Structure of frequency-interacting RNA helicase from Neurospora crassa reveals high flexibility in a domain critical for circadian rhythm and RNA surveillance

Morales, Yalemi; Olsen, Keith J.; Bulcher, Jacqueline M.; Johnson, Sean J.

doi:10.1371/journal.pone.0196642

Structure of frequency-interacting RNA helicase from Neurospora crassa reveals high flexibility in a domain critical for circadian rhythm and RNA surveillance

Journal Article · Wed May 02 00:00:00 EDT 2018 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0196642· OSTI ID:1903986

Morales, Yalemi ^[1]; Olsen, Keith J. ^[2]; Bulcher, Jacqueline M. ^[2]; ^[2]

Utah State Univ., Logan, UT (United States); OSTI
Utah State Univ., Logan, UT (United States)

The FRH (frequency-interacting RNA helicase) protein is the Neurospora crassa homolog of yeast Mtr4, an essential RNA helicase that plays a central role in RNA metabolism as an activator of the nuclear RNA exosome. FRH is also a required component of the circadian clock, mediating protein interactions that result in the rhythmic repression of gene expression. Here we show that FRH unwinds RNA substrates in vitro with a kinetic profile similar to Mtr4, indicating that while FRH has acquired additional functionality, its core helicase function remains intact. In contrast with the earlier FRH structures, a new crystal form of FRH results in an ATP binding site that is undisturbed by crystal contacts and adopts a conformation consistent with nucleotide binding and hydrolysis. Strikingly, this new FRH structure adopts an arch domain conformation that is dramatically altered from previous structures. Comparison of the existing FRH structures reveals conserved hinge points that appear to facilitate arch motion. Regions in the arch have been previously shown to mediate a variety of protein-protein interactions critical for RNA surveillance and circadian clock functions. The conformational changes highlighted in the FRH structures provide a platform for investigating the relationship between arch dynamics and Mtr4/FRH function.

View Accepted Manuscript (DOE)

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1903986

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 5 Vol. 13; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (38)

