Exceptionally widespread nanomachines composed of type IV pilins: The prokaryotic Swiss Army knives

FEMS Microbiology Reviews

Volumn 39, Issue 1, 2015, Pages 134-154

  Berry, Jamie Lee ^a   Pelicic, Vladimir ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Archaellum; Class III signal peptide; Prepilin peptidase; Type II secretion system; Type IV pilus

Indexed keywords

ADENOSINE TRIPHOSPHATASE; PERIPLASMIC PROTEIN; PILIN; SIGNAL PEPTIDE; TYPE IV PILIN; UNCLASSIFIED DRUG; FIMBRIA PROTEIN;

BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIUM PILUS; BIOGENESIS; CELL MEMBRANE; CELL MOTILITY; DNA BINDING; ELECTRIC CONDUCTANCE; GENETIC TRANSFORMATION; GENETIC VARIABILITY; NONHUMAN; PERMEABILITY BARRIER; PROKARYOTE; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; SURFACE PROPERTY; TWITCHING MOTILITY; TYPE II SECRETION SYSTEM; ARCHAEON; BACTERIUM; CHEMISTRY; CLASSIFICATION; FIMBRIA; METABOLISM; PROTEIN FOLDING; PROTEIN TERTIARY STRUCTURE;

ARCHAEA; BACTERIA; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84931270409     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuu001     Document Type: Review

References (250)

1. Aas FE, Winther-Larsen HC, Wolfgang M, et al. Substitutions in the N-terminal alpha helical spine of Neisseria gonorrhoeae pilin affect type IV pilus assembly, dynamics and associated functions. Mol Microbiol 2007;63:69-85.
2. Abendroth J, Bagdasarian M, Sandkvist M, et al. The structure of the cytoplasmic domain of EpsL, an inner membrane component of the type II secretion system of Vibrio cholerae: an unusual member of the actin-like ATPase superfamily. J Mol Biol 2004;344:619-33.
3. Abendroth J, Kreger AC, Hol WG. The dimer formed by the periplasmic domain of EpsL from the type 2 secretion system of Vibrio parahaemolyticus. J Struct Biol 2009;168:313-22.
4. Abendroth J, Mitchell DD, Korotkov KV, et al. The three dimensional structure of the cytoplasmic domains of EpsF from the type 2 secretion system of Vibrio cholerae. J Struct Biol 2009;166:303-15.
5. Abendroth J, Murphy P, Sandkvist M, et al. The X-ray structure of the type II secretion system complex formed by the Nterminal domain of EpsE and the cytoplasmic domain of EpsL of Vibrio cholerae. J Mol Biol 2005;348:845-55.
6. Abendroth J, Rice AE, McLuskey K, et al. The crystal structure of the periplasmic domain of the type II secretion system protein EpsM from Vibrio cholerae: the simplest version of the ferredoxin fold. J Mol Biol 2004;338:585-96.
7. Akahane K, Sakai D, Furuya N, et al. Analysis of the pilU gene for the prepilin peptidase involved in the biogenesis of type IV pili encoded by plasmid R64. Mol Genet Genomics 2005;273:350-9.
8. Alm RA, Bodero AJ, Free PD, et al. Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 1996;178:46-53.
9. Alm RA, Hallinan JP, Watson AA, et al. Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol Microbiol 1996;22:161-73.
10. Alm RA, Mattick JS. Genes involved in the biogenesis and function of type 4 fimbriae in Pseudomonas aeruginosa. Gene 1997;192:89-98.
11. Aly KA, Beebe ET, Chan CH, et al. Cell-free production of integral membrane aspartic acid proteases reveals zinc-dependent methyltransferase activity of the Pseudomonas aeruginosa prepilin peptidase PilD. Microbiologyopen 2013;2:94-104.
12. Arts J, de Groot A, Ball G, et al. Interaction domains in the Pseudomonas aeruginosa type II secretory apparatus component XcpS (GspF). Microbiology 2007;153:1582-92.
13. Arts J, van Boxtel R, Filloux A, et al. Export of the pseudopilin XcpT of the Pseudomonas aeruginosa type II secretion system via the signal recognition particle-Sec pathway. J Bacteriol 2007;189:2069-76.
14. Aukema KG, Kron EM, Herdendorf TJ, et al. Functional dissection of a conserved motif within the pilus retraction protein PilT. J Bacteriol 2005;187:611-8.
15. Ayers M, Howell PL, Burrows LL. Architecture of the type II secretion and type IV pilus machineries. Future Microbiol 2010;5:1203-18.
16. Ayers M, Sampaleanu LM, Tammam S, et al. PilM/N/O/P proteins form an inner membrane complex that affects the stability of the Pseudomonas aeruginosa type IV pilus secretin. J Mol Biol 2009;394:128-42.
17. Baker JL, Biais N, Tama F. Steered molecular dynamics simulations of a type IV pilus probe initial stages of a force-induced conformational transition. PLoS Comput Biol 2013;9:e1003032.
18. Balaban M, Battig P, Muschiol S, et al. Secretion of a pneumococcal type II secretion system pilus correlates with DNA uptake during transformation. Proc Natl Acad Sci USA 2014;111:E758-65.
19. Balasingham SV, Collins RF, Assalkhou R, et al. Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J Bacteriol 2007;189:5716-27.
