ATP-independent control of autotransporter virulence protein transport via the folding properties of the secreted protein

Chemistry and Biology

Volumn 19, Issue 2, 2012, Pages 287-296

  Renn, Jonathan P ^a,b   Junker, Mirco ^a,c   Besingi, Richard N ^a   Braselmann, Esther ^a   Clark, Patricia L ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AUTOTRANSPORTER PROTEIN; BACTERIAL PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN TRANSPORT;

ADENOSINE TRIPHOSPHATE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TETRAHYDROFOLATE DEHYDROGENASE; VIRULENCE FACTORS, BORDETELLA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84857175966     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2011.11.009     Document Type: Article

References (50)

1. J. Abramson, and E.M. Wright Structure and function of Na(+)-symporters with inverted repeats Curr. Opin. Struct. Biol. 19 2009 425 432
2. M. Arai, K. Maki, H. Takahashi, and M. Iwakura Testing the relationship between foldability and the early folding events of dihydrofolate reductase from Escherichia coli J. Mol. Biol. 328 2003 273 288 (Pubitemid 36390295)
3. R.D. Astumian Thermodynamics and kinetics of a Brownian motor Science 276 1997 917 922 (Pubitemid 27209083)
4. H.D. Bernstein Are bacterial 'autotransporters' really transporters? Trends Microbiol. 15 2007 441 447 (Pubitemid 350026356)
5. J.D. Bloom, S.T. Labthavikul, C.R. Otey, and F.H. Arnold Protein stability promotes evolvability Proc. Natl. Acad. Sci. USA 103 2006 5869 5874
6. P.L. Clark Protein folding in the cell: reshaping the folding funnel Trends Biochem. Sci. 29 2004 527 534 (Pubitemid 39265169)
7. N. Dautin, T.J. Barnard, D.E. Anderson, and H.D. Bernstein Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism EMBO J. 26 2007 1942 1952 (Pubitemid 46624049)
8. P.R. Dutta, R. Cappello, F. Navarro-García, and J.P. Nataro Functional comparison of serine protease autotransporters of enterobacteriaceae Infect. Immun. 70 2002 7105 7113 (Pubitemid 35387948)
9. P.R. Dutta, B.Q. Sui, and J.P. Nataro Structure-function analysis of the enteroaggregative Escherichia coli plasmid-encoded toxin autotransporter using scanning linker mutagenesis J. Biol. Chem. 278 2003 39912 39920 (Pubitemid 37248555)
10. P. Emsley, I.G. Charles, N.F. Fairweather, and N.W. Isaacs Structure of Bordetella pertussis virulence factor P.69 pertactin Nature 381 1996 90 92 (Pubitemid 26130010)
11. E.J. Enemark, and L. Joshua-Tor On helicases and other motor proteins Curr. Opin. Struct. Biol. 18 2008 243 257
12. K.A. Gangwer, D.J. Mushrush, D.L. Stauff, B. Spiller, M.S. McClain, T.L. Cover, and D.B. Lacy Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain Proc. Natl. Acad. Sci. USA 104 2007 16293 16298 (Pubitemid 350099399)
13. E.P. Garvey, and C.R. Matthews Effects of multiple replacements at a single position on the folding and stability of dihydrofolate reductase from Escherichia coli Biochemistry 28 1989 2083 2093
14. I.R. Henderson, F. Navarro-Garcia, and J.P. Nataro The great escape: structure and function of the autotransporter proteins Trends Microbiol. 6 1998 370 378 (Pubitemid 28473198)
15. R. Ieva, and H.D. Bernstein Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane Proc. Natl. Acad. Sci. USA 106 2009 19120 19125
16. M. Iwakura, B.E. Jones, C.J. Falzone, and C.R. Matthews Collapse of parallel folding channels in dihydrofolate reductase from Escherichia coli by site-directed mutagenesis Biochemistry 32 1993 13566 13574 (Pubitemid 24020233)
17. S. Jain, and M.B. Goldberg Requirement for YaeT in the outer membrane assembly of autotransporter proteins J. Bacteriol. 189 2007 5393 5398 (Pubitemid 47076086)
18. P.A. Jennings, B.E. Finn, B.E. Jones, and C.R. Matthews A reexamination of the folding mechanism of dihydrofolate reductase from Escherichia coli: verification and refinement of a four-channel model Biochemistry 32 1993 3783 3789 (Pubitemid 23126957)
19. T.A. Johnson, J. Qiu, A.G. Plaut, and T. Holyoak Active-site gating regulates substrate selectivity in a chymotrypsin-like serine protease the structure of haemophilus influenzae immunoglobulin A1 protease J. Mol. Biol. 389 2009 559 574
20. W.S. Jong, C.M. ten Hagen-Jongman, T. den Blaauwen, D.J. Slotboom, J.R. Tame, D. Wickström, J.W. de Gier, B.R. Otto, and J. Luirink Limited tolerance towards folded elements during secretion of the autotransporter Hbp Mol. Microbiol. 63 2007 1524 1536
21. J. Jose Autodisplay: efficient bacterial surface display of recombinant proteins Appl. Microbiol. Biotechnol. 69 2006 607 614 (Pubitemid 43130568)
22. J. Jose, and T.F. Meyer The autodisplay story, from discovery to biotechnical and biomedical applications Microbiol. Mol. Biol. Rev. 71 2007 600 619 (Pubitemid 350309179)
23. J. Jose, J. Krämer, T. Klauser, J. Pohlner, and T.F. Meyer Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Iga beta autotransporter pathway Gene 178 1996 107 110 (Pubitemid 26377136)
