Initiation of phage infection by partial unfolding and prolyl isomerization

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12979-12991

  Hoffmann Thoms, Stephanie ^a,c   Weininger, Ulrich ^b,d   Eckert, Barbara ^a,e   Jakob, Roman P ^a,f   Koch, Johanna R ^a   Balbach, Jochen ^b   Schmid, Franz X ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c Scil Proteins GmbH   (Germany)

^d LUND UNIVERSITY   (Sweden)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDE HYDROGENS; FILAMENTOUS PHAGE; INFECTIVITY ASSAY; LOCAL STABILITY; MOLECULAR PICTURES; PARTIAL UNFOLDING; PHAGE INFECTION;

ESCHERICHIA COLI; GENES; ISOMERIZATION; ISOMERS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN FOLDING;

PROTEINS;

PROLINE; PROLINE 213; PROLINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; BINDING SITE; ESCHERICHIA COLI; ISOMERIZATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN UNFOLDING;

GENE-3-PROTEIN; MOLECULAR TIMER; NUCLEAR MAGNETIC RESONANCE; PHAGE INFECTION; PROLYL ISOMERIZATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

BACTERIOPHAGE M13; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PILI, SEX; PROLINE; PROTEIN UNFOLDING; VIRAL PROTEINS;

ENTEROBACTERIA PHAGE FD; ESCHERICHIA COLI; GOSSWEILERODENDRON BALSAMIFERUM;

EID: 84877122773     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.442525     Document Type: Article

References (31)

