1887

Abstract

Type 4 filaments (T4F) are a superfamily of filamentous nanomachines – virtually ubiquitous in prokaryotes and functionally versatile – of which type 4 pili (T4P) are the defining member. T4F are polymers of type 4 pilins, assembled by conserved multi-protein machineries. They have long been an important topic for research because they are key virulence factors in numerous bacterial pathogens. Our poor understanding of the molecular mechanisms of T4F assembly is a serious hindrance to the design of anti-T4F therapeutics. This review attempts to shed light on the fundamental mechanistic principles at play in T4F assembly by focusing on similarities rather than differences between several (mostly bacterial) T4F. This holistic approach, complemented by the revolutionary ability of artificial intelligence to predict protein structures, led to an intriguing mechanistic model of T4F assembly.

Funding
This study was supported by the:
  • Agence Nationale de la Recherche (Award ANR-21-CE11-0008-01)
    • Principle Award Recipient: VladimirPelicic
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-03-22
2024-12-07
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References

  1. Proft T, Baker EN. Pili in Gram-negative and Gram-positive bacteria - structure, assembly and their role in disease. Cell Mol Life Sci 2009; 66:613–635 [View Article] [PubMed]
    [Google Scholar]
  2. Telford JL, Barocchi MA, Margarit I, Rappuoli R, Grandi G. Pili in Gram-positive pathogens. Nat Rev Microbiol 2006; 4:509–519 [View Article] [PubMed]
    [Google Scholar]
  3. Ramirez NA, Das A, Ton-That H. New paradigms of pilus assembly mechanisms in Gram-positive Actinobacteria. Trends Microbiol 2020; 28:999–1009 [View Article]
    [Google Scholar]
  4. Pradhan B, Liedtke J, Sleutel M, Lindbäck T, Zegeye ED et al. Endospore appendages: a novel pilus superfamily from the endospores of pathogenic Bacilli. EMBO J 2021; 40:e106887 [View Article]
    [Google Scholar]
  5. Chaudhury P, Quax TEF, Albers SV. Versatile cell surface structures of archaea. Mol Microbiol 2018; 107:298–311 [View Article] [PubMed]
    [Google Scholar]
  6. Duguid JP, Anderson ES. Terminology of bacterial fimbriae, or pili, and their types. Nature 1967; 215:89–90 [View Article] [PubMed]
    [Google Scholar]
  7. Hospenthal MK, Costa TRD, Waksman G. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat Rev Microbiol 2017; 15:365–379 [View Article] [PubMed]
    [Google Scholar]
  8. Berry JL, Pelicic V. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiol Rev 2015; 39:134–154 [View Article] [PubMed]
    [Google Scholar]
  9. Denise R, Abby SS, Rocha EPC. Diversification of the type IV filament superfamily into machines for adhesion, protein secretion, DNA uptake, and motility. PLoS Biol 2019; 17:e3000390 [View Article]
    [Google Scholar]
  10. Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature 2000; 407:98–102 [View Article] [PubMed]
    [Google Scholar]
  11. Skerker JM, Berg HC. Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci 2001; 98:6901–6904 [View Article]
    [Google Scholar]
  12. Maier B, Potter L, So M, Long CD, Seifert HS et al. Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci 2002; 99:16012–16017 [View Article]
    [Google Scholar]
  13. 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 [View Article]
    [Google Scholar]
  14. Duménil G. Type IV pili as a therapeutic target. Trends Microbiol 2019; 27:658–661 [View Article]
    [Google Scholar]
  15. Craig L, Forest KT, Maier B. Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol 2019; 17:429–440 [View Article]
    [Google Scholar]
  16. Ellison CK, Whitfield GB, Brun YV. Type IV Pili: dynamic bacterial nanomachines. FEMS Microbiol Rev 2022; 46:fuab053 [View Article]
    [Google Scholar]
  17. Barnier JP, Meyer J, Kolappan S, Bouzinba-Ségard H, Gesbert G et al. The minor pilin PilV provides a conserved adhesion site throughout the antigenically variable meningococcal type IV pilus. Proc Natl Acad Sci 2021; 118:e2109364118 [View Article]
    [Google Scholar]
  18. Giltner CL, van Schaik EJ, Audette GF, Kao D, Hodges RS et al. The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Mol Microbiol 2006; 59:1083–1096 [View Article]
    [Google Scholar]
