An alternative outer membrane secretion mechanism for an autotransporter protein lacking a C-terminal stable core

Molecular Microbiology

Volumn 90, Issue 5, 2013, Pages 1028-1045

  Besingi, Richard N ^a,b   Chaney, Julie L ^a   Clark, Patricia L ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOTRANSPORTER PROTEIN; CARRIER PROTEIN; ICSA PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; UNCLASSIFIED DRUG; YAPV PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GRAM NEGATIVE BACTERIUM; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STABILITY; SEQUENCE HOMOLOGY; SHIGELLA FLEXNERI; YERSINIA PESTIS;

MAMMALIA; NEGIBACTERIA; SHIGELLA; YERSINIA;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CIRCULAR DICHROISM; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; WISKOTT-ALDRICH SYNDROME PROTEIN; YERSINIA PESTIS;

EID: 84888316691     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12414     Document Type: Article

References (66)

1. Ackerman, M.S., and Shortle, D. (2002) Molecular alignment of denatured states of staphylococcal nuclease with strained polyacrylamide gels and surfactant liquid crystalline phases. Biochemistry 41: 3089-3095.
2. Alexandrescu, A.T., Abeygunawardana, C., and Shortle, D. (1994) Structure and dynamics of a denatured 131-residue fragment of staphylococcal nuclease: a heteronuclear NMR study. Biochemistry 33: 1063-1072.
3. Bagos, P.G., Liakopoulos, T.D., Spyropoulos, I.C., and Hamodrakas, S.J. (2004) PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res 32: W400-W404.
4. Barnard, T.J., Dautin, N., Lukacik, P., Bernstein, H.D., and Buchanan, S.K. (2007) Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat Struct Mol Biol 14: 1214-1220.
5. Benz, I., and Schmidt, M.A. (1992) AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule. Mol Microbiol 6: 1539-1546.
6. van den Berg, B. (2010) Crystal structure of a full-length autotransporter. J Mol Biol 396: 627-633.
7. Brunder, W., Schmidt, H., and Karch, H. (1997) EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V. Mol Microbiol 24: 767-778.
8. Celik, N., Webb, C.T., Leyton, D.L., Holt, K.E., Heinz, E., Gorrell, R., etal. (2012) A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS ONE 7: e43245.
9. Charbonneau, M.E., Berthiaume, F., and Mourez, M. (2006) Proteolytic processing is not essential for multiple functions of the Escherichia coli autotransporter adhesin involved in diffuse adherence (AIDA-I). J Bacteriol 188: 8504-8512.
10. Charbonneau, M.E., Janvore, J., and Mourez, M. (2009) Autoprocessing of the Escherichia coli AIDA-I autotransporter: a new mechanism involving acidic residues in the junction region. J Biol Chem 284: 17340-17351.
11. Dautin, N., and Bernstein, H.D. (2007) Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61: 89-112.
12. Dautin, N., Barnard, T.J., Anderson, D.E., and Bernstein, H.D. (2007) Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J 26: 1942-1952.
13. Deng, W., Burland, V., Plunkett, G., 3rd, Boutin, A., Mayhew, G.F., Liss, P., etal. (2002) Genome sequence of Yersinia pestis KIM. J Bacteriol 184: 4601-4611.
14. 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.
15. Eslava, C., Navarro-Garcia, F., Czeczulin, J.R., Henderson, I.R., Cravioto, A., and Nataro, J.P. (1998) Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66: 3155-3163.
16. Henderson, I.R., and Nataro, J.P. (2001) Virulence functions of autotransporter proteins. Infect Immun 69: 1231-1243.
17. Henderson, I.R., Navarro-Garcia, F., and Nataro, J.P. (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-378.
18. Henderson, I.R., Navarro-Garcia, F., Desvaux, M., Fernandez, R.C., and Ala'Aldeen, D. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692-744.
19. Hiller, K., Schobert, M., Hundertmark, C., Jahn, D., and Munch, R. (2003) JVirGel: calculation of virtual two-dimensional protein gels. Nucleic Acids Res 31: 3862-3865.
20. Ho, H.Y., Rohatgi, R., Lebensohn, A.M., Le, M., Li, J., Gygi, S.P., and Kirschner, M.W. (2004) Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell 118: 203-216.
