Mechanism of endonuclease cleavage by the HigB toxin
Abstract
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.
- Authors:
-
- Emory Univ. School of Medicine, Atlanta, GA (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Science Foundation (NSF); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); Office of Research Infrastructure Programs (ORIP); USDOE Office of Science (SC)
- OSTI Identifier:
- 1329416
- Grant/Contract Number:
- MCB 0953714; GM093278; 5T32GM8367; S10 RR029205; AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Volume: 44; Journal Issue: 16; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Schureck, Marc A., Repack, Adrienne, Miles, Stacey J., Marquez, Jhomar, and Dunham, Christine M. Mechanism of endonuclease cleavage by the HigB toxin. United States: N. p., 2016.
Web. doi:10.1093/nar/gkw598.
Schureck, Marc A., Repack, Adrienne, Miles, Stacey J., Marquez, Jhomar, & Dunham, Christine M. Mechanism of endonuclease cleavage by the HigB toxin. United States. https://doi.org/10.1093/nar/gkw598
Schureck, Marc A., Repack, Adrienne, Miles, Stacey J., Marquez, Jhomar, and Dunham, Christine M. Mon .
"Mechanism of endonuclease cleavage by the HigB toxin". United States. https://doi.org/10.1093/nar/gkw598. https://www.osti.gov/servlets/purl/1329416.
@article{osti_1329416,
title = {Mechanism of endonuclease cleavage by the HigB toxin},
author = {Schureck, Marc A. and Repack, Adrienne and Miles, Stacey J. and Marquez, Jhomar and Dunham, Christine M.},
abstractNote = {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.},
doi = {10.1093/nar/gkw598},
journal = {Nucleic Acids Research},
number = 16,
volume = 44,
place = {United States},
year = {Mon Jul 04 00:00:00 EDT 2016},
month = {Mon Jul 04 00:00:00 EDT 2016}
}
Web of Science
Works referenced in this record:
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu
text, January 2013
- Castro-Roa, Daniel; Garcia-Pino, Abel; De Gieter, Steven
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA
journal, March 2009
- Qin, Daoming; Fredrick, Kurt
- Molecular Microbiology, Vol. 71, Issue 5
RETRACTED: (p)ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity
journal, August 2013
- Maisonneuve, Etienne; Castro-Camargo, Manuela; Gerdes, Kenn
- Cell, Vol. 154, Issue 5
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository
The Structural Basis for mRNA Recognition and Cleavage by the Ribosome-Dependent Endonuclease RelE
journal, December 2009
- Neubauer, Cajetan; Gao, Yong-Gui; Andersen, Kasper R.
- Cell, Vol. 139, Issue 6
Specialized Persister Cells and the Mechanism of Multidrug Tolerance in Escherichia coli
journal, December 2004
- Keren, I.; Shah, D.; Spoering, A.
- Journal of Bacteriology, Vol. 186, Issue 24
Defining the mRNA recognition signature of a bacterial toxin protein
journal, October 2015
- Schureck, Marc A.; Dunkle, Jack A.; Maehigashi, Tatsuya
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 45
Structure of RNase Sa2 complexes with mononucleotides - new aspects of catalytic reaction and substrate recognition
journal, August 2009
- Bauerová-Hlinková, Vladena; Dvorský, Radovan; Perečko, Dušan
- FEBS Journal, Vol. 276, Issue 15
Quantitative, directional measurement of electric field heterogeneity in the active site of ketosteroid isomerase
journal, January 2012
- Fafarman, A. T.; Sigala, P. A.; Schwans, J. P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 6
Catalytic Strategies of Self-Cleaving Ribozymes
journal, August 2008
- Cochrane, Jesse C.; Strobel, Scott A.