  19. Kennouche P, Charles-Orszag A, Nishiguchi D, Goussard S, Imhaus AF et al. Deep mutational scanning of the Neisseria meningitidis major pilin reveals the importance of pilus tip-mediated adhesion. EMBO J 2019; 38:e102145 [View Article]
    [Google Scholar]
  20. Raynaud C, Sheppard D, Berry JL, Gurung I, Pelicic V. PilB from Streptococcus sanguinis is a bimodular type IV pilin with a direct role in adhesion. Proc Natl Acad Sci 2021; 118:e2102092118 [View Article]
    [Google Scholar]
  21. Shahin M, Sheppard D, Raynaud C, Berry JL, Gurung I et al. Characterization of a glycan-binding complex of minor pilins completes the analysis of Streptococcus sanguinis type 4 pili subunits. Proc Natl Acad Sci 2023; 120:e2216237120 [View Article]
    [Google Scholar]
  22. Nassif X, Beretti JL, Lowy J, Stenberg P, O’Gaora P et al. Roles of pilin and PilC in adhesion of Neisseria meningitidis to human epithelial and endothelial cells. Proc Natl Acad Sci 1994; 91:3769–3773 [View Article]
    [Google Scholar]
  23. Johnson MDL, Garrett CK, Bond JE, Coggan KA, Wolfgang MC et al. Pseudomonas aeruginosa PilY1 binds integrin in an RGD- and calcium-dependent manner. PLoS One 2011; 6:e29629 [View Article]
    [Google Scholar]
  24. Treuner-Lange A, Chang YW, Glatter T, Herfurth M, Lindow S et al. PilY1 and minor pilins form a complex priming the type IVa pilus in Myxococcus xanthus. Nat Commun 2020; 11:5054 [View Article]
    [Google Scholar]
  25. Rudel T, Scheurerpflug I, Meyer TF. Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 1995; 373:357–359 [View Article] [PubMed]
    [Google Scholar]
  26. Xue S, Mercier R, Guiseppi A, Kosta A, De Cegli R et al. The differential expression of PilY1 proteins by the HsfBA phosphorelay allows twitching motility in the absence of exopolysaccharides. PLoS Genet 2022; 18:e1010188 [View Article]
    [Google Scholar]
  27. Mattick JS. Type IV pili and twitching motility. Annu Rev Microbiol 2002; 56:289–314 [View Article] [PubMed]
    [Google Scholar]
  28. Burrows LL. Weapons of mass retraction. Mol Microbiol 2005; 57:878–888 [View Article] [PubMed]
    [Google Scholar]
  29. Persat A, Inclan YF, Engel JN, Stone HA, Gitai Z. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proc Natl Acad Sci 2015; 112:7563–7568 [View Article]
    [Google Scholar]
  30. Talà L, Fineberg A, Kukura P, Persat A. Pseudomonas aeruginosa orchestrates twitching motility by sequential control of type IV pili movements. Nat Microbiol 2019; 4:774–780 [View Article]
    [Google Scholar]
  31. Cehovin A, Simpson PJ, McDowell MA, Brown DR, Noschese R et al. Specific DNA recognition mediated by a type IV pilin. Proc Natl Acad Sci 2013; 110:3065–3070 [View Article]
    [Google Scholar]
  32. Berry JL, Xu Y, Ward PN, Lea SM, Matthews SJ et al. A comparative structure/function analysis of two type IV pilin DNA receptors defines a novel mode of DNA binding. Structure 2016; 24:926–934 [View Article]
    [Google Scholar]
  33. Ellison CK, Dalia TN, Vidal Ceballos A, Wang JY, Biais N et al. Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat Microbiol 2018; 3:773–780 [View Article]
    [Google Scholar]
  34. 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; 10:233–243 [View Article] [PubMed]
    [Google Scholar]
  35. Pugsley AP. The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 1993; 57:50–108 [View Article] [PubMed]
    [Google Scholar]
  36. Salmond GP, Reeves PJ. Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem Sci 1993; 18:7–12 [View Article] [PubMed]
    [Google Scholar]
  37. Nivaskumar M, Francetic O. Type II secretion system: a magic beanstalk or a protein escalator. Biochim Biophys Acta 2014; 1843:1568–1577 [View Article] [PubMed]
    [Google Scholar]
  38. Korotkov KV, Sandkvist M. Architecture, function, and substrates of the type II secretion system. EcoSal Plus 2019; 8: [View Article]
    [Google Scholar]
  39. Breitling R, Dubnau D. A membrane protein with similarity to N-methylphenylalanine pilins is essential for DNA binding by competent Bacillus subtilis. J Bacteriol 1990; 172:1499–1508 [View Article] [PubMed]
    [Google Scholar]
  40. Dubnau D, Blokesch M. Mechanisms of DNA uptake by naturally competent bacteria. Annu Rev Genet 2019; 53:217–237 [View Article]
    [Google Scholar]
  41. Chen I, Provvedi R, Dubnau D. A macromolecular complex formed by a pilin-like protein in competent Bacillus subtilis. J Biol Chem 2006; 281:21720–21727 [View Article]
    [Google Scholar]
