1932

Abstract

The phage shock protein (Psp) system was identified as a response to phage infection in , but rather than being a specific response to a phage, it detects and mitigates various problems that could increase inner-membrane (IM) permeability. Interest in the Psp system has increased significantly in recent years due to appreciation that Psp-like proteins are found in all three domains of life and because the bacterial Psp response has been linked to virulence and other important phenotypes. In this article, we summarize our current understanding of what the Psp system detects and how it detects it, how four core Psp proteins form a signal transduction cascade between the IM and the cytoplasm, and current ideas that explain how the Psp response keeps bacterial cells alive. Although recent studies have significantly improved our understanding of this system, it is an understanding that is still far from complete.

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2016-09-08
2024-06-21
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Literature Cited

  1. Ades SE. 1.  2008. Regulation by destruction: design of the σE envelope stress response. Curr. Opin. Microbiol. 11:535–40 [Google Scholar]
  2. Aseeva E, Ossenbuhl F, Sippel C, Cho WK, Stein B. 2.  et al. 2007. Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol. Biochem. 45:119–28 [Google Scholar]
  3. Becker LA, Bang IS, Crouch ML, Fang FC. 3.  2005. Compensatory role of PspA, a member of the phage shock protein operon, in rpoE mutant Salmonella enterica serovar Typhimurium. Mol. Microbiol. 56:1004–16 [Google Scholar]
  4. Bekker M, Alexeeva S, Laan W, Sawers G, Teixeira de Mattos J, Hellingwerf K. 4.  2010. The ArcBA two-component system of Escherichia coli is regulated by the redox state of both the ubiquinone and the menaquinone pool. J. Bacteriol. 192:746–54 [Google Scholar]
  5. Bergler H, Abraham D, Aschauer H, Turnowsky F. 5.  1994. Inhibition of lipid biosynthesis induces the expression of the pspA gene. Microbiology 140:1937–44 [Google Scholar]
  6. Bidle KA, Kirkland PA, Nannen JL, Maupin-Furlow JA. 6.  2008. Proteomic analysis of Haloferax volcanii reveals salinity-mediated regulation of the stress response protein PspA. Microbiology 154:1436–43 [Google Scholar]
  7. Brissette JL, Russel M. 7.  1990. Secretion and membrane integration of a filamentous phage-encoded morphogenetic protein. J. Mol. Biol. 211:565–80 [Google Scholar]
  8. Brissette JL, Russel M, Weiner L, Model P. 8.  1990. Phage shock protein, a stress protein of Escherichia coli. PNAS 87:862–66 [Google Scholar]
  9. Brissette JL, Weiner L, Ripmaster TL, Model P. 9.  1991. Characterization and sequence of the Escherichia coli stress-induced psp operon. J. Mol. Biol. 220:35–48 [Google Scholar]
  10. Bury-Moné S, Nomane Y, Reymond N, Barbet R, Jacquet E. 10.  et al. 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLOS Genet. 5:e1000651 [Google Scholar]
  11. Carlson JH, Silhavy TJ. 11.  1993. Signal sequence processing is required for the assembly of LamB trimers in the outer membrane of Escherichia coli. J. Bacteriol. 175:3998–4007 [Google Scholar]
  12. Cornelis GR. 12.  2002. The Yersinia Ysc-Yop ‘type III’ weaponry. Nat. Rev. Mol. Cell Biol. 3:742–52 [Google Scholar]
  13. Dartigalongue C, Missiakas D, Raina S. 13.  2001. Characterization of the Escherichia coli σE regulon. J. Biol. Chem. 276:20866–75 [Google Scholar]
  14. Darwin AJ. 14.  2005. The phage-shock-protein response. Mol. Microbiol. 57:621–28 [Google Scholar]
