The N-terminal amphipathic helices determine regulatory and effector functions of phage shock protein A (PspA) in escherichia coli

Journal of Molecular Biology

Volumn 426, Issue 7, 2014, Pages 1498-1511

  Jovanovic, Goran ^a   Mehta, Parul ^a   McDonald, Christopher ^a   Davidson, Anthony C ^a   Uzdavinys, Povilas ^a   Ying, Liming ^b   Buck, Martin ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

high order oligomers; membrane stress; proline 25; PspA HD1

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; ESCHERICHIA COLI PROTEIN; PHAGE SHOCK PROTEIN A; PROLINE; PROTEIN VARIANT; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; RIBONUCLEASE E;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; CELLULAR STRESS SIGNAL; ESCHERICHIA COLI; GENE CONTROL; GENE ORDER; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ARCHAEON; BACTERIAL OUTER MEMBRANE; CELL MEMBRANE; CELL MOTILITY; ENTEROBACTERIACEAE; FLUORESCENCE; FRACTIONATION; GEL FILTRATION; IN VITRO STUDY; IN VIVO STUDY; INNER MEMBRANE; MEMBRANE; MEMBRANE VESICLE; MOLECULE; PATHOGENESIS; PROMOTER REGION; SIGNAL DETECTION; TRANSCRIPTION INITIATION; VASCULAR PLANT;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; ENTEROBACTERIACEAE; ESCHERICHIA COLI;

HIGH-ORDER OLIGOMERS; MEMBRANE STRESS; NEGATIVE REGULATION OF AAA(+); PROLINE 25; PSPA HD1;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; PROTEIN STRUCTURE, SECONDARY;

EID: 84895929192     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.12.016     Document Type: Article

References (42)