  42. Jarrell KF, Albers SV. The archaellum: an old motility structure with a new name. Trends Microbiol 2012; 20:307–312 [View Article] [PubMed]
    [Google Scholar]
  43. Szabó Z, Stahl AO, Albers SV, Kissinger JC, Driessen AJM et al. Identification of diverse archaeal proteins with class III signal peptides cleaved by distinct archaeal prepilin peptidases. J Bacteriol 2007; 189:772–778 [View Article] [PubMed]
    [Google Scholar]
  44. 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; 50:1339–1347 [View Article]
    [Google Scholar]
  45. Shahapure R, Driessen RPC, Haurat MF, Albers SV, Dame RT. The archaellum: a rotating type IV pilus. Mol Microbiol 2014; 91:716–723 [View Article] [PubMed]
    [Google Scholar]
  46. Lassak K, Ghosh A, Albers SV. Diversity, assembly and regulation of archaeal type IV pili-like and non-type IV pili-like surface structures. Res Microbiol 2012; 163:630–644 [View Article] [PubMed]
    [Google Scholar]
  47. Bleves S, Voulhoux R, Michel G, Lazdunski A, Tommassen J et al. The secretion apparatus of Pseudomonas aeruginosa: identification of a fifth pseudopilin, XcpX (GspK family). Mol Microbiol 1998; 27:31–40 [View Article]
    [Google Scholar]
  48. Wang F, Craig L, Liu X, Rensing C, Egelman EH. Microbial nanowires: type IV pili or cytochrome filaments?. Trends Microbiol 2022S0966-842X(22)00312-2 [View Article]
    [Google Scholar]
  49. Giltner CL, Nguyen Y, Burrows LL. Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 2012; 76:740–772 [View Article] [PubMed]
    [Google Scholar]
  50. Sauvonnet N, Vignon G, Pugsley AP, Gounon P. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 2000; 19:2221–2228 [View Article]
    [Google Scholar]
  51. Vignon G, Köhler R, Larquet E, Giroux S, Prévost MC 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; 185:3416–3428 [View Article] [PubMed]
    [Google Scholar]
  52. López-Castilla A, Thomassin JL, Bardiaux B, Zheng W, Nivaskumar M et al. Structure of the calcium-dependent type 2 secretion pseudopilus. Nat Microbiol 2017; 2:1686–1695 [View Article] [PubMed]
    [Google Scholar]
  53. Balaban M, Bättig P, Muschiol S, Tirier SM, Wartha F et al. Secretion of a pneumococcal type II secretion system pilus correlates with DNA uptake during transformation. Proc Natl Acad Sci 2014; 111:E758–65 [View Article]
    [Google Scholar]
  54. Muschiol S, Erlendsson S, Aschtgen MS, Oliveira V, Schmieder P et al. Structure of the competence pilus major pilin ComGC in Streptococcus pneumoniae. J Biol Chem 2017; 292:14134–14146 [View Article] [PubMed]
    [Google Scholar]
  55. Sheppard D, Berry JL, Denise R, Rocha EPC, Matthews S et al. The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold. J Biol Chem 2020; 295:6594–6604 [View Article] [PubMed]
    [Google Scholar]
  56. Singh PK, Little J, Donnenberg MS. Landmark discoveries and recent advances in type IV pilus research. Microbiol Mol Biol Rev 2022; 86:e0007622 [View Article]
    [Google Scholar]
  57. Strom MS, Lory S. Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 1993; 47:565–596 [View Article] [PubMed]
    [Google Scholar]
  58. Gurung I, Berry JL, Hall AMJ, Pelicic V. Cloning-independent markerless gene editing in Streptococcus sanguinis: novel insights in type IV pilus biology. Nucleic Acids Res 2017; 45:e40 [View Article]
    [Google Scholar]
  59. Jonson G, Lebens M, Holmgren J. Cloning and sequencing of Vibrio cholerae mannose-sensitive haemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes. Mol Microbiol 1994; 13:109–118 [View Article]
    [Google Scholar]
  60. Kachlany SC, Planet PJ, Desalle R, Fine DH, Figurski DH et al. flp-1, the first representative of a new pilin gene subfamily, is required for non-specific adherence of Actinobacillus actinomycetemcomitans. Mol Microbiol 2001; 40:542–554 [View Article]
    [Google Scholar]
  61. Tomich M, Planet PJ, Figurski DH. The tad locus: postcards from the widespread colonization island. Nat Rev Microbiol 2007; 5:363–375 [View Article]
    [Google Scholar]
  62. Ellison CK, Kan J, Dillard RS, Kysela DT, Ducret A et al. Obstruction of pilus retraction stimulates bacterial surface sensing. Science 2017; 358:535–538 [View Article]
    [Google Scholar]
  63. Antunes LC, Poppleton D, Klingl A, Criscuolo A, Dupuy B et al. Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes. eLife 2016; 5: [View Article] [PubMed]
    [Google Scholar]