  15. Darwin AJ. 15.  2013. Stress relief during host infection: The phage shock protein response supports bacterial virulence in various ways. PLOS Pathog. 9:e1003388 [Google Scholar]
  16. Darwin AJ, Miller VL. 16.  1999. Identification of Yersinia enterocolitica genes affecting survival in an animal host using signature-tagged transposon mutagenesis. Mol. Microbiol. 32:51–62 [Google Scholar]
  17. Darwin AJ, Miller VL. 17.  2001. The psp locus of Yersinia enterocolitica is required for virulence and for growth in vitro when the Ysc type III secretion system is produced. Mol. Microbiol. 39:429–44 [Google Scholar]
  18. Datta P, Ravi J, Guerrini V, Chauhan R, Neiditch MB. 18.  et al. 2015. The Psp system of Mycobacterium tuberculosis integrates envelope stress-sensing and envelope-preserving functions. Mol. Microbiol. 97:408–22 [Google Scholar]
  19. DeLisa MP, Lee P, Palmer T, Georgiou G. 19.  2004. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J. Bacteriol. 186:366–73 [Google Scholar]
  20. Dominguez-Escobar J, Wolf D, Fritz G, Hofler C, Wedlich-Soldner R, Mascher T. 20.  2014. Subcellular localization, interactions and dynamics of the phage-shock protein-like Lia response in Bacillus subtilis. Mol. Microbiol. 92:716–32 [Google Scholar]
  21. Dworkin J, Jovanovic G, Model P. 21.  2000. The PspA protein of Escherichia coli is a negative regulator of σ54-dependent transcription. J. Bacteriol. 182:311–19 [Google Scholar]
  22. Elderkin S, Bordes P, Jones S, Rappas M, Buck M. 22.  2005. Molecular determinants for PspA-mediated repression of the AAA transcriptional activator PspF. J. Bacteriol. 187:3238–48 [Google Scholar]
  23. Elderkin S, Jones S, Schumacher J, Studholme D, Buck M. 23.  2002. Mechanism of action of the Escherichia coli phage shock protein PspA in repression of the AAA family transcription factor PspF. J. Mol. Biol. 320:23–37 [Google Scholar]
  24. Engl C, Beek AT, Bekker M, de Mattos JT, Jovanovic G, Buck M. 24.  2011. Dissipation of proton motive force is not sufficient to induce the phage shock protein response in Escherichia coli. Curr. Microbiol. 62:1374–85 [Google Scholar]
  25. Engl C, Jovanovic G, Lloyd LJ, Murray H, Spitaler M. 25.  et al. 2009. In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli. Mol. Microbiol. 73:382–96 [Google Scholar]
  26. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. 26.  2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103–18 [Google Scholar]
  27. Ferrieres L, Clarke DJ. 27.  2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol. Microbiol. 50:1665–82 [Google Scholar]
  28. Flores-Kim J, Darwin AJ. 28.  2012. Phage shock protein C (PspC) of Yersinia enterocolitica is a polytopic membrane protein with implications for regulation of the Psp stress response. J. Bacteriol. 194:6548–59 [Google Scholar]
  29. Flores-Kim J, Darwin AJ. 29.  2015. Activity of a bacterial cell envelope stress response is controlled by the interaction of a protein binding domain with different partners. J. Biol. Chem. 290:11417–30 [Google Scholar]
  30. Gage DJ, Neidhardt FC. 30.  1993. Adaptation of Escherichia coli to the uncoupler of oxidative phosphorylation 2,4-dinitrophenol. J. Bacteriol. 175:7105–8 [Google Scholar]
  31. Georgellis D, Kwon O, Lin EC. 31.  2001. Quinones as the redox signal for the Arc two-component system of bacteria. Science 292:2314–16 [Google Scholar]
  32. Green RC, Darwin AJ. 32.  2004. PspG, a new member of the Yersinia enterocolitica phage shock protein regulon. J. Bacteriol. 186:4910–20 [Google Scholar]
