The transmembrane protein KpOmpA anchoring the outer membrane of Klebsiella pneumoniae unfolds and refolds in response to tensile load

Structure

Volumn 20, Issue 1, 2012, Pages 121-127

  Bosshart, Patrick D ^a   Iordanov, Iordan ^b   Garzon Coral, Carlos ^a   Demange, Pascal ^b   Engel, Andreas ^c   Milon, Alain ^b   Müller, Daniel J ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; OUTER MEMBRANE PROTEIN A; PEPTIDOGLYCAN; PROTEIN KPOMPA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; KLEBSIELLA PNEUMONIAE; LIPID MEMBRANE; MECHANICAL STRESS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN UNFOLDING; TENSILE STRENGTH;

BACTERIAL OUTER MEMBRANE PROTEINS; CELL ADHESION; HYDRODYNAMICS; MODELS, MOLECULAR; OSMOTIC PRESSURE; PEPTIDOGLYCAN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; STRESS, MECHANICAL;

BACTERIA (MICROORGANISMS); KLEBSIELLA PNEUMONIAE; NEGIBACTERIA;

EID: 84855769023     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.11.002     Document Type: Article

References (49)

1. D. Alsteens, V. Dupres, S.A. Klotz, N.K. Gaur, P.N. Lipke, and Y.F. Dufrêne Unfolding individual Als5p adhesion proteins on live cells ACS Nano 3 2009 1677 1682
2. P. Aprikian, G. Interlandi, B.A. Kidd, I. Le Trong, V. Tchesnokova, O. Yakovenko, M.J. Whitfield, E. Bullitt, R.E. Stenkamp, W.E. Thomas, and E.V. Sokurenko The bacterial fimbrial tip acts as a mechanical force sensor PLoS Biol. 9 2011 e1000617
3. L. Bordoli, F. Kiefer, K. Arnold, P. Benkert, J. Battey, and T. Schwede Protein structure homology modeling using SWISS-MODEL workspace Nat. Protoc. 4 2009 1 13
4. P.D. Bosshart, F. Casagrande, P.L. Frederix, M. Ratera, C.A. Bippes, D.J. Müller, M. Palacin, A. Engel, and D. Fotiadis High-throughput single-molecule force spectroscopy for membrane proteins Nanotechnology 19 2008 384014
5. J.U. Bowie Membrane proteins: a new method enters the fold Proc. Natl. Acad. Sci. USA 101 2004 3995 3996 (Pubitemid 38405871)
6. M. Damaghi, C. Bippes, S. Köster, O. Yildiz, S.A. Mari, W. Kühlbrandt, and D.J. Muller pH-dependent interactions guide the folding and gate the transmembrane pore of the beta-barrel membrane protein OmpG J. Mol. Biol. 397 2010 878 882
7. M. Damaghi, S. Köster, C.A. Bippes, O. Yildiz, and D.J. Müller One β hairpin follows the other: exploring refolding pathways and kinetics of the transmembrane β-barrel protein OmpG Angew. Chem. Int. Ed. Engl. 50 2011 7422 7424
8. D. Debnath, K.L. Nielsen, and D.E. Otzen In vitro association of fragments of a beta-sheet membrane protein Biophys. Chem. 148 2010 112 120
9. H. Dietz, and M. Rief Exploring the energy landscape of GFP by single-molecule mechanical experiments Proc. Natl. Acad. Sci. USA 101 2004 16192 16197 (Pubitemid 39552821)
10. R. Endermann, C. Krämer, and U. Henning Major outer membrane proteins of Escherichia coli K-12: evidence for protein II being a transmembrane protein FEBS Lett. 86 1978 21 24 (Pubitemid 8264427)
11. R. Endermann, and U. Henning Nearest neighbors of major proteins in the outer membrane of Escherichia coli K12 FEBS Lett. 97 1979 339 342 (Pubitemid 9112869)
12. A. Engel, and H.E. Gaub Structure and mechanics of membrane proteins Annu. Rev. Biochem. 77 2008 127 148
13. D.M. Engelman, Y. Chen, C.N. Chin, A.R. Curran, A.M. Dixon, A.D. Dupuy, A.S. Lee, U. Lehnert, E.E. Matthews, and Y.K. Reshetnyak Membrane protein folding: beyond the two stage model FEBS Lett. 555 2003 122 125 (Pubitemid 37431108)