  64. Nolan LM, Whitchurch CB, Barquist L, Katrib M, Boinett CJ et al. A global genomic approach uncovers novel components for twitching motility-mediated biofilm expansion in Pseudomonas aeruginosa. Microb Genom 2018; 4: [View Article]
    [Google Scholar]
  65. Muir A, Gurung I, Cehovin A, Bazin A, Vallenet D et al. Construction of a complete set of Neisseria meningitidis defined mutants and its use for the phenotypic profiling of the genome of an important human pathogen. Nat Commun 2020; 11:5541
    [Google Scholar]
  66. Pelicic V. Type IV pili: e pluribus unum?. Mol Microbiol 2008; 68:827–837 [View Article] [PubMed]
    [Google Scholar]
  67. Alm RA, Bodero AJ, Free PD, Mattick JS. Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 1996; 178:46–53 [View Article]
    [Google Scholar]
  68. Alm RA, Hallinan JP, Watson AA, Mattick JS. 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; 22:161–173 [View Article]
    [Google Scholar]
  69. Carbonnelle E, Hélaine S, Prouvensier L, Nassif X, Pelicic V. Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol 2005; 55:54–64 [View Article]
    [Google Scholar]
  70. Gurung I, Spielman I, Davies MR, Lala R, Gaustad P et al. Functional analysis of an unusual type IV pilus in the Gram-positive Streptococcus sanguinis. Mol Microbiol 2016; 99:380–392 [View Article]
    [Google Scholar]
  71. Brown DR, Helaine S, Carbonnelle E, Pelicic V. Systematic functional analysis reveals that a set of seven genes is involved in fine-tuning of the multiple functions mediated by type IV pili in Neisseria meningitidis. Infect Immun 2010; 78:3053–3063 [View Article]
    [Google Scholar]
  72. Helaine S, Dyer DH, Nassif X, Pelicic V, Forest KT. 3D structure/function analysis of PilX reveals how minor pilins can modulate the virulence properties of type IV pili. Proc Natl Acad Sci 2007; 104:15888–15893 [View Article]
    [Google Scholar]
  73. Chang YW, Rettberg LA, Treuner-Lange A, Iwasa J, Søgaard-Andersen L et al. Architecture of the type IVa pilus machine. Science 2016; 351:aad2001 [View Article]
    [Google Scholar]
  74. Korotkov KV, Hol WGJ. Structure of the GspK–GspI–GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Nat Struct Mol Biol 2008; 15:462–468 [View Article]
    [Google Scholar]
  75. Escobar CA, Douzi B, Ball G, Barbat B, Alphonse S et al. Structural interactions define assembly adapter function of a type II secretion system pseudopilin. Structure 2021; 29:1116–1127 [View Article] [PubMed]
    [Google Scholar]
  76. Aly KA, Beebe ET, Chan CH, Goren MA, Sepúlveda C 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 [View Article]
    [Google Scholar]
  77. Sandkvist M, Bagdasarian M, Howard SP, DiRita VJ. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J 1995; 14:1664–1673 [View Article]
    [Google Scholar]
  78. 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 ATP-binding component and the membrane protein OutL. J Mol Biol 1999; 289:659–670 [View Article]
    [Google Scholar]
  79. Sandkvist M, Hough LP, Bagdasarian MM, Bagdasarian M. Direct interaction of the EpsL and EpsM proteins of the general secretion apparatus in Vibrio cholerae. J Bacteriol 1999; 181:3129–3135 [View Article]
    [Google Scholar]
  80. Py B, Loiseau L, Barras F. An inner membrane platform in the type II secretion machinery of Gram-negative bacteria. EMBO Rep 2001; 2:244–248 [View Article] [PubMed]
    [Google Scholar]
  81. Shiue SJ, Kao KM, Leu WM, Chen LY, Chan NL et al. XpsE oligomerization triggered by ATP binding, not hydrolysis, leads to its association with XpsL. EMBO J 2006; 25:1426–1435 [View Article]
    [Google Scholar]
  82. Ayers M, Sampaleanu LM, Tammam S, Koo J, Harvey H 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; 394:128–142 [View Article]
    [Google Scholar]
  83. Sampaleanu LM, Bonanno JB, Ayers M, Koo J, Tammam S et al. Periplasmic domains of Pseudomonas aeruginosa PilN and PilO form a stable heterodimeric complex. J Mol Biol 2009; 394:143–159 [View Article]
    [Google Scholar]
  84. Georgiadou M, Castagnini M, Karimova G, Ladant D, Pelicic V. 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; 84:857–873 [View Article]
    [Google Scholar]
  85. Tammam S, Sampaleanu LM, Koo J, Manoharan K, Daubaras M et al. PilMNOPQ from the Pseudomonas aeruginosa type IV pilus system form a transenvelope protein interaction network that interacts with PilA. J Bacteriol 2013; 195:2126–2135 [View Article]
