Sequential steps in the assembly of the multimeric outer membrane secretin PulD

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30700-30707

  Huysmans, Gerard H M ^a   Guilvout, Ingrid ^a   Pugsley, Anthony P ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEINS; MULTIMERIC; MULTISTEP PROCESS; NATIVE STRUCTURES; NOVEL PROTEINS; OUTER MEMBRANE; SECRETION SYSTEMS; SELF-ASSEMBLE;

BIOCHEMISTRY; BIOLOGY;

BIOLOGICAL MEMBRANES;

LIPOSOME; PULD PROTEIN; SECRETIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; KLEBSIELLA OXYTOCA; LIPID COMPOSITION; MEMBRANE FLUIDITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; TYPE II SECRETION SYSTEM;

KINETICS; MEMBRANE PROTEINS; PHOSPHOLIPID VESICLE; PROTEIN SELF-ASSEMBLY; PROTEIN SYNTHESIS; SECRETIN; TYPE II SECRETION;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; KLEBSIELLA PNEUMONIAE; LIPOSOMES; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY;

EID: 84886912356     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.489112     Document Type: Article

References (60)

1. Bondar, A. N., and White, S. H. (2012) Hydrogen bond dynamics in membrane protein function. Biochim. Biophys. Acta 1818, 942-950
2. Bowie, J. U. (2011) Membrane protein folding. How important are hydrogen bonds? Curr. Opin. Struct. Biol. 21, 42-49
3. Cao, Z., and Bowie, J. U. (2012) Shifting hydrogen bonds may produce flexible transmembrane helices. Proc. Natl. Acad. Sci. U.S.A. 109, 8121-8126
4. Curnow, P., Di Bartolo, N. D., Moreton, K. M., Ajoje, O. O., Saggese, N. P., and Booth, P. J. (2011) Stable folding core in the folding transition state of an -helical integral membrane protein. Proc. Natl. Acad. Sci. U.S.A. 108, 14133-14138
5. Fiedler, S., Broecker, J., and Keller, S. (2010) Protein folding in membranes. Cell Mol. Life Sci. 67, 1779-1798
6. Hong, H., and Bowie, J. U. (2011) Dramatic destabilization of transmembrane helix interactions by features of natural membrane environments. J. Am. Chem. Soc. 133, 11389-11398
7. Kalli, A. C., Campbell, I. D., and Sansom, M. S. (2011) Multiscale simulations suggest a mechanism for integrin inside-out activation. Proc. Natl. Acad. Sci. U.S.A. 108, 11890-11895
8. Moon, C. P., and Fleming, K. G. (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc. Natl. Acad. Sci. U.S.A. 108, 10174-10177
9. Amaral, M. D. (2004) CFTR and chaperones. Processing and degradation. J. Mol. Neurosci. 23, 41-48
10. Hagan, C. L., Silhavy, T. J., and Kahne, D. (2011) β-Barrel membrane protein assembly by the Bam complex. Annu. Rev. Biochem. 80, 189-210
11. Mogensen, J. E., and Otzen, D. E. (2005) Interactions between folding factors and bacterial outer membrane proteins. Mol. Microbiol. 57, 326-346
12. Curnow, P., and Booth, P. J. (2007) Combined kinetic and thermodynamic analysis of -helical membrane protein unfolding. Proc. Natl. Acad. Sci. U.S.A. 104, 18970-18975
13. Hong, H., and Tamm, L. K. (2004) Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. U.S.A. 101, 4065-4070
14. Huysmans, G. H., Baldwin, S. A., Brockwell, D. J., and Radford, S. E. (2010) The transition state for folding of an outer membrane protein. Proc. Natl. Acad. Sci. U.S.A. 107, 4099-4104
15. Cymer, F., and Schneider, D. (2012) Oligomerization of polytopic -helical membrane proteins. Causes and consequences. Biol. Chem. 393, 1215-1230
16. Clarke, O. B., and Gulbis, J. M. (2012) Oligomerization at the membrane. Potassium channel structure and function. Adv. Exp. Med. Biol. 747, 122-136
17. Meng, G., Fronzes, R., Chandran, V., Remaut, H., and Waksman, G. (2009) Protein oligomerization in the bacterial outer membrane (Review). Mol. Membr. Biol. 26, 136-145
18. Dunstone, M. A., and Tweten, R. K. (2012) Packing a punch. The mechanism of pore formation by cholesterol dependent cytolysins and membrane attack complex/perforin-like proteins. Curr. Opin. Struct. Biol. 22, 342-349
19. Nieva, J. L., Madan, V., and Carrasco, L. (2012) Viroporins. Structure and biological functions. Nat. Rev. Microbiol. 10, 563-574
20. Tilley, S. J., and Saibil, H. R. (2006) The mechanism of pore formation by bacterial toxins. Curr. Opin. Struct. Biol. 16, 230-236