21. 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 USA 106: 19120-19125.
22. Ieva, R., Tian, P., Peterson, J.H., and Bernstein, H.D. (2011) Sequential and spatially restricted interactions of assembly factors with an autotransporter beta domain. Proc Natl Acad Sci USA 108: E383-E391.
23. Jain, S., van Ulsen, P., Benz, I., Schmidt, M.A., Fernandez, R., Tommassen, J., and Goldberg, M.B. (2006) Polar localization of the autotransporter family of large bacterial virulence proteins. J Bacteriol 188: 4841-4850.
24. Jose, J., Jahnig, F., and Meyer, T.F. (1995) Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol Microbiol 18: 378-380.
25. Junker, M., Schuster, C.C., McDonnell, A.V., Sorg, K.A., Finn, M.C., Berger, B., and Clark, P.L. (2006) Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc Natl Acad Sci USA 103: 4918-4923.
26. Junker, M., Besingi, R.N., and Clark, P.L. (2009) Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol Microbiol 71: 1323-1332.
27. Larkin, M.A., Blackshields, G., Brown, N., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
28. Lenz, J.D., Lawrenz, M.B., Cotter, D.G., Lane, M.C., Gonzalez, R.J., Palacios, M., and Miller, V.L. (2011) Expression during host infection and localization of Yersinia pestis autotransporter proteins. J Bacteriol 193: 5936-5949.
29. Lenz, J.D., Temple, B.R., and Miller, V.L. (2012) Evolution and virulence contributions of the autotransporter proteins YapJ and YapK of Yersinia pestis CO92 and their homologs in Y.pseudotuberculosis IP32953. Infect Immun 80: 3693-3705.
30. Leyton, D.L., Sevastsyanovich, Y.R., Browning, D.F., Rossiter, A.E., Wells, T.J., Fitzpatrick, R.E., etal. (2011) Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins. J Biol Chem 286: 42283-42291.
31. Loveless, B.J., and Saier, M.H., Jr. (1997) A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol Membr Biol 14: 113-123.
32. McDonnell, A.V., Menke, M., Palmer, N., King, J., Cowen, L., and Berger, B. (2006) Fold recognition and accurate sequence-structure alignment of sequences directing beta-sheet proteins. Proteins 63: 976-985.
33. Mansell, T.J., Linderman, S.W., Fisher, A.C., and DeLisa, M.P. (2010) A rapid protein folding assay for the bacterial periplasm. Protein Sci 19: 1079-1090.
34. Marchler-Bauer, A., Zheng, C., Chitsaz, F., Derbyshire, M.K., Geer, L.Y., Geer, R.C., etal. (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41: D348-D352.
35. May, K.L., and Morona, R. (2008) Mutagenesis of the Shigella flexneri autotransporter IcsA reveals novel functional regions involved in IcsA biogenesis and recruitment of host neural Wiscott-Aldrich syndrome protein. J Bacteriol 190: 4666-4676.
36. Neira, J.L., and Fersht, A.R. (1999) Acquisition of native-like interactions in C-terminal fragments of barnase. J Mol Biol 287: 421-432.
37. Newman, C.L., and Stathopoulos, C. (2004) Autotransporter and two-partner secretion: delivery of large-size virulence factors by gram-negative bacterial pathogens. Crit Rev Microbiol 30: 275-286.
38. Nishimura, K., Tajima, N., Yoon, Y.H., Park, S.Y., and Tame, J.R. (2010) Autotransporter passenger proteins: virulence factors with common structural themes. J Mol Med 88: 451-458.
39. Ohnishi, Y., Nishiyama, M., Horinouchi, S., and Beppu, T. (1994) Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J Biol Chem 269: 32800-32806.
40. Oliver, D.C., Huang, G., and Fernandez, R.C. (2003a) Identification of secretion determinants of the Bordetella pertussis BrkA autotransporter. J Bacteriol 185: 489-495.
41. Oliver, D.C., Huang, G., Nodel, E., Pleasance, S., and Fernandez, R.C. (2003b) A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 47: 1367-1383.
42. Pavlova, O., Peterson, J.H., Ieva, R., and Bernstein, H.D. (2013) Mechanistic link between beta barrel assembly and the initiation of autotransporter secretion. Proc Natl Acad Sci USA 110: E938-E947.
43. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
