The antigen 43 structure reveals a molecular Velcrolike mechanism of autotransporter-mediated bacterial clumping

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages 457-462

  Heras, Begoña ^a   Totsika, Makrina ^b   Peters, Kate M ^b   Paxman, Jason J ^a,c   Gee, Christine L ^c   Jarrott, Russell J ^b   Perugini, Matthew A ^a   Whitten, Andrew E ^b   Schembri, Mark A ^b  

^a LA TROBE UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c AUSTRALIAN SYNCHROTRON   (Australia)

Author keywords

Ag43; Structural biology; Urinary tract infection; Virulence factor

Indexed keywords

ANTIGEN; ANTIGEN 43; AUTOTRANSPORTER PROTEIN; BACTERIAL PROTEIN; HYDROGEN; UNCLASSIFIED DRUG;

ANTIGEN STRUCTURE; ARTICLE; CELL AGGREGATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; MICROBIAL ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; UROPATHOGENIC ESCHERICHIA COLI;

AG43; STRUCTURAL BIOLOGY; URINARY TRACT INFECTION; VIRULENCE FACTOR;

ADHESINS, BACTERIAL; ADHESINS, ESCHERICHIA COLI; ANTIGENS, BACTERIAL; BIOFILMS; BIOLOGICAL TRANSPORT; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI; X-RAY DIFFRACTION;

EID: 84891924103     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311592111     Document Type: Article

References (49)

