Steered Molecular Dynamics Simulations of a Type IV Pilus Probe Initial Stages of a Force-Induced Conformational Transition

PLoS Computational Biology

Volumn 9, Issue 4, 2013, Pages

  Baker, Joseph L ^a   Biais, Nicolas ^b   Tama, Florence ^c  

^a University of Arizona   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRON MICROSCOPES; STABILITY;

BACTERIAL MOTILITY; CAUSATIVE AGENTS; CONFORMATIONAL TRANSITIONS; CRYO-ELECTRON MICROSCOPY; GONORRHOEAE; MICROCOLONIES; NEISSERIA GONORRHEAE; PROTEIN FILAMENTS; STEERED MOLECULAR DYNAMICS SIMULATIONS; TYPE IV PILUS;

MOLECULAR DYNAMICS;

BACTERIAL PROTEIN; PILIN; PILIN ALPHA1; TYPE 4 PILI PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIUM PILUS; BINDING AFFINITY; COMPUTER MODEL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR PROBE; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STABILITY; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 84876911425     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003032     Document Type: Article

References (41)

1. Craig L, Pique ME, Tainer JA, (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2: 363-378.
2. Craig L, Li J, (2008) Type IV pili: Paradoxes in form and function. Curr Opin Struct Biol 18: 267-277.
3. Strom MS, Lory S, (1993) Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 47: 565-596.
4. Soto GE, Hultgren SJ, (1999) Bacterial Adhesins: Common Themes and Variations in Architecture and Assembly. J Bacteriol 181: 1059-1071.
5. Maurer L, Orndorff PE, (1987) Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili. J Bacteriol 169: 640-645.
6. Merz AJ, So M, Sheetz MP, (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102.
7. Maier B, Potter L, So M, Seifert HS, Sheetz MP, (2002) Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci 99: 16012-16017.
8. Biais N, Ladoux B, Higashi D, So M, Sheetz M, (2008) Cooperative Retraction of Bundled Type IV Pili Enables Nanonewton Force Generation. PloS Biol 6: e87.
9. Howie HL, Glogauer M, So M, (2005) The N. gonorrhoeae Type IV Pilus Stimulates Mechanosensitive Pathways and Cytoprotection through a pilT-Dependent Mechanism. PloS Biol 3: e100.
10. Higashi DL, Lee SW, Snyder A, Weyand NJ, Bakke A, et al. (2007) Dynamics of Neisseria gonorrhoeae Attachment: Microcolony Development, Cortical Plaque Formation, and Cytoprotection. Infect Immun 75: 4743-4753.
11. Higashi DL, Zhang GH, Biais N, Myers LR, Weyand NJ, et al. (2009) Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex. Microbiology 155: 4084-4092.
12. Biais N, Higashi DL, Brujic J, So M, Sheetz MP, (2010) Force-dependent polymorphism in type IV pili reveals hidden epitopes. Proc Natl Acad Sci 107: 11358-11363.
13. Giltner CL, Van Schaik EJ, Audette GF, Kao D, Hodges RS, et al. (2006) The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol Microbiol 59: 1083-1096.
14. Hsieh JC, Tham DM, Feng W, Huang F, Embaie S, et al. (2005) Intranasal immunization strategy to impede pilin-mediated binding of Pseudomonas aeruginosa to airway epithelial cells. Infect Immun 73: 7705-7717.
15. Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED, et al. (1995) Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378: 32-38.
16. Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, et al. (2003) Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 11: 1139-1150.
17. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, et al. (2006) Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23: 651-662.
18. Marceau M, Forest KT, Beretti JL, Tainer J, Nassif X, (1998) Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 27: 705-715.
19. Forest KT, Dunham SA, Koomey M, Tainer JA, (1999) Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 31: 743-752.
20. Stimson E, Virji M, Makepeace K, Dell A, Morris HR, et al. (1995) Meningococcal pilin: a glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol 17: 1201-1214.
21. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, et al. (2011) Posttranslational Modification of Pili upon Cell Contact Triggers N. meningitidis Dissemination. Science 331: 778-782.
22. Virji M, Heckels JE, (1984) The role of common and type- specific pilus antigenic domains in adhesion and virulence of gonococci for human epithelial cells. J Gen Microbiol 130: 1089-1095.
23. Stern A, Nickel P, Meyer TF, So M, (1984) Opacity determinants of Neisseria gonorrhoeae: gene expression and chromosomal linkage to the gonococcal pilus gene. Cell 37: 447-456.
24. Hagblom P, Segal E, Billyard E, So M, (1985) Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315: 156-158.
25. Vignon G, Kohler R, Larquet E, Giroux S, Prevost MC, et al. (2003) Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides. J Bacteriol 185: 3416-3428.
26. Campos M, Francetic O, Nilges M, (2011) Modeling pilus structures from sparse data. J Struct Biol 173: 436-444.
27. Hartung S, Arvai AS, Wood T, Kolappan S, Shin DS, et al. (2011) Ultra-high resolution and full-length pilin structures with insights for filament assembly, pathogenic functions, and vaccine potential. J Biol Chem 51: 44254-44265.
28. Chu JW, Voth GA, (2006) Coarse-Grained Modeling of the Actin Filament Derived from Atomistic-Scale Simulations. Biophys J 90: 1572-1582.
29. Wells DB, Aksimentiev A, (2010) Mechanical Properties of a Complete Microtubule Revealed through Molecular Dynamics Simulation. Biophys J 99: 629-637.
30. Isralewitz B, Baudry J, Gullingsrud J, Kosztin D, Schulten K, (2001) Steered molecular dynamics investigations of protein function. J Mol Graph Model 19: 13-25.
31. Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV, (2002) Bacterial Adhesion to Target Cells Enhanced by Shear Force. Cell 109: 913-923.
32. Nilsson LM, Thomas WE, Sokurenko EV, Vogel V, (2008) Beyond Induced-Fit Receptor-Ligand Interactions: Structural Changes that Can Significantly Extend Bond Lifetimes. Structure 16: 1047-1058.
33. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38.
34. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comp Chem 26: 1781-1802.
35. Mackerell AD, Feig M, Brooks CL, (2004) Extending the treatment of backbone energetics in protein force fields: Limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comp Chem 25: 1400-1415.
36. Pastor RW, Brooks BR, Szabo A, (1988) An analysis of the accuracy of langevin and molecular-dynamics algorithms. Mol Phys 65: 1409-1419.
37. Levin PA, (2002) Light Microscopy Techniques for Bacterial Cell Biology. Methods in Microbiology 31: 115-132.
38. Forest KT, Bernstein SL, Getzoff ED, So M, Tribbick G, et al. (1996) Assembly and antigenicity of the Neisseria gonorrhoeae pilus mapped with antibodies. Infect Immun 64: 644-652.
39. Audette GF, van Schaik EJ, Hazes B, Irvin RT, (2004) DNA-Binding Protein Nanotubes: Learning from Nature's Nanotech Examples. Nano Lett 4: 1897-1902.
40. Li J, Lim MS, Li S, Brock M, Pique ME, et al. (2008) Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure 16: 137-148.
41. Craig L, Egelman EH, Li J, (2012) Structure of the Vibrio cholera Type IVb Pilus and Stability Comparison with the Neisseria gonorrhoeae Type IVa Pilus. J Mol Biol 418: 47-64.