20. Banerjee A, Neiner T, Tripp P, et al. Insights into subunit interactions in the Sulfolobus acidocaldarius archaellum cytoplasmic complex. FEBS J 2013;280:6141-9.
21. Bardy SL, Jarrell KF. Cleavage of preflagellins by an aspartic acid signal peptidase is essential for flagellation in the archaeon Methanococcus voltae. Mol Microbiol 2003;50:1339-47.
22. Bernard SC, Simpson N, Join-Lambert O, et al. Pathogenic Neisseria meningitidis utilizes CD147 for vascular colonization. Nat Med 2014;20:725-31.
23. Berry JL, Cehovin A, McDowell MA, et al. Functional analysis of the interdependence between DNA uptake sequence and its cognate ComP receptor during natural transformation in Neisseria species. PLoS Genet 2013;9:e1004014.
24. Berry JL, Phelan MM, Collins RF, et al. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS Pathog 2012;8:e1002923.
25. Bhaya D, Bianco NR, Bryant D, et al. Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Mol Microbiol 2000;37:941-51.
26. Biais N, Higashi DL, Brujic J, et al. Force-dependent polymorphism in type IV pili reveals hidden epitopes. Proc Natl Acad Sci USA 2010;107:11358-63.
27. Biais N, Ladoux B, Higashi D, et al. Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biol 2008;6:e87.
28. Bieber D, Ramer SW, Wu C, et al. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 1998;280:2114-8.
29. Blank TE, Donnenberg MS. Novel topology of BfpE, a cytoplasmic membrane protein required for type IV fimbrial biogenesis in enteropathogenic Escherichia coli. J Bacteriol 2001;183:4435-50.
30. Boesen T, Nielsen LP. Molecular dissection of bacterial nanowires. mBio 2013;4:e00270-13.
31. Bradley DE. Shortening of Pseudomonas aeruginosa pili after RNAphage adsorption. J Gen Microbiol 1972;72:303-19.
32. Bradley DE. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol 1980;26: 146-54.
33. Brossay L, Paradis G, Fox R, et al. Identification, localization, and distribution of the PilT protein in Neisseria gonorrhoeae. Infect Immun 1994;62:2302-8.
34. Brown D, Helaine S, Carbonnelle E, et al. Systematic functional analysis reveals that a set of 7 genes is involved in fine tuning of themultiple functions mediated by type IV pili in Neisseria meningitidis. Infect Immun 2010;78:3053-63.
35. Burkhardt J, Vonck J, Langer JD, et al. Unusual N-terminal ααßαßßα fold of PilQ from Thermus thermophilus mediates ring formation and is essential for piliation. J Biol Chem 2012;287:8484-94.
36. Camberg JL, Johnson TL, Patrick M, et al. Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids. EMBO J 2007;26:19-27.
37. Campos M, Francetic O, Nilges M. Modeling pilus structures from sparse data. J Struct Biol 2011;173:436-44.
38. Campos M, Nilges M, Cisneros DA, et al. Detailed structural and assembly model of the type II secretion pilus from sparse data. Proc Natl Acad Sci USA 2010;107:13081-6.
39. Carbonnelle E, Helaine S, Nassif X, et al. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol 2006;61:1510-22.
40. Carbonnelle E, Helaine S, Prouvensier L, et al. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fiber stability and function. Mol Microbiol 2005;55:54-64.
41. Cegelski L, Pinkner JS, Hammer ND, et al. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 2009;5:913-9.
42. Cehovin A, Simpson PJ, McDowell MA, et al. Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci USA 2013;110:3065-70.
43. Chaban B, Voisin S, Kelly J, et al. Identification of genes involved in the biosynthesis and attachment of Methanococcus voltae N-linked glycans: insight into N-linked glycosylation pathways in Archaea. Mol Microbiol 2006;61:259-68.
44. Chami M, Guilvout I, Gregorini M, et al. Structural insights into the secretin PulD and its trypsin-resistant core. J Biol Chem 2005;280:37732-41.
45. Chen I, Dubnau D. DNA uptake during bacterial transformation. Nat Rev Microbiol 2004;2:241-9.
46. Cheng Y, Johnson MD, Burillo-Kirch C, et al. Mutation of the conserved calcium-binding motif in Neisseria gonorrhoeae PilC1 impacts adhesion but not piliation. Infect Immun 2013;81:4280-9.
47. Chiang P, Habash M, Burrows LL. Disparate subcellular localization patterns of Pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J Bacteriol 2005;187:829-39.
48. Chiang SL, Taylor RK, Koomey M, et al. Single amino acid substitutions in the N-terminus of Vibrio cholerae TcpA affect colonization, autoagglutination, and serum resistance. Mol Microbiol 1995;17:1133-42.
49. Cisneros DA, Bond PJ, Pugsley AP, et al. Minor pseudopilin selfassembly primes type II secretion pseudopilus elongation. EMBO J 2012;31:1041-53.
50. Cisneros DA, Pehau-Arnaudet G, Francetic O. Heterologous assembly of type IV pili by a type II secretion system reveals the role of minor pilins in assembly initiation. Mol Microbiol 2012;86:805-18.
51. Collins RF, Frye SA, Balasingham S, et al. Interaction with type IV pili induces structural changes in the bacterial outer membrane secretin PilQ. J Biol Chem 2005;280:18923-30.
52. Collins RF, Frye SA, Kitmitto A, et al. Structure of the Neisseria meningitidis outer membrane PilQ secretin complex at 12 Å resolution. J Biol Chem 2004;279:39750-6.
