Sequential Unfolding of Beta Helical Protein by Single-Molecule Atomic Force Microscopy

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Alsteens, David ^a   Martinez, Nicolas ^b,c   Jamin, Marc ^b   Jacob Dubuisson, Françoise ^d  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c INSTITUT LAUE LANGEVIN   (France)

^d UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FILAMENTOUS HEMAGGLUTININ; PROTEIN TPSA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; MECHANICAL STRESS; MOLECULAR DYNAMICS; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN UNFOLDING; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION;

BACTERIAL PROTEINS; GLUCOSYLTRANSFERASES; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; PROTEINS;

EID: 84883243633     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073572     Document Type: Article

References (42)

1. Kajava AV, Steven AC, (2006) β-rolls, β-helices, and other β-solenoid proteins. Adv Protein Chem 73: 55-96.
2. Jenkins J, Pickersgill R, (2001) The architecture of parallel β-helices and related folds. Prog Biophys Mol Biol 77: 111-175.
3. Yoder MD, Keen NT, Jurnak F, (1993) New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 260: 1503-1507.
4. Bryan AW Jr, Starner-Kreinbrink JL, Hosur R, Clark PL, Berger B, (2011) Structure-based prediction reveals capping motifs that inhibit β-helix aggregation. Proc Natl Acad Sci USA 108: 11099-11104.
5. Bradley P, Cowen L, Menke M, King J, Berger B, (2001) BETAwrap: Successful prediction of parallel β-helices from primary sequence reveals an association with many microbial pathogens. Proc Natl Acad Sci USA 98: 14819-14824.
6. Kajava A, Stevens A, (2006) The turn of the screw: variations of the abundant beta-solenoid motif in passenger domains of Type V secretory proteins. J Struct Biol 155: 306-315.
7. Rief M, Gautel M, Oesterhelt F, Fernandez JM, Gaub HE, (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276: 1109-1112.
8. Rief M, Pascual J, Saraste M, Gaub HE, (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol 286: 553-561.
9. Emsley P, Charles IG, Fairweather NF, Isaacs NW, (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381: 90-92.
10. Otto BR, Sijbrandi R, Luirink J, Oudega B, Heddle, J G, et al. (2005) Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J Biol Chem 280: 17339-17345.
11. Gangwer KA, Mushrush DJ, Stauff DL, Spiller B, McClain MS, et al. (2007) Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc Natl Acad Sci USA 104: 16293-16298.
12. Clantin B, Hodak H, Willery E, Locht C, Jacob-Dubuisson F, et al. (2004) The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc Natl Acad Sci USA 101: 6194-6199.
13. Yeo HJ, Yokoyama T, Walkiewicz K, Kim Y, Grass S, et al. (2007) The structure of the Haemophilus influenzae HMW1 pro-piece reveals a structural domain essential for bacterial two-partner secretion. J Biol Chem 282: 31076-31084.
14. Weaver TM, Hocking JM, Bailey LJ, Wawrzyn GT, Howard DR, et al. (2009) Structural and functional studies of truncated hemolysin a from Proteus mirabilis. J Biol Chem 284: 22297-22309.
15. Jacob-Dubuisson F, Fernandez R, Coutte L, (2004) Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 1694: 235-257.
16. Jacob-Dubuisson F, Locht C (2007) The Bordetella adhesins. In Bordetella molecular microbiology (C Locht, ed.), pp. 69-95, Horizon Bioscience, Norfolk.
17. Makhov AM, Hannah JH, Brennan MJ, Trus BL, Kocsis E, et al. (1994) Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in β strands and turns. J Mol Biol 241: 110-124.
18. Kajava AV, Cheng N, Cleaver R, Kessel M, Simon MN, et al. (2001) β-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292.
19. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5: 725-738.
20. Clantin B, Delattre AS, Rucktooa P, Saint N, Meli AC, et al. (2007) Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317: 957-961.
21. Hodak H, Clantin B, Willery E, Villeret V, Locht C, et al. (2006) Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 61: 368-382.
22. Rief M, Oesterhelt F, Heymann B, Gaub HE, (1997) Single Molecule Force Spectroscopy on Polysaccharides by Atomic Force Microscopy. Science 275: 1295-1297.
23. Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM, (1998) Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 396: 661-664.
24. Oesterhelt F, Oesterhelt D, Pfeiffer M, Engel A, Gaub HE, et al. (2000) Unfolding pathways of individual bacteriorhodopsins. Science 288: 143-146.
25. Guédin S, Willery E, Locht C, Jacob-Dubuisson F, (1998) Evidence that a globular conformation is not compatible with FhaC-mediated secretion of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 29: 763-774.
26. Lee W, Zeng X, Zhou HX, Bennett V, Yang W, et al. (2010) Full reconstruction of a vectorial protein folding pathway by atomic force microscopy and molecular dynamics simulations. J Biol Chem 285: 38167-38172.
27. Serra DO, Conover MS, Arnal L, Sloan GP, Rodriguez ME, et al. (2012) FHA-mediated cell-substrate and cell-cell adhesions are critical for Bordetella pertussis biofilm formation on abiotic surfaces and in the mouse nose and the trachea. PLoS One 6(12): e28811.
28. Hertadi R, Gruswitz F, Silver L, Koide A, Koide S, et al. (2003) Unfolding mechanics of multiple OspA substructures investigated with single molecule force spectroscopy J Mol Biol. 333: 993-1002.
29. Hannah JH, Menozzi FD, Renauld G, Locht C, Brennan MJ, (1994) Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect Immun 62: 5010-5019.
30. Liu DF, Phillips E, Wizemann TM, Siegel MM, Tabei K, et al. (1997) Characterization of a recombinant fragment that contains a carbohydrate recognition domain of the filamentous hemagglutinin. Infect Immun 65: 3465-3468.
31. Relman D, Tuomanen E, Falkow S, Golenbock DT, Saukkonen K, et al. (1990) Recognition of a bacterial adhesin by an integrin: macrophage CR3 (αMβ2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61: 1375-1382.
32. Andrade MA, Perez-Iratxeta C, Ponting CP, (2001) Protein repeats: structures, functions, and evolution. J Struct Biol 134: 117-131.
33. Fürste JP, Pansegrau W, Frank R, Blöcker H, Scholz P, et al. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48: 119-131.
34. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
35. Lambert-Buisine C, Willery E, Locht C, Jacob-Dubuisson F, (1998) N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 28: 1283-1293.
36. Locht C, Geoffroy MC, Renauld G, (1992) Common accessory genes for the Bordetella pertussis filamentous hemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. EMBO J 11: 3175-3183.
37. Baud C, Hodak H, Willery E, Drobecq H, Locht C, et al. (2009) Role of DegP for two-partner secretion in Bordetella. Mol Microbiol 74: 315-329.30.
38. Bustamante C, Marko JF, Siggia ED, Smith S, (1994) Entropic elasticity of lamda-phage DNA. Science 265: 1599-1600.
39. Buscemi L, Ramonet D, Klingberg F, Formey A, Smith-Clerc J, et al. (2011) The single-molecule mechanics of the latent TGF-beta1 complex. Curr Biol 21: 2046-2054.
40. Clementi C, Nymeyer H, Onuchic JN, (2000) Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J Mol Biol 298: 937-953.
41. Noel JK, Whitford PC, Sanbonmatsu KY, Onuchic JN, (2010) SMOG@ctbp: simplified deployment of structure-based models in GROMACS Nucl Acid Res 38: W657-W661.
42. Hess B, Lindhal E, (2008) GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theory Comput 4: 435-447.