pH dependence of the stress regulator DksA

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Furman, Ran ^a,b   Danhart, Eric M ^a   NandyMazumdar, Monali ^a   Yuan, Chunhua ^a   Foster, Mark P ^a   Artsimovitch, Irina ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTIDINE; PROTEIN DKSA; RNA POLYMERASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; DKSA PROTEIN, E COLI; DNA DIRECTED RNA POLYMERASE; ESCHERICHIA COLI PROTEIN;

ACIDITY; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SURVIVAL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; IN VITRO STUDY; NONHUMAN; PH; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; TRANSCRIPTION INITIATION; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ESCHERICHIA COLI;

DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HISTIDINE; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STABILITY; STRESS, PHYSIOLOGICAL;

EID: 84925876489     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120746     Document Type: Article

References (52)

1. Paul BJ, Barker MM, Ross W, Schneider D.A., Webb C., Foster JW, et al. DksA: A critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGppand the initiating NTP. Cell. 2004; 118(3):311-22. PMID: 15294157
2. Paul BJ, Berkmen MB, Gourse RL. DksA potentiates direct activation of amino acid promoters by ppGpp. Proc Natl Acad Sci USA. 2005; 102(22):7823-8. PMID: 15899978
3. Tehranchi AK, Blankschien MD, Zhang Y, Halliday J.A., Srivatsan A., Peng J, et al. The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell. 2010; 141 (4):595-605. doi: 10.1016/j.cell.2010.03.036 PMID: 20478253
4. Aberg A, Fernandez-Vazquez J, Cabrer-Panes JD, Sanchez A, Balsalobre C. Similar and divergent effects of ppGpp and DksA deficiencies on transcription in Escherichia coli. J Bacteriol. 2009; 191 (10):3226-36. doi: 10.1128/JB.01410-08 PMID: 19251846
5. Lemke JJ, Durfee T, Gourse RL. DksA and ppGpp directly regulate transcription of the Escherichia coli flagellar cascade. Mol Microbiol. 2009; 74(6):1368-79. doi: 10.1111/j.1365-2958.2009.06939.x PMID: 19889089
6. Aberg A, Shingler V, Balsalobre C. Regulation of the fim B promoter: a case of differential regulation by ppGpp and DksA in vivo. Mol Microbiol. 2008; 67(6):1223-41. doi: 10.1111/j.1365-2958.2008. 06115.x PMID: 18284577
7. Jude F, Kohler T, Branny P., Perron K, Mayer MP, Comte R, et al. Posttranscriptional control of quorum-sensing-dependent virulence genes by DksA in Pseudomonas aeruginosa. J Bacteriol. 2003; 185 (12):3558-66. PMID: 12775693
8. Webb C, Moreno M, Wilmes-Riesenberg M, Curtiss R., Foster JW. Effects of DksA and CIpP protease on sigma S production and virulence in Salmonella typhimurium. Mol Microbiol. 1999; 34(1):112-23. PMID: 10540290
9. Henard CA, Tapscott T, Crawford M.A., Husain M., Doulias PT, Porwollik S, et al. The 4-cysteinezinc-finger motif of the RNA polymerase regulator DksA serves as a thiol switch for sensing oxidative and nitro-sative stress. Mol Microbiol. 2014; 91(4):790-804. doi: 10.1111/mmi.12498 PMID: 24354846
10. Gopalkrishnan S, Nicoloff H, Ades SE. Co-ordinated regulation of the extracytoplasmic stress factor, sigma E, with other Escherichia coli sigma factors by (p)ppGppand DksA may be achieved by specific regulation of individual holoenzymes. Mol Microbiol. 2014; 93(3):479-93. doi: 10.1111/mmi.12674 PMID: 24946009
11. Magnusson LU, Gummesson B, Joksimovic P., Farewell A, Nystrom T. Identical, independent, and opposing roles of ppGpp and DksA in Escherichia coli. J Bacteriol. 2007; 189(14):5193-202. PMID: 17496080
12. Potrykus K, Cashel M. (p)ppGpp: still magical? Ann Rev Microbiol. 2008; 62:35-51. doi: 10.1146/ annurev.micro.62.081307.162903 PMID: 18454629
13. Perederina A, Svetlov V, Vassylyeva M.N., Tahirov TH, Yokoyama S, Artsimovitch I, et al. Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell. 2004; 118(3):297-309. PMID: 15294156
14. Zuo Y, Wang Y, Steitz TA. The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex. Mol Cell. 2013; 50(3):430-6. doi: 10.1016/j.molcel.2013.03.020 PMID: 23623685
