Phage shock protein C (PspC) of Yersinia enterocolitica is a polytopic membrane protein with implications for regulation of the Psp stress response

Journal of Bacteriology

Volumn 194, Issue 23, 2012, Pages 6548-6559

  Flores Kim, josué ^a   Darwin, Andrew ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; PHAGE SHOCK PROTEIN C; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CHEMICAL LABELING; CONTROLLED STUDY; CYTOPLASM; IMMUNOBLOTTING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; STRESS; YERSINIA ENTEROCOLITICA;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PEPTIDE HYDROLASES; PROTEIN BINDING; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; YERSINIA ENTEROCOLITICA;

ESCHERICHIA COLI; YERSINIA ENTEROCOLITICA;

EID: 84871084335     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01250-12     Document Type: Article

References (59)

1. Adams H, Teertstra W, Demmers J, Boesten R, Tommassen J. 2003. Interactions between phage-shock proteins in Escherichia coli. J. Bacteriol. 185:1174-1180.
2. Beloin C, et al. 2004. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol. Micriobiol. 51:659-674.
3. Bernsel A, Viklund H, Hennerdal A, Elofsson A. 2009. TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res. 37:W465-W468. doi:10.1093/nar/gkp363.
4. Bidle KA, Kirkland PA, Nannen JL, Maupin-Furlow JA. 2008. Proteomic analysis of Haloferax volcanii reveals salinity-mediated regulation of the stress response protein PspA. Microbiology 154:1436-1443.
5. Danov M, Zhang W, Xie J, Dowhan W. 2005. Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAM): application to lipid-specific membrane protein topogenesis. Methods 36:148-171.
6. Brickman E, Beckwith J. 1975. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J. Mol. Biol. 96:307-316.
7. Brissette JL, Russel M, Weiner L, Model P. 1990. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 87:862-866.
8. Chiba S, Akiyama Y, Ito K. 2002. Membrane protein degradation by FtsH can be initiated from either end. J. Bacteriol. 184:4775-4782.
9. Chiba S, Akiyama Y, Mori H, Matsuo E, Ito K. 2000. Length recognition at the N-terminal tail for the initiation of FtsH-mediated proteolysis. EMBO Rep. 1:47-52.
10. Dale GE, Schonfeld HJ, Langen H, Stieger M. 1994. Increased solubility of trimethoprim-resistant type S1 DHFR from Staphylococcus aureus in Escherichia coli cells overproducing the chaperonins GroEL and GroES. Protein Eng. 7:925-931.
11. Danese PN, Silhavy TJ. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180:831-839.
12. Win AJ. 2005. The phage-shock-protein response. Mol. Micriobiol. 57:621-628.
13. Win AJ, Miller VL. 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. 39:429-444.
14. q/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24.
15. Derman AI, Beckwith J. 1995. Escherichia coli alkaline phosphatase localized to the cytoplasm slowly acquires enzymatic activity in cells whose growth has been suspended: a caution for gene fusion studies. J. Bacteriol. 177:3764-3770.
16. Drew D, et al. 2002. Rapid topology mapping of Escherichia coli innermembrane proteins by prediction and PhoA/GFP fusion analysis. Proc. Natl. Acad. Sci. U. S. A. 99:2690-2695.
17. 54-dependent transcription. J. Bacteriol. 182:311-319.
18. Elderkin S, Jones S, Schumacher J, Studholme D, Buck M. 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.
19. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
20. Feilmeier BJ, Iseminger G, Schroeder D, Webber H, Phillips GJ. 2000. Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J. Bacteriol. 182:4068-4076.
21. Fontaine F, Fuchs RT, Storz G. 2011. Membrane localization of small proteins in Escherichia coli. J. Biol. Chem. 286:32464-32474.
22. Genin S, Boucher CA. 1994. A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Mol. Gen. Genet. 243:112-118.
23. Green RC, Darwin AJ. 2004. PspG, a new member of the Yersinia enterocolitica phage shock protein regulon. J. Bacteriol. 186:4910-4920.
24. Gueguen E, Flores-Kim J, Darwin AJ. 2011. The Yersinia enterocolitica phage shock proteins B and C can form homodimers and heterodimers in vivo with the possibility of close association between multiple domains. J. Bacteriol. 193:5747-5758.
25. Gueguen E, Savitzky DC, Darwin AJ. 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. 74:619-633.
26. Guilvout I, Chami M, Engel A, Pugsley AP, Bayan N. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25:5241-5249.
27. Guyer MS, Reed RR, Steitz JA, Low KB. 1981. Identification of a sexfactor- affinity site in E. coli as gamma delta. Cold Spring Harb. Symp. Quant. Biol. 45:135-140.
