Mechanism of endonuclease cleavage by the HigB toxin

Schureck, Marc A.; Repack, Adrienne; Miles, Stacey J.; Marquez, Jhomar; Dunham, Christine M.

doi:10.1093/nar/gkw598

Mechanism of endonuclease cleavage by the HigB toxin

Journal Article · Mon Jul 04 00:00:00 EDT 2016 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkw598· OSTI ID:1329416

Schureck, Marc A. ^[1]; Repack, Adrienne ^[1]; Miles, Stacey J. ^[1]; Marquez, Jhomar ^[1]; Dunham, Christine M. ^[1]

Emory Univ. School of Medicine, Atlanta, GA (United States)

Bacteria encode multiple type II toxin–antitoxin modules that cleave ribosome-bound mRNAs in response to stress. All ribosome-dependent toxin family members structurally characterized to date adopt similar microbial RNase architectures despite possessing low sequence identities. Therefore, determining which residues are catalytically important in this specialized RNase family has been a challenge in the field. Structural studies of RelE and YoeB toxins bound to the ribosome provided significant insights but biochemical experiments with RelE were required to clearly demonstrate which residues are critical for acid-base catalysis of mRNA cleavage. Here, we solved an X-ray crystal structure of the wild-type, ribosome-dependent toxin HigB bound to the ribosome revealing potential catalytic residues proximal to the mRNA substrate. Using cell-based and biochemical assays, we further determined that HigB residues His54, Asp90, Tyr91 and His92 are critical for activity in vivo, while HigB H54A and Y91A variants have the largest effect on mRNA cleavage in vitro. Comparison of X-ray crystal structures of two catalytically inactive HigB variants with 70S-HigB bound structures reveal that HigB active site residues undergo conformational rearrangements likely required for recognition of its mRNA substrate. These data support the emerging concept that ribosome-dependent toxins have diverse modes of mRNA recognition.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); National Science Foundation (NSF); Office of Research Infrastructure Programs (ORIP); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1329416

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 16 Vol. 44; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (71)

