Light activation of staphylococcus aureus toxin YoeBSa 1 reveals guanosine-specific endoribonuclease activity

Biochemistry

Volumn 53, Issue 1, 2014, Pages 188-201

  Larson, Amy S ^a   Hergenrother, Paul J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDORIBONUCLEASE; FLUOROMETRIC ASSAY; LIGHT ACTIVATION; NOVEL STRATEGIES; RNA CLEAVAGE; SEQUENCE SPECIFICITY; STAPHYLOCOCCUS AUREUS; UNNATURAL AMINO ACIDS;

AMINO ACIDS; BACTERIA; BIOMOLECULES; CELL CULTURE; ESCHERICHIA COLI; RNA; TOXIC MATERIALS;

MACROMOLECULES;

ADENOSINE; AMINO ACID; ANTITOXIN; BACTERIAL TOXIN; GUANOSINE; MESSENGER RNA; RIBONUCLEASE; TYROSINE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME KINETICS; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; STAPHYLOCOCCUS AUREUS; TOXICITY;

BACTERIAL PROTEINS; BACTERIAL TOXINS; ENDORIBONUCLEASES; ENZYME ACTIVATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GUANOSINE; LIGHT; STAPHYLOCOCCUS AUREUS; SUBSTRATE SPECIFICITY; TYROSINE;

EID: 84892584112     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4008098     Document Type: Article

References (74)