14. E.A. Evans, and D.A. Calderwood Forces and bond dynamics in cell adhesion Science 316 2007 1148 1153 (Pubitemid 46877469)
15. J.D. Faraldo-Gómez, and M.S. Sansom Acquisition of siderophores in gram-negative bacteria Nat. Rev. Mol. Cell Biol. 4 2003 105 116 (Pubitemid 36172694)
16. J. Helenius, C.P. Heisenberg, H.E. Gaub, and D.J. Muller Single-cell force spectroscopy J. Cell Sci. 121 2008 1785 1791 (Pubitemid 351943371)
17. Y. Hizukuri, J.F. Morton, T. Yakushi, S. Kojima, and M. Homma The peptidoglycan-binding (PGB) domain of the Escherichia coli pal protein can also function as the PGB domain in E. coli flagellar motor protein MotB J. Biochem. 146 2009 219 229
18. H. Hong, G. Szabo, and L.K. Tamm Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening Nat. Chem. Biol. 2 2006 627 635 (Pubitemid 44610347)
19. G.H. Huysmans, S.A. Baldwin, D.J. Brockwell, and S.E. Radford The transition state for folding of an outer membrane protein Proc. Natl. Acad. Sci. USA 107 2010 4099 4104
20. P. Jeannin, T. Renno, L. Goetsch, I. Miconnet, J.P. Aubry, Y. Delneste, N. Herbault, T. Baussant, G. Magistrelli, and C. Soulas OmpA targets dendritic cells, induces their maturation and delivers antigen into the MHC class I presentation pathway Nat. Immunol. 1 2000 502 509
21. A. Kedrov, C. Ziegler, H. Janovjak, W. Kühlbrandt, and D.J. Müller Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy J. Mol. Biol. 340 2004 1143 1152 (Pubitemid 38968707)
22. A. Kedrov, H. Janovjak, C. Ziegler, W. Kuhlbrandt, and D.J. Muller Observing folding pathways and kinetics of a single sodium-proton antiporter from Escherichia coli J. Mol. Biol. 355 2006 2 8 (Pubitemid 41774134)
23. A. Kedrov, H. Janovjak, K.T. Sapra, and D.J. Müller Deciphering molecular interactions of native membrane proteins by single-molecule force spectroscopy Annu. Rev. Biophys. Biomol. Struct. 36 2007 233 260 (Pubitemid 46998118)
24. M. Kessler, K.E. Gottschalk, H. Janovjak, D.J. Muller, and H.E. Gaub Bacteriorhodopsin folds into the membrane against an external force J. Mol. Biol. 357 2006 644 654 (Pubitemid 43290762)
25. J.H. Kleinschmidt Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers Chem. Phys. Lipids 141 2006 30 47 (Pubitemid 43744430)
26. R. Koebnik Proposal for a peptidoglycan-associating α-helical motif in the C-terminal regions of some bacterial cell-surface proteins Mol. Microbiol. 16 1995 1269 1270
27. R. Koebnik In vivo membrane assembly of split variants of the E.coli outer membrane protein OmpA EMBO J. 15 1996 3529 3537 (Pubitemid 26239765)
28. R. Koebnik, K.P. Locher, and P. Van Gelder Structure and function of bacterial outer membrane proteins: barrels in a nutshell Mol. Microbiol. 37 2000 239 253 (Pubitemid 30481009)
29. D.J. Müller, and A. Engel Atomic force microscopy and spectroscopy of native membrane proteins Nat. Protoc. 2 2007 2191 2197 (Pubitemid 351565857)
30. D.J. Müller, M. Kessler, F. Oesterhelt, C. Möller, D. Oesterhelt, and H. Gaub Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy Biophys. J. 83 2002 3578 3588 (Pubitemid 36041975)
31. D.J. Müller, J. Helenius, D. Alsteens, and Y.F. Dufrêne Force probing surfaces of living cells to molecular resolution Nat. Chem. Biol. 5 2009 383 390