Cut to the chase–Regulating translation through RNA cleavage Sofos, Nicholas; Xu, Kehan; Dedic, Emil Biochimie, Vol. 114 https://doi.org/10.1016/j.biochi.2015.01.009	journal	July 2015
The Structural Basis for mRNA Recognition and Cleavage by the Ribosome-Dependent Endonuclease RelE Neubauer, Cajetan; Gao, Yong-Gui; Andersen, Kasper R. Cell, Vol. 139, Issue 6 https://doi.org/10.1016/j.cell.2009.11.015	journal	December 2009
RETRACTED: (p)ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity Maisonneuve, Etienne; Castro-Camargo, Manuela; Gerdes, Kenn Cell, Vol. 154, Issue 5 https://doi.org/10.1016/j.cell.2013.07.048	journal	August 2013
Conformational Change in the Catalytic Site of the Ribonuclease YoeB Toxin by YefM Antitoxin Kamada, Katsuhiko; Hanaoka, Fumio Molecular Cell, Vol. 19, Issue 4 https://doi.org/10.1016/j.molcel.2005.07.004	journal	August 2005
Molecular Mechanism of Bacterial Persistence by HipA Germain, Elsa; Castro-Roa, Daniel; Zenkin, Nikolay Molecular Cell, Vol. 52, Issue 2 https://doi.org/10.1016/j.molcel.2013.08.045	journal	October 2013
Catalytic Strategies of Self-Cleaving Ribozymes Cochrane, Jesse C.; Strobel, Scott A. Accounts of Chemical Research, Vol. 41, Issue 8 https://doi.org/10.1021/ar800050c	journal	August 2008
Crystal Structure of Ustilago sphaerogena Ribonuclease U2 at 1.8 .ANG. Resolution Noguchi, Shuji; Satow, Yoshinori; Uchida, Tsuneko Biochemistry, Vol. 34, Issue 47 https://doi.org/10.1021/bi00047a025	journal	November 1995
Bacterial Toxin RelE: A Highly Efficient Ribonuclease with Exquisite Substrate Specificity Using Atypical Catalytic Residues Griffin, Meghan A.; Davis, Jared H.; Strobel, Scott A. Biochemistry, Vol. 52, Issue 48 https://doi.org/10.1021/bi401325c	journal	November 2013
VapC20 of Mycobacterium tuberculosis cleaves the Sarcin–Ricin loop of 23S rRNA Winther, Kristoffer S.; Brodersen, Ditlev E.; Brown, Alistair K. Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms3796	journal	November 2013
Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase Cruz, Jonathan W.; Sharp, Jared D.; Hoffer, Eric D. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8480	journal	July 2015
Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA Winther, K. S.; Gerdes, K. Proceedings of the National Academy of Sciences, Vol. 108, Issue 18 https://doi.org/10.1073/pnas.1019587108	journal	April 2011
Quantitative, directional measurement of electric field heterogeneity in the active site of ketosteroid isomerase Fafarman, A. T.; Sigala, P. A.; Schwans, J. P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 6 https://doi.org/10.1073/pnas.1111566109	journal	January 2012
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Datsenko, K. A.; Wanner, B. L. Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645 https://doi.org/10.1073/pnas.120163297	journal	May 2000
Defining the mRNA recognition signature of a bacterial toxin protein Schureck, Marc A.; Dunkle, Jack A.; Maehigashi, Tatsuya Proceedings of the National Academy of Sciences, Vol. 112, Issue 45 https://doi.org/10.1073/pnas.1512959112	journal	October 2015
Doc toxin is a kinase that inactivates elongation factor Tu. Cruz, Jonathan W.; Rothenbacher, Francesca P.; Maehigashi, Tatsuya Journal of Biological Chemistry, Vol. 289, Issue 28 https://doi.org/10.1074/jbc.a113.544429	journal	July 2014
Bacterial Toxin RelE Mediates Frequent Codon-independent mRNA Cleavage from the 5′ End of Coding Regions in Vivo Hurley, Jennifer M.; Cruz, Jonathan W.; Ouyang, Ming Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.m110.108969	journal	February 2011
Structure of the Proteus vulgaris HigB-(HigA) ₂ -HigB Toxin-Antitoxin Complex Schureck, Marc A.; Maehigashi, Tatsuya; Miles, Stacey J. Journal of Biological Chemistry, Vol. 289, Issue 2 https://doi.org/10.1074/jbc.m113.512095	journal	November 2013
Structural and Functional Characterization of Escherichia coli Toxin-Antitoxin Complex DinJ-YafQ Liang, Yajing; Gao, Zengqiang; Wang, Fei Journal of Biological Chemistry, Vol. 289, Issue 30 https://doi.org/10.1074/jbc.m114.559773	journal	June 2014
Mechanisms of Toxin Inhibition and Transcriptional Repression by Escherichia coli DinJ-YafQ Ruangprasert, Ajchareeya; Maehigashi, Tatsuya; Miles, Stacey J. Journal of Biological Chemistry, Vol. 289, Issue 30 https://doi.org/10.1074/jbc.m114.573006	journal	June 2014
Inhibitory Mechanism of Escherichia coli RelE-RelB Toxin-Antitoxin Module Involves a Helix Displacement Near an mRNA Interferase Active Site Li, Guang-Yao; Zhang, Yonglong; Inouye, Masayori Journal of Biological Chemistry, Vol. 284, Issue 21 https://doi.org/10.1074/jbc.m809656200	journal	March 2009
Molecular basis of ribosome recognition and mRNA hydrolysis by the E. coli YafQ toxin Maehigashi, Tatsuya; Ruangprasert, Ajchareeya; Miles, Stacey J. Nucleic Acids Research, Vol. 43, Issue 16 https://doi.org/10.1093/nar/gkv791	journal	August 2015
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA Qin, Daoming; Fredrick, Kurt Molecular Microbiology, Vol. 71, Issue 5 https://doi.org/10.1111/j.1365-2958.2009.06598.x	journal	March 2009
