RNA regulatory networks diversified through curvature of the PUF protein scaffold
Abstract
Proteins bind and control mRNAs, directing their localization, translation and stability. Members of the PUF family of RNA-binding proteins control multiple mRNAs in a single cell, and play key roles in development, stem cell maintenance and memory formation. Here we identified the mRNA targets of a S. cerevisiae PUF protein, Puf5p, by ultraviolet-crosslinking-affinity purification and high-throughput sequencing (HITS-CLIP). The binding sites recognized by Puf5p are diverse, with variable spacer lengths between two specific sequences. Each length of site correlates with a distinct biological function. Crystal structures of Puf5p–RNA complexes reveal that the protein scaffold presents an exceptionally flat and extended interaction surface relative to other PUF proteins. In complexes with RNAs of different lengths, the protein is unchanged. A single PUF protein repeat is sufficient to induce broadening of specificity. Changes in protein architecture, such as alterations in curvature, may lead to evolution of mRNA regulatory networks.
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Biochemistry
- National Institutes of Health, Research Triangle Park, NC (United States). Epigenetics and Stem Cell Biology Lab.
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1214654
- Grant/Contract Number:
- AC02-06CH11357; W-31-109-ENG-38
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Wilinski, Daniel, Qiu, Chen, Lapointe, Christopher P., Nevil, Markus, Campbell, Zachary T., Tanaka Hall, Traci M., and Wickens, Marvin. RNA regulatory networks diversified through curvature of the PUF protein scaffold. United States: N. p., 2015.
Web. doi:10.1038/ncomms9213.
Wilinski, Daniel, Qiu, Chen, Lapointe, Christopher P., Nevil, Markus, Campbell, Zachary T., Tanaka Hall, Traci M., & Wickens, Marvin. RNA regulatory networks diversified through curvature of the PUF protein scaffold. United States. https://doi.org/10.1038/ncomms9213
Wilinski, Daniel, Qiu, Chen, Lapointe, Christopher P., Nevil, Markus, Campbell, Zachary T., Tanaka Hall, Traci M., and Wickens, Marvin. Mon .
"RNA regulatory networks diversified through curvature of the PUF protein scaffold". United States. https://doi.org/10.1038/ncomms9213. https://www.osti.gov/servlets/purl/1214654.
@article{osti_1214654,
title = {RNA regulatory networks diversified through curvature of the PUF protein scaffold},
author = {Wilinski, Daniel and Qiu, Chen and Lapointe, Christopher P. and Nevil, Markus and Campbell, Zachary T. and Tanaka Hall, Traci M. and Wickens, Marvin},
abstractNote = {Proteins bind and control mRNAs, directing their localization, translation and stability. Members of the PUF family of RNA-binding proteins control multiple mRNAs in a single cell, and play key roles in development, stem cell maintenance and memory formation. Here we identified the mRNA targets of a S. cerevisiae PUF protein, Puf5p, by ultraviolet-crosslinking-affinity purification and high-throughput sequencing (HITS-CLIP). The binding sites recognized by Puf5p are diverse, with variable spacer lengths between two specific sequences. Each length of site correlates with a distinct biological function. Crystal structures of Puf5p–RNA complexes reveal that the protein scaffold presents an exceptionally flat and extended interaction surface relative to other PUF proteins. In complexes with RNAs of different lengths, the protein is unchanged. A single PUF protein repeat is sufficient to induce broadening of specificity. Changes in protein architecture, such as alterations in curvature, may lead to evolution of mRNA regulatory networks.},
doi = {10.1038/ncomms9213},
journal = {Nature Communications},
number = ,
volume = 6,
place = {United States},
year = {2015},
month = {9}
}
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Works referenced in this record:
RNA regulons: coordination of post-transcriptional events
journal, July 2007
- Keene, Jack D.
- Nature Reviews Genetics, Vol. 8, Issue 7
CPEB: a life in translation
journal, June 2007
- Richter, Joel D.
- Trends in Biochemical Sciences, Vol. 32, Issue 6
RNA Protein Interaction in Neurons
journal, July 2013
- Darnell, Robert B.