  33. Gueguen E, Savitzky DC, Darwin AJ. 33.  2009. Analysis of the Yersinia enterocolitica PspBC proteins defines functional domains, essential amino acids and new roles within the phage-shock-protein response. Mol. Microbiol. 74:619–33 [Google Scholar]
  34. Guilvout I, Chami M, Engel A, Pugsley AP, Bayan N. 34.  2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25:5241–49 [Google Scholar]
  35. Hachmann AB, Angert ER, Helmann JD. 35.  2009. Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob. Agents Chemother. 53:1598–609 [Google Scholar]
  36. Hankamer BD, Elderkin SL, Buck M, Nield J. 36.  2004. Organization of the AAA+adaptor protein PspA is an oligomeric ring. J. Biol. Chem. 279:8862–66 [Google Scholar]
  37. Hardie KR, Lory S, Pugsley AP. 37.  1996. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15:978–88 [Google Scholar]
  38. Horstman NK, Darwin AJ. 38.  2012. Phage shock proteins B and C prevent lethal cytoplasmic membrane permeability in Yersinia enterocolitica. Mol. Microbiol. 85:445–60 [Google Scholar]
  39. Huvet M, Toni T, Sheng X, Thorne T, Jovanovic G. 39.  et al. 2011. The evolution of the phage shock protein response system: interplay between protein function, genomic organization, and system function. Mol. Biol. Evol. 28:1141–55 [Google Scholar]
  40. Joly N, Burrows PC, Engl C, Jovanovic G, Buck M. 40.  2009. A lower-order oligomer form of phage shock protein A (PspA) stably associates with the hexameric AAA+ transcription activator protein PspF for negative regulation. J. Mol. Biol. 394:764–75 [Google Scholar]
  41. Joly N, Engl C, Jovanovic G, Huvet M, Toni T. 41.  et al. 2010. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol. Rev. 34:797–827 [Google Scholar]
  42. Joly N, Schumacher J, Buck M. 42.  2006. Heterogeneous nucleotide occupancy stimulates functionality of phage shock protein F, an AAA+ transcriptional activator. J. Biol. Chem. 281:34997–5007 [Google Scholar]
  43. Jones SE, Lloyd LJ, Tan KK, Buck M. 43.  2003. Secretion defects that activate the phage shock response of Escherichia coli. J. Bacteriol. 185:6707–11 [Google Scholar]
  44. Jovanovic G, Engl C, Buck M. 44.  2009. Physical, functional and conditional interactions between ArcAB and phage shock proteins upon secretin-induced stress in Escherichia coli. Mol. Microbiol. 74:16–28 [Google Scholar]
  45. Jovanovic G, Engl C, Mayhew AJ, Burrows PC, Buck M. 45.  2010. Properties of the phage-shock-protein (Psp) regulatory complex that govern signal transduction and induction of the Psp response in Escherichia coli. Microbiology 156:2920–32 [Google Scholar]
  46. Jovanovic G, Lloyd LJ, Stumpf MP, Mayhew AJ, Buck M. 46.  2006. Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J. Biol. Chem. 281:21147–61 [Google Scholar]
  47. Jovanovic G, Mehta P, McDonald C, Davidson AC, Uzdavinys P. 47.  et al. 2014. The N-terminal amphipathic helices determine regulatory and effector functions of phage shock protein A (PspA) in Escherichia coli. J. Mol. Biol. 426:1498–511 [Google Scholar]
  48. Jovanovic G, Mehta P, Ying L, Buck M. 48.  2014. Anionic lipids and the cytoskeletal proteins MreB and RodZ define the spatio-temporal distribution and function of membrane stress controller PspA in Escherichia coli. Microbiol. 160:2374–86 [Google Scholar]
  49. Jovanovic G, Weiner L, Model P. 49.  1996. Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J. Bacteriol. 178:1936–45 [Google Scholar]
  50. Karlinsey JE, Maguire ME, Becker LA, Crouch ML, Fang FC. 50.  2010. The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium. Mol. Microbiol. 78:669–85 [Google Scholar]
  51. Kazmierczak BI, Mielke DL, Russel M, Model P. 51.  1994. pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer. J. Mol. Biol. 238:187–98 [Google Scholar]
