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}
}
Web of Science
Works referenced in this record:
ATP-Dependent Roles of the DEAD-Box Protein Mss116p in Group II Intron Splicing In Vitro and In Vivo
journal, August 2011
- Potratz, Jeffrey P.; Del Campo, Mark; Wolf, Rachel Z.
- Journal of Molecular Biology, Vol. 411, Issue 3
Characterization of the NTPase, RNA-Binding, and RNA Helicase Activities of the DEAH-Box Splicing Factor Prp22 †
journal, July 2005
- Tanaka, Naoko; Schwer, Beate
- Biochemistry, Vol. 44, Issue 28
Structural basis of RNA recognition and activation by innate immune receptor RIG-I
journal, September 2011
- Jiang, Fuguo; Ramanathan, Anand; Miller, Matthew T.
- Nature, Vol. 479, Issue 7373
Structural Basis of RNA Recognition and Activation by Innate Immune Receptor RIG-I
journal, January 2012
- Ramanathan, Anand; Jiang, Fuguo; Miller, Matthew T.
- Biophysical Journal, Vol. 102, Issue 3
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
Involvement of DEAD-box Proteins in Group I and Group II Intron Splicing. Biochemical Characterization of Mss116p, ATP Hydrolysis-dependent and -independent Mechanisms, and General RNA Chaperone Activity
journal, January 2007
- Halls, Coralie; Mohr, Sabine; Del Campo, Mark
- Journal of Molecular Biology, Vol. 365, Issue 3
Structure of the Yeast DEAD Box Protein Mss116p Reveals Two Wedges that Crimp RNA
journal, September 2009
- Del Campo, Mark; Lambowitz, Alan M.
- Molecular Cell, Vol. 35, Issue 5
Mechanism of Mss116 ATPase Reveals Functional Diversity of DEAD-Box Proteins
journal, June 2011
- Cao, Wenxiang; Coman, Maria Magdalena; Ding, Steve
- Journal of Molecular Biology, Vol. 409, Issue 3
Molecular structure of a complete turn of A-DNA
journal, September 1991
- Verdaguer, Nuria; Aymamí, Joan; Fernández-Forner, Dolors
- Journal of Molecular Biology, Vol. 221, Issue 2
High-Throughput Genetic Identification of Functionally Important Regions of the Yeast DEAD-Box Protein Mss116p
journal, November 2011
- Mohr, Georg; Del Campo, Mark; Turner, Kathryn G.
- Journal of Molecular Biology, Vol. 413, Issue 5
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA.
text, January 2010
- Henn, Arnon; Cao, Wenxiang; Licciardello, Nicholas
- Carnegie Mellon University
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen
journal, August 2020
- Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe
- JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6
ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding
journal, December 2008
- Liu, F.; Putnam, A.; Jankowsky, E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 51
The anatomy of A-, B-, and Z-DNA
journal, April 1982
- Dickerson, R.; Drew, H.; Conner, B.
- Science, Vol. 216, Issue 4545
Parts, assembly and operation of the RIG-I family of motors
journal, April 2014
- Rawling, David C.; Pyle, Anna Marie
- Current Opinion in Structural Biology, Vol. 25
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.
- Journal of Biological Chemistry, Vol. 271, Issue 40
Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase
journal, June 2014
- Tuteja, Narendra; Tarique, Mohammed; Banu, Mst. Sufara Akhter
- Plant Molecular Biology, Vol. 85, Issue 6
Scaling and assessment of data quality
journal, December 2005
- Evans, Philip
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82
SF1 and SF2 helicases: family matters
journal, June 2010
- Fairman-Williams, Margaret E.; Guenther, Ulf-Peter; Jankowsky, Eckhard
- Current Opinion in Structural Biology, Vol. 20, Issue 3
Mechanism of Mss116 ATPase reveals functional diversity of DEAD-Box proteins.
text, January 2018
- Cao, Wenxiang; Coman, Maria Magdalena; Ding, Steve
- Figshare
X-Ray Structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase Core and Its Complex with DNA
journal, May 2005
- Dürr, Harald; Körner, Christian; Müller, Marisa
- Cell, Vol. 121, Issue 3
Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail
journal, July 2011
- Mallam, A. L.; Jarmoskaite, I.; Tijerina, P.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 30
Translocation and Unwinding Mechanisms of RNA and DNA Helicases
journal, June 2008
- Pyle, Anna Marie
- Annual Review of Biophysics, Vol. 37, Issue 1
DEAD-Box Proteins Unwind Duplexes by Local Strand Separation
journal, October 2007
- Yang, Quansheng; Del Campo, Mark; Lambowitz, Alan M.
