Mechanism of endonuclease cleavage by the HigB toxin

Nucleic Acids Research

Volumn 44, Issue 16, 2016, Pages 7944-7953

  Schureck, Marc A ^a   Repack, Adrienne ^a   Miles, Stacey J ^a   Marquez, Jhomar ^a   Dunham, Christine M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; BACTERIAL TOXIN; ENDONUCLEASE; HIGB TOXIN; HISTIDINE; MESSENGER RNA; PROTEIN VARIANT; RIBOSOME PROTEIN; TYROSINE; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; HIGB PROTEIN, E COLI; RIBONUCLEASE;

ARTICLE; BIOCHEMICAL ANALYSIS; CATALYSIS; CELL ASSAY; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME MECHANISM; GENE REARRANGEMENT; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RIBOSOME; RNA CLEAVAGE; RNA CONFORMATION; RNA STRUCTURE; STRUCTURE ANALYSIS; TOXIN STRUCTURE; X RAY; AMINO ACID SEQUENCE; CHEMISTRY; ESCHERICHIA COLI; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RNA STABILITY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL TOXINS; CRYSTALLOGRAPHY, X-RAY; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; RNA STABILITY; RNA, MESSENGER;

EID: 84988972185     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw598     Document Type: Article

References (55)

1. Maisonneuve, E. and Gerdes, K. (2014) Molecular mechanisms underlying bacterial persisters. Cell, 157, 539-548.
2. Bernard, P. and Couturier, M. (1992) Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. J. Mol. Biol., 226, 735-745.
3. Zhang, Y. and Inouye, M. (2011) RatA (YfjG), an Escherichia coli toxin, inhibits 70S ribosome association to block translation initiation. Mol. Microbiol., 79, 1418-1429.
4. Pedersen, K., Zavialov, A.V., Pavlov, M.Y., Elf, J., Gerdes, K. and Ehrenberg, M. (2003) The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell, 112, 131-140.
5. Winther, K.S. and Gerdes, K. (2011) Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA. Proc. Natl. Acad. Sci. U.S.A., 108, 7403-7407.
6. Ainelo, A., Tamman, H., Leppik, M., Remme, J. and Horak, R. (2016) The toxin GraT inhibits ribosome biogenesis. Mol. Microbiol., 100, 719-734.
7. Mutschler, H., Gebhardt, M., Shoeman, R.L. and Meinhart, A. (2011) A novel mechanism of programmed cell death in bacteria by toxin-antitoxin systems corrupts peptidoglycan synthesis. PLoS Biol., 9, e1001033.
8. Tan, Q., Awano, N. and Inouye, M. (2011) YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB. Mol. Microbiol., 79, 109-118.
9. Germain, E., Roghanian, M., Gerdes, K. and Maisonneuve, E. (2015) Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases. Proc. Natl. Acad. Sci. U.S.A., 112, 5171-5176.
10. Keren, I., Shah, D., Spoering, A., Kaldalu, N. and Lewis, K. (2004) Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol., 186, 8172-8180.
11. Maisonneuve, E., Shakespeare, L.J., Jorgensen, M.G. and Gerdes, K. (2011) Bacterial persistence by RNA endonucleases. Proc. Natl. Acad. Sci. U.S.A., 108, 13206-13211.
12. Maisonneuve, E., Castro-Camargo, M. and Gerdes, K. (2013) (p)ppGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell, 154, 1140-1150.
13. Hu, Y., Kwan, B.W., Osbourne, D.O., Benedik, M.J. and Wood, T.K. (2015) Toxin YafQ increases persister cell formation by reducing indole signalling. Environ. Microbiol., 17, 1275-1285.
14. Helaine, S., Cheverton, A.M., Watson, K.G., Faure, L.M., Matthews, S.A. and Holden, D.W. (2014) Internalization of Salmonella by macrophages induces formation of nonreplicating persisters. Science, 343, 204-208.
