Conformational dynamics of protein transporter FhaC: Large-scale motions of plug helix

Molecular Microbiology

Volumn 92, Issue 6, 2014, Pages 1164-1176

  Guérin, Jérémy ^a,b   Baud, Catherine ^a,b   Touati, Nadia ^c   Saint, Nathalie ^d   Willery, Eve ^a,b   Locht, Camille ^a,b   Vezin, Hervé ^c   Jacob Dubuisson, Françoise ^a,b  

^a INSERM U1019   (France)

^b UNIV LILLE   (France)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^d HÔPITAL ARNAUD DE VILLENEUVE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOSOME; PROTEIN FHA; PROTEIN FHAC; PROTEIN TPSA; PROTEIN TPSB; UNCLASSIFIED DRUG; ADHESIN; BORDETELLA VIRULENCE FACTOR; FHAC PROTEIN, BORDETELLA PERTUSSIS; FILAMENTOUS HEMAGGLUTININ ADHESIN, BORDETELLA PERTUSSIS; OUTER MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CYTOPLASM; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; IN VIVO STUDY; MEMBRANE ELECTROPHYSIOLOGY; MICELLE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; BACTERIAL SECRETION SYSTEM; BORDETELLA PERTUSSIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM;

BORDETELLA PERTUSSIS; NEGIBACTERIA;

ADHESINS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; BORDETELLA PERTUSSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; VIRULENCE FACTORS, BORDETELLA;

EID: 84902107363     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12585     Document Type: Article

References (41)