53. Coureuil M, Lecuyer H, Scott MG, et al. Meningococcus hijacks a ß2-adrenoceptor/ß-arrestin pathway to cross brain microvasculature endothelium. Cell 2010;143: 1149-60.
54. Craig L, Pique ME, Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004;2:363-78.
55. Craig L, Taylor RK, Pique ME, et al. Type IV pilin structure and assembly. X-ray and EM analyses of Vibrio cholerae toxincoregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 2003;11:1139-50.
56. Craig L, Volkmann N, Arvai AS, et al. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 2006;23:651-62.
57. D'Enfert C, Pugsley AP. Klebsiella pneumoniae pulS gene encodes an outer membrane lipoprotein required for pullulanase secretion. J Bacteriol 1989;171:3673-9.
58. D'Enfert C, Ryter A, Pugsley AP. Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J 1987;6:3531-8.
59. Daefler S, Guilvout I, Hardie KR, et al. 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 1997;24:465-75.
60. Dalrymple B, Mattick JS. An analysis of the organization and evolution of type 4 fimbrial (MePhe) subunit proteins. J Mol Evol 1987;25:261-9.
61. de Bentzmann S, Aurouze M, Ball G, et al. FppA, a novel Pseudomonas aeruginosa prepilin peptidase involved in assembly of type IVb pili. J Bacteriol 2006;188:4851-60.
62. Desmond E, Brochier-Armanet C, Gribaldo S. Phylogenomics of the archaeal flagellum: rare horizontal gene transfer in a unique motility structure. BMC Evol Biol 2007;7:106.
63. Donnenberg MS, Zhang HZ, Stone KD. Biogenesis of the bundle forming pilus of enteropathogenic Escherichia coli: reconstitution of fimbriae in recombinant E. coli and role of DsbA in pilin stability-a review. Gene 1997;192:33-8.
64. Douzi B, Ball G, Cambillau C, et al. Deciphering the Xcp Pseudomonas aeruginosa type II secretion machinery throughmultiple interactions with substrates. J Biol Chem 2011;286:40792-801.
65. Douzi B, Durand E, Bernard C, et al. The XcpV/GspI pseudopilin has a central role in the assembly of a quaternary complex within the T2SS pseudopilus. J Biol Chem 2009;284:34580-9.
66. Douzi B, Filloux A, Voulhoux R. On the path to uncover the bacterial type II secretion system. Philos T Roy Soc B 2012;367:1059-72.
67. Drake SL, Sandstedt SA, Koomey M. PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae, affects expression of PilQ as a high-molecular-mass multimer. Mol Microbiol 1997;23:657-68.
68. Dupuy B, Taha MK, Pugsley AP, et al. Neisseria gonorrhoeae prepilin export studied in Escherichia coli. J Bacteriol 1991;173:7589-98.
69. Durand E, Bernadac A, Ball G, et al. Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure. J Bacteriol 2003;185:2749-58.
70. Durand E, Michel G, Voulhoux R, et al. XcpX controls biogenesis of the Pseudomonas aeruginosa XcpT-containing pseudopilus. J Biol Chem 2005;280:31378-89.
71. Forest KT, Dunham SA, Koomey M, et al. Crystallographic structure reveals phosphorylated pilin from Neisseria: phosphoserine sites modify type IV pilus surface chemistry and fibre morphology. Mol Microbiol 1999;31:743-52.
72. Francetic O, Buddelmeijer N, Lewenza S, et al. Signal recognition particle-dependent inner membrane targeting of the PulG pseudopilin component of a type II secretion system. J Bacteriol 2007;189:1783-93.
73. Friedrich C, Bulyha I, Sogaard-Andersen L. Outside-in assembly pathway of the type IV pilus system in Myxococcus xanthus. J Bacteriol 2014;196:378-90.
74. Fröls S, Ajon M, Wagner M, et al. UV-inducible cellular aggregation of the hyperthermophilic archaeon Sulfolobus solfataricus is mediated by pili formation. Mol Microbiol 2008;70:938-52.
75. Gault J, Malosse C, Dumenil G, et al. A combined mass spectrometry strategy for complete posttranslational modification mapping of Neisseria meningitidis major pilin. JMass Spectrom 2013;48:1199-206.
76. Georgiadou M, Castagnini M, Karimova G, et al. Large-scale study of the interactions between proteins involved in type IV pilus biology in Neisseria meningitidis: characterization of a subcomplex involved in pilus assembly. Mol Microbiol 2012;84:857-73.
77. Gibiansky ML, Conrad JC, Jin F, et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science 2010;330:197.
78. Giltner CL, Habash M, Burrows LL. Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 2010;398:444-61.
79. Giltner CL, Nguyen Y, Burrows LL. Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol R 2012;76:740-72.
80. Golovanov AP, Balasingham S, Tzitzilonis C, et al. The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new ß-sandwich fold. J Mol Biol 2006;364:186-95.
81. Gray MD, Bagdasarian M, Hol WG, et al. In vivo cross-linking of EpsG to EpsL suggests a role for EpsL as an ATPasepseudopilin coupling protein in the type II secretion system of Vibrio cholerae. Mol Microbiol 2011;79:786-98.
82. Gu S, Kelly G, Wang X, et al. Solution structure of homology region (HR) domain of type II secretion system. J Biol Chem 2012;287:9072-80.
