Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD

Schreiner M, Niemann H (2012)
BMC Structural Biology 12(1): 13.

Download
OA
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Volltext vorhanden für diesen Nachweis
Abstract / Bemerkung
Background Type III secretion systems are used by Gram-negative bacteria as “macromolecular syringes” to inject effector proteins into eukaryotic cells. Two hydrophobic proteins called translocators form the necessary pore in the host cell membrane. Both translocators depend on binding to a single chaperone in the bacterial cytoplasm to ensure their stability and efficient transport through the secretion needle. It was suggested that the conserved chaperones bind the more divergent translocators via a hexapeptide motif that is found in both translocators and conserved between species. Results We crystallized a synthetic decapeptide from the Yersinia enterocolitica minor type III secretion translocator YopD bound to its cognate chaperone SycD and determined the complex structure at 2.5 Å resolution. The structure of peptide-bound SycD is almost identical to that of apo SycD with an all helical fold consisting of three tetratricopeptide repeats (TPRs) and an additional C-terminal helix. Peptide-bound SycD formed a kinked head-to-head dimer that had previously been observed for the apo form of SycD. The homodimer interface comprises both helices of the first tetratricopeptide repeat. The YopD peptide bound in extended conformation into a mainly hydrophobic groove on the concave side of SycD. TPRs 1 and 2 of SycD form three hydrophobic pockets that accommodated the conserved hydrophobic residues at position 1, 3 and 6 of the translocator hexapeptide sequence. Two tyrosines that are highly conserved among translocator chaperones contribute to the hydrophobic patches but also form hydrogen bonds to the peptide backbone. Conclusions The interaction between SycD and YopD is very similar to the binding of the Pseudomonas minor translocator PopD to its chaperone PcrH and the Shigella major translocator IpaB to its chaperone IpgC. This confirms the prediction made by Kolbe and co-workers that a hexapeptide with hydrophobic residues at three positions is a conserved chaperone binding motif. Because the hydrophobic groove on the concave side of translocator chaperones is involved in binding of the major and the minor translocator, simultaneous binding of both translocators to a single type III secretion class II chaperone appears unlikely.
Erscheinungsjahr
Zeitschriftentitel
BMC Structural Biology
Band
12
Ausgabe
1
Seite(n)
13
ISSN
Finanzierungs-Informationen
Article Processing Charge funded by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
PUB-ID

Zitieren

Schreiner M, Niemann H. Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Structural Biology. 2012;12(1):13.
Schreiner, M., & Niemann, H. (2012). Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Structural Biology, 12(1), 13. doi:10.1186/1472-6807-12-13
Schreiner, M., and Niemann, H. (2012). Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Structural Biology 12, 13.
Schreiner, M., & Niemann, H., 2012. Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Structural Biology, 12(1), p 13.
M. Schreiner and H. Niemann, “Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD”, BMC Structural Biology, vol. 12, 2012, pp. 13.
Schreiner, M., Niemann, H.: Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD. BMC Structural Biology. 12, 13 (2012).
Schreiner, Madeleine, and Niemann, Hartmut. “Crystal structure of the Yersinia enterocolitica type III secretion chaperone SycD in complex with a peptide of the minor translocator YopD”. BMC Structural Biology 12.1 (2012): 13.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Copyright Statement:
This Item is protected by copyright and/or related rights. [...]
Volltext(e)
Access Level
OA Open Access
Zuletzt Hochgeladen
2012-09-24T14:21:15Z

9 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

The Structure and Function of Type III Secretion Systems.
Notti RQ, Stebbins CE., Microbiol Spectr 4(1), 2016
PMID: 26999392
Random mutagenesis identifies a C-terminal region of YopD important for Yersinia type III secretion function.
Solomon R, Zhang W, McCrann G, Bliska JB, Viboud GI., PLoS One 10(3), 2015
PMID: 25807250
Membrane and chaperone recognition by the major translocator protein PopB of the type III secretion system of Pseudomonas aeruginosa.
Discola KF, Förster A, Boulay F, Simorre JP, Attree I, Dessen A, Job V., J Biol Chem 289(6), 2014
PMID: 24297169
Binding mode analysis of a major T3SS translocator protein PopB with its chaperone PcrH from Pseudomonas aeruginosa.
Banerjee A, Dey S, Chakraborty A, Datta A, Basu A, Chakrabarti S, Datta S., Proteins 82(12), 2014
PMID: 25116453
The Deinococcus radiodurans DR1245 protein, a DdrB partner homologous to YbjN proteins and reminiscent of type III secretion system chaperones.
Norais C, Servant P, Bouthier-de-la-Tour C, Coureux PD, Ithurbide S, Vannier F, Guerin PP, Dulberger CL, Satyshur KA, Keck JL, Armengaud J, Cox MM, Sommer S., PLoS One 8(2), 2013
PMID: 23441204
Structure and biophysics of type III secretion in bacteria.
Chatterjee S, Chaudhury S, McShan AC, Kaur K, De Guzman RN., Biochemistry 52(15), 2013
PMID: 23521714
The SseC translocon component in Salmonella enterica serovar Typhimurium is chaperoned by SscA.
Cooper CA, Mulder DT, Allison SE, Pilar AV, Coombes BK., BMC Microbiol 13(), 2013
PMID: 24090070

60 References

Daten bereitgestellt von Europe PubMed Central.