    [Google Scholar]
  86. Wolfgang M, van Putten JP, Hayes SF, Dorward D, Koomey M. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J 2000; 19:6408–6418 [View Article] [PubMed]
    [Google Scholar]
  87. Majewski DD, Worrall LJ, Strynadka NC. Secretins revealed: structural insights into the giant gated outer membrane portals of bacteria. Curr Opin Struct Biol 2018; 51:61–72 [View Article] [PubMed]
    [Google Scholar]
  88. Barbat B, Douzi B, Voulhoux R. Structural lessons on bacterial secretins. Biochimie 2022S0300-9084(22)00223-1 [View Article]
    [Google Scholar]
  89. Berry JL, Phelan MM, Collins RF, Adomavicius T, Tønjum T et al. Structure and assembly of a trans-periplasmic channel for type IV pili in Neisseria meningitidis. PLoS Pathog 2012; 8:e1002923 [View Article]
    [Google Scholar]
  90. Koo J, Lamers RP, Rubinstein JL, Burrows LL, Howell PL. Structure of the Pseudomonas aeruginosa type IVa pilus secretin at 7.4 Å. Structure 2016; 24:1778–1787 [View Article]
    [Google Scholar]
  91. Koo J, Tang T, Harvey H, Tammam S, Sampaleanu L et al. Functional mapping of PilF and PilQ in the Pseudomonas aeruginosa type IV pilus system. Biochemistry 2013; 52:2914–2923 [View Article]
    [Google Scholar]
  92. Koo J, Tammam S, Ku SY, Sampaleanu LM, Burrows LL et al. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin. J Bacteriol 2008; 190:6961–6969 [View Article]
    [Google Scholar]
  93. Szeto TH, Dessen A, Pelicic V. Structure/function analysis of Neisseria meningitidis PilW, a conserved protein that plays multiple roles in type IV pilus biology. Infect Immun 2011; 79:3028–3035 [View Article]
    [Google Scholar]
  94. Gold VAM, Salzer R, Averhoff B, Kühlbrandt W. Structure of a type IV pilus machinery in the open and closed state. Elife 2015; 4:e07380 [View Article]
    [Google Scholar]
  95. Balasingham SV, Collins RF, Assalkhou R, Homberset H, Frye SA et al. Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis. J Bacteriol 2007; 189:5716–5727 [View Article]
    [Google Scholar]
  96. Tammam S, Sampaleanu LM, Koo J, Sundaram P, Ayers M et al. Characterization of the PilN, PilO and PilP type IVa pilus subcomplex. Mol Microbiol 2011; 82:1496–1514 [View Article] [PubMed]
    [Google Scholar]
  97. Wolfgang M, Park HS, Hayes SF, van Putten JPM, Koomey M. Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc Natl Acad Sci 1998; 95:14973–14978 [View Article]
    [Google Scholar]
  98. Heiniger RW, Winther-Larsen HC, Pickles RJ, Koomey M, Wolfgang MC. Infection of human mucosal tissue by Pseudomonas aeruginosa requires sequential and mutually dependent virulence factors and a novel pilus-associated adhesin. Cell Microbiol 2010; 12:1158–1173 [View Article]
    [Google Scholar]
  99. Winther-Larsen HC, Wolfgang M, Dunham S, Van Putten JPM, Dorward D et al. A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol Microbiol 2005; 56:903–917 [View Article]
    [Google Scholar]
  100. Carbonnelle E, Helaine S, Nassif X, Pelicic V. 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; 61:1510–1522 [View Article]
    [Google Scholar]
  101. Friedrich C, Bulyha I, Søgaard-Andersen L. Outside-in assembly pathway of the type IV pilus system in Myxococcus xanthus. J Bacteriol 2014; 196:378–390 [View Article]
    [Google Scholar]
  102. Goosens VJ, Busch A, Georgiadou M, Castagnini M, Forest KT et al. Reconstitution of a minimal machinery capable of assembling periplasmic type IV pili. Proc Natl Acad Sci 2017; 114:E4978–E4986 [View Article]
    [Google Scholar]
  103. Lu C, Korotkov KV, Hol WGJ. 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; 187:223–235 [View Article]
    [Google Scholar]
  104. Chernyatina AA, Low HH. Core architecture of a bacterial type II secretion system. Nat Commun 2019; 10:5437 [View Article] [PubMed]
    [Google Scholar]
  105. Possot OM, Vignon G, Bomchil N, Ebel F, Pugsley AP. Multiple interactions between pullulanase secreton components involved in stabilization and cytoplasmic membrane association of PulE. J Bacteriol 2000; 182:2142–2152 [View Article]
    [Google Scholar]
  106. 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; 86:805–818 [View Article] [PubMed]
    [Google Scholar]
  107. Douzi B, Ball G, Cambillau C, Tegoni M, Voulhoux R. Deciphering the Xcp Pseudomonas aeruginosa type II secretion machinery through multiple interactions with substrates. J Biol Chem 2011; 286:40792–40801 [View Article]
