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Structure of the Neisseria meningitidis Type IV pilus.

<div class='caption-title'>Sequence alignment between N. meningitidis and N. gonorrhoeae PilE and other Type IV pilin-like proteins.</div>
<div class='caption-title'>X-ray crystal structure of N. meningitidis ΔN-PilE and comparison with the full-length structure of Ng PilE.</div>
<div class='caption-title'>CryoEM reconstruction of the N. meningitidis T4P at 6 Å resolution.</div>
Kolappan S, Coureuil M, Yu X, Nassif X, Egelman EH, Craig L
OpenAccess logo Nat Commun 7 13015 (2016)
Cited: 71 times
EuropePMC logo PMID: 27698424

Abstract

Neisseria meningitidis use Type IV pili (T4P) to adhere to endothelial cells and breach the blood brain barrier, causing cause fatal meningitis. T4P are multifunctional polymers of the major pilin protein, which share a conserved hydrophobic N terminus that is a curved extended α-helix, α1, in X-ray crystal structures. Here we report a 1.44 Å crystal structure of the N. meningitidis major pilin PilE and a ∼6 Å cryo-electron microscopy reconstruction of the intact pilus, from which we built an atomic model for the filament. This structure reveals the molecular arrangement of the N-terminal α-helices in the filament core, including a melted central portion of α1 and a bridge of electron density consistent with a predicted salt bridge necessary for pilus assembly. This structure has important implications for understanding pilus biology.

Reviews - 5kua mentioned but not cited (1)

  1. Structure Determination of Microtubules and Pili: Past, Present, and Future Directions. Garnett JA, Atherton J. Front Mol Biosci 8 830304 (2021)

Articles - 5kua mentioned but not cited (7)

  1. Structure of the Neisseria meningitidis Type IV pilus. Kolappan S, Coureuil M, Yu X, Nassif X, Egelman EH, Craig L. Nat Commun 7 13015 (2016)
  2. Structure and Assembly of the Enterohemorrhagic Escherichia coli Type 4 Pilus. Bardiaux B, de Amorim GC, Luna Rico A, Zheng W, Guilvout I, Jollivet C, Nilges M, Egelman EH, Izadi-Pruneyre N, Francetic O. Structure 27 1082-1093.e5 (2019)
  3. PilB from Streptococcus sanguinis is a bimodular type IV pilin with a direct role in adhesion. Raynaud C, Sheppard D, Berry JL, Gurung I, Pelicic V. Proc Natl Acad Sci U S A 118 e2102092118 (2021)
  4. Deep mutational scanning of the Neisseria meningitidis major pilin reveals the importance of pilus tip-mediated adhesion. Kennouche P, Charles-Orszag A, Nishiguchi D, Goussard S, Imhaus AF, Dupré M, Chamot-Rooke J, Duménil G. EMBO J. 38 e102145 (2019)
  5. Predicting and Interpreting the Structure of Type IV Pilus of Electricigens by Molecular Dynamics Simulations. Shu C, Xiao K, Cao C, Ding D, Sun X. Molecules 22 (2017)
  6. Structure and Properties of a Natural Competence-Associated Pilin Suggest a Unique Pilus Tip-Associated DNA Receptor. Salleh MZ, Karuppiah V, Snee M, Thistlethwaite A, Levy CW, Knight D, Derrick JP. MBio 10 (2019)
  7. The minor pilin PilV provides a conserved adhesion site throughout the antigenically variable meningococcal type IV pilus. Barnier JP, Meyer J, Kolappan S, Bouzinba-Ségard H, Gesbert G, Jamet A, Frapy E, Schönherr-Hellec S, Capel E, Virion Z, Dupuis M, Bille E, Morand P, Schmitt T, Bourdoulous S, Nassif X, Craig L, Coureuil M. Proc Natl Acad Sci U S A 118 e2109364118 (2021)


Reviews citing this publication (18)

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  18. Twitch or swim: towards the understanding of prokaryotic motion based on the type IV pilus blueprint. Daum B, Gold V. Biol. Chem. 399 799-808 (2018)

Articles citing this publication (45)