83. Guberman JM, Ai J, Arnaiz O, et al. BioMart Central Portal: an open database network for the biological community. Database (Oxford) 2011:bar041.
84. Guilvout I, Chami M, Engel A, et al. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J 2006;25:5241-9.
85. Guzzo CR, Salinas RK, Andrade MO, et al. PilZ protein structure and interactions with PilB and the FimX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 2009;393:848-66.
86. Han X, Kennan RM, Parker D, et al. Type IV fimbrial biogenesis is required for protease secretion and natural transformation in Dichelobacter nodosus. J Bacteriol 2007;189:5022-33.
87. Hardie KR, Lory S, Pugsley AP. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J 1996;15:978-88.
88. Hardie KR, Seydel A, Guilvout I, et al. The secretin-specific, chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions. Mol Microbiol 1996;22:967-76.
89. Hartung S, Arvai AS, Wood T, et al. Ultrahigh resolution and full-length pilin structures with insights for filament assembly, pathogenic functions, and vaccine potential. J Biol Chem 2011;286: 44254-65.
90. Hegge FT, Hitchen PG, Aas FE, et al. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proc Natl Acad Sci USA 2004;101:10798-803.
91. Heiniger RW, Winther-Larsen HC, Pickles RJ, et al. Infection of human mucosal tissue by Pseudomonas aeruginosa requires sequential and mutually dependent virulence factors and a novel pilus-associated adhesin. Cell Microbiol 2010;12:1158-73.
92. Helaine S, Carbonnelle E, Prouvensier L, et al. PilX, a pilusassociated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol 2005;55:65-77.
93. Helaine S, Dyer DH, Nassif X, et al. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc Natl Acad Sci USA 2007;104:15888-93.
94. Henrichsen J. Bacterial surface translocation: a survey and a classification. Bacteriol Rev 1972;36:478-503.
95. Herdendorf TJ, McCaslin DR, Forest KT. Aquifex aeolicus PilT, homologue of a surface motility protein, is a thermostable oligomeric NTPase. J Bacteriol 2002;184:6465-71.
96. Hobbs M, Mattick JS. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol 1993;10:233-43.
97. Horiuchi T, Komano T. Mutational analysis of plasmid R64 thin pilus prepilin: the entire prepilin sequence is required for processing by type IV prepilin peptidase. J Bacteriol 1998;180:4613-20.
98. Howie HL, Glogauer M, So M. The N. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a PilT-dependent mechanism. PLoS Biol 2005;3:e100.
99. Hu J, Xue Y, Lee S, et al. The crystal structure of GXGD membrane protease FlaK. Nature 2011;475:528-31.
100. Hunter S, Jones P, Mitchell A, et al. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2012;40:D306-12.
101. Hyland RM, Sun J, Griener TP, et al. The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosaminespecific lectin. Cell Microbiol 2008;10:177-87.
102. Imam S, Chen Z, Roos DS, et al. Identification of surprisingly diverse type IV pili, across a broad range of Gram-positive bacteria. PLoS One 2011;6:e28919s.
103. Imhaus AF, Dumenil G. The number of Neisseria meningitidis type IV pili determines host cell interaction. EMBO J 2014;33:1767-83.
104. Jakovljevic V, Leonardy S, Hoppert M, et al. PilB and PilT are ATPases acting antagonistically in type IV pilus function in Myxococcus xanthus. J Bacteriol 2008;190:2411-21.
105. Jarrell KF, Albers SV. The archaellum: an old motility structure with a new name. Trends Microbiol 2012;20:307-12.
106. Jarrell KF, Bayley DP, Kostyukova AS. The archaeal flagellum: a unique motility structure. J Bacteriol 1996;178:5057-64.
107. Jarrell KF, Ding Y, Nair DB, et al. Surface appendages of archaea: structure, function, genetics and assembly. Life 2013;3:86-117.
108. Jin F, Conrad JC, Gibiansky ML, et al. Bacteria use type-IV pili to slingshot on surfaces. Proc Natl Acad Sci USA 2011;108:12617-22.
109. Johnson MD, Garrett CK, Bond JE, et al. Pseudomonas aeruginosa PilY1 binds integrin in an RGD-and calcium-dependent manner. PLoS One 2011;6:e29629.
110. Johnston C, Campo N, Berge MJ, et al. Streptococcus pneumoniae, le transformiste. Trends Microbiol 2014;22:113-9.
111. Jonsson AB, Nyberg G, Normark S. Phase variation of gonoccoccal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 1991;10:477-88.
112. Kachlany SC, Planet PJ, DeSalle R, et al. flp-1, the first representative of a newpilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol 2001;40:542-54.
113. Karuppiah V, Collins RF, Thistlethwaite A, et al. Structure and assembly of an inner membrane platform for initiation of type IV pilus biogenesis. Proc Natl Acad Sci USA 2013;110:E4638-47.
114. Karuppiah V, Derrick JP. Structure of the PilM-PilN inner membrane type IV pilus biogenesis complex from Thermus thermophilus. J Biol Chem 2011;286: 24434-42.
115. Karuppiah V, Hassan D, Saleem M, et al. Structure and oligomerization of the PilC type IV pilus biogenesis protein fromThermus thermophilus. Proteins 2010;78:2049-57.
116. Kaufman MR, Seyer JM, Taylor RK. Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by Gram-negative bacteria. Gene Dev 1991;5:1834-46.
