ANTIBIOTICS; ANTIGEN; BACTERIAL PATHOGENESIS; BLACK LIPID BILAYER; BLUE NATIVE PAGE; MEMBRANE PROTEIN; MEMBRANE TRANSPORT;

BACTERIAL PROTEINS; BORRELIA BURGDORFERI; DOSE-RESPONSE RELATIONSHIP, DRUG; ION CHANNEL GATING; LIPID BILAYERS; PORINS; POROSITY; SALTS; SUBSTRATE SPECIFICITY;

EID: 84903849314     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.539528     Document Type: Article

References (60)

1. Woese, C. R. (1987) Bacterial evolution. Microbiol. Rev. 51, 221-271
2. Obermeier, O. H. F., and Zeiss, H. (1873) Die entdeckung von fadenförmigen gebilden im blut von rückfallfieberkranken (1873) Eingeleitet und herausgegeben von Dr. Heinz Zeiss, Leipzig, J. A. Barth, 1926
3. Burgdorfer, W. (1984) Discovery of the Lyme disease spirochete and its relation to tick vectors. Yale J. Biol. Med. 57, 515-520
4. Burgdorfer, W., Barbour, A. G., Hayes, S. F., Benach, J. L., Grunwaldt, E., and Davis, J. P. (1982) Lyme disease-a tick-borne spirochetosis? Science 216, 1317-1319
5. Steere, A. C. (2001) Lyme disease. N. Engl. J. Med. 345, 115-125
6. Steere, A. C. (2006) Lyme borreliosis in 2005, 30 years after initial observations in Lyme Connecticut. Wien. Klin. Wochenschr. 118, 625-633
7. Barbour, A. G., and Hayes, S. F. (1986) Biology of Borrelia species. Microbiol. Rev. 50, 381-400
8. Fraser, C. M., Casjens, S., Huang, W. M., Sutton, G. G., Clayton, R., Lathigra, R., White, O., Ketchum, K. A., Dodson, R., Hickey, E. K., Gwinn, M., Dougherty, B., Tomb, J. F., Fleischmann, R. D., Richardson, D., Peterson, J., Kerlavage, A. R., Quackenbush, J., Salzberg, S., Hanson, M., van Vugt, R., Palmer, N., Adams, M. D., Gocayne, J., Weidman, J., Utterback, T., Watthey, L., McDonald, L., Artiach, P., Bowman, C., Garland, S., Fuji, C., Cotton, M. D., Horst, K., Roberts, K., Hatch, B., Smith, H. O., and Venter, J. C. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586
9. Hasle, G. (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect. Microbiol. 3, 48
10. Mannelli, A., Bertolotti, L., Gern, L., and Gray, J. (2012) Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems, influence of molecular processes and effects of climate change. FEMS Microbiol. Rev. 36, 837-861
11. Benz, R. (1994) Solute uptake through bacterial outer membranes. in Bacterial Cell Wall (Ghuysen, J. M., and Hakenbeck, R., eds. ) pp. 397-423, Elsevier Science Publishing Co., Inc., New York
12. Achouak, W., Heulin, T., and Pagès, J. M. (2001) Multiple facets of bacterial porins. FEMS Microbiol. Lett. 199, 1-7
13. Maier, C., Bremer, E., Schmid, A., and Benz, R. (1988) Pore-forming activity of the Tsx protein from the outer membrane of Escherichia coli. Demonstration of a nucleoside-specific binding site. J. Biol. Chem. 263, 2493-2499
14. Benz, R., Schmid, A., Maier, C., and Bremer, E. (1988) Characterization of the nucleoside-binding site inside the Tsx channel of Escherichia coli outer membrane. Reconstitution experiments with lipid bilayer membranes. Eur. J. Biochem. 176, 699-705
15. Benz, R., Schmid, A., and Vos-Scheperkeuter, G. H. (1987) Mechanism of sugar transport through the sugar-specific LamB channel of Escherichia coli outer membrane. J. Membr. Biol. 100, 21-29
16. Hancock, R. E., and Benz, R. (1986) Demonstration and chemical modification of a specific phosphate binding site in the phosphate- starvationinducible outer membrane porin protein P of Pseudomonas aeruginosa. Biochim. Biophys. Acta 860, 699-707
17. Kim, B. H., Andersen, C., and Benz, R. (2001) Identification of a cell wall channel of Streptomyces griseus: the channel contains a binding site for streptomycin. Mol. Microbiol. 41, 665-673
18. Bárcena-Uribarri, I., Thein, M., Sacher, A., Bunikis, I., Bonde, M., Bergstro m, S., and Benz, R. (2010) P66 porins are present in both Lyme disease and relapsing fever spirochetes: a comparison of the biophysical properties of P66 porins from six Borrelia species. Biochim. Biophys. Acta 1798, 1197-1203
