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

Journal of Bacteriology

Volumn 193, Issue 20, 2011, Pages 5747-5758

  Gueguen, Erwan ^a   Flores Kim, Josué ^a   Darwin, Andrew J ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE; DISULFIDE; FORMALDEHYDE; HETERODIMER; HOMODIMER; LEUCINE ZIPPER PROTEIN; PHAGE SHOCK PROTEIN B; PHAGE SHOCK PROTEIN C; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; COMPLEX FORMATION; CROSS LINKING; DIMERIZATION; HYDROPHOBICITY; IN VIVO STUDY; NONHUMAN; OPERON; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; TWO HYBRID SYSTEM; YERSINIA ENTEROCOLITICA;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DIMERIZATION; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; YERSINIA ENTEROCOLITICA;

BACTERIA (MICROORGANISMS); YERSINIA ENTEROCOLITICA;

EID: 80053599110     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05080-11     Document Type: Article

References (53)

1. Adams, H., W. Teertstra, J. Demmers, R. Boesten, and J. Tommassen. 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. Microbiol. 51:659-674.
3. Bidle, K. A., P. A. Kirkland, J. L. Nannen, and J. A. Maupin-Furlow. 2008. Proteomic analysis of Haloferax volcanii reveals salinity-mediated regulation of the stress response protein PspA. Microbiology 154:1436-1443.
4. Brissette, J. L., M. Russel, L. Weiner, and P. Model. 1990. Phage shock protein, a stress protein of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 87:862-866.
5. Combet, C., C. Blanchet, C. Geourjon, and G. Deléage. 2000. NPS@: network protein sequence analysis. Trends Biochem. Sci. 25:147-150.
6. Daniels, C., and R. Morona. 1999. Analysis of Shigella flexneri Wzz (Rol) function by mutagenesis and cross-linking: Wzz is able to oligomerize. Mol. Microbiol. 34:181-194.
7. Darwin, A. J. 2005. The phage-shock-protein response. Mol. Microbiol. 57:621-628.
8. Darwin, A. J., and V. L. Miller. 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.
9. q/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123:17-24.
10. Derouiche, R., H. Bénédetti, J. Lazzaroni, C. Lazdunski, and R. Lloube's. 1995. Protein complex within Escherichia coli inner membrane. J. Biol. Chem. 270:11078-11084.
11. Doublet, P., C. Grangeasse, B. Obadia, E. Vaganay, and A. J. Cozzone. 2002. Structural organization of the protein-tyrosine autokinase Wzc within Escherichia coli cells. J. Biol. Chem. 277:37339-37348.
12. Dworkin, J., G. Jovanovic, and P. Model. 2000. The PspA protein of Esch-erichia coli is a negative regulator of 54-dependent transcription. J. Bacteriol. 182:311-319.
13. Elderkin, S., S. Jones, J. Schumacher, D. Studholme, and M. Buck. 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.
14. Engl, C., et al. 2009. In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli. Mol. Microbiol. 73:382-396.
15. Eriksson, S., S. Lucchini, A. Thompson, M. Rhen, and J. C. Hinton. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
16. Genin, S., and C. A. Boucher. 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.
17. Goemaere, E. L., E. Cascales, and R. Lloubes. 2007. Mutational analyses define helix organization and key residues of a bacterial membrane energytransducing complex. J. Mol. Biol. 366:1424-1436.
18. Goemaere, E. L., A. Devert, R. Lloubes, and E. Cascales. 2007. Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex. J. Biol. Chem. 282:17749-17757.
19. Green, R. C., and A. J. Darwin. 2004. PspG, a new member of the Yersinia enterocolitica phage shock protein regulon. J. Bacteriol. 186:4910-4920.
20. Gueguen, E., D. C. Savitzky, and A. J. Darwin. 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.
21. Guilvout, I., M. Chami, A. Engel, A. P. Pugsley, and N. Bayan. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J. 25:5241-5249.
22. Guzman, L., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