117. Kazmierczak BI, Mielke DL, Russel M, et al. pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer. J Mol Biol 1994;238:187-98.
118. Kehl-Fie TE, Miller SE, St Geme JW, III. Kingella kingae expresses type IV pili that mediate adherence to respiratory epithelial and synovial cells. J Bacteriol 2008;190:7157-63.
119. Kirn TJ, Bose N, Taylor RK. Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol Microbiol 2003;49:81-92.
120. Kirn TJ, Lafferty MJ, Sandoe CMP, et al. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol Microbiol 2000;35:896-910.
121. Kolappan S, Craig L. Structure of the cytoplasmic domain of TcpE, the inner membrane core protein required for assembly of the Vibrio cholerae toxin-coregulated pilus. Acta Crystallogr D 2013;69:513-9.
122. Koo J, Burrows LL, Howell PL. Decoding the roles of pilotins and accessory proteins in secretin escort services. FEMS Microbiol Lett 2012;328:1-12.
123. Koo J, Tammam S, Ku SY, et al. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin. J Bacteriol 2008;190:6961-9.
124. Koo J, Tang T, Harvey H, et al. Functional mapping of PilF and PilQ in the Pseudomonas aeruginosa type IV pilus system. Biochemistry 2013;52:2914-23.
125. Korotkov KV, Gonen T, Hol WG. Secretins: dynamic channels for protein transport across membranes. Trends Biochem Sci 2011;36:433-43.
126. Korotkov KV, Hol WG. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 2008;15:462-8.
127. Korotkov KV, Johnson TL, Jobling MG, et al. Structural and functional studies on the interaction of GspC and GspD in the type II secretion system. PLoS Pathog 2011;7:e1002228.
128. Korotkov KV, Pardon E, Steyaert J, et al. Crystal structure of the N-terminal domain of the secretin GspD from ETEC determined with the assistance of a nanobody. Structure 2009;17:255-65.
129. Korotkov KV, Sandkvist M, Hol WG. The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 2012;10:336-51.
130. LaPointe CF, Taylor RK. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J Biol Chem 2000;275:1502-10.
131. Lario PI, Pfuetzner RA, Frey EA, et al. Structure and biochemical analysis of a secretin pilot protein. EMBO J 2005;24:1111-21.
132. Laurenceau R, Pehau-Arnaudet G, Baconnais S, et al. A type IV pilus mediates DNA binding during natural transformation in Streptococcus pneumoniae. PLoS Pathog 2013;9:e1003473.
133. Lemkul JA, Bevan DR. Characterization of interactions between PilA from Pseudomonas aeruginosa strain K and amodel membrane. J Phys Chem B 2011;115:8004-8.
134. Li J, Egelman EH, Craig L. Structure of the Vibrio cholerae type IVb pilus and stability comparison with the Neisseria gonorrhoeae type IVa pilus. J Mol Biol 2012;418:47-64.
135. Li J, Lim MS, Li S, et al. Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry. Structure 2008;16:137-48.
136. Lillington J, Geibel S, Waksman G. Biogenesis and adhesion of type 1 and P pili. Biochim Biophys Acta 2014;1840:2783-93.
137. Linderoth NA, Simon MN, Russel M. The filamentous phage pIV multimer visualized by scanning transmission electron microscopy. Science 1997;278:1635-8.
138. Low HH, Gubellini F, Rivera-Calzada A, et al. Structure of a type IV secretion system. Nature 2014;508:550-3.
139. Lu A, Magupalli VG, Ruan J, et al. Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes. Cell 2014;156:1193-206.
140. Lu C, Korotkov KV, Hol WG. Crystal structure of the full-Length ATPase GspE from the Vibrio vulnificus type II secretion system in complex with the cytoplasmic domain of GspL. J Struct Biol 2014;187:223-35.
141. Lu C, Turley S, Marionni ST, et al. Hexamers of the type II secretion ATPase GspE from Vibrio cholerae with increased ATPase activity. Structure 2013;21:1707-17.
142. Lu HM, Motley ST, Lory S. Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion. Mol Microbiol 1997;25:247-59.
143. Lybarger SR, Johnson TL, Gray MD, et al. Docking and assembly of the type II secretion complex of Vibrio cholerae. J Bacteriol 2009;191:3149-61.
144. Maier B, Chen I, Dubnau D, et al. DNA transport into Bacillus subtilis requires protonmotive force to generate largemolecular forces. Nat Struct Mol Biol 2004;11:643-9.
145. Maier B, Potter L, So M, et al. Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 2002;99:16012-7.
146. Manning PA. The tcp gene cluster of Vibrio cholerae. Gene 1997;192:63-70.
147. Marceau M, Forest K, Beretti J-L, et al. Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 1998;27:705-15.
148. Mattick JS. Type IV pili and twitching motility. Annu Rev Microbiol 2002;56:289-314.
149. Melville S, Craig L. Type IV pili in Gram-positive bacteria. Microbiol Mol Biol R 2013;77:323-41.
150. Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature 2000;407:98-102.
151. Mikaty G, Soyer M, Mairey E, et al. Extracellular bacterial pathogen induces host cell surface reorganization to resist shear stress. PLoS Pathog 2009;5:e1000314.
152. Misic AM, Satyshur KA, Forest KT. P. aeruginosa PilT structures with and without nucleotide reveal a dynamic type IV pilus retraction motor. J Mol Biol 2010;400:1011-21.
