CBR antimicrobials inhibit RNA polymerase via at least two bridge-helix cap-mediated effects on nucleotide addition

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

Volumn 112, Issue 31, 2015, Pages E4178-E4187

  Bae, Brian ^a   Nayak, Dhananjaya ^b   Ray, Ananya ^b   Mustaev, Arkady ^c   Landick, Robert ^b   Darst, Seth A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Cbr inhibitors; Rna polymerase; Transcription inhibition; X ray crystallography

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CBR COMPOUND; DINUCLEOTIDE; MAGNESIUM ION; NUCLEOTIDE; RNA POLYMERASE; UNCLASSIFIED DRUG; DNA DIRECTED RNA POLYMERASE; ENZYME INHIBITOR; MESSENGER RNA; PYROPHOSPHORIC ACID DERIVATIVE;

ANTIBACTERIAL ACTIVITY; ARTICLE; BRIDGE HELIX; CATALYSIS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ESCHERICHIA COLI; HYDROLYSIS; IC50; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RNA CLEAVAGE; STEREOISOMERISM; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SECONDARY STRUCTURE;

ESCHERICHIA COLI;

AMINO ACID SEQUENCE; ANTI-INFECTIVE AGENTS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIPHOSPHATES; DNA-DIRECTED RNA POLYMERASES; ENZYME INHIBITORS; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; PROTEIN STRUCTURE, SECONDARY; RNA, MESSENGER; TRANSCRIPTION ELONGATION, GENETIC;

EID: 84938703725     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1502368112     Document Type: Article

References (57)