- Molecular Cell, Vol. 28, Issue 2
Arabidopsis DEAD-Box RNA Helicase UAP56 Interacts with Both RNA and DNA as well as with mRNA Export Factors
journal, March 2013
- Kammel, Christine; Thomaier, Maren; Sørensen, Brian B.
- PLoS ONE, Vol. 8, Issue 3
Cofactor-dependent specificity of a DEAD-box protein
journal, April 2013
- Young, C. L.; Khoshnevis, S.; Karbstein, K.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 29
An A-DNA triplet code: thermodynamic rules for predicting A- and B-DNA.
journal, July 1995
- Basham, B.; Schroth, G. P.; Ho, P. S.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 14
From unwinding to clamping — the DEAD box RNA helicase family
journal, July 2011
- Linder, Patrick; Jankowsky, Eckhard
- Nature Reviews Molecular Cell Biology, Vol. 12, Issue 8
Enzyme Recruitment in Evolution of New Function
journal, October 1976
- Jensen, R. A.
- Annual Review of Microbiology, Vol. 30, Issue 1
Unwinding by Local Strand Separation Is Critical for the Function of DEAD-Box Proteins as RNA Chaperones
journal, June 2009
- Del Campo, Mark; Mohr, Sabine; Jiang, Yue
- Journal of Molecular Biology, Vol. 389, Issue 4
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
Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p
journal, September 2012
- Mallam, Anna L.; Del Campo, Mark; Gilman, Benjamin
- Nature, Vol. 490, Issue 7418
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
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
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
MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009
- Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
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
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
DEAD-Box Helicases Form Nucleotide-Dependent, Long-Lived Complexes with RNA
journal, January 2014
- Liu, Fei; Putnam, Andrea A.; Jankowsky, Eckhard
- Biochemistry, Vol. 53, Issue 2
Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
journal, August 1982
- Walker, J. E.; Saraste, M.; Runswick, M. J.
- The EMBO Journal, Vol. 1, Issue 8
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
Helicases: amino acid sequence comparisons and structure-function relationships
journal, June 1993
- Gorbalenya, Alexander E.; Koonin, Eugene V.
- Current Opinion in Structural Biology, Vol. 3, Issue 3
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA.
text, January 2010
- Henn, Arnon; Cao, Wenxiang; Licciardello, Nicholas
- Carnegie Mellon University
RNA Helicase Proteins as Chaperones and Remodelers
journal, June 2014
- Jarmoskaite, Inga; Russell, Rick
- Annual Review of Biochemistry, Vol. 83, Issue 1
Different conformations of double-stranded nucleic acid in solution as revealed by circular dichroism
journal, January 1973
- Ivanov, V. I.; Minchenkova, L. E.; Schyolkina, A. K.
- Biopolymers, Vol. 12, Issue 1
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
DEAD-box proteins as RNA helicases and chaperones: DEAD-box proteins
journal, September 2010
- Jarmoskaite, Inga; Russell, Rick
- Wiley Interdisciplinary Reviews: RNA, Vol. 2, Issue 1
Circular dichroism and conformational polymorphism of DNA
journal, January 2009
- Kypr, J.; Kejnovska, I.; Renciuk, D.
- Nucleic Acids Research, Vol. 37, Issue 6
Function of the C-terminal Domain of the DEAD-box Protein Mss116p Analyzed in Vivo and in Vitro
journal, February 2008
- Mohr, Georg; Del Campo, Mark; Mohr, Sabine
- Journal of Molecular Biology, Vol. 375, Issue 5
Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA
journal, February 2010
- Henn, A.; Cao, W.; Licciardello, N.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 9
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
Crystal Structure and Nucleotide Binding of the Thermus thermophilus RNA Helicase Hera N-terminal Domain
journal, August 2006
- Rudolph, Markus G.; Heissmann, Ramona; Wittmann, Julia G.
- Journal of Molecular Biology, Vol. 361, Issue 4
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 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
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
The splicing of yeast mitochondrial group I and group II introns requires a DEAD-box protein with RNA chaperone function
journal, December 2004
- Huang, H. -R.; Rowe, C. E.; Mohr, S.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 1
Different conformations of double-stranded nucleic acid in solution as revealed by circular dichroism
journal, January 1973
- Ivanov, V. I.; Minchenkova, L. E.; Schyolkina, A. K.
- Biopolymers, Vol. 12, Issue 1
Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
journal, August 1982
- Walker, J. E.; Saraste, M.; Runswick, M. J.
