Catalytic mechanism and allosteric regulation of an oligomeric (p)ppGpp synthetase by an alarmone

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

Volumn 112, Issue 43, 2015, Pages 13348-13353

  Steinchen, Wieland ^a   Schuhmacher, Jan S ^a   Altegoer, Florian ^a   Fage, Christopher D ^a   Srinivasan, Vasundara ^a   Linne, Uwe ^a   Marahiel, Mohamed A ^a   Bange, Gert ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

(p)ppGpp; Alarmone; Crystallography; Hydrogen deuterium exchange mass spectrometry; Stringent response

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; OLIGOMER; PYROPHOSPHATE; SYNTHETASE; SYNTHETASE SMALL ALARMONE SYNTHETASE 1; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; GUANOSINE 3',5'-POLYPHOSPHATE SYNTHETASES; LIGASE;

ALLOSTERISM; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; CATALYSIS; CELL FUNCTION; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ENZYME SYNTHESIS; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOPHILICITY; OLIGOMERIZATION; PRIORITY JOURNAL; REGULATORY MECHANISM; BIOSYNTHESIS; CHEMISTRY; CRYSTALLIZATION; ESCHERICHIA COLI; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ION EXCHANGE CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MOLECULAR CLONING; MUTAGENESIS; PHYSIOLOGY;

ALLOSTERIC REGULATION; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CATALYSIS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, ION EXCHANGE; CLONING, MOLECULAR; CRYSTALLIZATION; ESCHERICHIA COLI; GUANOSINE PENTAPHOSPHATE; GUANOSINE TETRAPHOSPHATE; LIGASES; MASS SPECTROMETRY; MUTAGENESIS;

EID: 84945558183     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505271112     Document Type: Article

References (48)