  52. Kinoshita N, Unemoto T, Kobayashi H. 52.  1984. Proton motive force is not obligatory for growth of Escherichia coli. J. Bacteriol. 160:1074–77 [Google Scholar]
  53. Kleerebezem M, Crielaard W, Tommassen J. 53.  1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 15:162–71 [Google Scholar]
  54. Kleerebezem M, Tommassen J. 54.  1993. Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol. Microbiol. 7:947–56 [Google Scholar]
  55. Kobayashi H, Yamamoto M, Aono R. 55.  1998. Appearance of a stress-response protein, phage-shock protein A, in Escherichia coli exposed to hydrophobic organic solvents. Microbiology 144:353–59 [Google Scholar]
  56. Kobayashi R, Suzuki T, Yoshida M. 56.  2007. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66:100–9 [Google Scholar]
  57. Koo J, Burrows LL, Howell PL. 57.  2012. Decoding the roles of pilotins and accessory proteins in secretin escort services. FEMS Microbiol. Lett. 328:1–12 [Google Scholar]
  58. Korotkov KV, Gonen T, Hol WG. 58.  2011. Secretins: dynamic channels for protein transport across membranes. Trends Biochem. Sci. 36:433–43 [Google Scholar]
  59. Liu X, De Wulf P. 59.  2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588–97 [Google Scholar]
  60. Lloyd LJ, Jones SE, Jovanovic G, Gyaneshwar P, Rolfe MD. 60.  et al. 2004. Identification of a new member of the phage shock protein response in Escherichia coli, the phage shock protein G (PspG). J. Biol. Chem. 279:55707–14 [Google Scholar]
  61. Lucchini S, Liu H, Jin Q, Hinton JC, Yu J. 61.  2005. Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect. Immun. 73:88–102 [Google Scholar]
  62. Majdalani N, Gottesman S. 62.  2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379–405 [Google Scholar]
  63. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D. 63.  2004. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. PNAS 101:13318–23 [Google Scholar]
  64. Mascher T, Zimmer SL, Smith TA, Helmann JD. 64.  2004. Antibiotic-inducible promoter regulated by the cell envelope stress-sensing two-component system LiaRS of Bacillus subtilis. Antimicrob. Agents Chemother. 48:2888–96 [Google Scholar]
  65. Maxson ME, Darwin AJ. 65.  2004. Identification of inducers of the Yersinia enterocolitica phage shock protein system and comparison to the regulation of the RpoE and Cpx extracytoplasmic stress responses. J. Bacteriol. 186:4199–208 [Google Scholar]
  66. Maxson ME, Darwin AJ. 66.  2006. PspB and PspC of Yersinia enterocolitica are dual function proteins: regulators and effectors of the phage-shock-protein response. Mol. Microbiol. 59:1610–23 [Google Scholar]
  67. McDonald C, Jovanovic G, Ces O, Buck M. 67.  2015. Membrane stored curvature elastic stress modulates recruitment of maintenance proteins PspA and Vipp1. mBio 6:e01188–15 [Google Scholar]
  68. Mehner D, Osadnik H, Lunsdorf H, Bruser T. 68.  2012. The Tat system for membrane translocation of folded proteins recruits the membrane-stabilizing Psp machinery in Escherichia coli. J. Biol. Chem. 287:27834–42 [Google Scholar]
  69. Mehta P, Jovanovic G, Lenn T, Bruckbauer A, Engl C. 69.  et al. 2013. Dynamics and stoichiometry of a regulated enhancer-binding protein in live Escherichia coli cells. Nat. Commun. 4:1997 [Google Scholar]
  70. Model P, Jovanovic G, Dworkin J. 70.  1997. The Escherichia coli phage-shock-protein (psp) operon. Mol. Microbiol. 24:255–61 [Google Scholar]
  71. Nielsen C, Goulian M, Andersen OS. 71.  1998. Energetics of inclusion-induced bilayer deformations. Biophys. J. 74:1966–83 [Google Scholar]