Yersinia outer proteins: Yops.
Trosky JE, Liverman AD, Orth K., Cell. Microbiol. 10(3), 2007
PMID: 18081726
The type III secretion injectisome.
Cornelis GR., Nat. Rev. Microbiol. 4(11), 2006
PMID: 17041629
Biogenesis, regulation, and targeting of the type III secretion system.
Izore T, Job V, Dessen A., Structure 19(5), 2011
PMID: 21565695
Type III secretion: more systems than you think.
Troisfontaines P, Cornelis GR., Physiology (Bethesda) 20(), 2005
PMID: 16174872
Structural dissection of the extracellular moieties of the type III secretion apparatus.
Wang Y, Zhang L, Picking WL, Picking WD, De Guzman RN., Mol Biosyst 4(12), 2008
PMID: 19396380
The structures of coiled-coil domains from type III secretion system translocators reveal homology to pore-forming toxins.
Barta ML, Dickenson NE, Patil M, Keightley A, Wyckoff GJ, Picking WD, Picking WL, Geisbrecht BV., J. Mol. Biol. 417(5), 2012
PMID: 22321794
EspA filament-mediated protein translocation into red blood cells.
Shaw RK, Daniell S, Ebel F, Frankel G, Knutton S., Cell. Microbiol. 3(4), 2001
PMID: 11298645
The purified Shigella IpaB and Salmonella SipB translocators share biochemical properties and membrane topology.
Hume PJ, McGhie EJ, Hayward RD, Koronakis V., Mol. Microbiol. 49(2), 2003
PMID: 12828640
The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes.
Goure J, Pastor A, Faudry E, Chabert J, Dessen A, Attree I., Infect. Immun. 72(8), 2004
PMID: 15271936
The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes.
Blocker A, Gounon P, Larquet E, Niebuhr K, Cabiaux V, Parsot C, Sansonetti P., J. Cell Biol. 147(3), 1999
PMID: 10545510
Membrane targeting and pore formation by the type III secretion system translocon.
Mattei PJ, Faudry E, Job V, Izore T, Attree I, Dessen A., FEBS J. 278(3), 2010
PMID: 21182592
The multitalented type III chaperones: all you can do with 15 kDa.
Feldman MF, Cornelis GR., FEMS Microbiol. Lett. 219(2), 2003
PMID: 12620614
The various and varying roles of specific chaperones in type III secretion systems.
Parsot C, Hamiaux C, Page AL., Curr. Opin. Microbiol. 6(1), 2003
PMID: 12615213
On the role of specific chaperones, the specific ATPase, and the proton motive force in type III secretion.
Wilharm G, Dittmann S, Schmid A, Heesemann J., Int. J. Med. Microbiol. 297(1), 2006
PMID: 17126597
Chaperone release and unfolding of substrates in type III secretion.
Akeda Y, Galan JE., Nature 437(7060), 2005
PMID: 16208377
Energizing type III secretion machines: what is the fuel?
Galan JE., Nat. Struct. Mol. Biol. 15(2), 2008
PMID: 18250631
Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD.
Neyt C, Cornelis GR., Mol. Microbiol. 31(1), 1999
PMID: 9987117
Structure of the Yersinia enterocolitica type III secretion translocator chaperone SycD.
Buttner CR, Sorg I, Cornelis GR, Heinz DW, Niemann HH., J. Mol. Biol. 375(4), 2007
PMID: 18054956
Crystal structure of the heteromolecular chaperone, AscE-AscG, from the type III secretion system in Aeromonas hydrophila.
Chatterjee C, Kumar S, Chakraborty S, Tan YW, Leung KY, Sivaraman J, Mok YK., PLoS ONE 6(4), 2011
PMID: 21559439
Structure of the heterotrimeric complex that regulates type III secretion needle formation.
Quinaud M, Ple S, Job V, Contreras-Martel C, Simorre JP, Attree I, Dessen A., Proc. Natl. Acad. Sci. U.S.A. 104(19), 2007
PMID: 17470796
IpaB-IpgC interaction defines binding motif for type III secretion translocator.
Lunelli M, Lokareddy RK, Zychlinsky A, Kolbe M., Proc. Natl. Acad. Sci. U.S.A. 106(24), 2009
PMID: 19478065
Structural basis of chaperone recognition of type III secretion system minor translocator proteins.
Job V, Mattei PJ, Lemaire D, Attree I, Dessen A., J. Biol. Chem. 285(30), 2010
PMID: 20385547
Inference of macromolecular assemblies from crystalline state.
Krissinel E, Henrick K., J. Mol. Biol. 372(3), 2007
PMID: 17681537
DaliLite workbench for protein structure comparison.
Holm L, Park J., Bioinformatics 16(6), 2000
PMID: 10980157
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
Statistical analysis of interface similarity in crystals of homologous proteins.
Xu Q, Canutescu AA, Wang G, Shapovalov M, Obradovic Z, Dunbrack RL Jr., J. Mol. Biol. 381(2), 2008
PMID: 18599072