  1. Cryoelectron Microscopy Reconstructions of the Pseudomonas aeruginosa and Neisseria gonorrhoeae Type IV Pili at Sub-nanometer Resolution. Wang F, Coureuil M, Osinski T, Orlova A, Altindal T, Gesbert G, Nassif X, Egelman EH, Craig L. Structure 25 1423-1435.e4 (2017)
  2. The molecular mechanism of the type IVa pilus motors. McCallum M, Tammam S, Khan A, Burrows LL, Howell PL. Nat Commun 8 15091 (2017)
  3. Structure and in situ organisation of the Pyrococcus furiosus archaellum machinery. Daum B, Vonck J, Bellack A, Chaudhury P, Reichelt R, Albers SV, Rachel R, Kühlbrandt W. Elife 6 (2017)
  4. Pili allow dominant marine cyanobacteria to avoid sinking and evade predation. Aguilo-Ferretjans MDM, Bosch R, Puxty RJ, Latva M, Zadjelovic V, Chhun A, Sousoni D, Polin M, Scanlan DJ, Christie-Oleza JA. Nat Commun 12 1857 (2021)
  5. DNA-uptake pili of Vibrio cholerae are required for chitin colonization and capable of kin recognition via sequence-specific self-interaction. Adams DW, Stutzmann S, Stoudmann C, Blokesch M. Nat Microbiol 4 1545-1557 (2019)
  6. Structure of the calcium-dependent type 2 secretion pseudopilus. López-Castilla A, Thomassin JL, Bardiaux B, Zheng W, Nivaskumar M, Yu X, Nilges M, Egelman EH, Izadi-Pruneyre N, Francetic O. Nat Microbiol 2 1686-1695 (2017)
  7. The Vibrio cholerae Minor Pilin TcpB Initiates Assembly and Retraction of the Toxin-Coregulated Pilus. Ng D, Harn T, Altindal T, Kolappan S, Marles JM, Lala R, Spielman I, Gao Y, Hauke CA, Kovacikova G, Verjee Z, Taylor RK, Biais N, Craig L. PLoS Pathog. 12 e1006109 (2016)
  8. Cryo-electron microscopy reveals two distinct type IV pili assembled by the same bacterium. Neuhaus A, Selvaraj M, Salzer R, Langer JD, Kruse K, Kirchner L, Sanders K, Daum B, Averhoff B, Gold VAM. Nat Commun 11 2231 (2020)
  9. Reconstitution of a minimal machinery capable of assembling periplasmic type IV pili. Goosens VJ, Busch A, Georgiadou M, Castagnini M, Forest KT, Waksman G, Pelicic V. Proc. Natl. Acad. Sci. U.S.A. 114 E4978-E4986 (2017)
  10. Refined Cryo-EM Structure of the T4 Tail Tube: Exploring the Lowest Dose Limit. Zheng W, Wang F, Taylor NMI, Guerrero-Ferreira RC, Leiman PG, Egelman EH. Structure 25 1436-1441.e2 (2017)
  11. Structure of the competence pilus major pilin ComGC in Streptococcus pneumoniae. Muschiol S, Erlendsson S, Aschtgen MS, Oliveira V, Schmieder P, de Lichtenberg C, Teilum K, Boesen T, Akbey U, Henriques-Normark B. J. Biol. Chem. 292 14134-14146 (2017)
  12. Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option. Walker DJF, Nevin KP, Holmes DE, Rotaru AE, Ward JE, Woodard TL, Zhu J, Ueki T, Nonnenmann SS, McInerney MJ, Lovley DR. ISME J 14 837-846 (2020)
  13. Motor Properties of PilT-Independent Type 4 Pilus Retraction in Gonococci. Zöllner R, Cronenberg T, Maier B. J Bacteriol 201 (2019)
  14. Functional reconstitution of the type IVa pilus assembly system from enterohaemorrhagic Escherichia coli. Luna Rico A, Zheng W, Petiot N, Egelman EH, Francetic O. Mol Microbiol 111 732-749 (2019)
  15. Polar N-terminal Residues Conserved in Type 2 Secretion Pseudopilins Determine Subunit Targeting and Membrane Extraction Steps during Fibre Assembly. Santos-Moreno J, East A, Guilvout I, Nadeau N, Bond PJ, Tran Van Nhieu G, Francetic O. J. Mol. Biol. 429 1746-1765 (2017)
  16. Pseudomonas aeruginosa defends against phages through type IV pilus glycosylation. Harvey H, Bondy-Denomy J, Marquis H, Sztanko KM, Davidson AR, Burrows LL. Nat Microbiol 3 47-52 (2018)