21. Cymer, F., and Schneider, D. (2010) A single glutamate residue controls the oligomerization, function, and stability of the aquaglyceroporin GlpF. Biochemistry 49, 279-286
22. Hong, H., Blois, T. M., Cao, Z., and Bowie, J. U. (2010) Method to measure strong protein-protein interactions in lipid bilayers using a steric trap. Proc. Natl. Acad. Sci. U.S.A. 107, 19802-19807
23. Stanley, A. M., Chuawong, P., Hendrickson, T. L., and Fleming, K. G. (2006) Energetics of outer membrane phospholipase A (OMPLA) dimerization. J. Mol. Biol. 358, 120-131
24. Dewald, A. H., Hodges, J. C., and Columbus, L. (2011) Physical determinants of -barrel membrane protein folding in lipid vesicles. Biophys. J. 100, 2131-2140
25. Ebie Tan, A., Burgess, N. K., DeAndrade, D. S., Marold, J. D., and Fleming, K. G. (2010) Self-association of unfolded outer membrane proteins. Macromol. Biosci. 10, 763-767
26. Masi, M., Duret, G., Delcour, A. H., and Misra, R. (2009) Folding and trimerization of signal sequence-less mature TolC in the cytoplasm of Escherichia coli. Microbiology 155, 1847-1857
27. Junge, F., Haberstock, S., Roos, C., Stefer, S., Proverbio, D., Dötsch, V., and Bernhard, F. (2011) Advances in cell-free protein synthesis for the functional and structural analysis of membrane proteins. N. Biotechnol. 28, 262-271
28. Guilvout, I., Chami, M., Berrier, C., Ghazi, A., Engel, A., Pugsley, A. P., and Bayan, N. (2008) In vitro multimerization and membrane insertion of bacterial outer membrane secretin PulD. J. Mol. Biol. 382, 13-23
29. Nickerson, N. N., Abby, S. S., Rocha, E. P., Chami, M., and Pugsley, A. P. (2012)Asingle amino acid substitution changes the self-assembly status of a type IV piliation secretin. J. Bacteriol. 194, 4951-4958
30. McLaughlin, L. S., Haft, R. J., and Forest, K. T. (2012) Structural insights into the type II secretion nanomachine. Curr. Opin. Struct. Biol. 22, 208-216
31. Collin, S., Guilvout, I., Chami, M., and Pugsley, A. P. (2007) YaeT-independent multimerization and outer membrane association of secretin PulD. Mol. Microbiol. 64, 1350-1357
32. Guilvout, I., Chami, M., Engel, A., Pugsley, A. P., and Bayan, N. (2006) Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25, 5241-5249
33. Guilvout, I., Nickerson, N. N., Chami, M., and Pugsley, A. P. (2011) Multimerization-defective variants of dodecameric secretin PulD. Res. Microbiol. 162, 180-190
34. Hardie, K. R., Lory, S., and Pugsley, A. P. (1996) Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15, 978-988
35. Collin, S., Krehenbrink, M., Guilvout, I., and Pugsley, A. P. (2013) The targeting, docking and anti-proteolysis functions of the secretin chaperone PulS. Res. Microbiol. 164, 390-396
36. Chami, M., Guilvout, I., Gregorini, M., Rémigy, H. W., Müller, S. A., Valerio, M., Engel, A., Pugsley, A. P., and Bayan, N. (2005) Structural insights into the secretin PulD and its trypsin-resistant core. J. Biol. Chem. 280, 37732-37741
37. Nouwen, N., Stahlberg, H., Pugsley, A. P., and Engel, A. (2000) Domain structure of secretin PulD revealed by limited proteolysis and electron microscopy. EMBO J. 19, 2229-2236
38. Wallace, L. A., and Matthews, C. R. (2002) Sequential vs. parallel proteinfolding mechanisms. Experimental tests for complex folding reactions. Biophys. Chem. 101, 113-131
39. Kleinschmidt, J. H., and Tamm, L. K. (1996) Folding intermediates of a -barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35, 12993-13000
40. Rodionova, N. A., Tatulian, S. A., Surrey, T., Jähnig, F., and Tamm, L. K. (1995) Characterization of two membrane-bound forms of OmpA. Biochemistry 34, 1921-1929
41. Tomita, T., Watanabe, M., and Yasuda, T. (1992) Influence of membrane fluidity on the assembly of Staphylococcus aureus -toxin, a channelforming protein, in liposome membrane. J. Biol. Chem. 267, 13391-13397
42. Collin, S., Guilvout, I., Nickerson, N. N., and Pugsley, A. P. (2011) Sorting of an integral outer membrane protein via the lipoprotein-specific Lol pathway and a dedicated lipoprotein pilotin. Mol. Microbiol. 80, 655-665
43. Blanton, M. P., and Cohen, J. B. (1992) Mapping the lipid-exposed regions in the Torpedo californica nicotinic acetylcholine receptor. Biochemistry 31, 3738-3750