32. F. Oesterhelt, D. Oesterhelt, M. Pfeiffer, A. Engel, H.E. Gaub, and D.J. Müller Unfolding pathways of individual bacteriorhodopsins Science 288 2000 143 146 (Pubitemid 30203048)
33. L. Pauling, R.B. Corey, and H.R. Branson The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain Proc. Natl. Acad. Sci. USA 37 1951 205 211
34. A. Pautsch, and G.E. Schulz Structure of the outer membrane protein A transmembrane domain Nat. Struct. Biol. 5 1998 1013 1017 (Pubitemid 28506635)
35. A. Pautsch, and G.E. Schulz High-resolution structure of the OmpA membrane domain J. Mol. Biol. 298 2000 273 282
36. M. Pichavant, Y. Delneste, P. Jeannin, C. Fourneau, A. Brichet, A.B. Tonnel, and P. Gosset Outer membrane protein A from Klebsiella rpneumoniae activates bronchial epithelial cells: implication in neutrophil recruitment J. Immunol. 171 2003 6697 6705 (Pubitemid 37532102)
37. A. Razatos, Y.L. Ong, M.M. Sharma, and G. Georgiou Molecular determinants of bacterial adhesion monitored by atomic force microscopy Proc. Natl. Acad. Sci. USA 95 1998 11059 11064 (Pubitemid 28450081)
38. M. Renault, O. Saurel, J. Czaplicki, P. Demange, V. Gervais, F. Löhr, V. Réat, M. Piotto, and A. Milon Solution state NMR structure and dynamics of KpOmpA, a 210 residue transmembrane domain possessing a high potential for immunological applications J. Mol. Biol. 385 2009 117 130
39. K.T. Sapra, M. Damaghi, S. Köster, O. Yildiz, W. Kühlbrandt, and D.J. Muller One beta hairpin after the other: exploring mechanical unfolding pathways of the transmembrane beta-barrel protein OmpG Angew. Chem. Int. Ed. Engl. 48 2009 8306 8308
40. M.P. Sheetz Cell control by membrane-cytoskeleton adhesion Nat. Rev. Mol. Cell Biol. 2 2001 392 396 (Pubitemid 33674052)
41. S. Shin, G. Lu, M. Cai, and K.S. Kim Escherichia coli outer membrane protein A adheres to human brain microvascular endothelial cells Biochem. Biophys. Res. Commun. 330 2005 1199 1204
42. S.G. Smith, V. Mahon, M.A. Lambert, and R.P. Fagan A molecular Swiss army knife: OmpA structure, function and expression FEMS Microbiol. Lett. 273 2007 1 11 (Pubitemid 47024891)
43. I. Sonntag, H. Schwarz, Y. Hirota, and U. Henning Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins J. Bacteriol. 136 1978 280 285 (Pubitemid 9037978)
44. C. Soulas, T. Baussant, J.P. Aubry, Y. Delneste, N. Barillat, G. Caron, T. Renno, J.Y. Bonnefoy, and P. Jeannin Outer membrane protein A (OmpA) binds to and activates human macrophages J. Immunol. 165 2000 2335 2340 (Pubitemid 30660674)
45. L.K. Tamm, H. Hong, and B. Liang Folding and assembly of beta-barrel membrane proteins Biochim. Biophys. Acta 1666 2004 250 263 (Pubitemid 39425208)
46. C. Verbelen, V. Dupres, D. Raze, C. Bompard, C. Locht, and Y.F. Dufrêne Interaction of the mycobacterial heparin-binding hemagglutinin with actin, as evidenced by single-molecule force spectroscopy J. Bacteriol. 190 2008 7614 7620
47. Y. Wang The function of OmpA in Escherichia coli Biochem. Biophys. Res. Commun. 292 2002 396 401 (Pubitemid 34694277)
48. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365 (Pubitemid 29319262)
49. O. Yakovenko, S. Sharma, M. Forero, V. Tchesnokova, P. Aprikian, B. Kidd, A. Mach, V. Vogel, E. Sokurenko, and W.E. Thomas FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation J. Biol. Chem. 283 2008 11596 11605