Structural biology of bacterial pathogenesis

Current Opinion in Structural Biology

Volumn 14, Issue 2, 2004, Pages 161-170

  Remaut, Han ^a,b   Waksman, Gabriel ^a,b,c  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AAD; ABC; All helical domain; ATP binding cassette; C terminal domain; CTD; GAP; GEF; GlcNAc; GTPase activating protein; Guanine exchange factor; N acetyl D glucosamine; N terminal domain; NBD; NTD; Nte; Nucleotide binding domain; OM; Outer membrane

Indexed keywords

ADHESIN;

BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOGENESIS; COMPLEX FORMATION; GRAM NEGATIVE BACTERIUM; HOST; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; SECRETION; STRUCTURE ANALYSIS;

ADHESINS, BACTERIAL; BACTERIAL PROTEINS; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; MODELS, MOLECULAR; VIRULENCE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 1842861589     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.03.004     Document Type: Review

References (73)

1. Stathopoulos C., Hendrixson D.R., Thanassi D.G., Hultgren S.J., St Geme J.W. III, Curtiss R. III Secretion of virulence determinants by the general secretory pathway in gram-negative pathogens: an evolving story. Microbes Infect. 2:2000;1061-1072.
2. Thanassi D.G., Hultgren S.J. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr Opin Cell Biol. 12:2000;420-430.
3. Marino M., Braun L., Cossart P., Ghosh P. Structure of the lnlB leucine-rich repeats, a domain that triggers host cell invasion by the bacterial pathogen L. monocytogenes. Mol. Cell. 4:1999;1063-1072.
4. Schubert W.D., Gobel G., Diepholz M., Darji A., Kloer D., Hain T., Chakraborty T., Wehland J., Domann E., Heinz D.W. Internalins from the human pathogen Listeria monocytogenes combine three distinct folds into a contiguous internalin domain. J Mol Biol. 312:2001;783-794.
5. Marino M., Banerjee M., Jonquieres R., Cossart P., Ghosh P. GW domains of the Listeria monocytogenes invasion protein InlB are SH3-like and mediate binding to host ligands. EMBO J. 21:2002;5623-5634.
6. Schubert W.D., Urbanke C., Ziehm T., Beier V., Machner M.P., Domann E., Wehland J., Chakraborty T., Heinz D.W. Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell. 111:2002;825-836 The structure of the InlA-human E-cadherin (hEC1) complex provides a detailed view of early events in Listeria infection: internalisation through adhesion to E-cadherins exposed on the host cell epithelium, followed by dissociation once inside the phagosome.
7. Deivanayagam C.C., Wann E.R., Chen W., Carson M., Rajashankar K.R., Hook M., Narayana S.V. A novel variant of the immunoglobulin fold in surface adhesins of Staphylococcus aureus: crystal structure of the fibrinogen-binding MSCRAMM, clumping factor A. EMBO J. 21:2002;6660-6672.
8. Ponnuraj K., Bowden M.G., Davis S., Gurusiddappa S., Moore D., Choe D., Xu Y., Hook M., Narayana S.V. A 'dock, lock, and latch' structural model for a staphylococcal adhesin binding to fibrinogen. Cell. 115:2003;217-228 This paper presents structures of the ligand-binding domain of the Staphylococcal adhesin SdrG as an apo-protein and in complex with a synthetic peptide analogous to its binding site in fibrinogen. The structures reveal how the ligand is 'locked' in the binding cleft through a conformational change upon complex formation. In addition, the complex rationalizes how SdrG can inhibit the release of chemotactic fibrinopeptide B, reducing the influx of phagocytic neutrophils.
9. Symersky J., Patti J.M., Carson M., House-Pompeo K., Teale M., Moore D., Jin L., Schneider A., DeLucas L.J., Hook M.et al. Structure of the collagen-binding domain from a Staphylococcus aureus adhesin. Nat. Struct. Biol. 4:1997;833-838.
10. Deivanayagam C.C., Rich R.L., Carson M., Owens R.T., Danthuluri S., Bice T., Hook M., Narayana S.V. Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure Fold Des. 8:2000;67-78.
11. Knight S.D., Berglund J., Choudhury D. Bacterial adhesins: structural studies reveal chaperone function and pilus biogenesis. Curr Opin Chem Biol. 4:2000;653-660.
12. Sauer F.G., Mulvey M.A., Schilling J.D., Martinez J.J., Hultgren S.J. Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol. 3:2000;65-72.