44. Perides, G., Harter, C., and Traub, P. (1987) Electrostatic and hydrophobic interactions of the intermediate filament protein vimentin and its amino terminus with lipid bilayers. J. Biol. Chem. 262, 13742-13749
45. Smith, D. P., Kilbourn, M. R., McDowell, J. H., Hargrave, P. A. (1981) Topography of rhodopsin in retinal rod outer segment disk membranes. Photochemical labeling with L-azidopyrene. Biochemistry 20, 2417-2424
46. Bitter, W., Koster, M., Latijnhouwers, M., de Cock, H., and Tommassen, J. (1998) Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Mol. Microbiol. 27, 209-219
47. Dowd, K. J., and Tweten, R. K. (2012) The cholesterol-dependent cytolysin signature motif. A critical element in the allosteric pathway that couples membrane binding to pore assembly. PLoS Pathog. 8, e1002787
48. Law, R. H., Lukoyanova, N., Voskoboinik, I., Caradoc-Davies, T. T., Baran, K., Dunstone, M. A., D'Angelo, M. E., Orlova, E. V., Coulibaly, F., Verschoor, S., Browne, K. A., Ciccone, A., Kuiper, M. J., Bird, P. I., Trapani, J. A., Saibil, H. R., and Whisstock, J. C. (2010) The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 468, 447-451
49. Rosado, C. J., Buckle, A. M., Law, R. H., Butcher, R. E., Kan, W. T., Bird, C. H., Ung, K., Browne, K. A., Baran, K., Bashtannyk-Puhalovich, T. A., Faux, N. G., Wong, W., Porter, C. J., Pike, R. N., Ellisdon, A. M., Pearce, M. C., Bottomley, S. P., Emsley, J., Smith, A. I., Rossjohn, J., Hartland, E. L., Voskoboinik, I., Trapani, J. A., Bird, P. I., Dunstone, M. A., and Whisstock, J. C. (2007) A common fold mediates vertebrate defense and bacterial attack. Science 317, 1548-1551
50. Lieberman, J. A., Frost, N. A., Hoppert, M., Fernandes, P. J., Vogt, S. L., Raivio, T. L., Blanpied, T. A., and Donnenberg, M. S. (2012) Outer membrane targeting, ultrastructure, and single molecule localization of the enteropathogenic Escherichia coli type IV pilus secretin BfpB. J. Bacteriol. 194, 1646-1658
51. Van der Meeren, R., Wen, Y., Van Gelder, P., Tommassen, J., Devreese, B., and Savvides, S. N. (2013) New insights into the assembly of bacterial secretins. Structural studies of the periplasmic domain of XcpQ from Pseudomonas aeruginosa. J. Biol. Chem. 288, 1214-1225
52. Wang, X., Pineau, C., Gu, S., Guschinskaya, N., Pickersgill, R. W., and Shevchik, V. E. (2012) Cysteine scanning mutagenesis and disulfide mapping analysis of arrangement of GspC and GspD protomers within the type 2 secretion system. J. Biol. Chem. 287, 19082-19093
53. Guilvout, I., Hardie, K. R., Sauvonnet, N., and Pugsley, A. P. (1999) Genetic dissection of the outer membrane secretin PulD. Are there distinct domains for multimerization and secretion specificity? J. Bacteriol. 181, 7212-7220
54. Daefler, S., Guilvout, I., Hardie, K. R., Pugsley, A. P., and Russel, M. (1997) The C-terminal domain of the secretin PulD contains the binding site for its cognate chaperone, PulS, and confers PulS dependence on pIVf1 function. Mol. Microbiol. 24, 465-475
55. Nickerson, N. N., Tosi, T., Dessen, A., Baron, B., Raynal, B., England, P., and Pugsley, A. P. (2011) Outer membrane targeting of secretin PulD protein relies on disordered domain recognition by a dedicated chaperone. J. Biol. Chem. 286, 38833-38843
56. Burgess, N. K., Dao, T. P., Stanley, A. M., and Fleming, K. G. (2008) β-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro. J. Biol. Chem. 283, 26748-26758
57. Huysmans, G. H., Radford, S. E., Baldwin, S. A., and Brockwell, D. J. (2012) Malleability of the folding mechanism of the outer membrane protein PagP. Parallel pathways and the effect of membrane elasticity. J. Mol. Biol. 416, 453-464
58. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656
59. McMorran, L. M., Bartlett, A. I., Huysmans, G. H., Radford, S. E., and Brockwell, D. J. (2013) Dissecting the effects of periplasmic chaperones on the in vitro folding of the outer membrane protein PagP. J. Mol. Biol 425, 3178-3191
60. Patel, G. J., Behrens-Kneip, S., Holst, O., and Kleinschmidt, J. H. (2009) The periplasmic chaperone Skp facilitates targeting, insertion, and folding of OmpA into lipid membranes with a negative membrane surface potential. Biochemistry 48, 10235-10245