A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL

Barden S, Lange S, Tegtmeyer N, Conradi J, Sewald N, Backert S, Niemann H (2013)
Structure (London, England : 1993) 21(11): 1931-1941.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ; ;
Abstract / Bemerkung
RGD tripeptide motifs frequently mediate ligand binding to integrins. The type IV secretion system (T4SS) protein CagL of the gastric pathogen Helicobacter pylori also contains an RGD motif. CagL decorates the T4SS pilus and may function as an adhesin for host cells. Whether CagL binds integrins via its RGD motif is under debate. Here, we present crystal structures of CagL revealing an elongated four-helix bundle that appears evolutionarily unrelated to the proposed VirB5 orthologs. The RGD motif is surface-exposed but located within a long α helix. This is unprecedented as previously characterized integrin-binding RGD motifs are located within extended or flexible loops. Yet, adhesion of gastric epithelial cells to CagL was strictly RGD-dependent. Comparison of seven crystallographically independent molecules reveals substantial structural flexibility. Intramolecular disulfide bonds engineered to reduce CagL flexibility resulted in more stable protein, but unable to support cell adhesion. CagL may thus partly unfold during receptor binding.
Erscheinungsjahr
Zeitschriftentitel
Structure (London, England : 1993)
Band
21
Ausgabe
11
Seite(n)
1931-1941
ISSN
PUB-ID

Zitieren

Barden S, Lange S, Tegtmeyer N, et al. A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL. Structure (London, England : 1993). 2013;21(11):1931-1941.
Barden, S., Lange, S., Tegtmeyer, N., Conradi, J., Sewald, N., Backert, S., & Niemann, H. (2013). A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL. Structure (London, England : 1993), 21(11), 1931-1941. doi:10.1016/j.str.2013.08.018
Barden, S., Lange, S., Tegtmeyer, N., Conradi, J., Sewald, N., Backert, S., and Niemann, H. (2013). A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL. Structure (London, England : 1993) 21, 1931-1941.
Barden, S., et al., 2013. A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL. Structure (London, England : 1993), 21(11), p 1931-1941.
S. Barden, et al., “A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL”, Structure (London, England : 1993), vol. 21, 2013, pp. 1931-1941.
Barden, S., Lange, S., Tegtmeyer, N., Conradi, J., Sewald, N., Backert, S., Niemann, H.: A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL. Structure (London, England : 1993). 21, 1931-1941 (2013).
Barden, Stephan, Lange, Stefanie, Tegtmeyer, Nicole, Conradi, Jens, Sewald, Norbert, Backert, Steffen, and Niemann, Hartmut. “A Helical RGD Motif Promoting Cell Adhesion: Crystal Structures of the Helicobacter pylori Type IV Secretion System Pilus Protein CagL”. Structure (London, England : 1993) 21.11 (2013): 1931-1941.

