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}
}
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