Structure of RNase Sa2 complexes with mononucleotides - new aspects of catalytic reaction and substrate recognition Bauerová-Hlinková, Vladena; Dvorský, Radovan; Perečko, Dušan FEBS Journal, Vol. 276, Issue 15 https://doi.org/10.1111/j.1742-4658.2009.07125.x	journal	August 2009
Structure of the 70S Ribosome Complexed with mRNA and tRNA Selmer, M. Science, Vol. 313, Issue 5795 https://doi.org/10.1126/science.1131127	journal	September 2006
Decoding in the Absence of a Codon by tmRNA and SmpB in the Ribosome Neubauer, C.; Gillet, R.; Kelley, A. C. Science, Vol. 335, Issue 6074 https://doi.org/10.1126/science.1217039	journal	March 2012
Specialized Persister Cells and the Mechanism of Multidrug Tolerance in Escherichia coli Keren, I.; Shah, D.; Spoering, A. Journal of Bacteriology, Vol. 186, Issue 24 https://doi.org/10.1128/jb.186.24.8172-8180.2004	journal	December 2004
Toxin-Antitoxin Systems in Bacteria and Archaea Yamaguchi, Yoshihiro; Park, Jung-Ho; Inouye, Masayori Annual Review of Genetics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-genet-110410-132412	journal	December 2011
PezT: A Bacterial Suicide Gene Sedwick, Caitlin PLoS Biology, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pbio.1001036	journal	March 2011
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu Castro-Roa, Daniel; Garcia-Pino, Abel; De Gieter, Steven Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/desy-2014-02574	text	January 2013
Specific Protein–DNA and Protein–Protein Interaction in the hig Gene System, a Plasmid-Borne Proteic Killer Gene System of Plasmid Rts1 Tian, Qing Bao; Ohnishi, Makoto; Murata, Takahiro Plasmid, Vol. 45, Issue 2 https://doi.org/10.1006/plas.2000.1506	journal	March 2001
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes Bernard, Philippe; Couturier, Martine Journal of Molecular Biology, Vol. 226, Issue 3 https://doi.org/10.1016/0022-2836(92)90629-X	journal	August 1992
Crystal structure of RNase T1 with 3'-guanylic acid and guanosine. Zegers, I.; Haikal, A. F.; Palmer, R. Journal of Biological Chemistry, Vol. 269, Issue 1 https://doi.org/10.1016/S0021-9258(17)42323-4	journal	January 1994
The Bacterial Toxin RelE Displays Codon-Specific Cleavage of mRNAs in the Ribosomal A Site Pedersen, Kim; Zavialov, Andrey V.; Pavlov, Michael Yu. Cell, Vol. 112, Issue 1 https://doi.org/10.1016/S0092-8674(02)01248-5	journal	January 2003
Molecular Mechanisms Underlying Bacterial Persisters Maisonneuve, Etienne; Gerdes, Kenn Cell, Vol. 157, Issue 3 https://doi.org/10.1016/j.cell.2014.02.050	journal	April 2014
Retraction Notice to: (p)ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity Maisonneuve, Etienne; Castro-Camargo, Manuela; Gerdes, Kenn Cell, Vol. 172, Issue 5 https://doi.org/10.1016/j.cell.2018.02.023	journal	February 2018
Transition State Charge Stabilization and Acid–Base Catalysis of mRNA Cleavage by the Endoribonuclease RelE Dunican, Brian F.; Hiller, David A.; Strobel, Scott A. Biochemistry, Vol. 54, Issue 47 https://doi.org/10.1021/acs.biochem.5b00866	journal	November 2015
Uncovering the Determinants of a Highly Perturbed Tyrosine p K _a in the Active Site of Ketosteroid Isomerase Schwans, Jason P.; Sunden, Fanny; Gonzalez, Ana Biochemistry, Vol. 52, Issue 44 https://doi.org/10.1021/bi401083b	journal	October 2013
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu Castro-Roa, Daniel; Garcia-Pino, Abel; De Gieter, Steven Nature Chemical Biology, Vol. 9, Issue 12 https://doi.org/10.1038/nchembio.1364	journal	October 2013
An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3 Schifano, Jason M.; Vvedenskaya, Irina O.; Knoblauch, Jared G. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4538	journal	April 2014
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases Nagata, Takuya; Shinya, Shoko; Ohnuma, Takayuki Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-81903-3	journal	January 2021
Bacterial persistence by RNA endonucleases Maisonneuve, Etienne; Shakespeare, Lana J.; Jørgensen, Mikkel Girke Proceedings of the National Academy of Sciences, Vol. 108, Issue 32, p. 13206-13211 https://doi.org/10.1073/pnas.1100186108	journal	July 2011
Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site Schifano, J. M.; Edifor, R.; Sharp, J. D. Proceedings of the National Academy of Sciences, Vol. 110, Issue 21 https://doi.org/10.1073/pnas.1222031110	journal	May 2013
Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases Germain, Elsa; Roghanian, Mohammad; Gerdes, Kenn Proceedings of the National Academy of Sciences, Vol. 112, Issue 16 https://doi.org/10.1073/pnas.1423536112	journal	April 2015
Mutation at position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis. Tapprich, W. E.; Goss, D. J.; Dahlberg, A. E. Proceedings of the National Academy of Sciences, Vol. 86, Issue 13 https://doi.org/10.1073/pnas.86.13.4927	journal	July 1989
