Strong cross-system interactions drive the activation of the QseB response regulator in the absence of its cognate sensor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 41, 2013, Pages 16592-16597

  Guckes, Kirsten R ^a   Kostakioti, Maria ^a,b   Breland, Erin J ^a   Gu, Alice P ^b   Shaffer, Carrie L ^a   Martineza, Charles R ^a   Hultgren, Scott J ^b,c   Hadjifrangiskou, Maria ^a,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Molecular Microbiology and Microbial Pathogenesis ^*  (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Phosphorylation; Regulatory networks; Signal transduction; UPEC

Indexed keywords

FERRIC ION; PMRB PROTEIN; POLYMYXIN; PROTEIN; QSEB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; MEMBRANE VESICLE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUORUM SENSING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION REGULATION; UPREGULATION; UROPATHOGENIC ESCHERICHIA COLI; WESTERN BLOTTING; WILD TYPE;

PHOSPHORYLATION; REGULATORY NETWORKS; SIGNAL TRANSDUCTION; UPEC;

BACTERIAL PROTEINS; DNA PRIMERS; DNA TRANSPOSABLE ELEMENTS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOBLOTTING; MUTAGENESIS; QUORUM SENSING; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION;

EID: 84885368239     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315320110     Document Type: Article

References (32)

1. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183-215.
2. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133-154.
3. Goulian M (2010) Two-component signaling circuit structure and properties. Curr Opin Microbiol 13(2):184-189.
4. Laub MT, Goulian M (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41:121-145.
5. Procaccini A, Lunt B, Szurmant H, Hwa T, Weigt M (2011) Dissecting the specificity of protein-protein interaction in bacterial two-component signaling: Orphans and crosstalks. PLoS ONE 6(5):e19729.
6. Bearson BL, Bearson SM (2008) The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb Pathog 44(4):271-278.
7. Bearson BL, Bearson SM, Lee IS, Brunelle BW (2010) The Salmonella enterica serovar TyphimuriumQseB response regulator negatively regulates bacterial motility and swine colonization in the absence of the QseC sensor kinase. Microb Pathog 48(6):214-219.
8. Hadjifrangiskou M, et al. (2011) A central metabolic circuit controlled by QseC in pathogenic Escherichia coli. Mol Microbiol 80(6):1516-1529.
9. Kostakioti M, Hadjifrangiskou M, Pinkner JS, Hultgren SJ (2009) QseC-mediated dephosphorylation of QseB is required for expression of genes associated with virulence in uropathogenic Escherichia coli. Mol Microbiol 73(6):1020-1031.
10. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131-147.
11. Kostakioti M, et al. (2012) Distinguishing the contribution of type 1 pili from that of other QseB-misregulated factors when QseC is absent during urinary tract infection. Infect Immun 80(8):2826-2834.
12. Justice SS, et al. (2004) Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci USA 101(5):1333-1338.
13. Tamayo R, Prouty AM, Gunn JS (2005) Identification and functional analysis of Salmonella enterica serovar Typhimurium PmrA-regulated genes. FEMS Immunol Med Microbiol 43(2):249-258.
14. Wösten MM, Groisman EA (1999) Molecular characterization of the PmrA regulon. J Biol Chem 274(38):27185-27190.
15. Kato A, Latifi T, Groisman EA (2003) Closing the loop: The PmrA/PmrB two-component system negatively controls expression of its posttranscriptional activator PmrD. Proc Natl Acad Sci USA 100(8):4706-4711.
16. Clarke MB, Sperandio V (2005) Transcriptional autoregulation by quorum sensing Escherichia coli regulators B and C (QseBC) in enterohaemorrhagic E. coli (EHEC). Mol Microbiol 58(2):441-455.
17. Tamayo R, Ryan SS, McCoy AJ, Gunn JS (2002) Identification and genetic characterization of PmrA-regulated genes and genes involved in polymyxin B resistance in Salmonella enterica serovar Typhimurium. Infect Immun 70(12):6770-6778.
18. Wösten MM, Kox LF, Chamnongpol S, Soncini FC, Groisman EA (2000) A signal transduction system that responds to extracellular iron. Cell 103(1):113-125.
19. Shin D, Lee EJ, Huang H, Groisman EA (2006) A positive feedback loop promotes transcription surge that jump-starts Salmonella virulence circuit. Science 314(5805): 1607-1609.
20. Yeo WS, et al. (2012) Intrinsic negative feedback governs activation surge in twocomponent regulatory systems. Mol Cell 45(3):409-421.
21. Russo FD, Silhavy TJ (1991) EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222(3):567-580.
22. Russo FD, Silhavy TJ (1993) The essential tension: Opposed reactions in bacterial twocomponent regulatory systems. Trends Microbiol 1(8):306-310.
23. Siryaporn A, Goulian M (2008) Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol Microbiol 70(2):494-506.
24. Amemura M, Makino K, Shinagawa H, Nakata A (1990) Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2. J Bacteriol 172(11):6300-6307.
25. Wanner BL (1992) Is cross regulation by phosphorylation of two-component response regulator proteins important in bacteria? J Bacteriol 174(7):2053-2058
26. Wanner BL, Wilmes MR, Young DC (1988) Control of bacterial alkaline phosphatase synthesis and variation in an Escherichia coli K-12 phoR mutant by adenyl cyclase, the cyclic AMP receptor protein, and the phoM operon. J Bacteriol 170(3):1092-1102.
27. Skerker JM, et al. (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133(6):1043-1054.
28. Hadjifrangiskou M, et al. (2012) Transposon mutagenesis identifies uropathogenic Escherichia coli biofilm factors. J Bacteriol 194(22):6195-6205.
29. Ducey TF, Carson MB, Orvis J, Stintzi AP, Dyer DW (2005) Identification of the ironresponsive genes of Neisseria gonorrhoeae by microarray analysis in defined medium. J Bacteriol 187(14):4865-4874.
30. Anriany Y, Sahu SN, Wessels KR, McCann LM, Joseph SW (2006) Alteration of the rugose phenotype in waaG and ddhC mutants of Salmonella enterica serovar Typhimurium DT104 is associated with inverse production of curli and cellulose. Appl Environ Microbiol 72(7):5002-5012.
31. Murphy KC, Campellone KG (2003) Lambda Red-mediated recombinogenic engineering of enterohemorrhagic and enteropathogenic E. coli. BMC Mol Biol 4:11.
32. Wright KJ, Seed PC, Hultgren SJ (2005) Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 73(11):7657-7668.