P. aeruginosa PilT Structures with and without Nucleotide Reveal a Dynamic Type IV Pilus Retraction Motor

Journal of Molecular Biology

Volumn 400, Issue 5, 2010, Pages 1011-1021

  Misic, Ana M ^a   Satyshur, Kenneth A ^a   Forest, Katrina T ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Crystallography; Motor protein; P loop ATPase; Type IV pili

Indexed keywords

MOLECULAR MOTOR; PROTEIN PILT; TYPE 4 PILI; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; HUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 77954623239     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.05.066     Document Type: Article

References (48)

1. Mattick J.S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 2002, 56:289-314.
2. Varga J.J., Nguyen V., O'Brien D.K., Rodgers K., Walker R.A., Melville S.B. Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other clostridia. Mol. Microbiol. 2006, 62:680-694.
3. Bradley D.E. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can. J. Microbiol. 1980, 26:146-154.
4. Hansen J.K., Forest K.T. Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. J. Mol. Microbiol. Biotechnol. 2006, 11:192-207.
5. Craig L., Li J. Type IV pili: paradoxes in form and function. Curr. Opin. Struct. Biol. 2008, 18:267-277.
6. Sampaleanu L.M., Bonanno J.B., Ayers M., Koo J., Tammam S., Burley S.K., et al. Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex. J. Mol. Biol. 2009, 394:143-159.
7. Maier B., Potter L., So M., Long C.D., Seifert H.S., Sheetz M.P. Single pilus motor forces exceed 100 pN. Proc. Natl Acad. Sci. USA 2002, 99:16012-16017.
8. Biais N., Ladoux B., Higashi D., So M., Sheetz M. Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biol. 2008, 6:e87.
9. Satyshur K.A., Worzalla G.A., Meyer L.S., Heiniger E.K., Aukema K.G., Misic A.M., Forest K.T. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 2007, 15:363-376.
10. Chiang P., Sampaleanu L.M., Ayers M., Pahuta M., Howell P.L., Burrows L.L. Functional role of conserved residues in the characteristic secretion NTPase motifs of the Pseudomonas aeruginosa type IV pilus motor proteins PilB, PilT and PilU. Microbiology 2008, 154:114-126.
11. Hare S., Bayliss R., Baron C., Waksman G. A large domain swap in the VirB11 ATPase of Brucella suis leaves the hexameric assembly intact. J. Mol. Biol. 2006, 360:56-66.
12. Robien M.A., Krumm B.E., Sandkvist M., Hol W.G. Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae. J. Mol. Biol. 2003, 333:657-674.
13. Yeo H.J., Savvides S.N., Herr A.B., Lanka E., Waksman G. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 2000, 6:1461-1472.
14. Yamagata A., Tainer J.A. Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism. EMBO J. 2007, 26:878-890.
15. Aukema K.G., Kron E.M., Herdendorf T.J., Forest K.T. Functional dissection of a conserved motif within the pilus retraction protein PilT. J. Bacteriol. 2005, 187:611-618.
16. Landau M., Mayrose I., Rosenberg Y., Glaser F., Martz E., Pupko T., Ben-Tal N. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 2005, 33:W299-W302.
17. Zaitseva J., Jenewein S., Jumpertz T., Holland I.B., Schmitt L. H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 2005, 24:1901-1910.
18. Svergun D., Barberato C., Koch M.H.J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 1995, 28:768-773.
19. Lee R.A., Razaz M., Hayward S. The DynDom database of protein domain motions. Bioinformatics 2003, 19:1290-1291.
20. Wang J. Nucleotide-dependent domain motions within rings of the RecA/AAA(+) superfamily. J. Struct. Biol. 2004, 148:259-267.
21. 1-ATPase from bovine heart mitochondria. Nature 1994, 370:621-628.