19. Skare, J. T., Mirzabekov, T. A., Shang, E. S., Blanco, D. R., Erdjument- Bromage, H., Bunikis, J., Bergström, S., Tempst, P., Kagan, B. L., Miller, J. N., and Lovett, M. A. (1997) The Oms66 (p66) protein is a Borrelia burgdorferi porin. Infect. Immun. 65, 3654-3661
20. Coburn, J., Chege, W., Magoun, L., Bodary, S. C., and Leong, J. M. (1999) Characterization of a candidate Borrelia burgdorferi -3-chain integrin ligand identified using a phage display library. Mol. Microbiol. 34, 926-940
21. Coburn, J., and Cugini, C. (2003) Targeted mutation of the outer membrane protein P66 disrupts attachment of the Lyme disease agent, Borrelia burgdorferi, to integrin-v-3. Proc. Natl. Acad. Sci. U. S. A. 100, 7301-7306
22. Thein, M., Bunikis, I., Denker, K., Larsson, C., Cutler, S., Drancourt, M., Schwan, T. G., Mentele, R., Lottspeich, F., Bergström, S., and Benz, R. (2008) Oms38 is the first identified pore-forming protein in the outer membrane of relapsing fever spirochetes. J. Bacteriol. 190, 7035-7042
23. Thein, M., Bonde, M., Bunikis, I., Denker, K., Sickmann, A., Bergström, S., and Benz, R. (2012) DipA, a pore-forming protein in the outer membrane of Lyme disease spirochetes exhibits specificity for the permeation of dicarboxylates. PLoS ONE 7, e36523
24. Ostberg, Y., Pinne, M., Benz, R., Rosa, P., and Bergström, S. (2002) Elimination of channel-forming activity by insertional inactivation of the p13 gene in Borrelia burgdorferi. J. Bacteriol. 184, 6811-6819
25. Noppa, L., Ostberg, Y., Lavrinovicha, M., and 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
26. Kumru, O. S., Bunikis, I., Sorokina, I., Bergström, S., and Zückert, W. R. (2011) Specificity and role of the Borrelia burgdorferi CtpA protease in outer membrane protein processing. J. Bacteriol. 193, 5759-5765
27. Pinne, M., Ostberg, Y., Comstedt, P., and Bergström, S. (2004) Molecular analysis of the channel-forming protein P13 and its paralogue family 48 from different Lyme disease Borrelia species. Microbiology 150, 549-559
28. Pinne, M., Denker, K., Nilsson, E., Benz, R., and Bergström, S. (2006) The BBA01 protein, a member of paralog family 48 from Borrelia burgdorferi, is potentially interchangeable with the channel-forming protein P13. J. Bacteriol. 188, 4207-4217
29. Skare, J. T., Champion, C. I., Mirzabekov, T. A., Shang, E. S., Blanco, D. R., Erdjument-Bromage, H., Tempst, P., Kagan, B. L., Miller, J. N., and Lovett, M. A. (1996) Porin activity of the native and recombinant outer membrane protein Oms28 of Borrelia burgdorferi. J. Bacteriol. 178, 4909-4918
30. Mulay, V., Caimano, M. J., Liveris, D., Desrosiers, D. C., Radolf, J. D., and Schwartz, I. (2007) Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J. Bacteriol. 189, 2063-2068
31. Cluss, R. G., Silverman, D. A., and Stafford, T. R. (2004) Extracellular secretion of the Borrelia burgdorferi Oms28 porin and Bgp, a glycosaminoglycan binding protein. Infect. Immun. 72, 6279-6286
32. Pinne, M., Thein, M., Denker, K., Benz, R., Coburn, J., and Bergström, S. (2007) Elimination of channel-forming activity by insertional inactivation of the p66 gene in Borrelia burgdorferi. FEMS Microbiol. Lett. 266, 241-249
33. Barbour, A. G. (1984) Isolation and cultivation of Lyme disease spirochetes. Yale. J. Biol. Med. 57, 521-525
34. Magnarelli, L. A., Anderson, J. F., and Barbour, A. G. (1989) Enzymelinked immunosorbent assays for Lyme disease: reactivity of subunits of Borrelia burgdorferi. J. Infect. Dis. 159, 43-49
35. Schägger, H. (2006) Tricine-SDS-PAGE. Nat. Protoc. 1, 16-22
36. Blum, H., Beier, H., and Gross, H. J. (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8, 93-99
37. Benz, R., Janko, K., and LaÜger, P. (1979) Ionic selectivity of pores formed by the matrix protein (porin) of Escherichia coli. Biochim. Biophys. Acta 551, 238-247
38. Montal, M., and Mueller, P. (1972) Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl. Acad. Sci. U. S. A. 69, 3561-3566
39. Benz, R., Janko, K., Boos, W., and LaÜger, P. (1978) Formation of large, ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli. Biochim. Biophys. Acta 511, 305-319