28. Heckman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130. 29. Heckman KL, Pease LR. 2007. Gene splicing and mutagenesis by PCRdriven overlap extension. Nat. Protoc. 2:924-932.
29. Heckman KL, Pease LR. 2007. Gene splicing and mutagenesis by PCRdriven overlap extension. Nat. Protoc. 2:924-932.
30. Horstman NK, Darwin AJ. 2012. Phage shock proteins B and C prevent lethal cytoplasmic membrane permeability in Yersinia enterocolitica. Mol. Microbiol. 85:445-460.
31. Joly N, et al. 2010. Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol. Rev. 34:797-827.
32. Jones SE, Lloyd LJ, Tan KK, Buck M. 2003. Secretion defects that activate the phage shock response of Escherichia coli. J. Bacteriol. 185:6707-6711.
33. Jovanovic G, Engl C, Buck M. 2009. Physical, functional and conditional interactions between ArcAB and phage shock proteins upon secretininduced stress in Escherichia coli. Mol. Microbiol. 74:16-28.
34. Jovanovic G, Engl C, Mayhew AJ, Burrows PC, Buck M. 2010. Properties of the phage-shock-protein (Psp) regulatory complex that govern signal transduction and induction of the Psp response in Escherichia coli. Microbiology 156:2920-2932.
35. Jovanovic G, Weiner L, Model P. 1996. Identification, nucleotide se quence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J. Bacteriol. 178:1936-1945.
36. Karimova G, Ullmann A, Ladant D. 2000. A bacterial two-hybrid system that exploits a cAMP signaling cascade in Escherichia coli. Methods Enzymol. 328:59-73.
37. Karlinsey JE, Maguire ME, Becker LA, Crouch ML, Fang FC. 2010. The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium. Mol. Microbiol. 78:669-685.
38. Kinder SA, Badger JL, Bryant GO, Pepe JC, Miller VL. 1993. Cloning of the YenI restriction endonuclease and methyltransferase from Yersinia enterocolitica serotype O8 and construction of a transformable R-M+mutant. Gene 136:271-275.
39. Kleerebezem M, Crielaard W, Tommassen J. 1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 15:162-171.
40. Korotkov KV, Gonen T, Hol WG. 2011. Secretins: dynamic channels for protein transport across membranes. Trends Biochem. Sci. 36:433-443.
41. Liu C, et al. 2007. The chloroplast HSP70B-CDJ2-CGE1 chaperones catalyse assembly and disassembly of VIPP1 oligomers in Chlamydomonas. Plant J. 50:265-277.
42. Lucchini S, Liu H, Jin Q, Hinton JC, Yu J. 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.
43. Maloy SR, Stewart VJ, Taylor RK. 1996. Genetic analysis of pathogenic bacteria: a laboratory manual. Cold Spring Harbor Laboratory Press, Plainview, NY.
44. Manoil C, Mekalanos JJ, Beckwith J. 1990. Alkaline phosphatase fusions: sensors of subcellular location. J. Bacteriol. 172:515-518.
45. Maxson ME, Darwin AJ. 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. 186:4199-4208.
46. Maxson ME, Darwin AJ. 2006. PspB and PspC of Yersinia enterocolitica are dual function proteins: regulators and effectors of the phage-shockprotein response. Mol. Microbiol. 59:1610-1623.
47. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Scholz O, Thiel A, Hillen W, Niederweis M. 2000. Quantitative analysis of gene expression with an improved green fluorescent protein. Eur. J. Biochem. 267:1565-1570.
49. Senes A, Engel DE, DeGrado WF. 2004. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14:465-479.
50. Seo J, Savitzky DC, Ford E, Darwin AJ. 2007. Global analysis of tolerance to secretin-induced stress in Yersinia enterocolitica suggests that the phageshock- protein system may be a remarkably self-contained stress response. Mol. Microbiol. 65:714-727.
51. Singh S, Darwin AJ. 2011. FtsH-dependent degradation of phage shock protein C in Yersinia enterocolitica and Escherichia coli. J. Bacteriol. 193: 6436-6442.
52. Studier FW, Moffatt BA. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189: 113-130.
53. Vega NM, Allison KR, Khalil AS, Collins JJ. 2012. Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8:431-433.
54. Vrancken K, Van Mellaert L, Anne J. 2008. Characterization of the Streptomyces lividans PspA response. J. Bacteriol. 190:3475-3481.
55. Wang RF, Kushner SR. 1991. Construction of versatile low-copynumber vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
56. Wolf D, et al. 2010. In-depth profiling of the LiaR response of Bacillus subtilis. J. Bacteriol. 192:4680-4693.
57. Yamaguchi S, Darwin AJ. 2012. Recent findings about the Yersinia enterocolitica phage shock protein response. J. Microbiol. 50:1-7.
58. Yamaguchi S, Gueguen E, Horstman NK, Darwin AJ. 2010. Membrane association of PspA depends on activation of the phage-shock-protein response in Yersinia enterocolitica. Mol. Microbiol. 78:429-443.
59. Zhang P, Wang J, Shi Y. 2010. Structure and mechanism of the S component of a bacterial ECF transporter. Nature 468:717-720.