23. Heckman, K. L., and L. R. Pease. 2007. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2:924-932.
24. Higgs, P. I., P. S. Myers, and K. Postle. 1998. Interactions in the TonBdependent energy transduction complex: ExbB and ExbD form homomultimers. J. Bacteriol. 180:6031-6038.
25. Ji, T. H., and C. R. Middaugh. 1980. Does random collisional cross-linking occur? Biochim. Biophys. Acta 603:371-374.
26. 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.
27. Jovanovic, G., C. Engl., and M. Buck. 2009. Physical, functional and conditional interactions between ArcAB and phage shock proteins upon secretininduced stress in Escherichia coli. Mol. Microbiol. 74:16-28.
28. Jovanovic, G., C. Engl, A. J. Mayhew, P. C. Burrows, and M. Buck. 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.
29. Jovanovic, G., L. Weiner, and P. Model. 1996. Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J. Bacteriol. 178:1936-1945.
30. Karimova, G., N. Dautin, and D. Ladant. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233-2243.
31. Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756.
32. Karimova, G., A. Ullmann, and D. Ladant. 2001. Protein-protein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J. Mol. Microbiol. Biotechnol. 3:73-82.
33. Karlinsey, J. E., M. E. Maguire, L. A. Becker, M. L. Crouch, and F. C. Fang. 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.
34. + mutant. Gene 136:271-275.
35. Kleerebezem, M., W. Crielaard, and J. Tommassen. 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.
36. Kunkel, G. R., M. Mehrabian, and H. G. Martinson. 1981. Contact-site cross-linking agents. Mol. Cell. Biochem. 34:3-13.
37. 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.
38. Lloyd, L. J., 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. 279:55707-55714.
39. Lucchini, S., H. Liu, Q. Jin, J. C. Hinton, and J. Yu. 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.
40. Maloy, S. R., V. J. Stewart, and R. K. Taylor. 1996. Genetic analysis of pathogenic bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Maxson, M. E., and A. J. Darwin. 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.
42. Maxson, M. E., and A. J. Darwin. 2005. Improved system for construction and analysis of single-copy -galactosidase operon fusions in Yersinia enterocolitica. Appl. Environ. Microbiol. 71:5614-5618.
43. Maxson, M. E., and A. J. Darwin. 2006. PspB and PspC of Yersinia enterocolitica are dual function proteins: regulators and effectors of the phageshock-protein response. Mol. Microbiol. 59:1610-1623.
44. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
45. Model, P., G. Jovanovic, and J. Dworkin. 1997. The Escherichia coli phageshock-protein (psp) operon. Mol. Microbiol. 24:255-261.
46. Seo, J., A. Brencic, and A. J. Darwin. 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.
47. Seo, J., D. C. Savitzky, E. Ford, and A. J. Darwin. 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. 65:714-727.
48. Uzzau, S., N. Bossi-Figueroa, S. Rubino, and L. Bossi. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl. Acad. Sci. U. S. A. 98: 15264-15269.
49. Vrancken, K., L. Van Mellaert, and J. Anne. 2008. Characterization of the Streptomyces lividans PspA response. J. Bacteriol. 190:3475-3481.
50. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copynumber vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
51. Weiner, L., J. L. Brissette, and P. Model. 1991. Stress-induced expression of the Escherichia coli phage shock protein operon is dependent on 54 and modulated by positive and negative feedback mechanisms. Genes Dev. 5:1912-1923.
52. Wolf, D., et al. 2010. In-depth profiling of the LiaR response of Bacillus subtilis. J. Bacteriol. 192:4680-4693.
53. Yamaguchi, S., E. Gueguen, N. K. Horstman, and A. J. Darwin. 2010. Membrane association of PspA depends on activation of the phage-shockprotein response in Yersinia enterocolitica. Mol. Microbiol. 78:429-443.