Gateway Arch to the RNA Exosome Losh, Jillian S.; van Hoof, Ambro Cell, Vol. 162, Issue 5 https://doi.org/10.1016/j.cell.2015.08.013	journal	August 2015
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
A New Twist on Clock Protein Phosphorylation: A Conformational Change Leads to Protein Degradation Menet, Jerome S.; Rosbash, Michael Molecular Cell, Vol. 43, Issue 5 https://doi.org/10.1016/j.molcel.2011.08.015	journal	September 2011
Conserved RNA Helicase FRH Acts Nonenzymatically to Support the Intrinsically Disordered Neurospora Clock Protein FRQ Hurley, Jennifer M.; Larrondo, Luis F.; Loros, Jennifer J. Molecular Cell, Vol. 52, Issue 6 https://doi.org/10.1016/j.molcel.2013.11.005	journal	December 2013
The crystal structure of Mtr4 reveals a novel arch domain required for rRNA processing Jackson, Ryan N.; Klauer, A. Alejandra; Hintze, Bradley J. The EMBO Journal, Vol. 29, Issue 13 https://doi.org/10.1038/emboj.2010.107	journal	May 2010
The RNA helicase FRH is an ATP-dependent regulator of CK1a in the circadian clock of Neurospora crassa Lauinger, Linda; Diernfellner, Axel; Falk, Sebastian Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4598	journal	April 2014
The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases Yang, Quansheng; Jankowsky, Eckhard Nature Structural & Molecular Biology, Vol. 13, Issue 11 https://doi.org/10.1038/nsmb1165	journal	October 2006
The exosome and RNA quality control in the nucleus Vanacova, Stepanka; Stefl, Richard EMBO reports, Vol. 8, Issue 7 https://doi.org/10.1038/sj.embor.7401005	journal	July 2007
Setting the pace of the Neurospora circadian clock by multiple independent FRQ phosphorylation events Tang, C. -T.; Li, S.; Long, C. Proceedings of the National Academy of Sciences, Vol. 106, Issue 26 https://doi.org/10.1073/pnas.0904898106	journal	June 2009
Structural analysis reveals the characteristic features of Mtr4, a DExH helicase involved in nuclear RNA processing and surveillance Weir, J. R.; Bonneau, F.; Hentschel, J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 27 https://doi.org/10.1073/pnas.1004953107	journal	June 2010
RNA unwinding by the Trf4/Air2/Mtr4 polyadenylation (TRAMP) complex Jia, H.; Wang, X.; Anderson, J. T. Proceedings of the National Academy of Sciences, Vol. 109, Issue 19 https://doi.org/10.1073/pnas.1201085109	journal	April 2012
Circadian clock locus frequency: protein encoded by a single open reading frame defines period length and temperature compensation. Aronson, B. D.; Johnson, K. A.; Dunlap, J. C. Proceedings of the National Academy of Sciences, Vol. 91, Issue 16 https://doi.org/10.1073/pnas.91.16.7683	journal	August 1994
Nuclear RNA surveillance: no sign of substrates tailing off Anderson, James T.; Wang, Xuying Critical Reviews in Biochemistry and Molecular Biology, Vol. 44, Issue 1 https://doi.org/10.1080/10409230802640218	journal	February 2009
The Mtr4 ratchet helix and arch domain both function to promote RNA unwinding Taylor, Lacy L.; Jackson, Ryan N.; Rexhepaj, Megi Nucleic Acids Research, Vol. 42, Issue 22 https://doi.org/10.1093/nar/gku1208	journal	November 2014
Regulation of the Neurospora circadian clock by an RNA helicase Cheng, Ping; He, Qun; He, Qiyang Genes & Development, Vol. 19, Issue 2 https://doi.org/10.1101/gad.1266805	journal	December 2004
PHENIX : building new software for automated crystallographic structure determination Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11 https://doi.org/10.1107/s0907444902016657	journal	October 2002
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/s0907444906045975	journal	December 2006
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/s0907444909042073	journal	December 2009
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
The cryo-EM structure of a ribosome–Ski2-Ski3-Ski8 helicase complex Schmidt, Christian; Kowalinski, Eva; Shanmuganathan, Vivekanandan Science, Vol. 354, Issue 6318 https://doi.org/10.1126/science.aaf7520	journal	December 2016
The Neurospora Circadian System Dunlap, Jay C.; Loros, Jennifer J. Journal of Biological Rhythms, Vol. 19, Issue 5 https://doi.org/10.1177/0748730404269116	journal	October 2004
Origins and activities of the eukaryotic exosome Lykke-Andersen, Søren; Brodersen, Ditlev E.; Jensen, Torben Heick Journal of Cell Science, Vol. 122, Issue 10 https://doi.org/10.1242/jcs.047399	journal	May 2009
Structural insights into the interaction of the nuclear exosome helicase Mtr4 with the preribosomal protein Nop53 Falk, Sebastian; Tants, Jan-Niklas; Basquin, Jerôme RNA, Vol. 23, Issue 12 https://doi.org/10.1261/rna.062901.117	journal	September 2017
Mutations in Mtr4 Structural Domains Reveal Their Important Role in Regulating tRNAiMet Turnover in Saccharomyces cerevisiae and Mtr4p Enzymatic Activities In Vitro Li, Yan; Burclaff, Joseph; Anderson, James T. PLOS ONE, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pone.0148090	journal	January 2016
Structure of the frequency‐interacting RNA helicase: a protein interaction hub for the circadian clock Conrad, Karen S.; Hurley, Jennifer M.; Widom, Joanne The EMBO Journal, Vol. 35, Issue 15 https://doi.org/10.15252/embj.201694327	journal	June 2016
FRQ-Interacting RNA Helicase Mediates Negative and Positive Feedback in the Neurospora Circadian Clock Shi, Mi; Collett, Michael; Loros, Jennifer J. Genetics, Vol. 184, Issue 2 https://doi.org/10.1534/genetics.109.111393	journal	February 2010
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
Ski2-like RNA helicase structures: Common themes and complex assemblies Johnson, Sean J.; Jackson, Ryan N. RNA Biology, Vol. 10, Issue 1 https://doi.org/10.4161/rna.22101	journal	January 2013
Size-Distribution Analysis of Macromolecules by Sedimentation Velocity Ultracentrifugation and Lamm Equation Modeling Schuck, Peter Biophysical Journal, Vol. 78, Issue 3 https://doi.org/10.1016/S0006-3495(00)76713-0	journal	March 2000
The Many Pathways of RNA Degradation Houseley, Jonathan; Tollervey, David Cell, Vol. 136, Issue 4 https://doi.org/10.1016/j.cell.2009.01.019	journal	February 2009
The Exosome Regulates Circadian Gene Expression in a Posttranscriptional Negative Feedback Loop Guo, Jinhu; Cheng, Ping; Yuan, Haiyan Cell, Vol. 138, Issue 6 https://doi.org/10.1016/j.cell.2009.06.043	journal	September 2009
The Exosome Is Recruited to RNA Substrates through Specific Adaptor Proteins Thoms, Matthias; Thomson, Emma; Baßler, Jochen Cell, Vol. 162, Issue 5 https://doi.org/10.1016/j.cell.2015.07.060	journal	August 2015
Circadian Conformational Change of the Neurospora Clock Protein FREQUENCY Triggered by Clustered Hyperphosphorylation of a Basic Domain Querfurth, Christina; Diernfellner, Axel C. R.; Gin, Elan Molecular Cell, Vol. 43, Issue 5 https://doi.org/10.1016/j.molcel.2011.06.033	journal	September 2011
The Molecular Architecture of the TRAMP Complex Reveals the Organization and Interplay of Its Two Catalytic Activities Falk, Sebastian; Weir, John R.; Hentschel, Jendrik Molecular Cell, Vol. 55, Issue 6 https://doi.org/10.1016/j.molcel.2014.07.020	journal	September 2014
CKI and CKII mediate the FREQUENCY-dependent phosphorylation of the WHITE COLLAR complex to close the Neurospora circadian negative feedback loop He, Q. Genes & Development, Vol. 20, Issue 18 https://doi.org/10.1101/gad.1463506	journal	September 2006
The circadian clock of Neurospora crassa Baker, Christopher L.; Loros, Jennifer J.; Dunlap, Jay C. FEMS Microbiology Reviews, Vol. 36, Issue 1 https://doi.org/10.1111/j.1574-6976.2011.00288.x	journal	January 2012
White Collar-1, a DNA Binding Transcription Factor and a Light Sensor He, Q. Science, Vol. 297, Issue 5582 https://doi.org/10.1126/science.1072795	journal	July 2002
White Collar-1, a Circadian Blue Light Photoreceptor, Binding to the frequency Promoter Froehlich, A. C. Science, Vol. 297, Issue 5582 https://doi.org/10.1126/science.1073681	journal	July 2002

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59 BASIC BIOLOGICAL SCIENCES
Neurospora crassa
RNA structure
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circadian rhythms
crystal structure
helicases
protein interactions
protein structure

Structure of frequency-interacting RNA helicase from Neurospora crassa reveals high flexibility in a domain critical for circadian rhythm and RNA surveillance

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