31 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

CagL polymorphisms D58/K59 are predominant in Helicobacter pylori strains isolated from Mexican patients with chronic gastritis.
Román-Román A, Martínez-Santos VI, Castañón-Sánchez CA, Albañil-Muñoz AJ, González-Mendoza P, Soto-Flores DG, Martínez-Carrillo DN, Fernández-Tilapa G., Gut Pathog 11(), 2019
PMID: 30805032
Type IV secretion in Gram-negative and Gram-positive bacteria.
Grohmann E, Christie PJ, Waksman G, Backert S., Mol Microbiol 107(4), 2018
PMID: 29235173
The type IV secretion system in Helicobacter pylori.
Yuan XY, Wang Y, Wang MY., Future Microbiol 13(), 2018
PMID: 29927340
Integrin but not CEACAM receptors are dispensable for Helicobacter pylori CagA translocation.
Zhao Q, Busch B, Jiménez-Soto LF, Ishikawa-Ankerhold H, Massberg S, Terradot L, Fischer W, Haas R., PLoS Pathog 14(10), 2018
PMID: 30365569
DNA Transfer and Toll-like Receptor Modulation by Helicobacter pylori.
Varga MG, Peek RM., Curr Top Microbiol Immunol 400(), 2017
PMID: 28124154
Helicobacter pylori: A Paradigm Pathogen for Subverting Host Cell Signal Transmission.
Naumann M, Sokolova O, Tegtmeyer N, Backert S., Trends Microbiol 25(4), 2017
PMID: 28057411
Bacterial thiol oxidoreductases - from basic research to new antibacterial strategies.
Bocian-Ostrzycka KM, Grzeszczuk MJ, Banaś AM, Jagusztyn-Krynicka EK., Appl Microbiol Biotechnol 101(10), 2017
PMID: 28409380
Genetic variants of Helicobacter pylori type IV secretion system components CagL and CagI and their association with clinical outcomes.
Ogawa H, Iwamoto A, Tanahashi T, Okada R, Yamamoto K, Nishiumi S, Yoshida M, Azuma T., Gut Pathog 9(), 2017
PMID: 28439300
Molecular dissection of protein-protein interactions between integrin α5β1 and the Helicobacter pylori Cag type IV secretion system.
Koelblen T, Bergé C, Cherrier MV, Brillet K, Jimenez-Soto L, Ballut L, Takagi J, Montserret R, Rousselle P, Fischer W, Haas R, Fronzes R, Terradot L., FEBS J 284(23), 2017
PMID: 29055076
Helicobacter pylori CagL Hypervariable Motif: A Global Analysis of Geographical Diversity and Association With Gastric Cancer.
Gorrell RJ, Zwickel N, Reynolds J, Bulach D, Kwok T., J Infect Dis 213(12), 2016
PMID: 26908724
Helicobacter pylori HP0231 Influences Bacterial Virulence and Is Essential for Gastric Colonization.
Zhong Y, Anderl F, Kruse T, Schindele F, Jagusztyn-Krynicka EK, Fischer W, Gerhard M, Mejías-Luque R., PLoS One 11(5), 2016
PMID: 27138472
A C-Terminal Coiled-Coil Region of CagL is Responsible for Helicobacter Pylori-Induced Il-8 Expression.
Wiedemann T, Hofbaur S, Loell E, Rieder G., Eur J Microbiol Immunol (Bp) 6(3), 2016
PMID: 27766167
Differences in amino acid frequency in CagA and VacA sequences of Helicobacter pylori distinguish gastric cancer from gastric MALT lymphoma.
Hashinaga M, Suzuki R, Akada J, Matsumoto T, Kido Y, Okimoto T, Kodama M, Murakami K, Yamaoka Y., Gut Pathog 8(), 2016
PMID: 27833662
Adhesion and Invasion of Gastric Mucosa Epithelial Cells by Helicobacter pylori.
Huang Y, Wang QL, Cheng DD, Xu WT, Lu NH., Front Cell Infect Microbiol 6(), 2016
PMID: 27921009
How pathogens use linear motifs to perturb host cell networks.
Via A, Uyar B, Brun C, Zanzoni A., Trends Biochem Sci 40(1), 2015
PMID: 25475989
Crystal structure of CagL from Helicobacter pylori K74 strain.
Choi JM, Choi YH, Sudhanva MS, Devakumar S, Lee KH, Cha JH, Lee SH., Biochem Biophys Res Commun 460(4), 2015
PMID: 25839651
Integrin engagement by the helical RGD motif of the Helicobacter pylori CagL protein is regulated by pH-induced displacement of a neighboring helix.
Bonsor DA, Pham KT, Beadenkopf R, Diederichs K, Haas R, Beckett D, Fischer W, Sundberg EJ., J Biol Chem 290(20), 2015
PMID: 25837254
Crystal structure of an engineered YopM-InlB hybrid protein.
Breitsprecher D, Gherardi E, Bleymüller WM, Niemann HH., BMC Struct Biol 14(), 2014
PMID: 24669959
Structure of a three-dimensional domain-swapped dimer of the Helicobacter pylori type IV secretion system pilus protein CagL.
Barden S, Schomburg B, Conradi J, Backert S, Sewald N, Niemann HH., Acta Crystallogr D Biol Crystallogr 70(pt 5), 2014
PMID: 24816107
Helicobacter pylori virulence and cancer pathogenesis.
Yamaoka Y, Graham DY., Future Oncol 10(8), 2014
PMID: 25052757
Pathogenesis of Helicobacter pylori infection.
de Bernard M, Josenhans C., Helicobacter 19 Suppl 1(), 2014
PMID: 25167940

59 References

Daten bereitgestellt von Europe PubMed Central.