1. Pandey, D. P. and Gerdes, K. (2005) Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes Nucleic Acids Res. 33, 966-976
2. Yamaguchi, Y., Park, J. H., and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea Annu. Rev. Genet. 45, 61-79
3. Masuda, H., Tan, Q., Awano, N., Wu, K. P., and Inouye, M. (2012) YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli Mol. Microbiol. 84, 979-989
4. Wang, X., Lord, D. M., Cheng, H. Y., Osbourne, D. O., Hong, S. H., Sanchez-Torres, V., Quiroga, C., Zheng, K., Herrmann, T., Peti, W., Benedik, M. J., Page, R., and Wood, T. K. (2012) A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS Nat. Chem. Biol. 8, 855-861
5. Gerdes, K., Christensen, S. K., and Lobner-Olesen, A. (2005) Prokaryotic toxin-antitoxin stress response loci Nat. Rev. Microbiol. 3, 371-382
6. Gerdes, K., Rasmussen, P. B., and Molin, S. (1986) Unique type of plasmid maintenance function: Postsegregational killing of plasmid-free cells Proc. Natl. Acad. Sci. U.S.A. 83, 3116-3120
7. Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Dreze, P., and Van Melderen, L. (2011) Diversity of bacterial type II toxin-antitoxin systems: A comprehensive search and functional analysis of novel families Nucleic Acids Res. 39, 5513-5525
8. Magnuson, R. D. (2007) Hypothetical functions of toxin-antitoxin systems J. Bacteriol. 189, 6089-6092
9. Schuster, C. F. and Bertram, R. (2013) Toxin-antitoxin systems are ubiquitous and versatile modulators of prokaryotic cell fate FEMS Microbiol. Lett. 340, 73-85
10. Pedersen, K., Christensen, S. K., and Gerdes, K. (2002) Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins Mol. Microbiol. 45, 501-510
11. Engelberg-Kulka, H., Sat, B., Reches, M., Amitai, S., and Hazan, R. (2004) Bacterial programmed cell death systems as targets for antibiotics Trends Microbiol. 12, 66-71
12. DeNap, J. C. and Hergenrother, P. J. (2005) Bacterial death comes full circle: Targeting plasmid replication in drug-resistant bacteria Org. Biomol. Chem. 3, 959-966
13. Williams, J. J. and Hergenrother, P. J. (2008) Exposing plasmids as the Achilles' heel of drug-resistant bacteria Curr. Opin. Chem. Biol. 12, 389-399
14. Williams, J. J. and Hergenrother, P. J. (2012) Artificial activation of toxin-antitoxin systems as an antibacterial strategy Trends Microbiol. 20, 291-298
15. Diekema, D. J., Pfaller, M. A., Schmitz, F. J., Smayevsky, J., Bell, J., Jones, R. N., and Beach, M. (2001) Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY Antimicrobial Surveillance Program, 1997-1999 Clin. Infect. Dis. 32 (Suppl. 2) S114-S132
16. Donegan, N. P. and Cheung, A. L. (2009) Regulation of the mazEF toxin-antitoxin module in Staphylococcus aureus and its impact on sigB expression J. Bacteriol. 191, 2795-2805
17. Donegan, N. P., Thompson, E. T., Fu, Z., and Cheung, A. L. (2010) Proteolytic regulation of toxin-antitoxin systems by ClpPC in Staphylococcus aureus J. Bacteriol. 192, 1416-1422
18. Makarova, K. S., Wolf, Y. I., and Koonin, E. V. (2009) Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes Biol. Direct 4, 19
19. Kamada, K. and Hanaoka, F. (2005) Conformational change in the catalytic site of the ribonuclease YoeB toxin by YefM antitoxin Mol. Cell 19, 497-509
20. Zhang, Y. and Inouye, M. (2009) The inhibitory mechanism of protein synthesis by YoeB, an Escherichia coli toxin J. Biol. Chem. 284, 6627-6638
21. Williams, J. J., Halvorsen, E. M., Dwyer, E. M., DiFazio, R. M., and Hergenrother, P. J. (2011) Toxin-antitoxin (TA) systems are prevalent and transcribed in clinical isolates of Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus FEMS Microbiol. Lett. 322, 41-50
22. Moritz, E. M. and Hergenrother, P. J. (2007) Toxin-antitoxin systems are ubiquitous and plasmid-encoded in vancomycin-resistant enterococci Proc. Natl. Acad. Sci. U.S.A. 104, 311-316
23. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22, 4673-4680
24. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool J. Mol. Biol. 215, 403-410
25. Miller, J. C., Silverman, S. K., England, P. M., Dougherty, D. A., and Lester, H. A. (1998) Flash decaging of tyrosine sidechains in an ion channel Neuron 20, 619-624
26. Wessel, D. and Flugge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Anal. Biochem. 138, 141-143