- Accounts of Chemical Research, Vol. 41, Issue 8
Cut to the chase–Regulating translation through RNA cleavage
journal, July 2015
- Sofos, Nicholas; Xu, Kehan; Dedic, Emil
- Biochimie, Vol. 114
Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA
journal, April 2011
- Winther, K. S.; Gerdes, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
RatA (YfjG), an Escherichia coli toxin, inhibits 70S ribosome association to block translation initiation: RatA, an inhibitor of 70S ribosome association
journal, February 2011
- Zhang, Yonglong; Inouye, Masayori
- Molecular Microbiology, Vol. 79, Issue 6
Crystal Structure of Ustilago sphaerogena Ribonuclease U2 at 1.8 .ANG. Resolution
journal, November 1995
- Noguchi, Shuji; Satow, Yoshinori; Uchida, Tsuneko
- Biochemistry, Vol. 34, Issue 47
Uncovering the Determinants of a Highly Perturbed Tyrosine p K a in the Active Site of Ketosteroid Isomerase
journal, October 2013
- Schwans, Jason P.; Sunden, Fanny; Gonzalez, Ana
- Biochemistry, Vol. 52, Issue 44
Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA
journal, April 2011
- Winther, K. S.; Gerdes, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
Toxin-Antitoxin Systems in Bacteria and Archaea
journal, December 2011
- Yamaguchi, Yoshihiro; Park, Jung-Ho; Inouye, Masayori
- Annual Review of Genetics, Vol. 45, Issue 1
Doc toxin is a kinase that inactivates elongation factor Tu.
journal, July 2014
- Cruz, Jonathan W.; Rothenbacher, Francesca P.; Maehigashi, Tatsuya
- Journal of Biological Chemistry, Vol. 289, Issue 28
Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes
journal, August 1992
- Bernard, Philippe; Couturier, Martine
- Journal of Molecular Biology, Vol. 226, Issue 3
Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase
journal, July 2015
- Cruz, Jonathan W.; Sharp, Jared D.; Hoffer, Eric D.
- Nature Communications, Vol. 6, Issue 1
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
Mycobacterial toxin MazF-mt6 inhibits translation through cleavage of 23S rRNA at the ribosomal A site
journal, May 2013
- Schifano, J. M.; Edifor, R.; Sharp, J. D.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 21
Dissection of the structural and functional role of a conserved hydration site in RNase T1
journal, January 1999
- Langhorst, Ulrike; Loris, Remy; Denisov, Vladimir P.
- Protein Science, Vol. 8, Issue 4
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000
- Datsenko, K. A.; Wanner, B. L.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
Catalytic Strategies of Self-Cleaving Ribozymes
journal, August 2008
- Cochrane, Jesse C.; Strobel, Scott A.
- Accounts of Chemical Research, Vol. 41, Issue 8
Molecular basis of ribosome recognition and mRNA hydrolysis by the E. coli YafQ toxin
journal, August 2015
- Maehigashi, Tatsuya; Ruangprasert, Ajchareeya; Miles, Stacey J.
- Nucleic Acids Research, Vol. 43, Issue 16
Bacterial Toxin RelE: A Highly Efficient Ribonuclease with Exquisite Substrate Specificity Using Atypical Catalytic Residues
journal, November 2013
- Griffin, Meghan A.; Davis, Jared H.; Strobel, Scott A.
- Biochemistry, Vol. 52, Issue 48
NMRPipe: A multidimensional spectral processing system based on UNIX pipes
journal, November 1995
- Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW.
- Journal of Biomolecular NMR, Vol. 6, Issue 3
Molecular Mechanism of Bacterial Persistence by HipA
journal, October 2013
- Germain, Elsa; Castro-Roa, Daniel; Zenkin, Nikolay
- Molecular Cell, Vol. 52, Issue 2
Molecular Mechanisms Underlying Bacterial Persisters
journal, April 2014
- Maisonneuve, Etienne; Gerdes, Kenn
- Cell, Vol. 157, Issue 3
VapC20 of Mycobacterium tuberculosis cleaves the Sarcin–Ricin loop of 23S rRNA
journal, November 2013
- Winther, Kristoffer S.; Brodersen, Ditlev E.; Brown, Alistair K.
- Nature Communications, Vol. 4, Issue 1
Structure of the 70S Ribosome Complexed with mRNA and tRNA
journal, September 2006
- Selmer, M.