1. Click, E. M., and Webster, R. E. (1997) Filamentous phage infection: required interactions with the TolA protein. J. Bacteriol. 179, 6464-6471 (Pubitemid 27443931)
2. Riechmann, L., and Holliger, P. (1997) The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 90, 351-360 (Pubitemid 27329719)
3. Lubkowski, J., Hennecke, F., Plückthun, A., and Wlodawer, A. (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7, 711-722 (Pubitemid 29277424)
4. Rakonjac, J., Bennett, N. J., Spagnuolo, J., Gagic, D., and Russel, M. (2011) Filamentous bacteriophage: biology, phage display, and nanotechnology applications. Curr. Issues Mol. Biol. 13, 51-76
5. Holliger, P., Riechmann, L., and Williams, R. L. (1999) Crystal structure of the two N-terminal domains of g3p from filamentous phage fd at 1.9 Ä: evidence for conformational lability. J. Mol. Biol. 288, 649-657 (Pubitemid 29240523)
6. Lubkowski, J., Hennecke, F., Plückthun, A., and Wlodawer, A. (1998) The structural basis of phage display elucidated by the crystal structure of the N-terminal domains of G3P. Nat. Struct. Biol. 5, 140-147 (Pubitemid 28086915)
7. Eckert, B., Martin, A., Balbach, J., and Schmid, F. X. (2005) Prolyl isomerization as a molecular timer in phage infection. Nat. Struct. Mol. Biol. 12, 619-623 (Pubitemid 40980813)
8. Eckert, B., and Schmid, F. X. (2007) A Conformational unfolding reaction activates phage fd for the infection of Escherichia coli. J. Mol. Biol. 373, 452-461 (Pubitemid 47445570)
9. Martin, A., and Schmid, F. X. (2003) The folding mechanism of a two-domain protein: folding kinetics and domain docking of the gene-3-protein of phage fd. J. Mol. Biol. 329, 599-610 (Pubitemid 36593214)
10. Martin, A., and Schmid, F. X. (2003) A proline switch controls folding and domain interactions in the gene-3-protein of the filamentous phage fd. J. Mol. Biol. 331, 1131-1140 (Pubitemid 36969970)
11. Martin, A., and Schmid, F. X. (2003) Evolutionary stabilization of the gene-3-protein of phage fd reveals the principles that govern the thermodynamic stability of two-domain proteins. J. Mol. Biol. 328, 863-875 (Pubitemid 36506892)
12. Weininger, U., Jakob, R. P., Eckert, B., Schweimer, K., Schmid, F. X., and Balbach, J. (2009) A remote prolyl isomerization controls domain assembly via a hydrogen bonding network. Proc. Natl. Acad. Sci. U.S.A. 106, 12335-12340
13. Jakob, R. P., and Schmid, F. X. (2008) Energetic coupling between native-state prolyl isomerization and conformational protein folding. J. Mol. Biol. 377, 1560-1575
14. Mayr, L. M., and Schmid, F. X. (1993) Stabilization of a protein by guanidinium chloride. Biochemistry 32, 7994-7998 (Pubitemid 23259656)
15. Krebber, C., Spada, S., Desplancq, D., Krebber, A., Ge, L., and Plückthun, A. (1997) Selectively-infective phage (SIP): a mechanistic dissection of a novel in vivo selection for protein-ligand interactions. J. Mol. Biol. 268, 607-618 (Pubitemid 27208078)
16. Sieber, V., Plückthun, A., and Schmid, F. X. (1998) Selecting proteins with improved stability by a phage-based method. Nat. Biotechnol. 16, 955-960 (Pubitemid 28483625)
17. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
18. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352
19. Lorenz, S. H., Jakob, R. P., Weininger, U., Balbach, J., Dobbek, H., and Schmid, F. X. (2011) The filamentous phages fd and IF1 use different mechanisms to infect Escherichia coli. J. Mol. Biol. 405, 989-1003
20. Russel, M., Whirlow, H., Sun, T. P., and Webster, R. E. (1988) Low-frequency infection of F- bacteria by transducing particles of filamentous bacteriophages. J. Bacteriol. 170, 5312-5316 (Pubitemid 18259467)
21. Holliger, P., and Riechmann, L. (1997) A conserved infection pathway for filamentous bacteriophages is suggested by the structure of the membrane penetration domain of the minor coat protein g3p from phage fd. Structure 5, 265-275 (Pubitemid 27158732)
22. Pletneva, E. V., Sundd, M., Fulton, D. B., and Andreotti, A. H. (2006) Molecular details of Itk activation by prolyl isomerization and phospholigand binding: the NMR structure of the Itk SH2 domain bound to a phosphopeptide. J. Mol. Biol. 357, 550-561 (Pubitemid 43290754)
23. Schwartz, T. U., Schmidt, D., Brohawn, S. G., and Blobel, G. (2006) Homodimerization of the G protein SRβ in the nucleotide-free state involves proline cis/trans isomerization in the switch II region. Proc. Natl. Acad. Sci. U.S.A. 103, 6823-6828
24. Sarkar, P., Reichman, C., Saleh, T., Birge, R. B., and Kalodimos, C. G. (2007) Proline cis-trans isomerization controls autoinhibition of a signaling protein. Mol. Cell 25, 413-426 (Pubitemid 46199288)
25. Zhou, X. Z., Kops, O., Werner, A., Lu, P. J., Shen, M., Stoller, G., Küllertz, G., Stark, M., Fischer, G., and Lu, K. P. (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol. Cell 6, 873-883
26. Fischer, G., and Aumüller, T. (2003) Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. Rev. Physiol. Biochem. Pharmacol. 148, 105-150
27. Thiele, A., Krentzlin, K., Erdmann, F., Rauh, D., Hause, G., Zerweck, J., Kilka, S., Pösel, S., Fischer, G., Schutkowski, M., and Weiwad, M. (2011) Parvulin 17 promotes microtubule assembly by its peptidyl-prolyl cis/trans isomerase activity. J. Mol. Biol. 411, 896-909
28. Andreotti, A. H. (2003) Native state proline isomerization: An intrinsic molecular switch. Biochemistry 42, 9515-9524
29. Lu, K. P., Finn, G., Lee, T. H., and Nicholson, L. K. (2007) Prolyl cis-trans isomerization as a molecular timer. Nat. Chem. Biol. 3, 619-629 (Pubitemid 47417709)
30. Reimer, U., Scherer, G., Drewello, M., Kruber, S., Schutkowski, M., and Fischer, G. (1998) Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol. 279, 449-460 (Pubitemid 28263982)
31. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York