1. Hartmann G, Honikel KO, Knüsel F, Nüesch J (1967) The specific inhibition of the DNAdirected RNA synthesis by rifamycin. Biochim Biophys Acta 145(3):843-844.
2. Campbell EA, et al. (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104(6):901-912.
3. Feklistov A, et al. (2008) Rifamycins do not function by allosteric modulation of binding of Mg2+ to the RNA polymerase active center. Proc Natl Acad Sci USA 105(39):14820-14825.
4. Floss HG, Yu T-W (2005) Rifamycin-mode of action, resistance, and biosynthesis. Chem Rev 105(2):621-632.
5. Bush K, et al. (2011) Tackling antibiotic resistance. Nat Rev Microbiol 9(12):894-896.
6. Artsimovitch I, Chu C, Lynch AS, Landick R (2003) A new class of bacterial RNA polymerase inhibitor affects nucleotide addition. Science 302(5645):650-654.
7. Lane WJ, Darst SA (2010) Molecular evolution of multisubunit RNA polymerases: Structural analysis. J Mol Biol 395(4):686-704.
8. Miropolskaya N, Artsimovitch I, Klimašauskas S, Nikiforov V, Kulbachinskiy A (2009) Allosteric control of catalysis by the F loop of RNA polymerase. Proc Natl Acad Sci USA 106(45):18942-18947.
9. Miropolskaya N, Nikiforov V, Klimašauskas S, Artsimovitch I, Kulbachinskiy A (2010) Modulation of RNA polymerase activity through the trigger loop folding. Transcription 1(2):89-94.
10. Miropolskaya N, et al. (2014) Interplay between the trigger loop and the F loop during RNA polymerase catalysis. Nucleic Acids Res 42(1):544-552.
11. Tan L, Wiesler S, Trzaska D, Carney HC, Weinzierl RO (2008) Bridge helix and trigger loop perturbations generate superactive RNA polymerases. J Biol 7(10):40.
12. Jovanovic M, et al. (2011) Activity map of the Escherichia coli RNA polymerase bridge helix. J Biol Chem 286(16):14469-14479.
13. Hein PP, Landick R (2010) The bridge helix coordinates movements of modules in RNA polymerase. BMC Biol 8:141.
14. Vassylyev DG, Vassylyeva MN, Perederina A, Tahirov TH, Artsimovitch I (2007) Structural basis for transcription elongation by bacterial RNA polymerase. Nature 448(7150):157-162.
15. Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: An RNA polymerase II elongation complex at 3.3 A resolution. Science 292(5523):1876-1882.
16. Kettenberger H, Armache K-J, Cramer P (2004) Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol Cell 16(6):955-965.
17. Korzheva N, et al. (2000) A structural model of transcription elongation. Science 289(5479):619-625.
18. Naji S, Bertero MG, Spitalny P, Cramer P, Thomm M (2008) Structure-function analysis of the RNA polymerase cleft loops elucidates initial transcription, DNA unwinding and RNA displacement. Nucleic Acids Res 36(2):676-687.
19. Thomm M, Reich C, Grünberg S, Naji S (2009) Mutational studies of archaeal RNA polymerase and analysis of hybrid RNA polymerases. Biochem Soc Trans 37(Pt 1):18-22.
20. Kireeva ML, Domecq C, Coulombe B, Burton ZF, Kashlev M (2011) Interaction of RNA polymerase II fork loop 2 with downstream non-template DNA regulates transcription elongation. J Biol Chem 286(35):30898-30910.
21. Malinen AM, et al. (2014) CBR antimicrobials alter coupling between the bridge helix and the β subunit in RNA polymerase. Nat Commun 5:3408.
22. Li L, Chen X, Mihalic JT, Cutler S (2004) Pyrazole Antimicrobial Agents. US Patent 6,673,923.
23. Li L, Chen X, Fan P, Mihalic JT, Cutler S (2006) Hydroxyamidines and Related Compounds Are Provided Which Are Suitable as Antibacterial Agents. US Patent 7,148,259.
24. Zuo Y, Wang Y, Steitz TA (2013) The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex. Mol Cell 50(3):430-436.
25. Murakami KS (2013) X-ray crystal structure of Escherichia coli RNA polymerase σ70 holoenzyme. J Biol Chem 288(13):9126-9134.
26. Bae B, et al. (2013) Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of σ70 domain 1.1. Proc Natl Acad Sci USA 110(49):19772-19777.
27. Malinen AM, et al. (2012) Active site opening and closure control translocation of multisubunit RNA polymerase. Nucleic Acids Res 40(15):7442-7451.
28. Vassylyev DG, et al. (2007) Structural basis for substrate loading in bacterial RNA polymerase. Nature 448(7150):163-168.
29. Wang D, Bushnell DA, Westover KD, Kaplan CD, Kornberg RD (2006) Structural basis of transcription: Role of the trigger loop in substrate specificity and catalysis. Cell 127(5):941-954.
30. Temiakov D, et al. (2005) Structural basis of transcription inhibition by antibiotic streptolydigin. Mol Cell 19(5):655-666.
31. Nayak D, Voss M, Windgassen T, Mooney RA, Landick R (2013) Cys-pair reporters detect a constrained trigger loop in a paused RNA polymerase. Mol Cell 50(6):882-893.
32. Toulokhonov I, Zhang J, Palangat M, Landick R (2007) A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol Cell 27(3):406-419.
33. Yuzenkova Y, Zenkin N (2010) Central role of the RNA polymerase trigger loop in intrinsic RNA hydrolysis. Proc Natl Acad Sci USA 107(24):10878-10883.
34. Sosunova E, et al. (2003) Donation of catalytic residues to RNA polymerase active center by transcription factor Gre. Proc Natl Acad Sci USA 100(26):15469-15474.
35. Sosunova E, Sosunov V, Epshtein V, Nikiforov V, Mustaev A (2013) Control of transcriptional fidelity by active center tuning as derived from RNA polymerase endonuclease reaction. J Biol Chem 288(9):6688-6703.
36. Yuzenkova Y, et al. (2010) Stepwise mechanism for transcription fidelity. BMC Biol 8(1):54.
37. Sydow JF, et al. (2009) Structural basis of transcription: Mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol Cell 34(6):710-721.
38. Wang D, et al. (2009) Structural basis of transcription: Backtracked RNA polymerase II at 3.4 angstrom resolution. Science 324(5931):1203-1206.
39. Sekine S, Murayama Y, Svetlov V, Nudler E, Yokoyama S (2015) The ratcheted and ratchetable structural states of RNA polymerase underlie multiple transcriptional functions. Mol Cell 57(3):408-421.
40. Rozovskaya TA, et al. (1984) The mechanism of pyrophosphorolysis of RNA by RNA polymerase. Endowment of RNA polymerase with artificial exonuclease activity. Biochem J 224(2):645-650.
41. Vitiello CL, Kireeva ML, Lubkowska L, Kashlev M, Gottesman M (2014) Coliphage HK022 Nun protein inhibits RNA polymerase translocation. Proc Natl Acad Sci USA 111(23):E2368-E2375.
42. Sosunov V, et al. (2003) Unified two-metal mechanism of RNA synthesis and degradation by RNA polymerase. EMBO J 22(9):2234-2244.
43. Zhang G, et al. (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell 98(6):811-824.
44. Epshtein V, et al. (2002) Swing-gate model of nucleotide entry into the RNA polymerase active center. Mol Cell 10(3):623-634.
45. Tuske S, et al. (2005) Inhibition of bacterial RNA polymerase by streptolydigin: Stabilization of a straight-bridge-helix active-center conformation. Cell 122(4):541-552.
46. Mukhopadhyay J, et al. (2008) The RNA polymerase "switch region" is a target for inhibitors. Cell 135(2):295-307.
47. Belogurov GA, et al. (2009) Transcription inactivation through local refolding of the RNA polymerase structure. Nature 457(7227):332-335.
48. Weinzierl RO (2010) The nucleotide addition cycle of RNA polymerase is controlled by two molecular hinges in the Bridge Helix domain. BMC Biol 8:134.
49. Degen D, et al. (2014) Transcription inhibition by the depsipeptide antibiotic salinamide A. eLife 3:e02451.
50. Cibian M, Ferreira JG, Hanan GS (2009) 4-Bromo-N-phenyl-benzamidoxime. Acta Crystallogr Sect E Struct Rep Online 65(Pt 11):o2820.
51. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data. Methods Enzymol 267:307-326.
52. Adams PD, et al. (2010) PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66(Pt 2):213-221.
53. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
54. Moriarty NW, Grosse-Kunstleve RW, Adams PD (2009) Electronic Ligand Builder and Optimization Workbench (eLBOW): A tool for ligand coordinate and restraint generation. Acta Crystallogr D Biol Crystallogr 65(Pt 10):1074-1080.
55. Schröder GF, Levitt M, Brunger AT (2010) Super-resolution biomolecular crystallography with low-resolution data. Nature 464(7292):1218-1222.
56. Brünger AT, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54(Pt 5):905-921.
57. O'Donovan DJ, et al. (2012) A grid-enabled web service for low-resolution crystal structure refinement. Acta Crystallogr D Biol Crystallogr 68(Pt 3):261-267.