PHENIX: a comprehensive Python-based system for macromolecular structure solution.
Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 2), 2010
PMID: 20124702
Biological diversity of prokaryotic type IV secretion systems.
Alvarez-Martinez CE, Christie PJ., Microbiol. Mol. Biol. Rev. 73(4), 2009
PMID: 19946141
VirB2 and VirB5 proteins: specialized adhesins in bacterial type-IV secretion systems?
Backert S, Fronzes R, Waksman G., Trends Microbiol. 16(9), 2008
PMID: 18706815
iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM.
Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG., Acta Crystallogr. D Biol. Crystallogr. 67(Pt 4), 2011
PMID: 21460445
Topological analysis of a putative virB8 homologue essential for the cag type IV secretion system in Helicobacter pylori.
Buhrdorf R, Forster C, Haas R, Fischer W., Int. J. Med. Microbiol. 293(2-3), 2003
PMID: 12868658
The CCP4 suite: programs for protein crystallography.
Collaborative Computational Project, Number 4., Acta Crystallogr. D Biol. Crystallogr. 50(Pt 5), 1994
PMID: 15299374
Cyclic RGD peptides interfere with binding of the Helicobacter pylori protein CagL to integrins αVβ3 and α5β1.
Conradi J, Huber S, Gaus K, Mertink F, Royo Gracia S, Strijowski U, Backert S, Sewald N., Amino Acids 43(1), 2011
PMID: 21915696
An RGD helper sequence in CagL of Helicobacter pylori assists in interactions with integrins and injection of CagA.
Conradi J, Tegtmeyer N, Wozna M, Wissbrock M, Michalek C, Gagell C, Cover TL, Frank R, Sewald N, Backert S., Front Cell Infect Microbiol 2(), 2012
PMID: 22919661
Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori?
Covacci A, Falkow S, Berg DE, Rappuoli R., Trends Microbiol. 5(5), 1997
PMID: 9160510
The Buccaneer software for automated model building. 1. Tracing protein chains.
Cowtan K., Acta Crystallogr. D Biol. Crystallogr. 62(Pt 9), 2006
PMID: 16929101
Structure of Bordetella pertussis virulence factor P.69 pertactin.
Emsley P, Charles IG, Fairweather NF, Isaacs NW., Nature 381(6577), 1996
PMID: 8609998
Features and development of Coot.
Emsley P, Lohkamp B, Scott WG, Cowtan K., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 4), 2010
PMID: 20383002
Scaling and assessment of data quality.
Evans P., Acta Crystallogr. D Biol. Crystallogr. 62(Pt 1), 2005
PMID: 16369096
The structural biology of type IV secretion systems.
Fronzes R, Christie PJ, Waksman G., Nat. Rev. Microbiol. 7(10), 2009
PMID: 19756009
Toward rational protein crystallization: A Web server for the design of crystallizable protein variants.
Goldschmidt L, Cooper DR, Derewenda ZS, Eisenberg D., Protein Sci. 16(8), 2007
PMID: 17656576
A novel NOD1- and CagA-independent pathway of interleukin-8 induction mediated by the Helicobacter pylori type IV secretion system
Gorrell, Cell. Microbiol. 15(), 2012
Cellular adhesion molecules as targets for bacterial infection.
Hauck CR, Agerer F, Muenzner P, Schmitter T., Eur. J. Cell Biol. 85(3-4), 2005
PMID: 16546567
Dali server: conservation mapping in 3D
Holm, Nucleic Acids Res. 38(Web Server issue), 2010