- Science, Vol. 313, Issue 5795
Structure of the Proteus vulgaris HigB-(HigA) 2 -HigB Toxin-Antitoxin Complex
journal, November 2013
- Schureck, Marc A.; Maehigashi, Tatsuya; Miles, Stacey J.
- Journal of Biological Chemistry, Vol. 289, Issue 2
Defining the mRNA recognition signature of a bacterial toxin protein
journal, October 2015
- Schureck, Marc A.; Dunkle, Jack A.; Maehigashi, Tatsuya
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 45
Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases
journal, April 2015
- Germain, Elsa; Roghanian, Mohammad; Gerdes, Kenn
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 16
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu
text, January 2013
- Castro-Roa, Daniel; Garcia-Pino, Abel; De Gieter, Steven
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Mutation at position 791 in Escherichia coli 16S ribosomal RNA affects processes involved in the initiation of protein synthesis.
journal, July 1989
- Tapprich, W. E.; Goss, D. J.; Dahlberg, A. E.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 13
Control of translation initiation involves a factor-induced rearrangement of helix 44 of 16S ribosomal RNA
journal, March 2009
- Qin, Daoming; Fredrick, Kurt
- Molecular Microbiology, Vol. 71, Issue 5
Structure of the 70S Ribosome Complexed with mRNA and tRNA
journal, September 2006
- Selmer, M.
- Science, Vol. 313, Issue 5795
RETRACTED: (p)ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity
journal, August 2013
- Maisonneuve, Etienne; Castro-Camargo, Manuela; Gerdes, Kenn
- Cell, Vol. 154, Issue 5
Bacterial Toxin HigB Associates with Ribosomes and Mediates Translation-dependent mRNA Cleavage at A-rich Sites
journal, May 2009
- Hurley, Jennifer M.; Woychik, Nancy A.
- Journal of Biological Chemistry, Vol. 284, Issue 28
VapC20 of Mycobacterium tuberculosis cleaves the Sarcin–Ricin loop of 23S rRNA
journal, November 2013
- Winther, Kristoffer S.; Brodersen, Ditlev E.; Brown, Alistair K.
- Nature Communications, Vol. 4, Issue 1
Determination and restrained least-squares refinement of the structures of ribonuclease Sa and its complex with 3'-guanylic acid at 1.8 Å resolution
journal, April 1991
- Sevcik, J.; Dodson, E. J.; Dodson, G. G.
- Acta Crystallographica Section B Structural Science, Vol. 47, Issue 2
Decoding in the Absence of a Codon by tmRNA and SmpB in the Ribosome
journal, March 2012
- Neubauer, C.; Gillet, R.; Kelley, A. C.
- Science, Vol. 335, Issue 6074
Doc toxin is a kinase that inactivates elongation factor Tu.
journal, July 2014
- Cruz, Jonathan W.; Rothenbacher, Francesca P.; Maehigashi, Tatsuya
- Journal of Biological Chemistry, Vol. 289, Issue 28
Transition State Charge Stabilization and Acid–Base Catalysis of mRNA Cleavage by the Endoribonuclease RelE
journal, November 2015
- Dunican, Brian F.; Hiller, David A.; Strobel, Scott A.
- Biochemistry, Vol. 54, Issue 47
The toxin GraT inhibits ribosome biogenesis: The toxin GraT disturbs ribosome biogenesis
journal, February 2016
- Ainelo, Andres; Tamman, Hedvig; Leppik, Margus
- Molecular Microbiology, Vol. 100, Issue 4
Retraction Notice to: (p)ppGpp Controls Bacterial Persistence by Stochastic Induction of Toxin-Antitoxin Activity
journal, February 2018
- Maisonneuve, Etienne; Castro-Camargo, Manuela; Gerdes, Kenn
- Cell, Vol. 172, Issue 5
Doc Toxin Is a Kinase That Inactivates Elongation Factor Tu
journal, January 2014
- Cruz, Jonathan W.; Rothenbacher, Francesca P.; Maehigashi, Tatsuya
- Journal of Biological Chemistry, Vol. 289, Issue 11
Conformational Change in the Catalytic Site of the Ribonuclease YoeB Toxin by YefM Antitoxin
journal, August 2005
- Kamada, Katsuhiko; Hanaoka, Fumio
- Molecular Cell, Vol. 19, Issue 4
YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB: YeeV targets the cytoskeleton proteins
journal, November 2010
- Tan, Qian; Awano, Naoki; Inouye, Masayori
- Molecular Microbiology, Vol. 79, Issue 1
Toxin-Antitoxin Systems in Bacteria and Archaea
journal, December 2011
- Yamaguchi, Yoshihiro; Park, Jung-Ho; Inouye, Masayori
- Annual Review of Genetics, Vol. 45, Issue 1
Toxin YafQ increases persister cell formation by reducing indole signalling: YafQ increases persisters by decreasing indole signalling
journal, August 2014
- Hu, Ying; Kwan, Brian W.; Osbourne, Devon O.