15. Castro-Roa, D., Garcia-Pino, A., De Gieter, S., van Nuland, N.A., Loris, R. and Zenkin, N. (2013) The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu. Nat. Chem. Biol., 9, 811-817.
16. Cruz, J.W., Rothenbacher, F.P., Maehigashi, T., Lane, W.S., Dunham, C.M. and Woychik, N.A. (2014) Doc toxin is a kinase that inactivates elongation factor Tu. J. Biol. Chem., 289, 7788-7798.
17. Germain, E., Castro-Roa, D., Zenkin, N. and Gerdes, K. (2013) Molecular mechanism of bacterial persistence by HipA. Mol. Cell, 52, 248-254.
18. Neubauer, C., Gillet, R., Kelley, A.C. and Ramakrishnan, V. (2012) Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science, 335, 1366-1369.
19. Feng, S., Chen, Y., Kamada, K., Wang, H., Tang, K., Wang, M. and Gao, Y.G. (2013) YoeB-ribosome structure: a canonical RNase that requires the ribosome for its specific activity. Nucleic Acids Res., 41, 9549-9556.
20. Schureck, M.A., Dunkle, J.A., Maehigashi, T., Miles, S.J. and Dunham, C.M. (2015) Defining the mRNA recognition signature of a bacterial toxin protein. Proc. Natl. Acad. Sci. U.S.A., 112, 13862-13867.
21. Winther, K.S., Brodersen, D.E., Brown, A.K. and Gerdes, K. (2013) VapC20 of Mycobacterium tuberculosis cleaves the Sarcin-Ricin loop of 23S rRNA. Nat. Commun., 4, 2796-2804.
22. Schifano, J.M., Edifor, R., Sharp, J.D., Ouyang, M., Konkimalla, A., Husson, R.N. and Woychik, N.A. (2013) Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site. Proc. Natl. Acad. Sci. U.S.A., 110, 8501-8506.
23. Schifano, J.M., Vvedenskaya, I.O., Knoblauch, J.G., Ouyang, M., Nickels, B.E. and Woychik, N.A. (2014) An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3. Nat. Commun., 5, 3538-3549.
24. Cruz, J.W., Sharp, J.D., Hoffer, E.D., Maehigashi, T., Vvedenskaya, I.O., Konkimalla, A., Husson, R.N., Nickels, B.E., Dunham, C.M. and Woychik, N.A. (2015) Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase. Nat. Commun., 6, 7480-7491.
25. Bauerova-Hlinkova, V., Dvorsky, R., Perecko, D., Povazanec, F. and Sevcik, J. (2009) Structure of RNase Sa2 complexes with mononucleotides-new aspects of catalytic reaction and substrate recognition. FEBS J., 276, 4156-4168.
26. Langhorst, U., Loris, R., Denisov, V.P., Doumen, J., Roose, P., Maes, D., Halle, B. and Steyaert, J. (1999) Dissection of the structural and functional role of a conserved hydration site in RNase T1. Protein Sci., 8, 722-730.
27. Cochrane, J.C. and Strobel, S.A. (2008) Catalytic strategies of self-cleaving ribozymes. Acc. Chem. Res., 41, 1027-1035.
28. Griffin, M.A., Davis, J.H. and Strobel, S.A. (2013) Bacterial toxin RelE: A highly efficient ribonuclease with exquisite substrate specificity using atypical catalytic residues. Biochemistry, 52, 8633-8642.
29. Dunican, B.F., Hiller, D.A. and Strobel, S.A. (2015) Transition state charge stabilization and acid-base catalysis of mRNA cleavage by the endoribonuclease RelE. Biochemistry, 54, 7048-7057.
30. 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.
31. 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.
32. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A., 97, 6640-6645.
33. Selmer, M., Dunham, C.M., Murphy, F.V.T., Weixlbaumer, A., Petry, S., Kelley, A.C., Weir, J.R. and Ramakrishnan, V. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935-1942.
34. Kabsch, W. (2010) Xds. Acta Crystallogr. D Biol Crystallogr., 66, 125-132.
35. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol Crystallogr., 66, 486-501.
36. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol Crystallogr., 66, 213-221.
