Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase
Abstract
How different helicase families with a conserved catalytic ‘helicase core’ evolved to function on varied RNA and DNA substrates by diverse mechanisms remains unclear. In this study, we used Mss116, a yeast DEAD-box protein that utilizes ATP to locally unwind dsRNA, to investigate helicase specificity and mechanism. Our results define the molecular basis for the substrate specificity of a DEAD-box protein. Additionally, they show that Mss116 has ambiguous substrate-binding properties and interacts with all four NTPs and both RNA and DNA. The efficiency of unwinding correlates with the stability of the ‘closed-state’ helicase core, a complex with nucleotide and nucleic acid that forms as duplexes are unwound. Crystal structures reveal that core stability is modulated by family-specific interactions that favor certain substrates. This suggests how present-day helicases diversified from an ancestral core with broad specificity by retaining core closure as a common catalytic mechanism while optimizing substrate-binding interactions for different cellular functions.
- Authors:
-
- Univ. of Texas, Austin, TX (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)
- OSTI Identifier:
- 1628825
- Grant/Contract Number:
- AC02-05CH11231; GM037951
- Resource Type:
- Accepted Manuscript
- Journal Name:
- eLife
- Additional Journal Information:
- Journal Volume: 3; Journal ID: ISSN 2050-084X
- Publisher:
- eLife Sciences Publications, Ltd.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Life Sciences & Biomedicine - Other Topics
Citation Formats
Mallam, Anna L., Sidote, David J., and Lambowitz, Alan M. Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase. United States: N. p., 2014.
Web. doi:10.7554/elife.04630.
Mallam, Anna L., Sidote, David J., & Lambowitz, Alan M. Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase. United States. https://doi.org/10.7554/elife.04630
Mallam, Anna L., Sidote, David J., and Lambowitz, Alan M. Fri .
"Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase". United States. https://doi.org/10.7554/elife.04630. https://www.osti.gov/servlets/purl/1628825.
@article{osti_1628825,
title = {Molecular insights into RNA and DNA helicase evolution from the determinants of specificity for a DEAD-box RNA helicase},
author = {Mallam, Anna L. and Sidote, David J. and Lambowitz, Alan M.},
abstractNote = {How different helicase families with a conserved catalytic ‘helicase core’ evolved to function on varied RNA and DNA substrates by diverse mechanisms remains unclear. In this study, we used Mss116, a yeast DEAD-box protein that utilizes ATP to locally unwind dsRNA, to investigate helicase specificity and mechanism. Our results define the molecular basis for the substrate specificity of a DEAD-box protein. Additionally, they show that Mss116 has ambiguous substrate-binding properties and interacts with all four NTPs and both RNA and DNA. The efficiency of unwinding correlates with the stability of the ‘closed-state’ helicase core, a complex with nucleotide and nucleic acid that forms as duplexes are unwound. Crystal structures reveal that core stability is modulated by family-specific interactions that favor certain substrates. This suggests how present-day helicases diversified from an ancestral core with broad specificity by retaining core closure as a common catalytic mechanism while optimizing substrate-binding interactions for different cellular functions.},
doi = {10.7554/elife.04630},
journal = {eLife},
number = ,
volume = 3,
place = {United States},
year = {Fri Dec 12 00:00:00 EST 2014},
month = {Fri Dec 12 00:00:00 EST 2014}
}
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Characterization of the NTPase, RNA-Binding, and RNA Helicase Activities of the DEAH-Box Splicing Factor Prp22 †
journal, July 2005
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- Biochemistry, Vol. 44, Issue 28
DEAD-Box Helicases Form Nucleotide-Dependent, Long-Lived Complexes with RNA
journal, January 2014
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Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p
journal, September 2012
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journal, July 2011
- Linder, Patrick; Jankowsky, Eckhard
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ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding
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Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail
journal, July 2011
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- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
An A-DNA triplet code: thermodynamic rules for predicting A- and B-DNA.
journal, July 1995
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- Proceedings of the National Academy of Sciences, Vol. 92, Issue 14
A Steady-state and Pre-steady-state Kinetic Analysis of the NTPase Activity Associated with the Hepatitis C Virus NS3 Helicase Domain
journal, October 1996
- Preugschat, Frank; Averett, Devron R.; Clarke, Berwyn E.
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IDT SciTools: a suite for analysis and design of nucleic acid oligomers
journal, May 2008
- Owczarzy, R.; Tataurov, A. V.; Wu, Y.
- Nucleic Acids Research, Vol. 36, Issue Web Server
Circular dichroism and conformational polymorphism of DNA
journal, January 2009
- Kypr, J.; Kejnovska, I.; Renciuk, D.
- Nucleic Acids Research, Vol. 37, Issue 6
Cytosolic Viral Sensor RIG-I Is a 5'-Triphosphate-Dependent Translocase on Double-Stranded RNA
journal, February 2009
- Myong, S.; Cui, S.; Cornish, P. V.
- Science, Vol. 323, Issue 5917
The anatomy of A-, B-, and Z-DNA
journal, April 1982
- Dickerson, R.; Drew, H.; Conner, B.
- Science, Vol. 216, Issue 4545
Enzyme Promiscuity: A Mechanistic and Evolutionary Perspective
journal, June 2010
- Khersonsky, Olga; Tawfik, Dan S.
- Annual Review of Biochemistry, Vol. 79, Issue 1, p. 471-505
Structure and Mechanism of Helicases and Nucleic Acid Translocases
journal, June 2007
- Singleton, Martin R.; Dillingham, Mark S.; Wigley, Dale B.
- Annual Review of Biochemistry, Vol. 76, Issue 1
Enzyme Recruitment in Evolution of New Function
journal, October 1976
- Jensen, R. A.
- Annual Review of Microbiology, Vol. 30, Issue 1
Mechanism of Mss116 ATPase reveals functional diversity of DEAD-Box proteins.
text, January 2018
- Cao, Wenxiang; Coman, Maria Magdalena; Ding, Steve
- Figshare
Comparative Structural Analysis of Human DEAD-Box RNA Helicases
journal, September 2010
- Schütz, Patrick; Karlberg, Tobias; van den Berg, Susanne
- PLoS ONE, Vol. 5, Issue 9
Arabidopsis DEAD-box RNA helicase UAP56 interacts with both RNA and DNA as well as with mRNA export factors
text, January 2013
- Kammel, Christine; Thomaier, Maren; Sørensen, Brian B.
- Universität Regensburg
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