13. Choudhury D., Thompson A., Stojanoff V., Langermann S., Pinkner J., Hultgren S.J., Knight S.D. X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science. 285:1999;1061-1066.
14. Hung C.S., Bouckaert J., Hung D., Pinkner J., Widberg C., DeFusco A., Auguste C.G., Strouse R., Langermann S., Waksman G., Hultgren S.J. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol. 44:2002;903-915.
15. Dodson K.W., Pinkner J.S., Rose T., Magnusson G., Hultgren S.J., Waksman G. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell. 105:2001;733-743.
16. Merckel M.C., Tanskanen J., Edelman S., Westerlund-Wikstrom B., Korhonen T.K., Goldman A. The structural basis of receptor-binding by Escherichia coli associated with diarrhea and septicemia. J Mol Biol. 331:2003;897-905.
17. Buts L., Bouckaert J., De Genst E., Loris R., Oscarson S., Lahmann M., Messens J., Brosens E., Wyns L., De Greve H. The fimbrial adhesin F17-G of enterotoxigenic Escherichia coli has an immunoglobulin-like lectin domain that binds N-acetylglucosamine. Mol Microbiol. 49:2003;705-715.
18. Sung M., Fleming K., Chen H.A., Matthews S. The solution structure of PapGII from uropathogenic E. coli and its recognition of glycolipids receptors. EMBO Rep. 19:2001;2452-2464.
19. Parge H.E., Forest K.T., Hickey M.J., Christensen D.A., Getzoff E.D., Tainer J.A. Structure of the fibre-forming protein pilin at 2.6 Å resolution. Nature. 378:1995;32-38.
20. Hazes B., Sastry P.A., Hayakawa K., Read R.J., Irvin R.T. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J. Mol. Biol. 299:2000;1005-1017.
21. Keizer D.W., Slupsky C.M., Kalisiak M., Campbell A.P., Crump M.P., Sastry P.A., Hazes B., Irvin R.T., Sykes B.D. Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili. J Biol Chem. 276:2001;24186-24193.
22. Craig L., Taylor R.K., Pique M.E., Adair B.D., Arvai A.S., Singh M., Lloyd S.J., Shin D.S., Getzoff E.D., Yeager M.et al. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell. 11:2003;1139-1150 The structure of the TCP (toxin-coregulated pilus) pilin TcpA provides hitherto lacking structural information on the type IVb pilin subclass and confirms the existence of a common scaffold for all type IV pilins. Structure-based TCP assembly models also generalize packing principles and explain distinct assembly architectures in type IV pili.
23. Emsley P., Charles I.G., Fairweather N.F., Isaacs N.W. Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature. 381:1996;90-92.
24. Hamburger Z.A., Brown M.S., Isberg R.R., Bjorkman P.J. Crystal structure of invasin: a bacterial integrin-binding protein. Science. 286:1999;291-295.
25. Batchelor M., Prasannan S., Daniell S., Reece S., Connerton I., Bloomberg G., Dougan G., Frankel G., Matthews S. Structural basis for recognition of the translocated intimin receptor (Tir) by intimin from enteropathogenic Escherichia coli. EMBO J. 19:2000;2452-2464.
26. Luo Y., Frey E.A., Pfuetzner R.A., Creagh A.L., Knoechel D.G., Haynes C.A., Finlay B.B., Strynadka N.C. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature. 405:2000;1073-1077.
27. Prince S.M., Achtman M., Derrick J.P. Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitidis. Proc Natl Acad Sci USA. 99:2002;3417-3421.
28. Fernandez L.A., Berenguer J. Secretion and assembly of regular surface structures in Gram-negative bacteria. FEMS Microbiol Rev. 24:2000;21-44.
29. Soto G.E., Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol. 181:1999;1059-1071.
30. Andersen C., Hughes C., Koronakis V. Protein export and drug efflux through bacterial channel-tunnels. Curr Opin Cell Biol. 13:2001;412-416.
31. Thanabalu T., Koronakis E., Hughes C., Koronakis V. Substrate-induced assembly of a contiguous channel for protein export from E. coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J. 17:1998;6487-6496.
32. Koronakis V., Sharff A., Koronakis E., Luisi B., Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature. 405:2000;914-919.
33. Andersen C., Koronakis E., Bokma E., Eswaran J., Humphreys D., Hughes C., Koronakis V. Transition to the open state of the TolC periplasmic tunnel entrance. Proc Natl Acad Sci USA. 99:2002;11103-11108 To assess how opening of the coiled-coil TolC tunnel is achieved, the authors disrupted interhelical connections and monitored changes in the aperture size by measuring the single-channel conductance of TolC derivatives in black lipid bilayers.