Hubbard, 1993
Helicobacter pylori type IV secretion apparatus exploits beta1 integrin in a novel RGD-independent manner.
Jimenez-Soto LF, Kutter S, Sewald X, Ertl C, Weiss E, Kapp U, Rohde M, Pirch T, Jung K, Retta SF, Terradot L, Fischer W, Haas R., PLoS Pathog. 5(12), 2009
PMID: 19997503
Solution for best rotation to relate 2 sets of vectors
Kabsch, Acta Crystallogr. A 32(), 1976
XDS.
Kabsch W., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 2), 2010
PMID: 20124692
Crystal structure of the zymogen form of the group A Streptococcus virulence factor SpeB: an integrin-binding cysteine protease.
Kagawa TF, Cooney JC, Baker HM, McSweeney S, Liu M, Gubba S, Musser JM, Baker EN., Proc. Natl. Acad. Sci. U.S.A. 97(5), 2000
PMID: 10681429
Structural insights into Helicobacter pylori oncoprotein CagA interaction with β1 integrin.
Kaplan-Turkoz B, Jimenez-Soto LF, Dian C, Ertl C, Remaut H, Louche A, Tosi T, Haas R, Terradot L., Proc. Natl. Acad. Sci. U.S.A. 109(36), 2012
PMID: 22908298
Protein subassemblies of the Helicobacter pylori Cag type IV secretion system revealed by localization and interaction studies
Kutter, J. Bacteriol. 190(), 2008
Helicobacter exploits integrin for type IV secretion and kinase activation.
Kwok T, Zabler D, Urman S, Rohde M, Hartig R, Wessler S, Misselwitz R, Berger J, Sewald N, Konig W, Backert S., Nature 449(7164), 2007
PMID: 17943123
Measurement of cell numbers by means of the endogenous enzyme hexosaminidase. Applications to detection of lymphokines and cell surface antigens
Landegren, J. Immunol. Methods 67(), 1984
The role of integrin binding sites in fibronectin matrix assembly in vivo.
Leiss M, Beckmann K, Giros A, Costell M, Fassler R., Curr. Opin. Cell Biol. 20(5), 2008
PMID: 18586094
Structure of a major immunogenic site on foot-and-mouth disease virus.
Logan D, Abu-Ghazaleh R, Blakemore W, Curry S, Jackson T, King A, Lea S, Lewis R, Newman J, Parry N., Nature 362(6420), 1993
PMID: 8385272
Phaser crystallographic software
McCoy, J. Appl. Cryst. 40(), 2007
Facilities for macromolecular crystallography at the Helmholtz-Zentrum Berlin
Mueller, J. Synchrotron Radiat. 19(), 2012
Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion.
Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R., Science 287(5457), 2000
PMID: 10688800
TLSMD web server for the generation of multi-group TLS models
Painter, J. Appl. Cryst. 39(), 2006
HKL2MAP: a graphcial user interface for phasing with SHELX programs
Pape, J. Appl. Cryst. 37(), 2004
CagI is an essential component of the Helicobacter pylori Cag type IV secretion system and forms a complex with CagL.
Pham KT, Weiss E, Jimenez Soto LF, Breithaupt U, Haas R, Fischer W., PLoS ONE 7(4), 2012
PMID: 22493745
RGD and other recognition sequences for integrins.
Ruoslahti E., Annu. Rev. Cell Dev. Biol. 12(), 1996
PMID: 8970741
Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase alpha subunit.
Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ., Gastroenterology 139(1), 2010
PMID: 20303353
Complex cellular responses of Helicobacter pylori-colonized gastric adenocarcinoma cells.
Schneider S, Carra G, Sahin U, Hoy B, Rieder G, Wessler S., Infect. Immun. 79(6), 2011
PMID: 21402757
The RGD finger of Del-1 is a unique structural feature critical for integrin binding.
Schurpf T, Chen Q, Liu JH, Wang R, Springer TA, Wang JH., FASEB J. 26(8), 2012
PMID: 22601780
Helicobacter pylori exploits a unique repertoire of type IV secretion system components for pilus assembly at the bacteria-host cell interface.
Shaffer CL, Gaddy JA, Loh JT, Johnson EM, Hill S, Hennig EE, McClain MS, McDonald WH, Cover TL., PLoS Pathog. 7(9), 2011
PMID: 21909278
Experimental phasing with SHELXC/D/E: combining chain tracing with density modification.
Sheldrick GM., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 4), 2010
PMID: 20383001
Latent TGF-β structure and activation.
Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA., Nature 474(7351), 2011
PMID: 21677751
Assembly of fibronectin extracellular matrix.
Singh P, Carraher C, Schwarzbauer JE., Annu. Rev. Cell Dev. Biol. 26(), 2010
PMID: 20690820
New surface contacts formed upon reductive lysine methylation: improving the probability of protein crystallization.
Sledz P, Zheng H, Murzyn K, Chruszcz M, Zimmerman MD, Chordia MD, Joachimiak A, Minor W., Protein Sci. 19(7), 2010
PMID: 20506323
Cell integrins: commonly used receptors for diverse viral pathogens.
Stewart PL, Nemerow GR., Trends Microbiol. 15(11), 2007
PMID: 17988871
A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation
Tegtmeyer, J. Biol. Chem. 285(), 2010
The role of epithelial integrin receptors in recognition of pulmonary pathogens
Ulanova, J. Innate Immun. 1(), 2009
Lysine methylation as a routine rescue strategy for protein crystallization.
Walter TS, Meier C, Assenberg R, Au KF, Ren J, Verma A, Nettleship JE, Owens RJ, Stuart DI, Grimes JM., Structure 14(11), 2006
PMID: 17098187
Helicobacter pylori CagL dependent induction of gastrin expression via a novel αvβ5-integrin-integrin linked kinase signalling complex.
Wiedemann T, Hofbaur S, Tegtmeyer N, Huber S, Sewald N, Wessler S, Backert S, Rieder G., Gut 61(7), 2012
PMID: 22287591
Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101.
Yeo HJ, Yuan Q, Beck MR, Baron C, Waksman G., Proc. Natl. Acad. Sci. U.S.A. 100(26), 2003
PMID: 14673074
The structure of the human adenovirus 2 penton.
Zubieta C, Schoehn G, Chroboczek J, Cusack S., Mol. Cell 17(1), 2005
PMID: 15629723

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 24076404
PubMed | Europe PMC

Suchen in

Google Scholar