  72. Ohyama T, Mugikura S, Nishikawa M, Igarashi K, Kobayashi H. 72.  1992. Osmotic adaptation of Escherichia coli with a negligible proton motive force in the presence of carbonyl cyanide m-chlorophenylhydrazone. J. Bacteriol. 174:2922–28 [Google Scholar]
  73. Osadnik H, Schöpfel M, Heidrich E, Mehner D, Lilie H. 73.  et al. 2015. The PspF-binding domain PspA1-144 and the PspA·F complex: new insights into the coiled-coil-dependent regulation of AAA+ proteins. Mol. Microbiol. 98:743–59 [Google Scholar]
  74. Oshima T, Aiba H, Masuda Y, Kanaya S, Sugiura M. 74.  et al. 2002. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol. Microbiol. 46:281–91 [Google Scholar]
  75. Polen T, Rittmann D, Wendisch VF, Sahm H. 75.  2003. DNA microarray analyses of the long-term adaptive response of Escherichia coli to acetate and propionate. Appl. Environ. Microbiol. 69:1759–74 [Google Scholar]
  76. Raivio TL. 76.  2014. Everything old is new again: an update on current research on the Cpx envelope stress response. Biochim. Biophys. Acta 1843:1529–41 [Google Scholar]
  77. Raivio TL, Leblanc SK, Price NL. 77.  2013. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J. Bacteriol. 195:2755–67 [Google Scholar]
  78. Raivio TL, Silhavy TJ. 78.  1999. The σE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr. Opin. Microbiol. 2:159–65 [Google Scholar]
  79. Rau R, Darwin AJ. 79.  2015. Identification of YsaP, the pilotin of the Yersinia enterocolitica Ysa type III secretion system. J. Bacteriol. 197:2770–79 [Google Scholar]
  80. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. 80.  2006. Conserved and variable functions of the σE stress response in related genomes. PLOS Biol. 4:e2 [Google Scholar]
  81. Robichon C, Bonhivers M, Pugsley AP. 81.  2003. An intramolecular disulphide bond reduces the efficacy of a lipoprotein plasma membrane sorting signal. Mol. Microbiol. 49:1145–54 [Google Scholar]
  82. Russel M. 82.  1994. Mutants at conserved positions in gene IV, a gene required for assembly and secretion of filamentous phages. Mol. Microbiol. 14:357–69 [Google Scholar]
  83. Russel M, Kazmierczak B. 83.  1993. Analysis of the structure and subcellular location of filamentous phage pIV. J. Bacteriol. 175:3998–4007 [Google Scholar]
  84. Seo J, Brencic A, Darwin AJ. 84.  2009. Analysis of secretin-induced stress in Pseudomonas aeruginosa suggests prevention rather than response and identifies a novel protein involved in secretin function. J. Bacteriol. 191:898–908 [Google Scholar]
  85. Seo J, Savitzky DC, Ford E, Darwin AJ. 85.  2007. Global analysis of tolerance to secretin-induced stress in Yersinia enterocolitica suggests that the phage-shock-protein system may be a remarkably self-contained stress response. Mol. Microbiol. 65:714–27 [Google Scholar]
  86. Silhavy TJ, Kahne D, Walker S. 86.  2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:a000414 [Google Scholar]
  87. Southern SJ, Male A, Milne T, Sarkar-Tyson M, Tavassoli A, Oyston PC. 87.  2015. Evaluating the role of phage-shock protein A in Burkholderia pseudomallei. Microbiology 161:2192–203 [Google Scholar]
  88. Spagnuolo J, Opalka N, Wen WX, Gagic D, Chabaud E. 88.  et al. 2010. Identification of the gate regions in the primary structure of the secretin pIV. Mol. Microbiol. 76:133–50 [Google Scholar]
  89. Standar K, Mehner D, Osadnik H, Berthelmann F, Hause G. 89.  et al. 2008. PspA can form large scaffolds in Escherichia coli. FEBS Lett. 582:3585–89 [Google Scholar]