24. M. Junker, and P.L. Clark Slow formation of aggregation-resistant β-sheet folding intermediates Proteins 78 2010 812 824
25. M. Junker, C.C. Schuster, A.V. McDonnell, K.A. Sorg, M.C. Finn, B. Berger, and P.L. Clark Pertactin β-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins Proc. Natl. Acad. Sci. USA 103 2006 4918 4923
26. M. Junker, R.N. Besingi, and P.L. Clark Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion Mol. Microbiol. 71 2009 1323 1332
27. A.V. Kajava, N. Cheng, R. Cleaver, M. Kessel, M.N. Simon, E. Willery, F. Jacob-Dubuisson, C. Locht, and A.C. Steven β-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins Mol. Microbiol. 42 2001 279 292 (Pubitemid 32990120)
28. T. Klauser, J. Pohlner, and T.F. Meyer Extracellular transport of cholera toxin B subunit using Neisseria IgA protease β-domain: conformation-dependent outer membrane translocation EMBO J. 9 1990 1991 1999
29. H. Krishnamurthy, C.L. Piscitelli, and E. Gouaux Unlocking the molecular secrets of sodium-coupled transporters Nature 459 2009 347 355
30. E. Leininger, M. Roberts, J.G. Kenimer, I.G. Charles, N. Fairweather, P. Novotny, and M.J. Brennan Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells Proc. Natl. Acad. Sci. USA 88 1991 345 349 (Pubitemid 21915462)
31. D.L. Leyton, Y.R. Sevastsyanovich, D.F. Browning, A.E. Rossiter, T.J. Wells, R.E. Fitzpatrick, M. Overduin, A.F. Cunningham, and I.R. Henderson Size and conformation limits to secretion of disulfide-bonded loops in autotransporter proteins J. Biol. Chem. 286 2011 42283 42291
32. B.J. Loveless, and M.H. Saier Jr. A novel family of channel-forming, autotransporting, bacterial virulence factors Mol. Membr. Biol. 14 1997 113 123 (Pubitemid 27478675)
33. D.S. Martin, R. Fathi, T.J. Mitchison, and J. Gelles FRET measurements of kinesin neck orientation reveal a structural basis for processivity and asymmetry Proc. Natl. Acad. Sci. USA 107 2010 5453 5458
34. S. Myong, and T. Ha Stepwise translocation of nucleic acid motors Curr. Opin. Struct. Biol. 20 2010 121 127
35. F. Navarro-García, A. Canizalez-Roman, J. Luna, C. Sears, and J.P. Nataro Plasmid-encoded toxin of enteroaggregative Escherichia coli is internalized by epithelial cells Infect. Immun. 69 2001 1053 1060 (Pubitemid 32109573)
36. B.R. Otto, R. Sijbrandi, J. Luirink, B. Oudega, J.G. Heddle, K. Mizutani, S.Y. Park, and J.R. Tame Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli J. Biol. Chem. 280 2005 17339 17345 (Pubitemid 41389203)
37. C. Park, and S. Marqusee Pulse proteolysis: a simple method for quantitative determination of protein stability and ligand binding Nat. Methods 2 2005 207 212 (Pubitemid 41122128)
38. K.M. Perry, J.J. Onuffer, N.A. Touchette, C.S. Herndon, M.S. Gittelman, C.R. Matthews, J.T. Chen, R.J. Mayer, K. Taira, and S.J. Benkovic Effect of single amino acid replacements on the folding and stability of dihydrofolate reductase from Escherichia coli Biochemistry 26 1987 2674 2682 (Pubitemid 17084637)
39. J.H. Peterson, P. Tian, R. Ieva, N. Dautin, and H.D. Bernstein Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment Proc. Natl. Acad. Sci. USA 107 2010 17739 17744
40. J.P. Renn, and P.L. Clark A conserved stable core structure in the passenger domain β-helix of autotransporter virulence proteins Biopolymers 89 2008 420 427
41. A. Sauri, Z. Soprova, D. Wickström, J.W. de Gier, R.C. Van der Schors, A.B. Smit, W.S. Jong, and J. Luirink The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease Microbiology 155 2009 3982 3991
42. K.M. Skillman, T.J. Barnard, J.H. Peterson, R. Ghirlando, and H.D. Bernstein Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter Mol. Microbiol. 58 2005 945 958 (Pubitemid 41667217)
43. J.G. Sklar, T. Wu, D. Kahne, and T.J. Silhavy Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli Genes Dev. 21 2007 2473 2484 (Pubitemid 47529375)
44. D.G. Thanassi, C. Stathopoulos, A. Karkal, and H. Li Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of gram-negative bacteria (review) Mol. Membr. Biol. 22 2005 63 72 (Pubitemid 40692155)
45. N.A. Touchette, K.M. Perry, and C.R. Matthews Folding of dihydrofolate reductase from Escherichia coli Biochemistry 25 1986 5445 5452
46. B. van den Berg Crystal structure of a full-length autotransporter J. Mol. Biol. 396 2010 627 633
47. E. Veiga, V. de Lorenzo, and L.A. Fernández Structural tolerance of bacterial autotransporters for folded passenger protein domains Mol. Microbiol. 52 2004 1069 1080 (Pubitemid 38916174)
48. R. Voulhoux, M.P. Bos, J. Geurtsen, M. Mols, and J. Tommassen Role of a highly conserved bacterial protein in outer membrane protein assembly Science 299 2003 262 265 (Pubitemid 36125214)
49. F. Zhang, M. Hu, G. Tian, P. Zhang, D. Finley, P.D. Jeffrey, and Y. Shi Structural insights into the regulatory particle of the proteasome from Methanocaldococcus jannaschii Mol. Cell 34 2009 473 484
50. M. Zolkiewski A camel passes through the eye of a needle: protein unfolding activity of Clp ATPases Mol. Microbiol. 61 2006 1094 1100 (Pubitemid 44215414)