  17. Type IV pilus retraction enables sustained bacteremia and plays a key role in the outcome of meningococcal sepsis in a humanized mouse model. Barnier JP, Euphrasie D, Join-Lambert O, Audry M, Schonherr-Hellec S, Schmitt T, Bourdoulous S, Coureuil M, Nassif X, El Behi M. PLoS Pathog 17 e1009299 (2021)
  18. Adhesion to nanofibers drives cell membrane remodeling through one-dimensional wetting. Charles-Orszag A, Tsai FC, Bonazzi D, Manriquez V, Sachse M, Mallet A, Salles A, Melican K, Staneva R, Bertin A, Millien C, Goussard S, Lafaye P, Shorte S, Piel M, Krijnse-Locker J, Brochard-Wyart F, Bassereau P, Duménil G. Nat Commun 9 4450 (2018)
  19. Cryo-EM structure of an extracellular Geobacter OmcE cytochrome filament reveals tetrahaem packing. Wang F, Mustafa K, Suciu V, Joshi K, Chan CH, Choi S, Su Z, Si D, Hochbaum AI, Egelman EH, Bond DR. Nat Microbiol 7 1291-1300 (2022)
  20. Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes. Bray MS, Wu J, Padilla CC, Stewart FJ, Fowle DA, Henny C, Simister RL, Thompson KJ, Crowe SA, Glass JB. Environ Microbiol Rep 12 49-57 (2020)
  21. Species-Specific Recognition of Sulfolobales Mediated by UV-Inducible Pili and S-Layer Glycosylation Patterns. van Wolferen M, Shajahan A, Heinrich K, Brenzinger S, Black IM, Wagner A, Briegel A, Azadi P, Albers SV. mBio 11 (2020)
  22. 3D blood-brain barrier-organoids as a model for Lyme neuroborreliosis highlighting genospecies dependent organotropism. Adams Y, Clausen AS, Jensen PØ, Lager M, Wilhelmsson P, Henningson AJ, Lindgren PE, Faurholt-Jepsen D, Mens H, Kraiczy P, Kragh KN, Bjarnsholt T, Kjaer A, Lebech AM, Jensen AR. iScience 26 105838 (2023)
  23. An archaellum filament composed of two alternating subunits. Gambelli L, Isupov MN, Conners R, McLaren M, Bellack A, Gold V, Rachel R, Daum B. Nat Commun 13 710 (2022)
  24. An extensively glycosylated archaeal pilus survives extreme conditions. Wang F, Cvirkaite-Krupovic V, Kreutzberger MAB, Su Z, de Oliveira GAP, Osinski T, Sherman N, DiMaio F, Wall JS, Prangishvili D, Krupovic M, Egelman EH. Nat Microbiol 4 1401-1410 (2019)
  25. Assessing the Stability of Biological Fibrils by Molecular-Scale Simulations. Moreira RA, Baker JL, Guzman HV, Poma AB. Methods Mol Biol 2340 357-378 (2022)
  26. Blocking bacterial appendage attachment to wastewater treatment membranes using anti-adhesins. Zamora R, McEvoy J, Colbert C, Chacana Olivares J, Kaewlom P, Khan E. Chemosphere 323 138246 (2023)
  27. Characterization of a glycan-binding complex of minor pilins completes the analysis of Streptococcus sanguinis type 4 pili subunits. Shahin M, Sheppard D, Raynaud C, Berry JL, Gurung I, Silva LM, Feizi T, Liu Y, Pelicic V. Proc Natl Acad Sci U S A 120 e2216237120 (2023)
  28. CryoEM structure of the type IVa pilus secretin required for natural competence in Vibrio cholerae. Weaver SJ, Ortega DR, Sazinsky MH, Dalia TN, Dalia AB, Jensen GJ. Nat Commun 11 5080 (2020)
  29. Dynamics of a type 2 secretion system pseudopilus unraveled by complementary approaches. Bardiaux B, Cordier F, Brier S, López-Castilla A, Izadi-Pruneyre N, Nilges M. J. Biomol. NMR 73 293-303 (2019)
  30. Electrical Conductivity, Selective Adhesion, and Biocompatibility in Bacteria-Inspired Peptide-Metal Self-Supporting Nanocomposites. Guterman T, Ing NL, Fleischer S, Rehak P, Basavalingappa V, Hunashal Y, Dongre R, Raghothama S, Král P, Dvir T, Hochbaum AI, Gazit E. Adv Mater 31 e1807285 (2019)