153. Morand PC, Bille E, Morelle S, et al. Type IV pilus retraction in pathogenic Neisseria is regulated by the PilC proteins. EMBO J 2004;23:2009-17.
154. Nassif X, Beretti J-L, Lowy J, et al. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci USA 1994;91:3769-73.
155. Ng SY, VanDyke DJ, Chaban B, et al. Different minimal signal peptide lengths recognized by the archaeal prepilin-like peptidases FlaK and PibD. J Bacteriol 2009;191:6732-40.
156. Ng SY, Wu J, Nair DB, et al. Genetic and mass spectrometry analyses of the unusual type IV-like pili of the archaeon Methanococcus maripaludis. J Bacteriol 2011;193:804-14.
157. Nishiyama M, Ishikawa T, Rechsteiner H, et al. Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 2008;320:376-9.
158. Nivaskumar M, Bouvier G, Campos M, et al. Distinct docking and stabilization steps of the pseudopilus conformational transition path suggest rotational assembly of type IV pilus-like fibers. Structure 2014;22:685-96.
159. Nivaskumar M, Francetic O. Type II secretion system: a magic beanstalk or a protein escalator. Biochim Biophys Acta 2014;1843:1568-77.
160. Nouwen N, Ranson N, Saibil H, et al. Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proc Natl Acad Sci USA 1999;96:8173-7.
161. Nudleman E, Wall D, Kaiser D. Polar assembly of the type IV pilus secretin in Myxococcus xanthus. Mol Microbiol 2006;60: 16-29.
162. Nunn D, Bergman S, Lory S. Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J Bacteriol 1990;172:2911-9.
163. Nunn DN, Lory S. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci USA 1991;88:3281-5.
164. Nunn DN, Lory S. Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and-W. J Bacteriol 1993;175:4375-82.
165. O'Toole G, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. MolMicrobiol 1998;30:295-304.
166. Opalka N, Beckmann R, Boisset N, et al. Structure of the filamentous phage pIV multimer by cryo-electron microscopy. J Mol Biol 2003;325:461-70.
167. Orans J, Johnson MD, Coggan KA, et al. Crystal structure analysis reveals Pseudomonas PilY1 as an essential calciumdependent regulator of bacterial surface motility. Proc Natl Acad Sci USA 2010;107:1065-70.
168. Ottow JC. Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol 1975;29:79-108.
169. Paranchych W, Sastry PA, Frost LS, et al. Biochemical studies on pili isolated from Pseudomonas aeruginosa strain PAO. Can J Microbiol 1979;25:1175-81.
170. Parge HE, Forest KT, Hickey MJ, et al. Structure of the fibreforming protein pilin at 2.6 Å resolution. Nature 1995;378:32-8.
171. Pasloske BL, Paranchych W. The expression of mutant pilins in Pseudomonas aeruginosa: fifth position glutamate affects pilin methylation. Mol Microbiol 1988;2:489-95.
172. Pasloske BL, Scraba DG, Paranchych W. Assembly of mutant pilins in Pseudomonas aeruginosa: formation of pili composed of heterologous subunits. J Bacteriol 1989;171:2142-7.
173. Patrick M, Korotkov KV, Hol WG, et al. Oligomerization of EpsE coordinates residues from multiple subunits to facilitate ATPase activity. J Biol Chem 2011;286:10378-86.
174. Peabody CR, Chung YJ, Yen MR, et al. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 2003;149:3051-72.
175. Pegden RS, Larson MA, Grant RJ, et al. Adherence of the Grampositive bacterium Ruminococcus albus to cellulose and identification of a novel form of cellulose-binding protein which belongs to the Pil family of proteins. J Bacteriol 1998;180:5921-7.
176. Pelicic V. Type IV pili: e pluribus unum? Mol Microbiol 2008;68:827-37.
177. Phan G, Remaut H, Wang T, et al. Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 2011;474:49-53.
178. Piepenbrink KH, Maldarelli GA, de la Pena CF, et al. Structure of Clostridium difficile PilJ exhibits unprecedented divergence from known type IV pilins. J Biol Chem 2014;289:4334-45.
179. Pinkner JS, Remaut H, Buelens F, et al. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci USA 2006;103:17897-902.
180. Planet PJ, Kachlany SC, DeSalle R, et al. Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc Natl Acad Sci USA 2001;98:2503-8.
181. Porsch EA, Johnson MD, Broadnax AD, et al. Calcium binding properties of the Kingella kingae PilC1 and PilC2 proteins have differential effects on type IV pilus-mediated adherence and twitching motility. J Bacteriol 2013;195:886-95.
182. Possot O, Pugsley AP. Molecular characterization of PulE, a protein required for pullulanase secretion. Mol Microbiol 1994;12:287-99.
183. Possot OM, Gerard-Vincent M, Pugsley AP. Membrane association andmultimerization of secreton component PulC. J Bacteriol 1999;181:4004-11.
184. Possot OM, Vignon G, Bomchil N, et al. Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J Bacteriol 2000;182:2142-52.
185. Pugsley AP. Processing and methylation of PuIG, a pilin-like component of the general secretory pathway of Klebsiella oxytoca. Mol Microbiol 1993;9:295-308.