- Environmental Microbiology, Vol. 17, Issue 4
Inhibitory Mechanism of Escherichia coli RelE-RelB Toxin-Antitoxin Module Involves a Helix Displacement Near an mRNA Interferase Active Site
journal, March 2009
- Li, Guang-Yao; Zhang, Yonglong; Inouye, Masayori
- Journal of Biological Chemistry, Vol. 284, Issue 21
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Internalization of Salmonella by Macrophages Induces Formation of Nonreplicating Persisters
journal, January 2014
- Helaine, S.; Cheverton, A. M.; Watson, K. G.
- Science, Vol. 343, Issue 6167
A Novel Mechanism of Programmed Cell Death in Bacteria by Toxin–Antitoxin Systems Corrupts Peptidoglycan Synthesis
journal, March 2011
- Mutschler, Hannes; Gebhardt, Maike; Shoeman, Robert L.
- PLoS Biology, Vol. 9, Issue 3
Bacterial persistence by RNA endonucleases
journal, July 2011
- Maisonneuve, Etienne; Shakespeare, Lana J.; Jørgensen, Mikkel Girke
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 32, p. 13206-13211
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
Bacterial Toxin RelE Mediates Frequent Codon-independent mRNA Cleavage from the 5′ End of Coding Regions in Vivo
journal, February 2011
- Hurley, Jennifer M.; Cruz, Jonathan W.; Ouyang, Ming
- Journal of Biological Chemistry, Vol. 286, Issue 17
Features and development of Coot
journal, March 2010
- Emsley, P.; Lohkamp, B.; Scott, W. G.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
Cut to the chase–Regulating translation through RNA cleavage
journal, July 2015
- Sofos, Nicholas; Xu, Kehan; Dedic, Emil
- Biochimie, Vol. 114
Mechanisms of Toxin Inhibition and Transcriptional Repression by Escherichia coli DinJ-YafQ
journal, June 2014
- Ruangprasert, Ajchareeya; Maehigashi, Tatsuya; Miles, Stacey J.
- Journal of Biological Chemistry, Vol. 289, Issue 30
Crystallographic Study of Mechanism of Ribonuclease Ti-Catalysed Specific RNA Hydrolysis
journal, October 1983
- Heinemann, Udo; Saenger, Wolfram
- Journal of Biomolecular Structure and Dynamics, Vol. 1, Issue 2
Bacterial Toxin RelE: A Highly Efficient Ribonuclease with Exquisite Substrate Specificity Using Atypical Catalytic Residues
journal, November 2013
- Griffin, Meghan A.; Davis, Jared H.; Strobel, Scott A.
- Biochemistry, Vol. 52, Issue 48
Molecular Mechanism of Bacterial Persistence by HipA
journal, October 2013
- Germain, Elsa; Castro-Roa, Daniel; Zenkin, Nikolay
- Molecular Cell, Vol. 52, Issue 2
The Bacterial Toxin RelE Displays Codon-Specific Cleavage of mRNAs in the Ribosomal A Site
journal, January 2003
- Pedersen, Kim; Zavialov, Andrey V.; Pavlov, Michael Yu.
- Cell, Vol. 112, Issue 1
The Structural Basis for mRNA Recognition and Cleavage by the Ribosome-Dependent Endonuclease RelE
text, January 2009
- Neubauer, C.; Gao, Y. -G.; Andersen, K. R.