Yersinia enterocolitica type III secretion chaperone SycD: recombinant expression, purification and characterization of a homodimer.
Schmid A, Dittmann S, Grimminger V, Walter S, Heesemann J, Wilharm G., Protein Expr. Purif. 49(2), 2006
PMID: 16750393
Crystallization and preliminary crystallographic analysis of the type III secretion translocator chaperone SicA from Salmonella enterica
AUTHOR UNKNOWN, 2010
Evidence for alternative quaternary structure in a bacterial Type III secretion system chaperone.
Barta ML, Zhang L, Picking WL, Geisbrecht BV., BMC Struct. Biol. 10(), 2010
PMID: 20633281
Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20.
Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D., Cell 100(5), 2000
PMID: 10721992
Structural basis for recruitment of mitochondrial fission complexes by Fis1.
Zhang Y, Chan DC., Proc. Natl. Acad. Sci. U.S.A. 104(47), 2007
PMID: 17998537
Peroxisomal targeting signal-1 recognition by the TPR domains of human PEX5.
Gatto GJ Jr, Geisbrecht BV, Gould SJ, Berg JM., Nat. Struct. Biol. 7(12), 2000
PMID: 11101887
Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine.
Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I., Cell 101(2), 2000
PMID: 10786835
Chaperoned ubiquitylation--crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex.
Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, Prodromou C, Pearl LH., Mol. Cell 20(4), 2005
PMID: 16307917
Tetratricopeptide-like repeats in type-III-secretion chaperones and regulators.
Pallen MJ, Francis MS, Futterer K., FEMS Microbiol. Lett. 223(1), 2003
PMID: 12799000
Preparation and characterization of translocator/chaperone complexes and their component proteins from Shigella flexneri.
Birket SE, Harrington AT, Espina M, Smith ND, Terry CM, Darboe N, Markham AP, Middaugh CR, Picking WL, Picking WD., Biochemistry 46(27), 2007
PMID: 17571858
Oligomerization of type III secretion proteins PopB and PopD precedes pore formation in Pseudomonas.
Schoehn G, Di Guilmi AM, Lemaire D, Attree I, Weissenhorn W, Dessen A., EMBO J. 22(19), 2003
PMID: 14517235
Investigation of EscA as a chaperone for the Edwardsiella tarda type III secretion system putative translocon component EseC.
Wang B, Mo ZL, Mao YX, Zou YX, Xiao P, Li J, Yang JY, Ye XH, Leung KY, Zhang PJ., Microbiology (Reading, Engl.) 155(Pt 4), 2009
PMID: 19332827
EscC is a chaperone for the Edwardsiella tarda type III secretion system putative translocon components EseB and EseD.
Zheng J, Li N, Tan YP, Sivaraman J, Mok YK, Mo ZL, Leung KY., Microbiology (Reading, Engl.) 153(Pt 6), 2007
PMID: 17526852
Anatomy of hot spots in protein interfaces.
Bogan AA, Thorn KS., J. Mol. Biol. 280(1), 1998
PMID: 9653027
Tetratricopeptide repeats in the type III secretion chaperone, LcrH: their role in substrate binding and secretion.
Edqvist PJ, Broms JE, Betts HJ, Forsberg A, Pallen MJ, Francis MS., Mol. Microbiol. 59(1), 2006
PMID: 16359316
Yersinia pestis YopD 150-287 fragment is partially unfolded in the native state.
Raab R, Swietnicki W., Protein Expr. Purif. 58(1), 2007
PMID: 18160307
XDS.
Kabsch W., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 2), 2010
PMID: 20124692
Scaling and assessment of data quality.
Evans P., Acta Crystallogr. D Biol. Crystallogr. 62(Pt 1), 2005
PMID: 16369096
The CCP4 suite: programs for protein crystallography.
Collaborative Computational Project, Number 4., Acta Crystallogr. D Biol. Crystallogr. 50(Pt 5), 1994
PMID: 15299374
Phaser crystallographic software.
McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ., J Appl Crystallogr 40(Pt 4), 2007
PMID: 19461840
Features and development of Coot.
Emsley P, Lohkamp B, Scott WG, Cowtan K., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 4), 2010
PMID: 20383002
MolProbity: all-atom structure validation for macromolecular crystallography.
Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC., Acta Crystallogr. D Biol. Crystallogr. 66(Pt 1), 2009
PMID: 20057044

AUTHOR UNKNOWN, 2011
Electrostatics of nanosystems: application to microtubules and the ribosome.
Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA., Proc. Natl. Acad. Sci. U.S.A. 98(18), 2001
PMID: 11517324

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 22708907
PubMed | Europe PMC

Suchen in

Google Scholar