186. Pugsley AP. The complete general secretory pathway in Gramnegative bacteria. Microbiol Rev 1993;57:50-108.
187. Py B, Loiseau L, Barras F. Assembly of the type II secretion machinery of Erwinia chrysanthemi: direct interaction and associated conformational change between OutE, the putative ATPbinding component and the membrane protein OutL. J Mol Biol 1999;289:659-70.
188. Py B, Loiseau L, Barras F. An inner membrane platform in the type II secretion machinery of Gram-negative bacteria. EMBO Rep 2001;2:244-8.
189. Rahman M, Källström H, Normark S, et al. PilC of pathogenic Neisseria is associated with the bacterial cell surface. Mol Microbiol 1997;25:11-25.
190. Rakotoarivonina H, Jubelin G, Hebraud M, et al. Adhesion to cellulose of the Gram-positive bacterium Ruminococcus albus involves type IV pili. Microbiology 2002;148:1871-80.
191. Reardon PN, Mueller KT. Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J Biol Chem 2013;288:29260-6.
192. Reguera G, McCarthy KD, Mehta T, et al. Extracellular electron transfer via microbial nanowires. Nature 2005;435:1098-101.
193. Reindl S, Ghosh A, Williams GJ, et al. Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 2013;49:1069-82.
194. Robert V, Filloux A, Michel GP. Subcomplexes from the Xcp secretion system of Pseudomonas aeruginosa. FEMS Microbiol Lett 2005;252:43-50.
195. Rose I, Biukovic G, Aderhold P, et al. Identification and characterization of a unique, zinc-containing transport ATPase essential for natural transformation in Thermus thermophilus HB27. Extremophiles 2011;15:191-202.
196. Rudel T, Scheuerpflug I, Meyer TF. Neisseria PilC protein identified as a type-4 pilus-tip located adhesin. Nature 1995;373:357-9.
197. Rudel T, van Putten JPM, Gibbs CP, et al. Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol Microbiol 1992;6:3439-50.
198. Sakai D, Horiuchi T, Komano T. ATPase activity and multimer formation of PilQ protein are required for thin pilus biogenesis in plasmid R64. J Biol Chem 2001;276:17968-75.
199. Sampaleanu LM, Bonanno JB, Ayers M, et al. Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex. J Mol Biol 2009;394:143-59.
200. Sandkvist M, Bagdasarian M, Howard SP, et al. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J 1995;14:1664-73.
201. Sandkvist M, Hough LP, Bagdasarian MM, et al. Direct interaction of the EpsL and EpsM proteins of the general secretion apparatus in Vibrio cholerae. J Bacteriol 1999;181:3129-35.
202. Satyshur KA, Worzalla GA, Meyer LS, et al. Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility. Structure 2007;15:363-76.
203. Sauvonnet N, Vignon G, Pugsley AP, et al. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 2000;19:2221-8.
204. Schmidt SA, Bieber D, Ramer SW, et al. Structure-function analysis of BfpB, a secretin-like protein encoded by the bundleforming-pilus operon of enteropathogenic Escherichia coli. J Bacteriol 2001;183:4848-59.
205. Schuch R, Maurelli AT. MxiM and MxiJ, base elements of the Mxi-Spa type III secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope. J Bacteriol 2001;183:6991-8.
206. Shahapure R, Driessen RP, Haurat MF, et al. The archaellum: a rotating type IV pilus. Mol Microbiol 2014;91:716-23.
207. Shevchik VE, Robert-Baudouy J, Condemine G. Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO J 1997;16:3007-16.
208. Shiue SJ, Kao KM, Leu WM, et al. XpsE oligomerization triggered by ATP binding, not hydrolysis, leads to its association with XpsL. EMBO J 2006;25:1426-35.
209. Siewering K, Jain S, Friedrich C, et al. Peptidoglycan-binding protein TsaP functions in surface assembly of type IV pili. Proc Natl Acad Sci USA 2014;111:E953-61.
210. Skerker JM, Shapiro L. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 2000;19:3223-34.
211. Smedley JG, III, Jewell E, Roguskie J, et al. Influence of pilin glycosylation on Pseudomonas aeruginosa 1244 pilus function. Infect Immun 2005;73:7922-31.
212. Sohel I, Puente JL, Ramer SW, et al. Enteropathogenic Escherichia coli: identification of a gene cluster coding for bundleforming pilus morphogenesis. J Bacteriol 1996;178:2613-28.
213. Stone KD, Zhang HZ, Carlson LK, et al. A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus. Mol Microbiol 1996;20:325-37.
214. Strom MS, Lory S. Mapping of export signals of Pseudomonas aeruginosa pilin with alkaline phosphatase fusions. J Bacteriol 1987;169:3181-8.
215. Strom MS, Lory S. Amino acid substitutions in pilin of Pseudomonas aeruginosa. Effect on leader peptide cleavage, aminoterminal methylation, and pilus assembly. J Biol Chem 1991;266:1656-64.
216. Strom MS, Nunn DN, Lory S. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 1993;90:2404-8.
217. Szabó Z, Stahl AO, Albers SV, et al. Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases. J Bacteriol 2007;189:772-8.
218. Szeto TH, Dessen A, Pelicic V. Structure/function analysis of Neisseria meningitidis PilW, a conserved protein playing multiple roles in type IV pilus biology. Infect Immun 2011;79:3028-35.
219. Takhar HK, Kemp K, Kim M, et al. The platform protein is essential for type IV pilus biogenesis. J Biol Chem 2013;288:9721-8.
