Two-partner secretion of gram-negative bacteria: A single β-barrel protein enables transport across the outer membrane

Journal of Biological Chemistry

Volumn 287, Issue 4, 2012, Pages 2591-2599

  Fan, Enguo ^a   Fiedler, Silke ^a   Jacob Dubuisson, Françoise ^b   Müller, Matthias ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b INSERM U1019   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; MEMBRANES;

CELLULAR MEMBRANES; GRAM-NEGATIVE BACTERIA; OUTER MEMBRANE PROTEIN; PATHOGENIC BACTERIUM; PROTEIN SECRETION; PROTEIN TRANSLOCATION; PROTEOLIPOSOMES; SECRETION SYSTEMS;

PROTEINS;

BACTERIAL PROTEIN; BETA BARREL PROTEIN; CARRIER PROTEIN; LIPOSOME; OUTER MEMBRANE PROTEIN; PROTEIN FHAC; PROTEIN TPSA; PROTEIN TPSB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL SECRETION SYSTEM; BORDETELLA PERTUSSIS; CONTROLLED STUDY; IN VITRO STUDY; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION;

BORDETELLA PERTUSSIS; NEGIBACTERIA;

EID: 84863418948     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.293068     Document Type: Article

References (50)

1. Desvaux, M., Hébraud, M., Talon, R., and Henderson, I. R. (2009) Secretion and subcellular localizations of bacterial proteins. A semantic awareness issue. Trends Microbiol. 17, 139-145
2. Economou, A., Christie, P. J., Fernandez, R. C., Palmer, T., Plano, G. V., and Pugsley, A. P. (2006) Secretion by numbers. Protein traffic in prokaryotes. Mol. Microbiol. 62, 308-319 (Pubitemid 44477223)
3. Dautin, N., and Bernstein, H. D. (2007) Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61, 89-112 (Pubitemid 350058201)
4. Jacob-Dubuisson, F., Fernandez, R., and Coutte, L. (2004) Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 1694, 235-257 (Pubitemid 39535072)
5. Emsley, P., Charles, I. G., Fairweather, N. F., and Isaacs, N. W. (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381, 90-92 (Pubitemid 26130010)
6. Clantin, B., Hodak, H., Willery, E., Locht, C., Jacob-Dubuisson, F., and Villeret, V. (2004) The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 6194-6199 (Pubitemid 38520550)
7. Nummelin, H., Merckel, M. C., Leo, J. C., Lankinen, H., Skurnik, M., and Goldman, A. (2004) The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel β-roll. EMBO J. 23, 701-711 (Pubitemid 38418738)
8. Gentle, I. E., Burri, L., and Lithgow, T. (2005) Molecular architecture and function of the Omp85 family of proteins. Mol. Microbiol. 58, 1216-1225 (Pubitemid 41705404)
9. Schleiff, E., and Soll, J. (2005) Membrane protein insertion. Mixing eukaryotic and prokaryotic concepts. EMBO Rep. 6, 1023-1027 (Pubitemid 41637645)
10. Soll, J., and Schleiff, E. (2004) Protein import into chloroplasts. Nat. Rev. Mol. Cell Biol. 5, 198-208 (Pubitemid 38325801)
11. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M., and Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265 (Pubitemid 36125214)
12. Werner, J., and Misra, R. (2005) YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol. Microbiol. 57, 1450-1459 (Pubitemid 41176535)
13. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J., and Kahne, D. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121, 235-245 (Pubitemid 40546391)
14. Gentle, I., Gabriel, K., Beech, P., Waller, R., and Lithgow, T. (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 164, 19-24 (Pubitemid 38082453)
15. Paschen, S. A., Waizenegger, T., Stan, T., Preuss, M., Cyrklaff, M., Hell, K., Rapaport, D., and Neupert, W. (2003) Evolutionary conservation of biogenesis of β-barrel membrane proteins. Nature 426, 862-866 (Pubitemid 38056874)