15. Jishage M, Kvint K, Shingler V., Nystrom T. Regulation of sigma factor competition by the alarmone ppGpp. Genes & development. 2002; 16(10):1260-70.
16. Bernardo LM, Johansson LU, Solera D, Skarfstad E., Shingler V. The guanosine tetraphosphate (ppGpp) alarmone, DksA and promoter affinity for RNA polymerase in regulation of sigma-dependent transcription. Mol Microbiol. 2006; 60(3):749-64. PMID: 16629675
17. Costanzo A, Nicoloff H, Barchinger S.E., Banta AB, Gourse RL, Ades SE. ppGppand DksA likely regulate the activity of the extracytoplasmic stress factor sigmaE in Escherichia coli by both direct and indirect mechanisms. Mol Microbiol. 2008; 67(3):619-32. PMID: 18086212
18. Lamour V, Hogan BP, Erie D.A., Darst SA. Crystal structure of Thermus aquaticus Gfh1 aGre-factor paralog that inhibits ratherthan stimulates transcript cleavage. J Mol Biol. 2006; 356(1):179-88. PMID: 16337964
19. Laptenko O, Lee J, Lomakin I., Borukhov S. Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase. EMBO J. 2003; 22(23):6322-34. PMID: 14633991
20. Vassylyeva MN, Svetlov V, Dearborn A.D., Klyuyev S., Artsimovitch I, Vassylyev DG. The carboxy-termi-nal coiled-coil of the RNA polymerase beta '-subunit is the main binding site for Gre factors. EMBO Rep. 2007; 8(11): 1038-43. PMID: 17917675
21. Laptenko O, Kim SS, Lee J, Starodubtseva M., Cava F, Berenguer J, et al. pH-dependentconformational switch activates the inhibitor of transcription elongation. EMBO J. 2006; 25(10):2131-41. PMID: 16628221
22. Lee JH, Lennon CW, Ross W, Gourse RL. Role of the coiled-coil tip of Escherichia coil DksA in promoter control. J Mol Biol. 2012; 416(4):503-17. doi: 10.1016/j.jmb.2011.12.028 PMID: 22200485
23. Roghanian M, Yuzenkova Y, Zenkin N. Controlled interplay between trigger loop and Gre factor in the RNA polymerase active centre. Nucleic Acids Res. 2011; 39(10):4352-9. doi: 10.1093/nar/gkq1359 PMID: 21266474
24. Lennon CW, Ross W, Martin-Tumasz S, Toulokhonov I., Vrentas CE, Rutherford ST, et al. Direct interactions between the coiled-coil tip of DksA and the trigger loop of RNA polymerase mediate transcriptional regulation. Genes Dev. 2012; 26:2634-46. doi: 10.1101/gad.204693.112 PMID: 23207918
25. Furman R, Tsodikov OV, Wolf Y.I., Artsimovitch I. An insertion in the catalytic trigger loop gates the secondary channel of RNA polymerase. Journal of Molecular Biology. 2013; 425(1):82-93. doi: 10.1016/j. jmb.2012.11.008 PMID: 23147217
26. Rutherford ST, Lemke JJ, Vrentas C.E., Gaal T., Ross W, Gourse RL. Effects of Dks A, Gre A, and GreB on transcription initiation: Insights into the mechanisms of factors that bind in the secondary channel of RNA polymerase. J Mol Biol. 2007; 366(4):1243-57. PMID: 17207814
27. Mogull SA, Runyen-Janecky LJ, Hong M., Payne SM. dksAis required for intercellular spread of Shigella flexneri via an RpoS-independent mechanism. Infect Immun. 2001; 69(9):5742-51. PMID: 11500451
28. Blaby-Haas CE, Furman R, Rodionov D.A., Artsimovitch I., de Crecy-Lagard V. Role of a Zn-independent DksA in Zn homeostasis and stringent response. Mol Microbiol. 2011; 79(3):700-15. doi: 10.1111/j.1365-2958.2010.07475.x PMID: 21255113
29. Lavinder JJ, Hari SB, Sullivan B.J., Magliery TJ. High-throughput thermal scanning: ageneral, rapid dye-binding thermal shift screen for protein engineering. J AmChem Soc. 2009; 131(11):3794-5. doi: 10. 1021/ja8049063 PMID: 19292479
30. Garrett DS, Seok YJ, Peterkofsky A, Clore G.M., Gronenborn AM. Identification by NMR of the binding surface for the histidine-containing phosphocarrier protein HPronthe N-terminal domain of enzyme I of the Escherichia coli phosphotransferase system. Biochemistry. 1997; 36(15):4393-8. PMID: 9109646
31. Nichols RJ, Sen S, Choo Y.J., Beltrao P., Zietek M, Chaba R, et al. Phenotypic landscape of a bacterial cell. Cell. 2011; 144(1):143-56. doi: 10.1016/j.cell.2010.11.052 PMID: 21185072
32. Furman R, Sevostyanova A, Artsimovitch I. Transcription initiation factor DksA has diverse effects on RNA chain elongation. Nucleic Acids Res. 2012; 40(8):3392-402. doi: 10.1093/nar/gkr1273 PMID: 22210857