- The EMBO Journal, Vol. 1, Issue 8
Pisum sativum p68 DEAD-box protein is ATP-dependent RNA helicase and unique bipolar DNA helicase
journal, June 2014
- Tuteja, Narendra; Tarique, Mohammed; Banu, Mst. Sufara Akhter
- Plant Molecular Biology, Vol. 85, Issue 6
X-Ray Structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase Core and Its Complex with DNA
journal, May 2005
- Dürr, Harald; Körner, Christian; Müller, Marisa
- Cell, Vol. 121, Issue 3
Unwinding by Local Strand Separation Is Critical for the Function of DEAD-Box Proteins as RNA Chaperones
journal, June 2009
- Del Campo, Mark; Mohr, Sabine; Jiang, Yue
- Journal of Molecular Biology, Vol. 389, Issue 4
ATP-Dependent Roles of the DEAD-Box Protein Mss116p in Group II Intron Splicing In Vitro and In Vivo
journal, August 2011
- Potratz, Jeffrey P.; Del Campo, Mark; Wolf, Rachel Z.
- Journal of Molecular Biology, Vol. 411, Issue 3
High-Throughput Genetic Identification of Functionally Important Regions of the Yeast DEAD-Box Protein Mss116p
journal, November 2011
- Mohr, Georg; Del Campo, Mark; Turner, Kathryn G.
- Journal of Molecular Biology, Vol. 413, Issue 5
Structure of the Yeast DEAD Box Protein Mss116p Reveals Two Wedges that Crimp RNA
journal, September 2009
- Del Campo, Mark; Lambowitz, Alan M.
- Molecular Cell, Vol. 35, Issue 5
SF1 and SF2 helicases: family matters
journal, June 2010
- Fairman-Williams, Margaret E.; Guenther, Ulf-Peter; Jankowsky, Eckhard
- Current Opinion in Structural Biology, Vol. 20, Issue 3
Characterization of the NTPase, RNA-Binding, and RNA Helicase Activities of the DEAH-Box Splicing Factor Prp22 †
journal, July 2005
- Tanaka, Naoko; Schwer, Beate
- Biochemistry, Vol. 44, Issue 28
DEAD-Box Helicases Form Nucleotide-Dependent, Long-Lived Complexes with RNA
journal, January 2014
- Liu, Fei; Putnam, Andrea A.; Jankowsky, Eckhard
- Biochemistry, Vol. 53, Issue 2
Structural basis of RNA recognition and activation by innate immune receptor RIG-I
journal, September 2011
- Jiang, Fuguo; Ramanathan, Anand; Miller, Matthew T.
- Nature, Vol. 479, Issue 7373
Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p
journal, September 2012
- Mallam, Anna L.; Del Campo, Mark; Gilman, Benjamin
- Nature, Vol. 490, Issue 7418
From unwinding to clamping — the DEAD box RNA helicase family
journal, July 2011
- Linder, Patrick; Jankowsky, Eckhard
- Nature Reviews Molecular Cell Biology, Vol. 12, Issue 8
ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding
journal, December 2008
- Liu, F.; Putnam, A.; Jankowsky, E.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 51
Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail
journal, July 2011
- Mallam, A. L.; Jarmoskaite, I.; Tijerina, P.
- 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
- Basham, B.; Schroth, G. P.; Ho, P. S.
- 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.
- Journal of Biological Chemistry, Vol. 271, Issue 40
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
Works referencing / citing this record:
Distinct RNA-unwinding mechanisms of DEAD-box and DEAH-box RNA helicase proteins in remodeling structured RNAs and RNPs
journal, November 2017
- Gilman, Benjamin; Tijerina, Pilar; Russell, Rick
- Biochemical Society Transactions, Vol. 45, Issue 6
Plasmodium falciparum specific helicase 3 is nucleocytoplasmic protein and unwinds DNA duplex in 3′ to 5′ direction
journal, October 2017
- Chauhan, Manish; Tarique, Mohammed; Tuteja, Renu
- Scientific Reports, Vol. 7, Issue 1
An aromatic-rich loop couples DNA binding and ATP hydrolysis in the PriA DNA helicase
journal, August 2016
- Windgassen, Tricia A.; Keck, James L.
- Nucleic Acids Research
The DEAD-box helicase Mss116 plays distinct roles in mitochondrial ribogenesis and mRNA-specific translation
journal, May 2017
- De Silva, Dasmanthie; Poliquin, Sarah; Zeng, Rui
- Nucleic Acids Research, Vol. 45, Issue 11
A DEAD-box protein regulates ribosome assembly through control of ribosomal protein synthesis
journal, June 2019
- Iost, Isabelle; Jain, Chaitanya
- Nucleic Acids Research, Vol. 47, Issue 15
Structure of the full kinetoplastids mitoribosome and insight on its large subunit maturation
journal, January 2020
- Soufari, Heddy; Waltz, Florent; Parrot, Camila
- BioRxiv