16. Wiedemann, N., Kozjak, V., Chacinska, A., Schönfisch, B., Rospert, S., Ryan, M. T., Pfanner, N., and Meisinger, C. (2003) Machinery for protein sorting and assembly in the mitochondrial outer membrane. Nature 424, 565-571 (Pubitemid 36975779)
17. Hagan, C. L., Kim, S., and Kahne, D. (2010) Reconstitution of outer membrane protein assembly from purified components. Science 328, 890-892
18. Clantin, B., Delattre, A. S., Rucktooa, P., Saint, N., Méli, A. C., Locht, C., Jacob-Dubuisson, F., and Villeret, V. (2007) Structure of the membrane protein FhaC. A member of the Omp85-TpsB transporter superfamily. Science 317, 957-961 (Pubitemid 47301325)
19. Locht, C., Bertin, P., Menozzi, F. D., and Renauld, G. (1993) The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol. Microbiol. 9, 653-660 (Pubitemid 23253491)
20. Chevalier, N., Moser, M., Koch, H. G., Schimz, K. L., Willery, E., Locht, C., Jacob-Dubuisson, F., and Müller, M. (2004) Membrane targeting of a bacterial virulence factor harbouring an extended signal peptide. J. Mol. Microbiol. Biotechnol. 8, 7-18 (Pubitemid 40468745)
21. Domenighini, M., Relman, D., Capiau, C., Falkow, S., Prugnola, A., Scarlato, V., and Rappuoli, R. (1990) Genetic characterization of Bordetella pertussis filamentous haemagglutinin. A protein processed from an unusually large precursor. Mol. Microbiol. 4, 787-800
22. Coutte, L., Antoine, R., Drobecq, H., Locht, C., and Jacob-Dubuisson, F. (2001) Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J. 20, 5040-5048 (Pubitemid 32910900)
23. Jacob-Dubuisson, F., Buisine, C., Mielcarek, N., Clément, E., Menozzi, F. D., and Locht, C. (1996) Amino-terminal maturation of the Bordetella pertussis filamentous haemagglutinin. Mol. Microbiol. 19, 65-78 (Pubitemid 26025870)
24. Méli, A. C., Hodak, H., Clantin, B., Locht, C., Molle, G., Jacob-Dubuisson, F., and Saint, N. (2006) Channel properties of TpsB transporter FhaC point to two functional domains with a C-terminal protein-conducting pore. J. Biol. Chem. 281, 158-166 (Pubitemid 43671174)
25. Guédin, S., Willery, E., Locht, C., and Jacob-Dubuisson, F. (1998) Evidence that a globular conformation is not compatible with FhaC-mediated secretion of the Bordetella pertussis filamentous haemagglutinin. Mol. Microbiol. 29, 763-774 (Pubitemid 28365463)
26. Moser, M., Panahandeh, S., Holzapfel, E., and Müller, M. (2007) In vitro analysis of the bacterial twin-arginine-dependent protein export. Methods Mol. Biol. 390, 63-79 (Pubitemid 350183652)
27. van der Does, C., de Keyzer, J., van der Laan, M., and Driessen, A. J. (2003) Reconstitution of purified bacterial preprotein translocase in liposomes. Methods Enzymol. 372, 86-98
28. Vogel, H. J., and Bonner, D. M. (1956) Acetylornithinase of Escherichia coli:. Partial purification and some properties. J. Biol. Chem. 218, 97-106
29. Neumann-Haefelin, C., Schäfer, U., Müller, M., and Koch, H. G. (2000) SRP-dependent co-translational targeting and SecA-dependent translocation analyzed as individual steps in the export of a bacterial protein. EMBO J. 19, 6419-6426
30. van Dalen, A., van der Laan, M., Driessen, A. J., Killian, J. A., and de Kruijff, B. (2002) Components required for membrane assembly of newly synthesized K+ channel KcsA. FEBS Lett. 511, 51-58 (Pubitemid 34127822)
31. Hodak, H., Clantin, B., Willery, E., Villeret, V., Locht, C., and Jacob-Dubuisson, F. (2006) Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol. Microbiol. 61, 368-382 (Pubitemid 44356569)
32. Jain, S., and Goldberg, M. B. (2007) Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J. Bacteriol. 189, 5393-5398 (Pubitemid 47076086)
33. Ieva, R., and Bernstein, H. D. (2009) Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 19120-19125