27. McKenzie, J. L., Duyvestyn, J. M., Smith, T., Bendak, K., Mackay, J., Cursons, R., Cook, G. M., and Arcus, V. L. (2012) Determination of ribonuclease sequence-specificity using Pentaprobes and mass spectrometry RNA 18, 1267-1278
28. Yoshizumi, S., Zhang, Y., Yamaguchi, Y., Chen, L., Kreiswirth, B. N., and Inouye, M. (2009) Staphylococcus aureus YoeB homologues inhibit translation initiation J. Bacteriol. 191, 5868-5872
29. Wang, L., Brock, A., Herberich, B., and Schultz, P. G. (2001) Expanding the genetic code of Escherichia coli Science 292, 498-500
30. Liu, C. C. and Schultz, P. G. (2010) Adding new chemistries to the genetic code Annu. Rev. Biochem. 79, 413-444
31. Davis, L. and Chin, J. W. (2012) Designer proteins: Applications of genetic code expansion in cell biology Nat. Rev. Mol. Cell Biol. 13, 168-182
32. Deiters, A., Groff, D., Ryu, Y., Xie, J., and Schultz, P. G. (2006) A genetically encoded photocaged tyrosine Angew. Chem., Int. Ed. 45, 2728-2731
33. Chou, C., Young, D. D., and Deiters, A. (2009) A light-activated DNA polymerase Angew. Chem., Int. Ed. 48, 5950-5953
34. Edwards, W. F., Young, D. D., and Deiters, A. (2009) Light-activated Cre recombinase as a tool for the spatial and temporal control of gene function in mammalian cells ACS Chem. Biol. 4, 441-445
35. Chou, C., Young, D. D., and Deiters, A. (2010) Photocaged T7 RNA polymerase for the light activation of transcription and gene function in pro-and eukaryotic cells ChemBioChem 11, 972-977
36. Chou, C. and Deiters, A. (2011) Light-activated gene editing with a photocaged zinc-finger nuclease Angew. Chem., Int. Ed. 50, 6839-6842
37. Zhao, H., Sterner, E. S., Coughlin, E. B., and Theato, P. (2012) o-Nitrobenzyl alcohol derivatives: Opportunities in polymer and materials science Macromolecules 45, 1723-1736
38. Young, T. S., Ahmad, I., Yin, J. A., and Schultz, P. G. (2010) An enhanced system for unnatural amino acid mutagenesis in E. coli J. Mol. Biol. 395, 361-374
39. Karancsi, T. and Slegel, P. (1999) Reliable molecular mass determination of aromatic nitro compounds: Elimination of gas-phase reduction occurring during atmospheric pressure chemical ionization J. Mass Spectrom. 34, 975-977
40. Bendak, K., Loughlin, F. E., Cheung, V., O'Connell, M. R., Crossley, M., and Mackay, J. P. (2012) A rapid method for assessing the RNA-binding potential of a protein Nucleic Acids Res. 40, e105
41. Wang, N. R. and Hergenrother, P. J. (2007) A continuous fluorometric assay for the assessment of MazF ribonuclease activity Anal. Biochem. 371, 173-183
42. van Rensburg, J. J. and Hergenrother, P. J. (2013) Detection of endogenous MazF enzymatic activity in Staphylococcus aureus Anal. Biochem. 443, 81-87
43. Michaelis, L., Menten, M. L., Johnson, K. A., and Goody, R. S. (2011) The original Michaelis constant: Translation of the 1913 Michaelis-Menten paper Biochemistry 50, 8264-8269
44. Nelson, D. L., Lehninger, A. L., and Cox, M. M. (2008) Lehninger Principles of Biochemistry, 5 th ed., W. H. Freeman, New York.
45. max estimates Comments on Theoretical Biology 8, 169-187
46. Griffiths, J. R. (1979) Steady-state enzyme kinetics in mutual depletion systems Biochem. Soc. Trans. 7, 429-439
47. Laurent, M. and Kellershohn, N. (1984) Apparent co-operativity for highly concentrated Michaelian and allosteric enzymes J. Mol. Biol. 174, 543-555
48. Hill, A. V. (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves J. Physiol. 40, iv-vii
49. Porter, C. M. and Miller, B. G. (2012) Cooperativity in monomeric enzymes with single ligand-binding sites Bioorg. Chem. 43, 44-50
50. Halvorsen, E. M., Williams, J. J., Bhimani, A. J., Billings, E. A., and Hergenrother, P. J. (2011) Txe, an endoribonuclease of the enterococcal Axe-Txe toxin-antitoxin system, cleaves mRNA and inhibits protein synthesis Microbiology 157, 387-397
51. Sevillano, L., Diaz, M., Yamaguchi, Y., Inouye, M., and Santamaria, R. I. (2012) Identification of the first functional toxin-antitoxin system in Streptomyces PLoS One 7, e32977
52. Nolle, N., Schuster, C. F., and Bertram, R. (2013) Two paralogous yefM-yoeB loci from Staphylococcus equorum encode functional toxin-antitoxin systems Microbiology 159 (Part 8) 1575-1585
53. Wilcox, M., Viola, R. W., Johnson, K. W., Billington, A. P., Carpenter, B. K., Mccray, J. A., Guzikowski, A. P., and Hess, G. P. (1990) Synthesis of photolabile precursors of amino-acid neurotransmitters J. Org. Chem. 55, 1585-1589