  31. Genetic incorporation of non-canonical amino acid photocrosslinkers in Neisseria meningitidis: New method provides insights into the physiological function of the function-unknown NMB1345 protein. Takahashi H, Dohmae N, Kim KS, Shimuta K, Ohnishi M, Yokoyama S, Yanagisawa T. PLoS One 15 e0237883 (2020)
  32. Genetic variants linked to the phenotypic outcome of invasive disease and carriage of Neisseria meningitidis. Eriksson L, Johannesen TB, Stenmark B, Jacobsson S, Säll O, Hedberg ST, Fredlund H, Stegger M, Mölling P. Microb Genom 9 (2023)
  33. Global biochemical and structural analysis of the type IV pilus from the Gram-positive bacterium Streptococcus sanguinis. Berry JL, Gurung I, Anonsen JH, Spielman I, Harper E, Hall AMJ, Goosens VJ, Raynaud C, Koomey M, Biais N, Matthews S, Pelicic V. J. Biol. Chem. 294 6796-6808 (2019)
  34. Molecular interactions between Neisseria meningitidis and its human host. Coureuil M, Jamet A, Bille E, Lécuyer H, Bourdoulous S, Nassif X. Cell. Microbiol. 21 e13063 (2019)
  35. Motor-independent retraction of type IV pili is governed by an inherent property of the pilus filament. Chlebek JL, Denise R, Craig L, Dalia AB. Proc Natl Acad Sci U S A 118 e2102780118 (2021)
  36. Multiple conformations facilitate PilT function in the type IV pilus. McCallum M, Benlekbir S, Nguyen S, Tammam S, Rubinstein JL, Burrows LL, Howell PL. Nat Commun 10 5198 (2019)
  37. Receptor recognition by meningococcal type IV pili relies on a specific complex N-glycan. Le Guennec L, Virion Z, Bouzinba-Ségard H, Robbe-Masselot C, Léonard R, Nassif X, Bourdoulous S, Coureuil M. Proc Natl Acad Sci U S A 117 2606-2612 (2020)
  38. Sialic acid mediated mechanical activation of β2 adrenergic receptors by bacterial pili. Virion Z, Doly S, Saha K, Lambert M, Guillonneau F, Bied C, Duke RM, Rudd PM, Robbe-Masselot C, Nassif X, Coureuil M, Marullo S. Nat Commun 10 4752 (2019)
  39. Structure of a heteropolymeric type 4 pilus from a monoderm bacterium. Anger R, Pieulle L, Shahin M, Valette O, Le Guenno H, Kosta A, Pelicic V, Fronzes R. Nat Commun 14 7143 (2023)
  40. Systematic functional analysis of the Com pilus in Streptococcus sanguinis: a minimalistic type 4 filament dedicated to DNA uptake in monoderm bacteria. Mom J, Chouikha I, Valette O, Pieulle L, Pelicic V. mBio 15 e0266723 (2024)
  41. Tad Pili Play a Dynamic Role in Caulobacter crescentus Surface Colonization. Sangermani M, Hug I, Sauter N, Pfohl T, Jenal U. MBio 10 (2019)
  42. Tad and toxin-coregulated pilus structures reveal unexpected diversity in bacterial type IV pili. Sonani RR, Sanchez JC, Baumgardt JK, Kundra S, Wright ER, Craig L, Egelman EH. Proc Natl Acad Sci U S A 120 e2316668120 (2023)
  43. The Vibrio cholerae minor pilin TcpB mediates uptake of the cholera toxin phage CTXφ. Gutierrez-Rodarte M, Kolappan S, Burrell BA, Craig L. J. Biol. Chem. 294 15698-15710 (2019)
  44. The major subunit of widespread competence pili exhibits a novel and conserved type IV pilin fold. Sheppard D, Berry JL, Denise R, Rocha EPC, Matthews S, Pelicic V. J Biol Chem 295 6594-6604 (2020)
  45. The structures of two archaeal type IV pili illuminate evolutionary relationships. Wang F, Baquero DP, Su Z, Beltran LC, Prangishvili D, Krupovic M, Egelman EH. Nat Commun 11 3424 (2020)


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