Bacterial Toxin HigB Associates with Ribosomes and Mediates Translation-dependent mRNA Cleavage at A-rich Sites Hurley, Jennifer M.; Woychik, Nancy A. Journal of Biological Chemistry, Vol. 284, Issue 28 https://doi.org/10.1074/jbc.M109.008763	journal	May 2009
Bacterial Toxin RelE Mediates Frequent Codon-independent mRNA Cleavage from the 5′ End of Coding Regions in Vivo Hurley, Jennifer M.; Cruz, Jonathan W.; Ouyang, Ming Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.M110.108969	journal	February 2011
Structure of the Proteus vulgaris HigB-(HigA) ₂ -HigB Toxin-Antitoxin Complex Schureck, Marc A.; Maehigashi, Tatsuya; Miles, Stacey J. Journal of Biological Chemistry, Vol. 289, Issue 2 https://doi.org/10.1074/jbc.M113.512095	journal	November 2013
Doc Toxin Is a Kinase That Inactivates Elongation Factor Tu Cruz, Jonathan W.; Rothenbacher, Francesca P.; Maehigashi, Tatsuya Journal of Biological Chemistry, Vol. 289, Issue 11 https://doi.org/10.1074/jbc.M113.544429	journal	January 2014
Structural and Functional Characterization of Escherichia coli Toxin-Antitoxin Complex DinJ-YafQ Liang, Yajing; Gao, Zengqiang; Wang, Fei Journal of Biological Chemistry, Vol. 289, Issue 30 https://doi.org/10.1074/jbc.M114.559773	journal	June 2014
Mechanisms of Toxin Inhibition and Transcriptional Repression by Escherichia coli DinJ-YafQ Ruangprasert, Ajchareeya; Maehigashi, Tatsuya; Miles, Stacey J. Journal of Biological Chemistry, Vol. 289, Issue 30 https://doi.org/10.1074/jbc.M114.573006	journal	June 2014
Inhibitory Mechanism of Escherichia coli RelE-RelB Toxin-Antitoxin Module Involves a Helix Displacement Near an mRNA Interferase Active Site Li, Guang-Yao; Zhang, Yonglong; Inouye, Masayori Journal of Biological Chemistry, Vol. 284, Issue 21 https://doi.org/10.1074/jbc.M809656200	journal	March 2009
Crystallographic Study of Mechanism of Ribonuclease Ti-Catalysed Specific RNA Hydrolysis Heinemann, Udo; Saenger, Wolfram Journal of Biomolecular Structure and Dynamics, Vol. 1, Issue 2 https://doi.org/10.1080/07391102.1983.10507459	journal	October 1983
YoeB–ribosome structure: a canonical RNase that requires the ribosome for its specific activity Feng, Shu; Chen, Yun; Kamada, Katsuhiko Nucleic Acids Research, Vol. 41, Issue 20 https://doi.org/10.1093/nar/gkt742	journal	August 2013
Determination and restrained least-squares refinement of the structures of ribonuclease Sa and its complex with 3'-guanylic acid at 1.8 Å resolution Sevcik, J.; Dodson, E. J.; Dodson, G. G. Acta Crystallographica Section B Structural Science, Vol. 47, Issue 2 https://doi.org/10.1107/S0108768190009569	journal	April 1991
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Dissection of the structural and functional role of a conserved hydration site in RNase T1 Langhorst, Ulrike; Loris, Remy; Denisov, Vladimir P. Protein Science, Vol. 8, Issue 4 https://doi.org/10.1110/ps.8.4.722	journal	January 1999
Toxin YafQ increases persister cell formation by reducing indole signalling: YafQ increases persisters by decreasing indole signalling Hu, Ying; Kwan, Brian W.; Osbourne, Devon O. Environmental Microbiology, Vol. 17, Issue 4 https://doi.org/10.1111/1462-2920.12567	journal	August 2014
YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB: YeeV targets the cytoskeleton proteins Tan, Qian; Awano, Naoki; Inouye, Masayori Molecular Microbiology, Vol. 79, Issue 1 https://doi.org/10.1111/j.1365-2958.2010.07433.x	journal	November 2010
RatA (YfjG), an Escherichia coli toxin, inhibits 70S ribosome association to block translation initiation: RatA, an inhibitor of 70S ribosome association Zhang, Yonglong; Inouye, Masayori Molecular Microbiology, Vol. 79, Issue 6 https://doi.org/10.1111/j.1365-2958.2010.07506.x	journal	February 2011
The toxin GraT inhibits ribosome biogenesis: The toxin GraT disturbs ribosome biogenesis Ainelo, Andres; Tamman, Hedvig; Leppik, Margus Molecular Microbiology, Vol. 100, Issue 4 https://doi.org/10.1111/mmi.13344	journal	February 2016
Internalization of Salmonella by Macrophages Induces Formation of Nonreplicating Persisters Helaine, S.; Cheverton, A. M.; Watson, K. G. Science, Vol. 343, Issue 6167 https://doi.org/10.1126/science.1244705	journal	January 2014
Specialized Persister Cells and the Mechanism of Multidrug Tolerance in Escherichia coli Keren, I.; Shah, D.; Spoering, A. Journal of Bacteriology, Vol. 186, Issue 24 https://doi.org/10.1128/JB.186.24.8172-8180.2004	journal	December 2004
A Novel Mechanism of Programmed Cell Death in Bacteria by Toxin–Antitoxin Systems Corrupts Peptidoglycan Synthesis Mutschler, Hannes; Gebhardt, Maike; Shoeman, Robert L. PLoS Biology, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pbio.1001033	journal	March 2011
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
The Structural Basis for mRNA Recognition and Cleavage by the Ribosome-Dependent Endonuclease RelE Neubauer, C.; Gao, Y. -G.; Andersen, K. R. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/phppubdb-12236	text	January 2009

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