220. Tammam S, Sampaleanu LM, Koo J, et al. Characterization of the PilN, PilO and PilP type IVa pilus subcomplex. Mol Microbiol 2011;82:1496-514.
221. Tammam S, Sampaleanu LM, Koo J, et al. PilMNOPQ from the Pseudomonas aeruginosa type IV pilus system form a transenvelope protein interaction network that interacts with PilA. J Bacteriol 2013;195:2126-35.
222. Thomas JD, Reeves PJ, Salmond GP. The general secretion pathway of Erwinia carotovora subsp. carotovora: analysis of the membrane topology of OutC and OutF. Microbiology 1997;143:713-20.
223. Thomas NA, Chao ED, Jarrell KF. Identification of amino acids in the leader peptide of Methanococcus voltae preflagellin that are important in posttranslational processing. Arch Microbiol 2001;175:263-9.
224. Tomich M, Fine DH, Figurski DH. The TadV protein of Actinobacillus actinomycetemcomitans is a novel aspartic acid prepilin peptidase required for maturation of the Flp1 pilin and TadE and TadF pseudopilins. J Bacteriol 2006;188:6899-914.
225. Tomich M, Planet PJ, Figurski DH. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 2007;5:363-75.
226. Tosi T, Estrozi LF, Job V, et al. Structural similarity of secretins from type II and type III secretion systems. Structure 2014;22:1348-55.
227. Tosi T, Nickerson NN, Mollica L, et al. Pilotin-secretin recognition in the type II secretion system of Klebsiella oxytoca. Mol Microbiol 2011;82:1422-32.
228. Tripathi SA, Taylor RK. Membrane association and multimerization of TcpT, the cognate ATPase ortholog of the Vibrio cholerae toxin co-regulated pilus biogenesis apparatus. J Bacteriol 2007;189:4401-9.
229. Turner LR, Lara JC, Nunn DN, et al. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J Bacteriol 1993;175:4962-9.
230. van Schaik EJ, Giltner CL, Audette GF, et al. DNA binding: a novel function of Pseudomonas aeruginosa type IV pili. J Bacteriol 2005;187:1455-64.
231. VanDyke DJ, Wu J, Ng SY, et al. Identification of a putative acetyltransferase gene, MMP0350, which affects proper assembly of both flagella and pili in the archaeon Methanococcus maripaludis. J Bacteriol 2008;190:5300-7.
232. Vargas M, Malvankar NS, Tremblay PL, et al. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 2013;4:e00105-13.
233. Viarre V, Cascales E, Ball G, et al. HxcQ liposecretin is selfpiloted to the outer membrane by its N-terminal lipid anchor. J Biol Chem 2009;284:33815-23.
234. Vignon G, Kohler R, Larquet E, et al. Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides. J Bacteriol 2003;185:3416-28.
235. von Heijne G, Gavel Y. Topogenic signals in integral membrane proteins. Eur J Biochem 1988;174:671-8.
236. Voulhoux R, Bos MP, Geurtsen J, et al. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 2003;299:262-5.
237. Wang YA, Yu X, Ng SY, et al. The structure of an archaeal pilus. J Mol Biol 2008;381:456-66.
238. Wehbi H, Portillo E, Harvey H, et al. The peptidogly can binding protein FimV promotes assembly of the Pseudomonas aeruginosa type IV pilus secretin. J Bacteriol 2011;193:540-50.
239. Winther-Larsen HC, Hegge FT, Wolfgang M, et al. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 2001;98:15276-81.
240. Winther-Larsen HC, Wolfgang M, Dunham S, et al. A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol Microbiol 2005;56:903-17.
241. Wolfgang M, Lauer P, Park HS, et al. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Mol Microbiol 1998;29:321-30.
242. Wolfgang M, Park HS, Hayes SF, et al. Suppression of an absolute defect in type IV pilus biogenesis by loss-offunction mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc Natl Acad Sci USA 1998;95:14973-8.
243. Wolfgang M, van Putten JP, Hayes SF, et al. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 2000;19:6408-18.
244. Yamagata A, Milgotina E, Scanlon K, et al. Structure of an essential type IV pilus biogenesis protein provides insights into pilus and type II secretion systems. J Mol Biol 2012;419:110-24.
245. Yamagata A, Tainer JA. Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism. EMBO J 2007;26:878-90.
246. Yoshida T, Furuya N, Ishikura M, et al. Purification and characterization of thin pili of Inc I1 plasmids ColIb-P9 and R64: formation of PilV-specific cell aggregates by type IV pili. J Bacteriol 1998;180:2842-8.
247. Yoshida T, Kim SR, Komano T. Twelve pil genes are required for biogenesis of the R64 thin pilus. J Bacteriol 1999;181:2038-43.
248. Yu X, Goforth C, Meyer C, et al. Filaments from Ignicoccus hospitalis show diversity of packing in proteins containing N-terminal type IV pilin helices. J Mol Biol 2012;422:274-81.
249. Zahavi EE, Lieberman JA, Donnenberg MS, et al. Bundle-forming pilus retraction enhances enteropathogenic Escherichia coli infectivity. Mol Biol Cell 2011;22:2436-47.
250. Zolghadr B, Weber S, Szabo Z, et al. Identification of a system required for the functional surface localization of sugar binding proteins with class III signal peptides in Sulfolobus solfataricus. Mol Microbiol 2007;64:795-806.