- Deutsches Elektronen-Synchrotron, DESY, Hamburg
Structural and Functional Characterization of Escherichia coli Toxin-Antitoxin Complex DinJ-YafQ
journal, June 2014
- Liang, Yajing; Gao, Zengqiang; Wang, Fei
- Journal of Biological Chemistry, Vol. 289, Issue 30
Growth-regulating Mycobacterium tuberculosis VapC-mt4 toxin is an isoacceptor-specific tRNase
journal, July 2015
- Cruz, Jonathan W.; Sharp, Jared D.; Hoffer, Eric D.
- Nature Communications, Vol. 6, Issue 1
Specific Protein–DNA and Protein–Protein Interaction in the hig Gene System, a Plasmid-Borne Proteic Killer Gene System of Plasmid Rts1
journal, March 2001
- Tian, Qing Bao; Ohnishi, Makoto; Murata, Takahiro
- Plasmid, Vol. 45, Issue 2
Conformational Change in the Catalytic Site of the Ribonuclease YoeB Toxin by YefM Antitoxin
journal, August 2005
- Kamada, Katsuhiko; Hanaoka, Fumio
- Molecular Cell, Vol. 19, Issue 4
Quantitative, directional measurement of electric field heterogeneity in the active site of ketosteroid isomerase
journal, January 2012
- Fafarman, A. T.; Sigala, P. A.; Schwans, J. P.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 6
Structure of RNase Sa2 complexes with mononucleotides - new aspects of catalytic reaction and substrate recognition
journal, August 2009
- Bauerová-Hlinková, Vladena; Dvorský, Radovan; Perečko, Dušan
- FEBS Journal, Vol. 276, Issue 15
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products
journal, May 2000
- Datsenko, K. A.; Wanner, B. L.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645
The Fic protein Doc uses an inverted substrate to phosphorylate and inactivate EF-Tu
journal, October 2013
- Castro-Roa, Daniel; Garcia-Pino, Abel; De Gieter, Steven
- Nature Chemical Biology, Vol. 9, Issue 12
Molecular basis of ribosome recognition and mRNA hydrolysis by the E. coli YafQ toxin
journal, August 2015
- Maehigashi, Tatsuya; Ruangprasert, Ajchareeya; Miles, Stacey J.
- Nucleic Acids Research, Vol. 43, Issue 16
YoeB–ribosome structure: a canonical RNase that requires the ribosome for its specific activity
journal, August 2013
- Feng, Shu; Chen, Yun; Kamada, Katsuhiko
- Nucleic Acids Research, Vol. 41, Issue 20
An RNA-seq method for defining endoribonuclease cleavage specificity identifies dual rRNA substrates for toxin MazF-mt3
journal, April 2014
- Schifano, Jason M.; Vvedenskaya, Irina O.; Knoblauch, Jared G.
- Nature Communications, Vol. 5, Issue 1
The Structural Basis for mRNA Recognition and Cleavage by the Ribosome-Dependent Endonuclease RelE
journal, December 2009
- Neubauer, Cajetan; Gao, Yong-Gui; Andersen, Kasper R.
- Cell, Vol. 139, Issue 6
Crystal Structure of Ustilago sphaerogena Ribonuclease U2 at 1.8 .ANG. Resolution
journal, November 1995
- Noguchi, Shuji; Satow, Yoshinori; Uchida, Tsuneko
- Biochemistry, Vol. 34, Issue 47
Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases
journal, January 2021
- Nagata, Takuya; Shinya, Shoko; Ohnuma, Takayuki
- Scientific Reports, Vol. 11, Issue 1
Decoding in the Absence of a Codon by tmRNA and SmpB in the Ribosome
journal, March 2012
- Neubauer, C.; Gillet, R.; Kelley, A. C.
- Science, Vol. 335, Issue 6074
Crystal structure of RNase T1 with 3'-guanylic acid and guanosine.
journal, January 1994
- Zegers, I.; Haikal, A. F.; Palmer, R.