1. Benz I, Schmidt MA (2011) Structures and functions of autotransporter proteins in microbial pathogens. Int J Med Microbiol 301(6): 461-468.
2. Kajava AV, Steven AC (2006) The turn of the screw: Variations of the abundant betasolenoid motif in passenger domains of type V secretory proteins. J Struct Biol 155(2): 306-315.
3. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D (2004) Type V protein secretion pathway: The autotransporter story. Microbiol Mol Biol Rev 68(4): 692-744.
4. Celik N, et al. (2012) A bioinformatic strategy for the detection, classification and analysis of bacterial autotransporters. PLoS ONE 7(8):e43245.
5. Henderson IR, Cappello R, Nataro JP (2000) Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol 8(12): 529-532.
6. Ieva R, Bernstein HD (2009) Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc Natl Acad Sci USA 106(45): 19120-19125.
7. Selkrig J, et al. (2012) Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol 19(5): 506-510.
8. Wells TJ, Totsika M, Schembri MA (2010) Autotransporters of Escherichia coli: A sequence- based characterization. Microbiology 156(Pt 8): 2459-2469.
9. Leyton DL, Rossiter AE, Henderson IR (2012) From self sufficiency to dependence: Mechanisms and factors important for autotransporter biogenesis. Nat Rev Microbiol 10(3): 213-225.
10. Ulett GC, et al. (2007) Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 75(7): 3233-3244.
11. Roche A, McFadden J, Owen P (2001) Antigen 43, the major phase-variable protein of the Escherichia coli outer membrane, can exist as a family of proteins encoded by multiple alleles. Microbiology 147(Pt 1): 161-169.
12. Henderson IR, Meehan M, Owen P (1997) Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol Lett 149(1): 115-120.
13. Danese PN, Pratt LA, Dove SL, Kolter R (2000) The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol Microbiol 37(2): 424-432.
14. Klemm P, Hjerrild L, Gjermansen M, Schembri MA (2004) Structure-function analysis of the self-recognizing Antigen 43 autotransporter protein from Escherichia coli. Mol Microbiol 51(1): 283-296.
15. Anderson GG, et al. (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301(5629): 105-107.
16. Webb CT, Heinz E, Lithgow T (2012) Evolution of the β-barrel assembly machinery. Trends Microbiol 20(12): 612-620.
17. Schembri MA, Hjerrild L, Gjermansen M, Klemm P (2003) Differential expression of the Escherichia coli autoaggregation factor antigen 43. J Bacteriol 185(7): 2236-2242.
18. Meng G, Spahich N, Kenjale R, Waksman G, St Geme JW III (2011) Crystal structure of the Haemophilus influenzae Hap adhesin reveals an intercellular oligomerization mechanism for bacterial aggregation. EMBO J 30(18): 3864-3874.
19. Xu Q, et al. (2008) Statistical analysis of interface similarity in crystals of homologous proteins. J Mol Biol 381(2): 487-507.
20. Reisner A, Molin S, Zechner EL (2002) Recombinogenic engineering of conjugative plasmids with fluorescent marker cassettes. FEMS Microbiol Ecol 42(2): 251-259.
21. Kjaergaard K, Schembri MA, Ramos C, Molin S, Klemm P (2000) Antigen 43 facilitates formation of multispecies biofilms. Environ Microbiol 2(6): 695-702.
22. Reisner A, Haagensen JA, Schembri MA, Zechner EL, Molin S (2003) Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol 48(4): 933-946.
23. Serruto D, Bottomley MJ, Ram S, Giuliani MM, Rappuoli R (2012) The new multicomponent vaccine against meningococcal serogroup B, 4CMenB: Immunological, functional and structural characterization of the antigens. Vaccine 30(Suppl 2): B87-B97.
24. Poolman JT, Hallander HO (2007) Acellular pertussis vaccines and the role of pertactin and fimbriae. Expert Rev Vaccines 6(1): 47-56.
25. Emsley P, Charles IG, Fairweather NF, Isaacs NW (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381(6577): 90-92.
26. van den Berg B (2010) Crystal structure of a full-length autotransporter. J Mol Biol 396(3): 627-633.
27. Gangwer KA, et al. (2007) Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc Natl Acad Sci USA 104(41): 16293-16298.
28. Johnson TA, Qiu J, Plaut AG, Holyoak T (2009) Active-site gating regulates substrate selectivity in a chymotrypsin-like serine protease: The structure of Haemophilus influenzae immunoglobulin A1 protease. J Mol Biol 389(3): 559-574.
29. Khan S, Mian HS, Sandercock LE, Chirgadze NY, Pai EF (2011) Crystal structure of the passenger domain of the Escherichia coli autotransporter EspP. J Mol Biol 413(5): 985-1000.
30. Otto BR, et al. (2005) Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J Biol Chem 280(17): 17339-17345.
31. Barnard TJ, Dautin N, Lukacik P, Bernstein HD, Buchanan SK (2007) Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat Struct Mol Biol 14(12): 1214-1220.
32. Zhai Y, et al. (2011) Autotransporter passenger domain secretion requires a hydrophobic cavity at the extracellular entrance of the β-domain pore. Biochem J 435(3): 577-587.
33. Oomen CJ, et al. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23(6): 1257-1266.
34. Tajima N, Kawai F, Park SY, Tame JR (2010) A novel intein-like autoproteolytic mechanism in autotransporter proteins. J Mol Biol 402(4): 645-656.
35. Hartmann MD, et al. (2012) Complete fiber structures of complex trimeric autotransporter adhesins conserved in enterobacteria. Proc Natl Acad Sci USA 109(51): 20907-20912.
36. Grijpstra J, Arenas J, Rutten L, Tommassen J (2013) Autotransporter secretion: Varying on a theme. Res Microbiol 164(6): 562-582.
37. Hooton TM (2012) Clinical practice. Uncomplicated urinary tract infection. N Engl J Med 366(11): 1028-1037.
38. Totsika M, et al. (2012) Uropathogenic Escherichia coli mediated urinary tract infection. Curr Drug Targets 13(11): 1386-1399.
39. Sherlock O, Schembri MA, Reisner A, Klemm P (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: Cell aggregation and biofilm formation. J Bacteriol 186(23): 8058-8065.
40. Heras B, et al. (2003) Dehydration converts DsbG crystal diffraction from low to high resolution. Structure 11(2): 139-145.
41. Kabsch W (2010) XDS. Acta Crystallogr D Biol Crystallogr 66(Pt 2): 125-132.
42. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62(Pt 1): 72-82.
43. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
44. Adams PD, et al. (2002) PHENIX: Building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58(Pt 11): 1948-1954.
45. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1): 2126-2132.
46. Painter J, Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62(Pt 4): 439-450.
47. DeLano WL (2002) The PyMOL Molecular Graphics System (DeLano Scientific, San Carlos, CA).
48. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14): 4121-4130.
49. Kjaergaard K, Schembri MA, Hasman H, Klemm P (2000) Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens. J Bacteriol 182(17): 4789-4796.