    [Google Scholar]
  108. Chang YW, Kjær A, Ortega DR, Kovacikova G, Sutherland JA et al. Architecture of the Vibrio cholerae toxin-coregulated pilus machine revealed by electron cryotomography. Nat Microbiol 2017; 2:16269 [View Article]
    [Google Scholar]
  109. Ramer SW, Schoolnik GK, Wu CY, Hwang J, Schmidt SA et al. The type IV pilus assembly complex: biogenic interactions among the bundle-forming pilus proteins of enteropathogenic Escherichia coli. J Bacteriol 2002; 184:3457–3465 [View Article]
    [Google Scholar]
  110. 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 [View Article]
    [Google Scholar]
  111. Kawahara K, Oki H, Fukakusa S, Yoshida T, Imai T et al. Homo-trimeric structure of the type IVb minor pilin CofB suggests mechanism of CFA/III pilus assembly in human enterotoxigenic Escherichia coli. J Mol Biol 2016; 428:1209–1226 [View Article]
    [Google Scholar]
  112. Oki H, Kawahara K, Maruno T, Imai T, Muroga Y et al. Interplay of a secreted protein with type IVb pilus for efficient enterotoxigenic Escherichia coli colonization. Proc Natl Acad Sci 2018; 115:7422–7427 [View Article]
    [Google Scholar]
  113. Tripathi SA, Taylor RK. Membrane association and multimerization of TcpT, the cognate ATPase ortholog of the Vibrio cholerae toxin-coregulated-pilus biogenesis apparatus. J Bacteriol 2007; 189:4401–4409 [View Article]
    [Google Scholar]
  114. Kachlany SC, Planet PJ, Bhattacharjee MK, Kollia E, DeSalle R et al. Nonspecific adherence by Actinobacillus actinomycetemcomitans requires genes widespread in Bacteria and Archaea. J Bacteriol 2000; 182:6169–6176 [View Article]
    [Google Scholar]
  115. Christen M, Beusch C, Bösch Y, Cerletti D, Flores-Tinoco CE et al. Quantitative selection analysis of bacteriophage φCbK susceptibility in Caulobacter crescentus. J Mol Biol 2016; 428:419–430 [View Article]
    [Google Scholar]
  116. Chung YS, Dubnau D. All seven comG open reading frames are required for DNA binding during transformation of competent Bacillus subtilis. J Bacteriol 1998; 180:41–45 [View Article]
    [Google Scholar]
  117. Chung YS, Dubnau D. ComC is required for the processing and translocation of ComGC, a pilin-like competence protein of Bacillus subtilis. Mol Microbiol 1995; 15:543–551 [View Article]
    [Google Scholar]
  118. Gambelli L, Isupov MN, Conners R, McLaren M, Bellack A et al. An archaellum filament composed of two alternating subunits. Nat Commun 2022; 13:710 [View Article] [PubMed]
    [Google Scholar]
  119. Imam S, Chen Z, Roos DS, Pohlschröder M, Donlin MJ. Identification of surprisingly diverse type IV pili, across a broad range of Gram-positive bacteria. PLoS One 2011; 6:e28919 [View Article]
    [Google Scholar]
  120. Teufel F, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 2022; 40:1023–1025 [View Article]
    [Google Scholar]
  121. Jones P, Binns D, Chang HY, Fraser M, Li W et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 2014; 30:1236–1240 [View Article] [PubMed]
    [Google Scholar]
  122. Francetic O, Buddelmeijer N, Lewenza S, Kumamoto CA, Pugsley AP. Signal recognition particle-dependent inner membrane targeting of the PulG pseudopilin component of a type II secretion system. J Bacteriol 2007; 189:1783–1793 [View Article]
    [Google Scholar]
  123. Arts J, van Boxtel R, Filloux A, Tommassen J, Koster M. Export of the pseudopilin XcpT of the Pseudomonas aeruginosa type II secretion system via the signal recognition particle-Sec pathway. J Bacteriol 2007; 189:2069–2076 [View Article] [PubMed]
    [Google Scholar]
  124. Heijne G, Gavel Y. Topogenic signals in integral membrane proteins. Eur J Biochem 1988; 174:671–678 [View Article] [PubMed]
    [Google Scholar]
  125. Strom MS, Lory S. Mapping of export signals of Pseudomonas aeruginosa pilin with alkaline phosphatase fusions. J Bacteriol 1987; 169:3181–3188 [View Article]
    [Google Scholar]
  126. Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED et al. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature 1995; 378:32–38 [View Article] [PubMed]
    [Google Scholar]
  127. Gu Y, Srikanth V, Salazar-Morales AI, Jain R, O’Brien JP et al. Structure of Geobacter pili reveals secretory rather than nanowire behaviour. Nature 2021; 597:430–434 [View Article]