33. Lyzen R, Kochanowska M, Wegrzyn G., Szalewska-Palasz A. Transcription from bacteriophage lambda pR promoter is regulated independently and antagonistically by DksA and ppGpp. Nucleic Acids Res. 2009; 37(20):6655-64. doi: 10.1093/nar/gkp676 PMID: 19759216
34. Blankschien MD, Lee JH, Grace E.D., Lennon CW, Halliday JA, Ross W, et al. Super DksAs: substitutions in DksA enhancing its effects on transcription initiation. EMBO J. 2009; 28(12):1720-31. doi: 10. 1038/emboj.2009.126 PMID: 19424178
35. Lennon CW, Gaal T, Ross W., Gourse RL. Escherichia coli DksA binds to free RNA polymerase with higher affinity than to RNA polymerase in an open complex. J Bacteriol. 2009; 191(18):5854-8. doi: 10. 1128/JB.00621-09 PMID: 19617357
36. Ruan WJ, Lehmann E, Thomm M., Kostrewa D, Cramer P. Evolution of two modes of intrinsic RNA polymerase transcript ceavage. J Biol Chem. 2011; 286(21):18701-7. doi: 10.1074/jbc.M111.222273 PMID: 21454497
37. Vedadi M, Niesen FH, Allali-Hassani A, Fedorov O.Y., Finerty PJ, Wasney GA, et al. Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination. Proc Natl Acad Sci USA. 2006; 103(43):15835-40. PMID: 17035505
38. Greenfield NJ. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions. Nature protocols. 2006; 1(6):2527-35. PMID: 17406506
39. Chandrangsu P, Lemke JJ, Gourse RL. The dksA promoter is negatively feedback regulated by DksA and ppGpp. Mol Microbiol. 2011; 80(5):1337-48. doi: 10.1111/j.1365-2958.2011.07649.x PMID: 21496125
40. Buc H, McClure WR. Kinetics of open complex formation between Escherichia coli RNA polymerase and the lac UV5 promoter. Evidence for a sequential mechanism involving three steps. Biochemistry. 1985; 24(11):2712-23. PMID: 3896304
41. Rich AM, Bombarda E, Schenk A.D., Lee PE, Cox EH, Spuches AM, et al. Thermodynamics of Zn2+ binding to Cys2His2 and Cys2HisCys zinc fingers and a Cys4 transcription factor site. J Am Chem Soc. 2012; 134(25):10405-18. doi: 10.1021/ja211417g PMID: 22591173
42. Magnusson LU, Nystrom T, Farewell A. Underproduction of sigma 70 mimics a stringent response. A proteome approach. J Biol Chem. 2003; 278(2):968-73. PMID: 12421813
43. Vinella D, Potrykus K, Murphy H., Cashel M. Effects on growth by changes of the balance between Gre A, Gre B, and DksA suggest mutual competition and functional redundancy in Escherichia coli. J Bacteriol. 2012; 194(2):261-73. doi: 10.1128/JB.06238-11 PMID: 22056927
44. Mechold U, Potrykus K, Murphy H., Murakami KS, Cashel M. Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res. 2013; 41(12):6175-89. doi: 10.1093/nar/gkt302 PMID: 23620295
45. Ross W, Vrentas CE, Sanchez-Vazquez P, Gaal T., Gourse RL. The magic spot: a ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation. Mol Cell. 2013; 50 (3):420-9. doi: 10.1016/j.molcel.2013.03.021 PMID: 23623682
46. Foster JW. Escherichia coli acid resistance: Tales of an amateur acidophile. Nat Rev Microbiol. 2004; 2 (11):898-907. PMID: 15494746
47. Richard H, Foster JW. Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pHand reverse transmembrane potential. J Bacteriol. 2004; 186(18):6032-41. PMID: 15342572
48. De Biase D, Tramonti A, Bossa F., Visca P. The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol. 1999; 32(6):1198-211. PMID: 10383761
49. Kanjee U, Gutsche I, Alexopoulos E., Zhao BY, El Bakkouri M, Thibault G, et al. Linkage between the bacterial acid stress and stringent responses: the structure of the inducible lysine decarboxylase. EMBO J. 2011; 30(5):931-44. doi: 10.1038/emboj.2011.5 PMID: 21278708
50. Artsimovitch I, Svetlov V, Anthony L., Burgess RR, Landick R. RNA polymerases from Bacillus subtilis and Escherichia coli differ in recognition of regulatory signals in vitro. J Bacteriol. 2000; 182(21):6027-35. PMID: 11029421
51. Furman R, Biswas T, Danhart E.M., Foster MP, Tsodikov OV, Artsimovitch I. DksA2, a zinc-independent structural analog of the transcription factor Dks A. FEBS letters. 2013; 587(6):614-9. doi: 10.1016/j. febslet.2013.01.073 PMID: 23416301
52. Belogurov GA, Vassylyeva MN, Svetlov V, Klyuyev S., Grishin NV, Vassylyev DG, et al. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol Cell. 2007; 26(1):117-29. PMID: 17434131