34. Thanassi D.G., Saulino E.T., Hultgren S.J. The chaperone/usher pathway: a major terminal branch of the general secretory pathway. Curr. Opin. Microbiol. 1:1998;223-231.
35. Sauer F.G., Barnhart M., Choudhury D., Knight S.D., Waksman G., Hultgren S.J. Chaperone-assisted pilus assembly and bacterial attachment. Curr Opin Struct Biol. 10:2000;548-556.
36. Sauer F.G., Futterer K., Pinkner J.S., Dodson K.W., Hultgren S.J., Waksman G. Structural basis of chaperone function and pilus biogenesis. Science. 285:1999;1058-1061.
37. Ntd in complex with the PapD chaperone and the PapK Nte peptide demonstrate how the chaperone primes pilus subunits for assembly in the absence of a NTP-driven step by preserving part of their folding energy.
38. Zavialov A.V., Berglund J., Pudney A.F., Fooks L.J., Ibrahim T.M., MacIntyre S., Knight S.D. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell. 113:2003;587-596 The Caf1 pilin and Caf1M chaperone structures provide the first structural information on the FGL subclass of chaperone-usher components, responsible for the formation of atypical fibrillar pili. The structure of the Caf1M-Caf1-Caf1 ternary complex reveals the minimal F1 fibre and confirms the principle of trapping the chaperone-usher pilins in a high-energy folding intermediate to prime them for fibre formation.
39. Blocker A., Jouihri N., Larquet E., Gounon P., Ebel F., Parsot C., Sansonetti P., Allaoui A. Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol. 39:2001;652-663.
40. Cordes F.S., Komoriya K., Larquet E., Yang S., Egelman E.H., Blocker A., Lea S.M. Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem. 278:2003;17103-17107.
41. Kubori T., Matsushima Y., Nakamura D., Uralil J., Lara-Tejero M., Sukhan A., Galan J.E., Aizawa S.I. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science. 280:1998;602-605.
42. Sekiya K., Ohishi M., Ogino T., Tamano K., Sasakawa C., Abe A. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci USA. 98:2001;11638-11643.
43. Stebbins C.E., Galan J.E. Structural mimicry in bacterial virulence. Nature. 412:2001;701-705.
44. Stebbins C.E., Galan J.E. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature. 414:2001;77-81.
45. Birtalan S.C., Phillips R.M., Ghosh P. Three-dimensional secretion signals in chaperone-effector complexes of bacterial pathogens. Mol Cell. 9:2002;971-980 The structure of the SycE-YopE complex confirms that the chaperone-binding domains of type III effectors bind their chaperones in a partially folded state. However, the authors show that the action of the chaperone is localized to the chaperone-binding domain only and is not transmitted to the effector domain.
46. Yonekura K., Maki-Yonekura S., Namba K. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature. 424:2003;643-650.
47. Luo Y., Bertero M.G., Frey E.A., Pfuetzner R.A., Wenk M.R., Creagh L., Marcus S.L., Lim D., Sicheri F., Kay C.et al. Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat. Struct. Biol. 8:2001;1031-1036.
48. Birtalan S., Ghosh P. Structure of the Yersinia type III secretory system chaperone SycE. Nat Struct Biol. 8:2001;974-978.
49. Evdokimov A.G., Tropea J.E., Routzahn K.M., Waugh D.S. Three-dimensional structure of the type III secretion chaperone SycE from Yersinia pestis. Acta Crystallogr D Biol Crystallogr. 58:2002;398-406.
50. Buchwald G., Friebel A., Galan J.E., Hardt W.D., Wittinghofer A., Scheffzek K. Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE. EMBO J. 21:2002;3286-3295 This paper reports the structure of the catalytic domain of the bacterial GEF SopE in complex with the human Rho GTPase Cdc42. SopE represents the first example of a non-Dbl-like protein capable of inducing nucleotide exchange in Rho family proteins.
51. Stebbins C.E., Galan J.E. Modulation of host signaling by a bacterial mimic: structure of the Salmonella effector SptP bound to Rac1. Mol Cell. 6:2000;1449-1460.
52. Wurtele M., Wolf E., Pederson K.J., Buchwald G., Ahmadian M.R., Barbieri J.T., Wittinghofer A. How the Pseudomonas aeruginosa ExoS toxin downregulates Rac. Nat Struct Biol. 8:2001;23-26.