44. Peterson, J.H., Tian, P., Ieva, R., Dautin, N., and Bernstein, H.D. (2010) Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment. Proc Natl Acad Sci USA 107: 17739-17744.
45. Renn, J.P., and Clark, P.L. (2008) A conserved stable core structure in the passenger domain beta-helix of autotransporter virulence proteins. Biopolymers 89: 420-427.
46. Renn, J.P., Junker, M., Besingi, R.N., Braselmann, E., and Clark, P.L. (2012) ATP-independent control of autotransporter virulence protein transport via the folding properties of the secreted protein. Chem Biol 19: 287-296.
47. Ruiz-Perez, F., Henderson, I.R., Leyton, D.L., Rossiter, A.E., Zhang, Y., and Nataro, J.P. (2009) Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191: 6571-6583.
48. Ruiz-Perez, F., Henderson, I.R., and Nataro, J. (2010) Interaction of FkpA, a peptidyl-prolyl cis/trans isomerase with EspP autotransporter protein. Gut Microbes 1: 339-344.
49. St Geme, J.W., 3rd, and Cutter, D. (2000) The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J Bacteriol 182: 6005-6013.
50. Sauri, A., Oreshkova, N., Soprova, Z., Jong, W.S., Sani, M., Peters, P.J., etal. (2011) Autotransporter beta-domains have a specific function in protein secretion beyond outer-membrane targeting. J Mol Biol 412: 553-567.
51. Sauri, A., Ten Hagen-Jongman, C.M., van Ulsen, P., and Luirink, J. (2012) Estimating the size of the active translocation pore of an autotransporter. J Mol Biol 416: 335-345.
52. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
53. Shere, K.D., Sallustio, S., Manessis, A., D'Aversa, T.G., and Goldberg, M.B. (1997) Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol Microbiol 25: 451-462.
54. Shortle, D., and Ackerman, M.S. (2001) Persistence of native-like topology in a denatured protein in 8M urea. Science 293: 487-489.
55. Song, Y., Tong, Z., Wang, J., Wang, L., Guo, Z., Han, Y., etal. (2004) Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res 11: 179-197.
56. Soprova, Z., Sauri, A., van Ulsen, P., Tame, J.R., den Blaauwen, T., Jong, W.S., and Luirink, J. (2010) A conserved aromatic residue in the autochaperone domain of the autotransporter Hbp is critical for initiation of outer membrane translocation. J Biol Chem 285: 38224-38233.
57. Suzuki, T., Miki, H., Takenawa, T., and Sasakawa, C. (1998) Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J 17: 2767-2776.
58. Suzuki, T., Mimuro, H., Suetsugu, S., Miki, H., Takenawa, T., and Sasakawa, C. (2002) Neural Wiskott-Aldrich syndrome protein (N-WASP) is the specific ligand for Shigella VirG among the WASP family and determines the host cell type allowing actin-based spreading. Cell Microbiol 4: 223-233.
59. Teh, M.Y., and Morona, R. (2013) Identification of Shigella flexneri IcsA residues affecting interaction with N-WASP, and evidence for IcsA-IcsA co-operative interaction. PLoS ONE 8: e55152.
60. Teh, M.Y., Tran, E.N., and Morona, R. (2012) Absence of O antigen suppresses Shigella flexneri IcsA autochaperone region mutations. Microbiology 158: 2835-2850.
61. Thanassi, D.G., Stathopoulos, C., Karkal, A., and Li, H. (2005) Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of gram-negative bacteria. Mol Membr Biol 22: 63-72.
62. 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.
63. Watts, K.M., and Hunstad, D.A. (2008) Components of SurA required for outer membrane biogenesis in uropathogenic Escherichia coli. PLoS ONE 3: e3359.
64. Wing, H.J., Yan, A.W., Goldman, S.R., and Goldberg, M.B. (2004) Regulation of IcsP, the outer membrane protease of the Shigella actin tail assembly protein IcsA, by virulence plasmid regulators VirF and VirB. J Bacteriol 186: 699-705.
65. Yanagida, N., Uozumi, T., and Beppu, T. (1986) Specific excretion of Serratia marcescens protease through the outer membrane of Escherichia coli. J Bacteriol 166: 937-944.
66. Yen, Y.T., Karkal, A., Bhattacharya, M., Fernandez, R.C., and Stathopoulos, C. (2007) Identification and characterization of autotransporter proteins of Yersinia pestis KIM. Mol Membr Biol 24: 28-40.