1. Boutte CC, Crosson S (2013) Bacterial lifestyle shapes stringent response activation. Trends Microbiol 21(4):174-180.
2. Potrykus K, Cashel M (2008) (p)ppGpp: Still magical? Annu Rev Microbiol 62:35-51.
3. Liu K, Bittner AN, Wang JD (2015) Diversity in (p)ppGpp metabolism and effectors. Curr Opin Microbiol 24:72-79.
4. Takahashi K, Kasai K, Ochi K (2004) Identification of the bacterial alarmone guanosine 5′-diphosphate 3′-diphosphate (ppGpp) in plants. Proc Natl Acad Sci USA 101(12): 4320-4324.
5. van der Biezen EA, Sun J, Coleman MJ, Bibb MJ, Jones JD (2000) Arabidopsis RelA/SpoT homologs implicate (p)ppGpp in plant signaling. Proc Natl Acad Sci USA 97(7): 3747-3752.
6. Masuda S, et al. (2008) The bacterial stringent response, conserved in chloroplasts, controls plant fertilization. Plant Cell Physiol 49(2):135-141.
7. Vogt SL, et al. (2011) The stringent response is essential for Pseudomonas aeruginosa virulence in the rat lung agar bead and Drosophila melanogaster feeding models of infection. Infect Immun 79(10):4094-4104.
8. Weiss LA, Stallings CL (2013) Essential roles for Mycobacterium tuberculosis Rel beyond the production of (p)ppGpp. J Bacteriol 195(24):5629-5638.
9. Dalebroux ZD, Swanson MS (2012) ppGpp: Magic beyond RNA polymerase. Nat Rev Microbiol 10(3):203-212.
10. Lewis K (2010) Persister cells. Annu Rev Microbiol 64:357-372.
11. Amato SM, Orman MA, Brynildsen MP (2013) Metabolic control of persister formation in Escherichia coli. Mol Cell 50(4):475-487.
12. He H, Cooper JN, Mishra A, Raskin DM (2012) Stringent response regulation of biofilm formation in Vibrio cholerae. J Bacteriol 194(11):2962-2972.
13. Syal K, Maiti K, Naresh K, Chatterji D, Jayaraman N (2015) Synthetic glycolipids and (p)ppGpp analogs: Development of inhibitors for mycobacterial growth, biofilm and stringent response. Adv Exp Med Biol 842:309-327.
14. Wexselblatt E, et al. (2012) Relacin, a novel antibacterial agent targeting the Stringent Response. PLoS Pathog 8(9):e1002925.
15. Kanjee U, Ogata K, Houry WA (2012) Direct binding targets of the stringent response alarmone (p)ppGpp. Mol Microbiol 85(6):1029-1043.
16. Wang JD, Sanders GM, Grossman AD (2007) Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128(5):865-875.
17. Mechold U, Potrykus K, Murphy H, Murakami KS, Cashel M (2013) Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res 41(12): 6175-6189.
18. Atkinson GC, Tenson T, Hauryliuk V (2011) The RelA/SpoT homolog (RSH) superfamily: Distribution and functional evolution of ppGpp synthetases and hydrolases across the tree of life. PLoS One 6(8):e23479.
19. Hogg T, Mechold U, Malke H, Cashel M, Hilgenfeld R (2004) Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response [corrected]. Cell 117(1):57-68.
20. Wendrich TM, Blaha G, Wilson DN, Marahiel MA, Nierhaus KH (2002) Dissection of the mechanism for the stringent factor RelA. Mol Cell 10(4):779-788.
21. Agirrezabala X, et al. (2013) The ribosome triggers the stringent response by RelA via a highly distorted tRNA. EMBO Rep 14(9):811-816.
22. Avarbock D, Avarbock A, Rubin H (2000) Differential regulation of opposing RelMtb activities by the aminoacylation state of a tRNA.ribosome.mRNA. RelMtb complex. Biochemistry 39(38):11640-11648.
23. Mechold U, Murphy H, Brown L, Cashel M (2002) Intramolecular regulation of the opposing (p)ppGpp catalytic activities of Rel(Seq), the Rel/Spo enzyme from Streptococcus equisimilis. J Bacteriol 184(11):2878-2888.
24. Geiger T, Kästle B, Gratani FL, Goerke C, Wolz C (2014) Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J Bacteriol 196(4):894-902.
25. Nanamiya H, et al. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67(2):291-304.
26. Lemos JA, Lin VK, Nascimento MM, Abranches J, Burne RA (2007) Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol Microbiol 65(6): 1568-1581.
27. Srivatsan A, et al. (2008) High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4(8):e1000139.
28. Gaca AO, et al. (2015) From (p)ppGpp to (pp)pGpp: Characterization of Regulatory Effects of pGpp Synthesized by the Small Alarmone Synthetase of Enterococcus faecalis. J Bacteriol 197(18):2908-2919.
29. Ryals J, Little R, Bremer H (1982) Control of rRNA and tRNA syntheses in Escherichia coli by guanosine tetraphosphate. J Bacteriol 151(3):1261-1268.
30. Nishino T, Gallant J, Shalit P, Palmer L, Wehr T (1979) Regulatory nucleotides involved in the Rel function of Bacillus subtilis. J Bacteriol 140(2):671-679.
31. Arnez JG, Augustine JG, Moras D, Francklyn CS (1997) The first step of aminoacylation at the atomic level in histidyl-tRNA synthetase. Proc Natl Acad Sci USA 94(14): 7144-7149.
32. Cavarelli J, et al. (1994) The active site of yeast aspartyl-tRNA synthetase: Structural and functional aspects of the aminoacylation reaction. EMBO J 13(2):327-337.
33. Stammers DK, et al. (1999) 2.0 A X-ray structure of the ternary complex of 7,8-dihydro-6-hydroxymethylpterinpyrophosphokinase from Escherichia coli with ATP and a substrate analogue. FEBS Lett 456(1):49-53.
34. Bennett BD, et al. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5(8):593-599.
35. Bittner AN, Kriel A, Wang JD (2014) Lowering GTP level increases survival of amino acid starvation but slows growth rate for Bacillus subtilis cells lacking (p)ppGpp. J Bacteriol 196(11):2067-2076.
36. Kriel A, et al. (2014) GTP dysregulation in Bacillus subtilis cells lacking (p)ppGpp results in phenotypic amino acid auxotrophy and failure to adapt to nutrient downshift and regulate biosynthesis genes. J Bacteriol 196(1):189-201.
37. Kriel A, et al. (2012) Direct regulation of GTP homeostasis by (p)ppGpp: A critical component of viability and stress resistance. Mol Cell 48(2):231-241.
38. Liu K, et al. (2015) Molecular mechanism and evolution of guanylate kinase regulation by (p)ppGpp. Mol Cell 57(4):735-749.
39. Tagami K, et al. (2012) Expression of a small (p)ppGpp synthetase, Ywa C, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. MicrobiologyOpen 1(2):115-134.
40. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66(Pt 2):125-132.
41. Winn MD, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67(Pt 4):235-242.
42. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60(Pt 12 Pt 1):2126-2132.
43. 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.
44. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Cryst 40(Pt 4):658-674.
45. Wales TE, Fadgen KE, Gerhardt GC, Engen JR (2008) High-speed and high-resolution UPLC separation at zero degrees Celsius. Anal Chem 80(17):6815-6820.
46. Nevin P, Lu X, Zhang K, Engen JR, Beuning PJ (2015) Noncognate DNA damage prevents the formation of the active conformation of the Y-family DNA polymerases DinB and DNA polymerase κ. FEBS J 282(14):2646-2660.
47. Geromanos SJ, et al. (2009) The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LCMS/MS. Proteomics 9(6):1683-1695.
48. Zhang Z, Smith DL (1993) Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation. Protein Sci 2(4):522-531.