34. Sauri, A., Soprova, Z., Wickström, D., de Gier, J. W., Van der Schors, R. C., Smit, A. B., Jong, W. S., and Luirink, J. (2009) The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155, 3982-3991
35. Choi, P. S., and Bernstein, H. D. (2010) Sequential translocation of an Escherchia coli two-partner secretion pathway exoprotein across the inner and outer membranes. Mol. Microbiol. 75, 440-451
36. Renauld-Mongénie, G., Cornette, J., Mielcarek, N., Menozzi, F. D., and Locht, C. (1996) Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J. Bacteriol. 178, 1053-1060 (Pubitemid 26048021)
37. Jacob-Dubuisson, F., El-Hamel, C., Saint, N., Guédin, S., Willery, E., Molle, G., and Locht, C. (1999) Channel formation by FhaC, the outer membrane protein involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J. Biol. Chem. 274, 37731-37735 (Pubitemid 30026833)
38. Jacob-Dubuisson, F., Villeret, V., Clantin, B., Delattre, A. S., and Saint, N. (2009) First structural insights into the TpsB/Omp85 superfamily. Biol. Chem. 390, 675-684
39. Oomen, C. J., van Ulsen, P., van Gelder, P., Feijen, M., Tommassen, J., and Gros, P. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23, 1257-1266 (Pubitemid 38524998)
40. Brandon, L. D., Goehring, N., Janakiraman, A., Yan, A. W., Wu, T., Beckwith, J., and Goldberg, M. B. (2003) IcsA, a polarly localized autotransporter with an atypical signal peptide, uses the Sec apparatus for secretion, although the Sec apparatus is circumferentially distributed. Mol. Microbiol. 50, 45-60 (Pubitemid 37222785)
41. Marín, E., Bodelón, G., and Fernández, L. Á. (2010) Comparative analysis of the biochemical and functional properties of C-terminal domains of autotransporters. J. Bacteriol. 192, 5588-5602
42. Skillman, K. M., Barnard, T. J., Peterson, J. H., Ghirlando, R., and Bernstein, H. D. (2005) Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol. Microbiol. 58, 945-958 (Pubitemid 41667217)
43. Bodelón, G., Marín, E., and Fernández, L. A. (2009) Role of periplasmic chaperones and BamA (YaeT/Omp85) in folding and secretion of intimin from enteropathogenic Escherichia coli strains. J. Bacteriol. 191, 5169-5179
44. Wagner, J. K., Heindl, J. E., Gray, A. N., Jain, S., and Goldberg, M. B. (2009) Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri. J. Bacteriol. 191, 815-821
45. Bennion, D., Charlson, E. S., Coon, E., and Misra, R. (2010) Dissection of β-barrel outer membrane protein assembly pathways through characterizing BamA POTRA 1 mutants of Escherichia coli. Mol. Microbiol. 77, 1153-1171
46. Baud, C., Hodak, H., Willery, E., Drobecq, H., Locht, C., Jamin, M., and Jacob-Dubuisson, F. (2009) Role of DegP for two-partner secretion in Bordetella. Mol. Microbiol. 74, 315-329
47. Baud, C., Gutsche, I., Willery, E., de Paepe, D., Drobecq, H., Gilleron, M., Locht, C., Jamin, M., and Jacob-Dubuisson, F. (2011) Membrane-associated DegP in Bordetella chaperones a repeat-rich secretory protein. Mol. Microbiol. 80, 1625-1636
48. Schäfer, U., Beck, K., and Müller, M. (1999) Skp, a molecular chaperone of Gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J. Biol. Chem. 274, 24567-24574
49. Harms, N., Koningstein, G., Dontje, W., Muller, M., Oudega, B., Luirink, J., and de Cock, H. (2001) The early interaction of the outer membrane protein phoe with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J. Biol. Chem. 276, 18804-18811
50. Skórko-Glonek, J., Lipińska, B., Krzewski, K., Zolese, G., Bertoli, E., and Tanfani, F. (1997) HtrA heat shock protease interacts with phospholipid membranes and undergoes conformational changes. J. Biol. Chem. 272, 8974-8982 (Pubitemid 27154896)