53. Wurtele M., Renault L., Barbieri J.T., Wittinghofer A., Wolf E. Structure of the ExoS GTPase activating domain. FEBS Lett. 491:2001;26-29.
54. Evdokimov A.G., Tropea J.E., Routzahn K.M., Waugh D.S. Crystal structure of the Yersinia pestis GTPase activator YopE. Protein Sci. 11:2002;401-408.
55. Smith C.L., Khandelwal P., Keliikuli K., Zuiderweg E.R., Saper M.A. Structure of the type III secretion and substrate-binding domain of Yersinia YopH phosphatase. Mol Microbiol. 42:2001;967-979.
56. Khandelwal P., Keliikuli K., Smith C.L., Saper M.A., Zuiderweg E.R. Solution structure and phosphopeptide binding to the N-terminal domain of Yersinia YopH: comparison with a crystal structure. Biochemistry. 41:2002;11425-11437.
57. Sun J.P., Wu L., Fedorov A.A., Almo S.C., Zhang Z.Y. Crystal structure of the Yersinia protein-tyrosine phosphatase YopH complexed with a specific small molecule inhibitor. J Biol Chem. 278:2003;33392-33399.
58. Evdokimov A.G., Anderson D.E., Routzahn K.M., Waugh D.S. Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J Mol Biol. 312:2001;807-821.
59. Lilic M., Galkin V.E., Orlova A., VanLoock M.S., Egelman E.H., Stebbins C.E. Salmonella SipA polymerizes actin by stapling filaments with nonglobular protein arms. Science. 301:2003;1918-1921 By combining X-ray crystallography of Salmonella invasin protein A (SipA) with electron microscopy and image analysis of SipA-actin filaments, the authors show that SipA acts a 'molecular staple', tethering and stabilizing subunits in opposing strands.
60. Christie P.J. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol Microbiol. 40:2001;294-305.
61. Yeo H.J., Savvides S.N., Herr A.B., Lanka E., Waksman G. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol Cell. 6:2000;1461-1472.
62. Savvides S.N., Yeo H.J., Beck M.R., Blaesing F., Lurz R., Lanka E., Buhrdorf R., Fischer W., Haas R., Waksman G. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:2003;1969-1980.
63. Gomis-Ruth F.X., Moncalian G., Perez-Luque R., Gonzalez A., Cabezon E., de la Cruz F., Coll M. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature. 409:2001;573-575.
64. Gomis-Ruth F.X., Moncalian G., de la Cruz F., Coll M. Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein. Detailed structural features and mapping of the active site cleft. J Biol Chem. 277:2002;7556-7566.
65. Yeo H.J., Yuan Q., Beck M.R., Baron C., Waksman G. Structural and functional characterization of the VirB5 protein from the type IV secretion system encoded by the conjugative plasmid pKM101. Proc Natl Acad Sci USA. 100:2003;15947-15952.
66. Stein P.E., Boodhoo A., Armstrong G.D., Cockle S.A., Klein M.H., Read R.J. The crystal structure of pertussis toxin. Structure. 2:1994;45-57.
67. Hazes B., Boodhoo A., Cockle S.A., Read R.J. Crystal structure of the pertussis toxin-ATP complex: a molecular sensor. J Mol Biol. 258:1996;661-671.
68. Stein P.E., Boodhoo A., Armstrong G.D., Heerze L.D., Cockle S.A., Klein M.H., Read R.J. Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nat Struct Biol. 1:1994;591-596.
69. Datta S., Larkin C., Schildbach J.F. Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Structure (Camb). 11:2003;1369-1379.
70. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of proteins structures. J Appl Crystallogr. 24:1991;946-950.
71. Oomen CJ, van Ulsen P, Van Gelder P, Feijen M, Tommassen J, Gros P: Structure of the translocator domain of a bacterial autotransporter. EMBO J 2004, in press. The in vitro folded NalP translocator domain comprises a 12-stranded β-barrel with a hydrophilic pore of 10 × 12.5 Å that is filled by an N-terminal α-helix. This is consistent with a model of passenger-domain transport through the hydrophilic channel within the β-barrel in an unfolded form.
72. Nummelin H, Merckel MC, Leo JC, Lankinen H, Skurnik M, Goldman A: The Yersinia adhesin YadA collagen-binding domain structure is a novel left-handed parallel β-roll. EMBO J 2004, in press.
73. Yeo H-J, Cotter SH, Laarman S, Juehne T, St Geme JW III, Waksman G: Structural basis for host recognition by the Haemophilus influenzae Hia autotransporter. EMBO J 2004, in press.