- Journal of Biological Chemistry, Vol. 269, Issue 1
Works referencing / citing this record:
High genomic variability in the plant pathogenic bacterium Pectobacterium parmentieri deciphered from de novo assembled complete genomes
journal, October 2018
- Zoledowska, S.; Motyka-Pomagruk, A.; Sledz, W.
- BMC Genomics, Vol. 19, Issue 1
Identifying a Molecular Mechanism That Imparts Species-Specific Toxicity to YoeB Toxins
journal, May 2020
- Ames, Jessica R.; McGillick, Julia; Murphy, Tamiko
- Frontiers in Microbiology, Vol. 11
High genomic variability in the plant pathogenic bacterium Pectobacterium parmentieri deciphered from de novo assembled complete genomes
journal, October 2018
- Zoledowska, S.; Motyka-Pomagruk, A.; Sledz, W.
- BMC Genomics, Vol. 19, Issue 1
HigB Reciprocally Controls Biofilm Formation and the Expression of Type III Secretion System Genes through Influencing the Intracellular c-di-GMP Level in Pseudomonas aeruginosa
journal, October 2018
- Zhang, Yueying; Xia, Bin; Li, Mei
- Toxins, Vol. 10, Issue 11
Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability
journal, September 2019
- Pavelich, Ian J.; Maehigashi, Tatsuya; Hoffer, Eric D.
- Nucleic Acids Research, Vol. 47, Issue 19
Expression of different ParE toxins results in conserved phenotypes with distinguishable classes of toxicity
journal, July 2019
- Ames, Jessica R.; Muthuramalingam, Meenakumari; Murphy, Tamiko
- MicrobiologyOpen, Vol. 8, Issue 10
Structural Insights Into the Transcriptional Regulation of HigBA Toxin–Antitoxin System by Antitoxin HigA in Pseudomonas aeruginosa
journal, January 2020
- Liu, Ying; Gao, Zengqiang; Liu, Guangfeng
- Frontiers in Microbiology, Vol. 10
Antitoxin HigA inhibits virulence gene mvfR expression in Pseudomonas aeruginosa
journal, April 2019
- Guo, Yunxue; Sun, Chenglong; Li, Yangmei
- Environmental Microbiology, Vol. 21, Issue 8
HigB of Pseudomonas aeruginosa Enhances Killing of Phagocytes by Up-Regulating the Type III Secretion System in Ciprofloxacin Induced Persister Cells
journal, October 2016
- Li, Mei; Long, Yuqing; Liu, Ying
- Frontiers in Cellular and Infection Microbiology, Vol. 6
A dual role in regulation and toxicity for the disordered N-terminus of the toxin GraT
journal, February 2019
- Talavera, Ariel; Tamman, Hedvig; Ainelo, Andres
- Nature Communications, Vol. 10, Issue 1
HigB of Pseudomonas aeruginosa Enhances Killing of Phagocytes by Up-Regulating the Type III Secretion System in Ciprofloxacin Induced Persister Cells
journal, October 2016
- Li, Mei; Long, Yuqing; Liu, Ying
- Frontiers in Cellular and Infection Microbiology, Vol. 6
Structural basis of transcriptional regulation by the HigA antitoxin
journal, April 2019
- Schureck, Marc A.; Meisner, Jeffrey; Hoffer, Eric D.
- Molecular Microbiology, Vol. 111, Issue 6
Monomeric YoeB toxin retains RNase activity but adopts an obligate dimeric form for thermal stability
journal, September 2019
- Pavelich, Ian J.; Maehigashi, Tatsuya; Hoffer, Eric D.
- Nucleic Acids Research, Vol. 47, Issue 19
Expression of different ParE toxins results in conserved phenotypes with distinguishable classes of toxicity
journal, July 2019
- Ames, Jessica R.; Muthuramalingam, Meenakumari; Murphy, Tamiko
- MicrobiologyOpen, Vol. 8, Issue 10
Endogenous rRNA Sequence Variation Can Regulate Stress Response Gene Expression and Phenotype
journal, October 2018
- Kurylo, Chad M.; Parks, Matthew M.; Juette, Manuel F.
- Cell Reports, Vol. 25, Issue 1