  90. van der Laan M, Urbanus ML, Ten Hagen-Jongman CM, Nouwen N, Oudega B. 90.  et al. 2003. A conserved function of YidC in the biogenesis of respiratory chain complexes. PNAS 100:5801–6 [Google Scholar]
  91. Vogt SL, Raivio TL. 91.  2012. Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol. Lett. 326:2–11 [Google Scholar]
  92. Vothknecht UC, Otters S, Hennig R, Schneider D. 92.  2012. Vipp1: a very important protein in plastids?. J. Exp. Bot. 63:1699–712 [Google Scholar]
  93. Vrancken K, De Keersmaeker S, Geukens N, Lammertyn E, Anne J, Van Mellaert L. 93.  2007. pspA overexpression in Streptomyces lividans improves both Sec- and Tat-dependent protein secretion. Appl. Microbiol. Biotechnol. 73:1150–57 [Google Scholar]
  94. Vrancken K, Van Mellaert L, Anne J. 94.  2008. Characterization of the Streptomyces lividans PspA response. J. Bacteriol. 190:3475–81 [Google Scholar]
  95. Wallrodt I, Jelsbak L, Thomsen LE, Brix L, Lemire S. 95.  et al. 2014. Removal of the phage-shock protein PspB causes reduction of virulence in Salmonella enterica serovar Typhimurium independently of NRAMP1. J. Med. Microbiol. 63:788–95 [Google Scholar]
  96. Wang P, Kuhn A, Dalbey RE. 96.  2010. Global change of gene expression and cell physiology in YidC-depleted Escherichia coli. J. Bacteriol. 192:2193–209 [Google Scholar]
  97. Weiner L, Brissette JL, Model P. 97.  1991. Stress-induced expression of the Escherichia coli phage shock protein operon is dependent on σ54 and modulated by positive and negative feedback mechanisms. Genes Dev. 5:1912–23 [Google Scholar]
  98. Weiner L, Brissette JL, Ramani N, Model P. 98.  1995. Analysis of the proteins and cis-acting elements regulating the stress-induced phage shock protein operon. Nucleic Acids Res. 23:2030–36 [Google Scholar]
  99. Weiner L, Model P. 99.  1994. Role of an Escherichia coli stress-response operon in stationary-phase survival. PNAS 91:2191–95 [Google Scholar]
  100. Wenzel M, Kohl B, Munch D, Raatschen N, Albada HB. 100.  et al. 2012. Proteomic response of Bacillus subtilis to lantibiotics reflects differences in interaction with the cytoplasmic membrane. Antimicrob. Agents Chemother. 56:5749–57 [Google Scholar]
  101. Westphal S, Heins L, Soll J, Vothknecht UC. 101.  2001. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis?. PNAS 98:4243–48 [Google Scholar]
  102. White MJ, Savaryn JP, Bretl DJ, He H, Penoske RM. 102.  et al. 2011. The HtrA-like serine protease PepD interacts with and modulates the Mycobacterium tuberculosis 35-kDa antigen outer envelope protein. PLOS ONE 6:e18175 [Google Scholar]
  103. Wolf D, Kalamorz F, Wecke T, Juszczak A, Mäder U. 103.  et al. 2010. In-depth profiling of the LiaR response of Bacillus subtilis. J. Bacteriol. 192:4680–93 [Google Scholar]
  104. Yamaguchi S, Gueguen E, Horstman NK, Darwin AJ. 104.  2010. Membrane association of PspA depends on activation of the phage-shock-protein response in Yersinia enterocolitica. Mol. Microbiol. 78:429–43 [Google Scholar]
  105. Yamaguchi S, Reid DA, Rothenberg E, Darwin AJ. 105.  2013. Changes in Psp protein binding partners, localization and behaviour upon activation of the Yersinia enterocolitica phage shock protein response. Mol. Microbiol. 87:656–71 [Google Scholar]
  106. Zhang L, Sakamoto W. 106.  2015. Possible function of VIPP1 in maintaining chloroplast membranes. Biochim. Biophys. Acta 1847:831–37 [Google Scholar]
  107. Zhang N, Simpson T, Lawton E, Uzdavinys P, Joly N. 107.  et al. 2013. A key hydrophobic patch identified in an AAA+ protein essential for its in trans inhibitory regulation. J. Mol. Biol. 425:2656–69 [Google Scholar]
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