54. Zhang, Z., Papageorgiou, G., Corrie, J. E. T., and Grewer, C. (2007) Pre-steady-state currents in neutral amino acid transporters induced by photolysis of a new caged alanine derivative Biochemistry 46, 3872-3880
55. Nakayama, K., Heise, I., Gorner, H., and Gartner, W. (2011) Peptide release upon photoconversion of 2-nitrobenzyl compounds into nitroso derivatives Photochem. Photobiol. 87, 1031-1035
56. Neubauer, C., Gao, Y. G., Andersen, K. R., Dunham, C. M., Kelley, A. C., Hentschel, J., Gerdes, K., Ramakrishnan, V., and Brodersen, D. E. (2009) The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE Cell 139, 1084-1095
57. Bahassi, E. M., Salmon, M. A., Van Melderen, L., Bernard, P., and Couturier, M. (1995) F plasmid CcdB killer protein: ccdB gene mutants coding for non-cytotoxic proteins which retain their regulatory functions Mol. Microbiol. 15, 1031-1037
58. Loris, R., Dao-Thi, M. H., Bahassi, E. M., Van Melderen, L., Poortmans, F., Liddington, R., Couturier, M., and Wyns, L. (1999) Crystal structure of CcdB, a topoisomerase poison from E. coli J. Mol. Biol. 285, 1667-1677
59. Magnuson, R. and Yarmolinsky, M. B. (1998) Corepression of the P1 addiction operon by Phd and Doc J. Bacteriol. 180, 6342-6351
60. Mattison, K., Wilbur, J. S., So, M., and Brennan, R. G. (2006) Structure of FitAB from Neisseria gonorrhoeae bound to DNA reveals a tetramer of toxin-antitoxin heterodimers containing pin domains and ribbon-helix-helix motifs J. Biol. Chem. 281, 37942-37951
61. Hurley, J. M. and Woychik, N. A. (2009) Bacterial toxin HigB associates with ribosomes and mediates translation-dependent mRNA cleavage at A-rich sites J. Biol. Chem. 284, 18605-18613
62. Korch, S. B. and Hill, T. M. (2006) Ectopic overexpression of wild-type and mutant hipA genes in Escherichia coli: Effects on macromolecular synthesis and persister formation J. Bacteriol. 188, 3826-3836
63. Kamphuis, M. B., Bonvin, A. M., Monti, M. C., Lemonnier, M., Munoz-Gomez, A., van den Heuvel, R. H., Diaz-Orejas, R., and Boelens, R. (2006) Model for RNA binding and the catalytic site of the RNase Kid of the bacterial parD toxin-antitoxin system J. Mol. Biol. 357, 115-126
64. Li, G. Y., Zhang, Y., Chan, M. C., Mal, T. K., Hoeflich, K. P., Inouye, M., and Ikura, M. (2006) Characterization of dual substrate binding sites in the homodimeric structure of Escherichia coli mRNA interferase MazF J. Mol. Biol. 357, 139-150
65. Brown, B. L., Grigoriu, S., Kim, Y., Arruda, J. M., Davenport, A., Wood, T. K., Peti, W., and Page, R. (2009) Three dimensional structure of the MqsR:MqsA complex: A novel TA pair comprised of a toxin homologous to RelE and an antitoxin with unique properties PLoS Pathog. 5, e1000706
66. Agarwal, S., Mishra, N. K., Bhatnagar, S., and Bhatnagar, R. (2010) PemK toxin of Bacillus anthracis is a ribonuclease: An insight into its active site, structure, and function J. Biol. Chem. 285, 7254-7270
67. Khoo, S. K., Loll, B., Chan, W. T., Shoeman, R. L., Ngoo, L., Yeo, C. C., and Meinhart, A. (2007) Molecular and structural characterization of the PezAT chromosomal toxin-antitoxin system of the human pathogen Streptococcus pneumoniae J. Biol. Chem. 282, 19606-19618
68. Sedwick, C. (2011) PezT: A bacterial suicide gene PLoS Biol. 9, e1001036
69. 2+ ion in the active site and a putative RNA-binding site Protein Sci. 21, 1754-1767
70. Miallau, L., Faller, M., Chiang, J., Arbing, M., Guo, F., Cascio, D., and Eisenberg, D. (2009) Structure and proposed activity of a member of the VapBC family of toxin-antitoxin systems. VapBC-5 from Mycobacterium tuberculosis J. Biol. Chem. 284, 276-283
71. Dienemann, C., Boggild, A., Winther, K. S., Gerdes, K., and Brodersen, D. E. (2011) Crystal structure of the VapBC toxin-antitoxin complex from Shigella flexneri reveals a hetero-octameric DNA-binding assembly J. Mol. Biol. 414, 713-722
72. Armalyte, J., Jurenaite, M., Beinoraviciute, G., Teiserskas, J., and Suziedeliene, E. (2012) Characterization of Escherichia coli dinJ-yafQ toxin-antitoxin system using insights from mutagenesis data J. Bacteriol. 194, 1523-1532
73. 2 complex formation Proc. Natl. Acad. Sci. U.S.A. 100, 1661-1666
74. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: A sequence logo generator Genome Res. 14, 1188-1190