22. Bochtler M., Hartmann C., Song H.K., Bourenkov G.P., Bartunik H.D., Huber R. The structures of HsIU and the ATP-dependent protease HsIU-HsIV. Nature 2000, 403:800-805.
23. Sousa M.C., Trame C.B., Tsuruta H., Wilbanks S.M., Reddy V.S., McKay D.B. Crystal and solution structures of an HslUV protease-chaperone complex. Cell 2000, 103:633-643.
24. Rohrwild M., Coux O., Huang H.C., Moerschell R.P., Yoo S.J., Seol J.H., et al. HslV-HslU: a novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome. Proc. Natl Acad. Sci. USA 1996, 93:5808-5813.
25. Boyer P.D. Catalytic site forms and controls in ATP synthase catalysis. Biochim. Biophys. Acta 2000, 1458:252-262.
26. Clausen M., Koomey M., Maier B. Dynamics of type IV pili is controlled by switching between multiple states. Biophys. J. 2009, 96:1169-1177.
27. Craig L., Volkmann N., Arvai A.S., Pique M.E., Yeager M., Egelman E.H., Tainer J.A. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol. Cell 2006, 23:651-662.
28. + motors reveal operating principles for ATP-fuelled machines. Nature 2005, 437:1115-1120.
29. Farr G.W., Furtak K., Rowland M.B., Ranson N.A., Saibil H.R., Kirchhausen T., Horwich A.L. Multivalent binding of nonnative substrate proteins by the chaperonin GroEL. Cell 2000, 100:561-573.
30. Chiang P., Habash M., Burrows L.L. Disparate subcellular localization patterns of Pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J. Bacteriol. 2005, 187:829-839.
31. Karuppiah V., Hassan D., Saleem M., Derrick J.P. Structure and oligomerization of the PilC type IV pilus biogenesis protein from Thermus thermophilus. Proteins 2010, 78:2049-2057.
32. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
33. Ter Horst R., Lolkema J.S. Rapid screening of membrane topology of secondary transport proteins. Biochim. Biophys. Acta 1798, 672-680.
34. Erlandson K.J., Miller S.B., Nam Y., Osborne A.R., Zimmer J., Rapoport T.A A role for the two-helix finger of the SecA ATPase in protein translocation. Nature 2008, 455:984-987.
35. + protein-unfolding machine. Cell 2009, 139:744-756.
36. + motor revealed by multiscale molecular simulations. Proc. Natl Acad. Sci. USA 2009, 106:18237-18242.
37. Crowther L.J., Anantha R.P., Donnenberg M.S. The inner membrane subassembly of the enteropathogenic Escherichia coli bundle-forming pilus machine. Mol. Microbiol. 2004, 52:67-79.
38. Pelicic V. Type IV pili: e pluribus unum?. Mol. Microbiol. 2008, 68:827-837.
39. Reyes N., Ginter C., Boudker O. Transport mechanism of a bacterial homologue of glutamate transporters. Nature 2009, 462:880-885.
40. Collins B.K., Tomanicek S.J., Lyamicheva N., Kaiser M.W., Mueser T.C. A preliminary solubility screen used to improve crystallization trials: crystallization and preliminary X-ray structure determination of Aeropyrum pernix flap endonuclease-1. Acta Crystallogr. Sect. D 2004, 60:1674-1678.
41. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003, 31:3784-3788.
42. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods in Enzymology: Macromolecular Crystallography, part A 1997, vol. 276:307-326. Academic Press, San Diego, CA. C.W. Carter, R.M. Sweet (Eds.).
43. Storoni L.C., McCoy A.J., Read R.J. Likelihood-enhanced fast rotation functions. Acta Crystallogr. Sect. D 2004, 60:432-438.
44. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 1999, 125:156-165.
45. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. Sect. D 1999, 55:247-255.
46. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
47. Tina K.G., Bhadra R., Srinivasan N. PIC: Protein Interactions Calculator. Nucleic Acids Res. 2007, 35:W473-W476.
48. DeLano W.L. The PyMOL Molecular Graphics System 2002, DeLano Scientific, Palo Alto, CA.