1. A.J. Darwin The phage-shock-protein response Mol Microbiol 57 2005 621 628
2. N. Joly, C. Engl, G. Jovanovic, M. Huvet, T. Toni, and X. Sheng et al. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology FEMS Microbiol Rev 34 2010 797 827
3. P. Model, G. Jovanovic, and J. Dworkin The Escherichia coli phage-shock-protein (psp) operon Mol Microbiol 24 1997 255 261
4. E. Aseeva, F. Ossenbühl, L.A. Eichacker, G. Wanner, J. Soll, and U.C. Vothnecht Complex formation of Vipp1 depends on it's α-helical PspA-like domain J Biol Chem 279 2004 35535 35541
5. L. Zhang, and W. Sakamoto Possible function of VIPP1 in thylakoids Plant Signal Behav 8 2013 e22860
6. U.C. Vothknecht, S. Otters, R. Hennig, and D. Schneider Vipp1: a very important protein in plastids?! J Exp Bot 63 2012 1699 1712
7. N.M. Vega, K.R. Allison, A.N. Samuels, M.S. Klempner, and J.J. Collins Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance Proc Natl Acad Sci USA 110 2013 14420 14425
8. A.J. Darwin Stress relief during host infection: the phage shock protein response supports bacterial virulence in various ways PLoS Pathog 9 2013 e1003388
9. + protein essential for in trans inhibitory regulation J Mol Biol 425 2013 2656 2669
10. G. Jovanovic, C. Engl, A.J. Mayhew, P.C. Burrows, and M. Buck Properties of the phage-shock-protein (Psp) regulatory complex that govern signal transduction and induction of the Psp response in Escherichia coli Microbiol SGM 156 2010 2920 2932
11. S. Yamaguchi, E. Gueguen, N.K. Horstman, and A.J. Darwin Membrane association of PspA depends on activation of the phage-shock-protein response in Yersinia enterocolitica Mol Microbiol 78 2010 429 443
12. L.J. Lloyd, S.E. Jones, G. Jovanovic, P. Gyaneshwar, M.D. Rolfe, and A. Thompson et al. Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG) J Biol Chem 279 2004 55707 55714
13. S. Elderkin, P. Bordes, S. Jones, M. Rappas, and M. Buck Molecular determinants for PspA-mediated repression of the AAA transcriptional activator PspF J Bacteriol 187 2005 3238 3248
14. + transcription activator protein PspF for negative regulation J Mol Biol 34 2009 764 775
15. R. Kobayashi, T. Suzuki, and M. Yoshida Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes Mol Microbiol 66 2007 100 109
16. P. Mehta, G. Jovanovic, T. Lenn, A. Bruckbauer, C. Engl, and L. Ying et al. Localisations, dynamics and stoichiometry of a regulated enhancer-binding protein in live Escherichia coli cells Nat Commun 4 2013 1997
17. S. Yamaguchi, A.R. Dylan, E. Rothenberg, and A.J. Darwin Changes in Psp protein binding partners, localization and behavior upon activation of the Yersinia enterocolitica phage shock protein response Mol Microbiol 87 2013 656 671
18. C. Engl, G. Jovanovic, L.J. Lloyd, H. Murray, L. Ying, and J. Errington et al. In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli Mol Microbiol 73 2009 382 396
19. T. Lenn, C.N. Gkekas, L. Bernard, C. Engl, G. Jovanovic, and M. Buck et al. Measuring the stoichiometry of functional PspA complexes in living bacterial cells by single molecule photobleaching Chem Commun 47 2011 400 402
20. G. Jovanovic, L.J. Lloyd, M.P.H. Stumpf, A.J. Mayhew, and M. Buck Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli J Biol Chem 281 2006 21147 21161
21. A. Taghbalout, and L. Rothfield RNaseE and the other constituents of the RNA degradosome are components of the bacterial cytoskeleton Proc Natl Acad Sci USA 104 2007 1667 1672
22. R.B. Cornell, and S.G. Taneva Amphipathic helices as mediators of the membrane interaction of amphitropic proteins, and as modulators of bilayer physical properties Curr Protein Pept Sci 7 2006 539 552
23. H. Strahl, and L.W. Hamoen Membrane potential is important for bacterial cell division Proc Natl Acad Sci USA 107 2010 12281 12286
24. S. Westphal, L. Heins, J. Soll, and U.C. Vothknecht Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc Natl Acad Sci USA 98 2001 4238 4242
25. M.P. DeLisa, P. Lee, T. Palmer, and G. Georgiou Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway J Bacteriol 186 2004 366 373
26. E. Aseeva, F. Ossenbühl, C. Sippel, W.K. Cho, and B. Stein et al. Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes Plant Physiol Biochem 45 2007 119 128
27. G. Dhamdhere, and H.I. Zgurskaya Metabolic shutdown in Escherichia coli cells lacking the outer membrane channel TolC Mol Microbiol 77 2010 743 754
28. S. Elderkin, S. Jones, J. Schumacher, D. Studholme, and M. Buck Mechanism of action of the Escherichia coli phage shock protein PspA in repression of the AAA family transcription factor PspF J Mol Biol 320 2002 23 37
29. J. Flores-Kim, and A.J. Darwin Phage shock protein C (PspC) of Yersinia enterocolitica is a polytopic membrane protein with implications for regulation of the Psp stress response J Bacteriol 194 2012 6548 6559
30. F. Lu, and A. Taghbalout Membrane association via amino-terminal amphipathic helix is required for the cellular organization and function of RNase II J Biol Chem 288 2013 7241 7251
31. D. Wolf, F. Kalamorz, T. Wecke, A. Juszczak, U. Mäder, and G. Homuth et al. In-depth profiling of the LiaR response of Bacillus subtilis J Bacteriol 192 2010 4680 4963
32. L. Zhang, Y. Kato, S. Otters, U.C. Vothknecht, and W. Sakamoto Essential role of Vipp1 in chloroplast envelope maintenance in Arabidopsis Plant Cell 24 2012 3695 3707
33. S. Otters, P. Braun, J. Hubner, G. Wanner, U.C. Vothknecht, and F. Chigri The first α-helical domain of the vesicle-inducing protein in plastids 1 promotes oligomerization and lipid binding Planta 237 2013 529 540
34. P. Wang, A. Kuhn, and R.E. Dalbey Global change of gene expression and cell physiology in YidC-depleted Escherichia coli J Bacteriol 192 2010 2193 2209
35. C. Engl, A.T. Beek, M. Bekker, J.T. de Mattos, G. Jovanovic, and M. Buck Dissipation of proton motive force is not sufficient to induce the phage shock protein response in Escherichia coli Curr Microbiol 62 2011 1374 1385
36. T. Mascher, S.L. Zimmer, T.A. Smith, and J.D. Helmann Antibiotic inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis Antimicrob Agents Chemother 48 2004 2888 2896
37. J.H. Miller A short course in Bacterial Genetics: a laboratory manual and handbook for Escherichia coli and related bacteria 1992 Cold Spring Harbor Laboratory Press Cold Spring Harbor
38. G. Karimova, N. Dautin, and D. Ladant Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis J Bacteriol 187 2005 2233 2243
39. G. Karimova, J. Pidoux, A. Ullmann, and D. Ladant A bacterial two-hybrid system based on a reconstituted signal transduction pathway Proc Natl Acad Sci USA 95 1998 5752 5756
40. M. Russel, and B. Kaźmierczak Analysis of the structure and subcellular location of filamentous phage pIV J Bacteriol 175 1993 3998 4007
41. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J Biol Chem 193 1951 265 275
42. A. Roy, A. Kucukural, and Y. Zhang I-TASSER: a unified platform for automated protein structure and function prediction Nat Protoc 5 2010 725 738