1. Alsteens, D., Martinez, N., Jamin, M., and Jacob-Dubuisson, F. (2013) Sequential unfolding of beta helical protein by single-molecule atomic force microscopy. PLoS ONE 8: e73572.
2. Antoine, R., Huvent, I., Chemlal, K., Deray, I., Raze, D., Locht, C., and Jacob-Dubuisson, F. (2005) The periplasmic binding protein of a tripartite tricarboxylate transporter is involved in signal transduction. J Mol Biol 351: 799-809.
3. Bardwell, J.C.A., Mc Govern, K., and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589.
4. 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.
5. Bordignon, E. (2012) Site-directed spin labeling of membrane proteins. Top Curr Chem 321: 121-157.
6. Bos, M.P., and Tommassen, J. (2004) Biogenesis of the Gram-negative bacterial outer membrane. Curr Opin Microbiol 7: 610-616.
7. Chevalier, N., Moser, M., Koch, H.G., Schimz, K.L., Willery, E., Locht, C., etal. (2004) Membrane targeting of a bacterial virulence factor harbouring an extended signal peptide. J Mol Microbiol Biotechnol 8: 7-18.
8. 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 USA 101: 6194-6199.
9. Clantin, B., Delattre, A.S., Rucktooa, P., Saint, N., Meli, A.C., Locht, C., etal. (2007) Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317: 957-961.
10. Delattre, A.S., Clantin, B., Saint, N., Locht, C., Villeret, V., and Jacob-Dubuisson, F. (2010) Functional importance of a conserved sequence motif in FhaC, a prototypic member of the TpsB/Omp85 superfamily. FEBS J 277: 4755-4765.
11. Delattre, A.S., Saint, N., Clantin, B., Willery, E., Lippens, G., Locht, C., etal. (2011) Substrate recognition by the POTRA domains of TpsB transporter FhaC. Mol Microbiol 81: 99-112.
12. Dwyer, R.S., Ricci, D.P., Colwell, L.J., Silhavy, T.J., and Wingreen, N.S. (2013) Predicting functionally informative mutations in Escherichia coli BamA using evolutionary co-variance analysis. Genetics 195: 443-455.
13. Fairman, J.W., Noinaj, N., and Buchanan, S.K. (2011) The structural biology of beta-barrel membrane proteins: a summary of recent reports. Curr Opin Struct Biol 21: 523-531.
14. Fan, E., Fiedler, S., Jacob-Dubuisson, F., and Muller, M. (2012) Two-partner secretion of gram-negative bacteria: a single beta-barrel protein enables transport across the outer membrane. J Biol Chem 287: 2591-2599.
15. Fanucci, G.E., Cadieux, N., Piedmont, C.A., Kadner, R.J., and Cafiso, D.S. (2002) Structure and dynamics of the beta-barrel of the membrane transporter BtuB by site-directed spin labeling. Biochemistry 41: 11543-11551.
16. Fanucci, G.E., Coggshall, K.A., Cadieux, N., Kim, M., Kadner, R.J., and Cafiso, D.S. (2003) Substrate-induced conformational changes of the periplasmic N-terminus of an outer-membrane transporter by site-directed spin labeling. Biochemistry 42: 1391-1400.
17. Gentle, I.E., Burri, L., and Lithgow, T. (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58: 1216-1225.
18. Gruss, F., Zahringer, F., Jakob, R.P., Burmann, B.M., Hiller, S., and Maier, T. (2013) The structural basis of autotransporter translocation by TamA. Nat Struct Mol Biol 20: 1318-1320.
19. Guédin, S., Willery, E., Tommassen, J., Fort, E., Drobecq, H., Locht, C., and Jacob-Dubuisson, F. (2000) Novel topological features of FhaC, the outer membrane transporter involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J Biol Chem 275: 30202-30210.
20. 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.
21. Huvent, I., Berhali, H., Antoine, R., Bompard, C., Locht, C., Jacob-Dubuisson, F., and Villeret, V. (2006) Structural analysis of the glutamate receptor BugE of Bordetella pertussis in a bound conformation. Acta Cryst D 62: 1375-1381.
22. Jacob-Dubuisson, F., Locht, C., and Antoine, R. (2001) Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 40: 306-313.
23. Jacob-Dubuisson, F., Fernandez, R., and Coutte, L. (2004) Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 1694: 235-257.
24. 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.
25. Jacob-Dubuisson, F., Guerin, J., Baelen, S., and Clantin, B. (2013) Two-partner secretion: as simple as it sounds? Res Microbiol 164: 583-595.
26. Jeschke, G., Koch, A., Jonas, U., and Godt, A. (2002) Direct conversion of EPR dipolar time evolution data to distance distributions. J Magnet Reson 155: 72-82.
27. Jeschke, G., Chechik, V., Ionita, P., Godt, A., Zimmermann, H., Banham, J., etal. (2006) DeerAnalysis2006 - a comprehensive software package for analyzing pulsed ELDOR data. Appl Magn Reson 30: 473-498.
28. Jong, W.S., ten Hagen-Jongman, C.M., den Blaauwen, T., Jan Slotboom, D., Tame, J.R., Wickstrom, D., etal. (2007) Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol Microbiol 63: 1524-1536.
29. Kajava, A.V., Cheng, N., Cleaver, R., Kessel, M., Simon, M.N., Willery, E., etal. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292.
30. McHaourab, H.S., Lietzow, M.A., Hideg, K., and Hubbell, W.L. (1996) Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35: 7692-7704.
31. 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.
32. Noinaj, N., Kuszak, A.J., Gumbart, J.C., Lukacik, P., Chang, H., Easley, N.C., etal. (2013) Structural insight into the biogenesis of beta-barrel membrane proteins. Nature 501: 385-390.
33. Polyhach, Y., Bordignon, E., and Jeschke, G. (2011) Rotamer libraries of spin labelled cysteines for protein studies. Phys Chem Chem Phys 13: 2356-2366.
34. Rice, A.J., Alvarez, F.J., Schultz, K.M., Klug, C.S., Davidson, A.L., and Pinkett, H.W. (2013) EPR spectroscopy of MolB2C2-a reveals mechanism of transport for a bacterial type II molybdate importer. J Biol Chem 288: 21228-21235.
35. Rigel, N.W., Schwalm, J., Ricci, D.P., and Silhavy, T.J. (2012) BamE modulates the Escherichia coli beta-barrel assembly machine component BamA. J Bacteriol 194: 1002-1008.
36. Seelig, J. (1970) Spin label studies of oriented smectic crystals, a model sytem for lipid bilayers. J Am Chem Soc 92: 3881-3887.
37. Sen, K.I., Logan, T.M., and Fajer, P.G. (2007) Protein dynamics and monomer-monomer interactions in AntR activation by electron paramagnetic resonance and double electron-electron resonance. Biochemistry 46: 11639-11649.
38. Stegmeier, J.F., and Andersen, C. (2006) Characterization of pores formed by YaeT (Omp85) from Escherichia coli. J Biochem (Tokyo) 140: 275-283.
39. Stoll, S., and Schweiger, A. (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J Magn Reson 178: 42-55.
40. Tikhonov, Y., and Arsenin, V. (1977) Solutions of Ill-posed Problems. New York: John Wiley & Sons.
41. van Ulsen, P., Rahman, S., Jong, W., Daleke-Schermerhorn, M., and Luirink, J. (2013) Type V secretion: from biogenesis to biotechnology. Biochem Biophys Acta Nov 22. pii: S0167-4889(13)00397-2. doi: 10.1016/j.bbamcr.2013.11.006. [Epub ahead of print].