    [Google Scholar]
  128. Kolappan S, Coureuil M, Yu X, Nassif X, Egelman EH et al. Structure of the Neisseria meningitidis type IV pilus. Nat Commun 2016; 7:13015 [View Article]
    [Google Scholar]
  129. Wang F, Coureuil M, Osinski T, Orlova A, Altindal T et al. Cryoelectron microscopy reconstructions of the Pseudomonas aeruginosa and Neisseria gonorrhoeae type IV pili at sub-nanometer resolution. Structure 2017; 25:1423–1435 [View Article]
    [Google Scholar]
  130. Bardiaux B, de Amorim GC, Luna Rico A, Zheng W, Guilvout I et al. Structure and assembly of the enterohemorrhagic Escherichia coli type 4 pilus. Structure 2019; 27:1082–1093 [View Article]
    [Google Scholar]
  131. Neuhaus A, Selvaraj M, Salzer R, Langer JD, Kruse K et al. Cryo-electron microscopy reveals two distinct type IV pili assembled by the same bacterium. Nat Commun 2020; 11:2231 [View Article] [PubMed]
    [Google Scholar]
  132. Egelman EH. Cryo-EM of bacterial pili and archaeal flagellar filaments. Curr Opin Struct Biol 2017; 46:31–37 [View Article] [PubMed]
    [Google Scholar]
  133. Karami Y, López-Castilla A, Ori A, Thomassin JL, Bardiaux B et al. Computational and biochemical analysis of type IV pilus dynamics and stability. Structure 2021; 29:1397–1409 [View Article]
    [Google Scholar]
  134. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M et al. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 2006; 23:651–662 [View Article] [PubMed]
    [Google Scholar]
  135. Campos M, Nilges M, Cisneros DA, Francetic O. Detailed structural and assembly model of the type II secretion pilus from sparse data. Proc Natl Acad Sci 2010; 107:13081–13086 [View Article]
    [Google Scholar]
  136. 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. Genes Dev 1991; 5:1834–1846 [View Article] [PubMed]
    [Google Scholar]
  137. Nunn DN, Lory S. Product of the Pseudomonas aeruginosa gene pilD is a prepilin leader peptidase. Proc Natl Acad Sci 1991; 88:3281–3285 [View Article]
    [Google Scholar]
  138. Dupuy B, Taha MK, Pugsley AP, Marchal C. Neisseria gonorrhoeae prepilin export studied in Escherichia coli. J Bacteriol 1991; 173:7589–7598 [View Article]
    [Google Scholar]
  139. Reeves PJ, Douglas P, Salmond GP. beta-Lactamase topology probe analysis of the OutO NMePhe peptidase, and six other Out protein components of the Erwinia carotovora general secretion pathway apparatus. Mol Microbiol 1994; 12:445–457 [View Article]
    [Google Scholar]
  140. 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 1993; 90:2404–2408 [View Article]
    [Google Scholar]
  141. 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; 188:6899–6914 [View Article]
    [Google Scholar]
  142. Frost LS, Carpenter M, Paranchych W. N-methylphenylalanine at the N-terminus of pilin isolated from Pseudomonas aeruginosa K. Nature 1978; 271:87–89 [View Article]
    [Google Scholar]
  143. Santos-Moreno J, East A, Guilvout I, Nadeau N, Bond PJ et al. Polar N-terminal residues conserved in type 2 secretion pseudopilins determine subunit targeting and membrane extraction steps during fibre assembly. J Mol Biol 2017; 429:1746–1765 [View Article]
    [Google Scholar]
  144. Strom MS, Bergman P, Lory S. Identification of active-site cysteines in the conserved domain of PilD, the bifunctional type IV pilin leader peptidase/N-methyltransferase of Pseudomonas aeruginosa. J Biol Chem 1993; 268:15788–15794 [View Article]
    [Google Scholar]
  145. LaPointe CF, Taylor RK. The type 4 prepilin peptidases comprise a novel family of aspartic acid proteases. J Biol Chem 2000; 275:1502–1510 [View Article] [PubMed]
    [Google Scholar]
  146. Akahane K, Sakai D, Furuya N, Komano T. 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; 273:350–359 [View Article] [PubMed]
    [Google Scholar]
  147. de Bentzmann S, Aurouze M, Ball G, Filloux A. FppA, a novel Pseudomonas aeruginosa prepilin peptidase involved in assembly of type IVb pili. J Bacteriol 2006; 188:4851–4860 [View Article]
    [Google Scholar]
  148. Szabó Z, Albers SV, Driessen AJM. Active-site residues in the type IV prepilin peptidase homologue PibD from the archaeon Sulfolobus solfataricus. J Bacteriol 2006; 188:1437–1443 [View Article]
    [Google Scholar]
  149. Klebe G. Aspartic protease inhibitors. In Klebe G. eds Drug Design Berlin, Heidelberg: Springer; 2013 pp 533–564
    [Google Scholar]