37. Maehigashi, T., Ruangprasert, A., Miles, S.J. and Dunham, C.M. (2015) Molecular basis of ribosome recognition and mRNA hydrolysis by the E. coli YafQ toxin. Nucleic Acids Res., 43, 8002-8012.
38. Otwinowski, Z. and Minor, W. (1997) In: Carter, JCW and Sweet, RM (eds). Methods in Enzymology. Academic Press, NY, Vol. 276, pp. 307-326.
39. Sevcik, J., Dodson, E.J. and Dodson, G.G. (1991) Determination and restrained least-squares refinement of the structures of ribonuclease Sa and its complex with 3′-guanylic acid at 1.8 A resolution. Acta Crystallogr. B, 47, 240-253.
40. Heinemann, U. and Saenger, W. (1983) Crystallographic study of mechanism of ribonuclease T1-catalysed specific RNA hydrolysis. J. Biomol. Struct. Dyn., 1, 523-538.
41. Noguchi, S., Satow, Y., Uchida, T., Sasaki, C. and Matsuzaki, T. (1995) Crystal structure of Ustilago sphaerogena ribonuclease U2 at 1.8 A resolution. Biochemistry, 34, 15583-15591.
42. Li, G.Y., Zhang, Y., Inouye, M. and Ikura, M. (2009) Inhibitory mechanism of Escherichia coli RelE-RelB toxin-antitoxin module involves a helix displacement near an mRNA interferase active site. J. Biol. Chem., 284, 14628-14636.
43. Ruangprasert, A., Maehigashi, T., Miles, S.J., Giridharan, N., Liu, J.X. and Dunham, C.M. (2014) Mechanisms of toxin inhibition and transcriptional repression by Escherichia coli DinJ-YafQ. J. Biol. Chem., 289, 20559-20569.
44. Liang, Y., Gao, Z., Wang, F., Zhang, Y., Dong, Y. and Liu, Q. (2014) Structural and functional characterization of Escherichia coli toxin-antitoxin complex DinJ-YafQ. J. Biol. Chem., 289, 21191-21202.
45. 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.
46. Schureck, M.A., Maehigashi, T., Miles, S.J., Marquez, J., Cho, S.E., Erdman, R. and Dunham, C.M. (2014) Structure of the Proteus vulgaris HigB-(HigA)2-HigB toxin-antitoxin complex. J. Biol. Chem., 289, 1060-1070.
47. Hurley, J.M., Cruz, J.W., Ouyang, M. and Woychik, N.A. (2011) Bacterial toxin RelE mediates frequent codon-independent mRNA cleavage from the 5′ end of coding regions in vivo. J. Biol. Chem., 286, 14770-14778.
48. Tian, Q.B., Ohnishi, M., Murata, T., Nakayama, K., Terawaki, Y. and Hayashi, T. (2001) Specific protein-DNA and protein-protein interaction in the hig gene system, a plasmid-borne proteic killer gene system of plasmid Rts1. Plasmid, 45, 63-74.
49. Qin, D. and Fredrick, K. (2009) Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA. Mol. Microbiol., 71, 1239-1249.
50. Tapprich, W.E., Goss, D.J. and Dahlberg, A.E. (1989) Mutation at position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis. Proc. Natl. Acad. Sci. U.S.A., 86, 4927-4931.
51. Fafarman, A.T., Sigala, P.A., Schwans, J.P., Fenn, T.D., Herschlag, D. and Boxer, S.G. (2012) Quantitative, directional measurement of electric field heterogeneity in the active site of ketosteroid isomerase. Proc. Natl. Acad. Sci. U.S.A., 109, E299-E308.
52. Schwans, J.P., Sunden, F., Gonzalez, A., Tsai, Y. and Herschlag, D. (2013) Uncovering the determinants of a highly perturbed tyrosine pKa in the active site of ketosteroid isomerase. Biochemistry, 52, 7840-7855.
53. Yamaguchi, Y., Park, J.H. and Inouye, M. (2011) Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet., 45, 61-79.
54. Sofos, N., Xu, K., Dedic, E. and Brodersen, D.E. (2015) Cut to the chase-Regulating translation through RNA cleavage. Biochimie, 114, 10-17.
55. Zegers, I., Haikal, A.F., Palmer, R. and Wyns, L. (1994) Crystal structure of RNase T1 with 3′-guanylic acid and guanosine. J. Biol. Chem., 269, 127-133.