40. Mahendran, K. R., Hajjar, E., Mach, T., Lovelle, M., Kumar, A., Sousa, I., Spiga, E., Weingart, H., Gameiro, P., Winterhalter, M., and Ceccarelli, M. (2010) Molecular basis of enrofloxacin translocation through OmpF, an outer membrane channel of Escherichia coli: when binding does not imply translocation. J. Phys. Chem. B 114, 5170-5179
41. Ludwig, O., De Pinto, V., Palmieri, F., and Benz, R. (1986) Pore formation by the mitochondrial porin of rat brain in lipid bilayer membranes. Biochim. Biophys. Acta 860, 268-276
42. Benz, R., Schmid, A., Nakae, T., and Vos-Scheperkeuter, G. H. (1986) Pore formation by LamB of Escherichia coli in lipid bilayer membranes. J. Bacteriol. 165, 978-986
43. Krasilnikov, O. V., Da Cruz, J. B., Yuldasheva, L. N., Varanda, W. A., and Nogueira, R. A. (1998) A novel approach to study the geometry of the water lumen of ion channels: colicin Ia channels in planar lipid bilayers. J. Membr. Biol. 161, 83-92
44. Sabirov, R. Z., Krasilnikov, O. V., Ternovsky, V. I., and Merzliak, P. G. (1993) Relation between ionic channel conductance and conductivity of media containing different nonelectrolytes. A novel method of pore size determination. Gen. Physiol. Biophys. 12, 95-111
45. Krasilnikov, O. V., Sabirov, R. Z., Ternovsky, V. I., Merzliak, P. G., and Muratkhodjaev, J. N. (1992) A simple method for the determination of the pore radius of ion channels in planar lipid bilayer membranes. FEMS Microbiol. Immunol. 5, 93-100
46. Mark, J. E., and Flory, P. J. (1965) The configuration of the polyoxyethylene chain. J. Am. Chem. Soc. 87, 1415-1422
47. Rempp, P. (1957) Contribution a l'étude des solution de molecules en chain a squelette oxigène. J. Chem. Phys. 54, 432-453
48. Andersen, C., Schiffler, B., Charbit, A., and Benz, R. (2002) PH-induced collapse of the extracellular loops closes Escherichia coli maltoporin and allows the study of asymmetric sugar binding. J. Biol. Chem. 277, 41318-41325
49. Benz, R. (ed) (2001) Porins: Structure and Function, WILEY-VCH Verlag GmbH, Weinheim, Germany
50. Schägger, H., Cramer, W. A., and von Jagow, G. (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by twodimensional native electrophoresis. Anal. Biochem. 217, 220-230
51. Lide, D. R. (ed) (1998) CRC Handbook of Chemistry and Physics, 71st Edition, Section 5, p. 99, CRC Press, Inc., Boca Raton, FL
52. Bárcena-Uribarri, I., Thein, M., Maier, E., Bonde, M., Bergström, S., and Benz, R. (2013) Use of nonelectrolytes reveals the channel size and oligomeric constitution of the Borrelia burgdorferi P66 porin. PLoS ONE 8, e78272
53. Skare, J. T., Shang, E. S., Foley, D. M., Blanco, D. R., Champion, C. I., Mirzabekov, T., Sokolov, Y., Kagan, B. L., Miller, J. N., and Lovett, M. A. (1995) Virulent strain associated outer membrane proteins of Borrelia burgdorferi. J. Clin. Invest. 96, 2380-2392
54. Belisle, J. T., Brandt, M. E., Radolf, J. D., and Norgard, M. V. (1994) Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J. Bacteriol. 176, 2151-2157
55. Tristram-Nagle, S., Kim, D. J., Akhunzada, N., Kucerka, N., Mathai, J. C., Katsaras, J., Zeidel, M., and Nagle, J. F. (2010) Structure and water permeability of fully hydrated diphytanoylPC. Chem. Phys. Lipids 163, 630-637
56. Nablo, B. J., Halverson, K. M., Robertson, J. W., Nguyen, T. L., Panchal, R. G., Gussio, R., Bavari, S., Krasilnikov, O. V., and Kasianowicz, J. J. (2008) Sizing the Bacillus anthracis PA63 channel with nonelectrolyte poly(ethylene glycols). Biophys. J. 95, 1157-1164
57. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656
58. Hancock, R. E., and Bell, A. (1988) Antibiotic uptake into gram-negative bacteria. Eur. J. Clin. Microbiol. Infect. Dis. 7, 713-720
59. Delcour, A. H. (2009) Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta 1794, 808-816
60. Sicklinger, M., Wienecke, R., and Neubert, U. (2003) In vitro susceptibility testing of four antibiotics against Borrelia burgdorferi: a comparison of results for the three genospecies Borrelia afzelii, Borrelia garinii, and Borrelia burgdorferi sensu stricto. J. Clin. Microbiol.41,1791- 1793.