  150. Hu J, Xue Y, Lee S, Ha Y. The crystal structure of GXGD membrane protease FlaK. Nature 2011; 475:528–531 [View Article] [PubMed]
    [Google Scholar]
  151. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. Highly accurate protein structure prediction with AlphaFold. Nature 2021; 596:583–589 [View Article] [PubMed]
    [Google Scholar]
  152. Perrakis A, Sixma TK. AI revolutions in biology: the joys and perils of AlphaFold. EMBO Rep 2021; 22:e54046 [View Article]
    [Google Scholar]
  153. Vale RD. AAA proteins. Lords of the ring. J Cell Biol 2000; 150:F13–9 [View Article]
    [Google Scholar]
  154. McCallum M, Tammam S, Khan A, Burrows LL, Howell PL. The molecular mechanism of the type IVa pilus motors. Nat Commun 2017; 8:15091 [View Article] [PubMed]
    [Google Scholar]
  155. Lu C, Turley S, Marionni ST, Park YJ, Lee KK et al. Hexamers of the type II secretion ATPase GspE from Vibrio cholerae with increased ATPase activity. Structure 2013; 21:1707–1717 [View Article]
    [Google Scholar]
  156. Reindl S, Ghosh A, Williams GJ, Lassak K, Neiner T et al. Insights into FlaI functions in archaeal motor assembly and motility from structures, conformations, and genetics. Mol Cell 2013; 49:1069–1082 [View Article] [PubMed]
    [Google Scholar]
  157. Mancl JM, Black WP, Robinson H, Yang Z, Schubot FD. Crystal structure of a type IV pilus assembly ATPase: insights into the molecular mechanism of PilB from Thermus thermophilus. Structure 2016; 24:1886–1897 [View Article]
    [Google Scholar]
  158. Solanki V, Kapoor S, Thakur KG. Structural insights into the mechanism of type IVa pilus extension and retraction ATPase motors. FEBS J 2018; 285:3402–3421 [View Article]
    [Google Scholar]
  159. Thomas JD, Reeves PJ, Salmond GPC. The general secretion pathway of Erwinia carotovora subsp. carotovora: analysis of the membrane topology of OutC and OutF. Microbiology 1997; 143 (Pt 3):713–720 [View Article]
    [Google Scholar]
  160. Hallgren J, Tsirigos KD, Pedersen MD, Almagro Armenteros JJ, Marcatili P et al. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. bioRxiv 2022 [View Article]
    [Google Scholar]
  161. Arts J, de Groot A, Ball G, Durand E, Khattabi ME et al. Interaction domains in the Pseudomonas aeruginosa type II secretory apparatus component XcpS (GspF). Microbiology 2007; 153:1582–1592 [View Article]
    [Google Scholar]
  162. Bischof LF, Friedrich C, Harms A, Søgaard-Andersen L, van der Does C. The type IV pilus assembly ATPase PilB of Myxococcus xanthus interacts with the inner membrane platform protein PilC and the nucleotide-binding protein PilM. J Biol Chem 2016; 291:6946–6957 [View Article]
    [Google Scholar]
  163. Gray MD, Bagdasarian M, Hol WGJ, Sandkvist M. In vivo cross-linking of EpsG to EpsL suggests a role for EpsL as an ATPase-pseudopilin coupling protein in the type II secretion system of Vibrio cholerae. Mol Microbiol 2011; 79:786–798 [View Article]
    [Google Scholar]
  164. Abendroth J, Mitchell DD, Korotkov KV, Johnson TL, Kreger A 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; 166:303–315 [View Article]
    [Google Scholar]
  165. Karuppiah V, Hassan D, Saleem M, Derrick JP. Structure and oligomerization of the PilC type IV pilus biogenesis protein from Thermus thermophilus. Proteins 2010; 78:2049–2057 [View Article]
    [Google Scholar]
  166. 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 Biol Crystallogr 2013; 69:513–519 [View Article]
    [Google Scholar]
  167. Collins RF, Saleem M, Derrick JP. Purification and three-dimensional electron microscopy structure of the Neisseria meningitidis type IV pilus biogenesis protein PilG. J Bacteriol 2007; 189:6389–6396 [View Article]
    [Google Scholar]
  168. Evans R, O’Neill M, Pritzel A, Antropova N, Senior A et al. Protein complex prediction with AlphaFold-Multimer. bioRxiv 2022 [View Article]
    [Google Scholar]
  169. Seal RL, Braschi B, Gray K, Jones TEM, Tweedie S et al. Genenames.org: the HGNC resources in 2023. Nucleic Acids Res 2023; 51:D1003–D1009 [View Article]
    [Google Scholar]
  170. 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; 172:2911–2919 [View Article]
    [Google Scholar]
  171. Omasits U, Ahrens CH, Müller S, Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 2014; 30:884–886 [View Article] [PubMed]
    [Google Scholar]
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