- Annual Review of Neuroscience, Vol. 36, Issue 1
PUF proteins: repression, activation and mRNA localization
journal, February 2011
- Quenault, Tara; Lithgow, Trevor; Traven, Ana
- Trends in Cell Biology, Vol. 21, Issue 2
A PUF family portrait: 3′UTR regulation as a way of life
journal, March 2002
- Wickens, Marvin; Bernstein, David S.; Kimble, Judith
- Trends in Genetics, Vol. 18, Issue 3
Extensive Association of Functionally and Cytotopically Related mRNAs with Puf Family RNA-Binding Proteins in Yeast
journal, March 2004
- Gerber, André P.; Herschlag, Daniel; Brown, Patrick O.
- PLoS Biology, Vol. 2, Issue 3
Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator
journal, February 2010
- Kershner, Aaron M.; Kimble, Judith
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 8
A protein-RNA specificity code enables targeted activation of an endogenous human transcript
journal, June 2014
- Campbell, Zachary T.; Valley, Cary T.; Wickens, Marvin
- Nature Structural & Molecular Biology, Vol. 21, Issue 8
Expanding the RNA-recognition code of PUF proteins
journal, August 2014
- Hall, Traci M. Tanaka
- Nature Structural & Molecular Biology, Vol. 21, Issue 8
Redistribution of Silencing Proteins from Telomeres to the Nucleolus Is Associated with Extension of Life Span in S. cerevisiae
journal, May 1997
- Kennedy, Brian K.; Gotta, Monica; Sinclair, David A.
- Cell, Vol. 89, Issue 3
Post-transcriptional regulation through the HO 3'-UTR by Mpt5, a yeast homolog of Pumilio and FBF
journal, February 2001
- Tadauchi, T.
- The EMBO Journal, Vol. 20, Issue 3
CLIP Identifies Nova-Regulated RNA Networks in the Brain
journal, November 2003
- Ule, J.
- Science, Vol. 302, Issue 5648
Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP
journal, April 2010
- Hafner, Markus; Landthaler, Markus; Burger, Lukas
- Cell, Vol. 141, Issue 1
Pyicos: a versatile toolkit for the analysis of high-throughput sequencing data
journal, October 2011
- Althammer, Sonja; González-Vallinas, Juan; Ballaré, Cecilia
- Bioinformatics, Vol. 27, Issue 24
Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data
journal, June 2011
- Zhang, Chaolin; Darnell, Robert B.
- Nature Biotechnology, Vol. 29, Issue 7
A three-hybrid screen identifies mRNAs controlled by a regulatory protein
journal, June 2006
- Seay, D.
- RNA, Vol. 12, Issue 8
Control of Signaling in a MAP-kinase Pathway by an RNA-Binding Protein
journal, February 2007
- Prinz, Susanne; Aldridge, Christine; Ramsey, Stephen A.
- PLoS ONE, Vol. 2, Issue 2
Patterns and plasticity in RNA-protein interactions enable recruitment of multiple proteins through a single site
journal, March 2012
- Valley, C. T.; Porter, D. F.; Qiu, C.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 16
Translational repression by PUF proteins in vitro
journal, April 2010
- Chritton, J. J.; Wickens, M.
- RNA, Vol. 16, Issue 6
HITS-CLIP yields genome-wide insights into brain alternative RNA processing
journal, November 2008
- Licatalosi, Donny D.; Mele, Aldo; Fak, John J.
- Nature, Vol. 456, Issue 7221
Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays
journal, December 2000
- Tenenbaum, S. A.; Carson, C. C.; Lager, P. J.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 26
Cooperativity in RNA-Protein Interactions: Global Analysis of RNA Binding Specificity
journal, May 2012
- Campbell, Zachary T.; Bhimsaria, Devesh; Valley, Cary T.
- Cell Reports, Vol. 1, Issue 5
Pervasive and dynamic protein binding sites of the mRNA transcriptome in Saccharomyces cerevisiae
journal, January 2013
- Freeberg, Mallory A.; Han, Ting; Moresco, James J.
- Genome Biology, Vol. 14, Issue 2
A 5' cytosine binding pocket in Puf3p specifies regulation of mitochondrial mRNAs
journal, November 2009
- Zhu, D.; Stumpf, C. R.; Krahn, J. M.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 48
Natural history and evolutionary principles of gene duplication in fungi
journal, September 2007
- Wapinski, Ilan; Pfeffer, Avi; Friedman, Nir
- Nature, Vol. 449, Issue 7158
RNA-protein interactions in the yeast three-hybrid system: Affinity, sensitivity, and enhanced library screening
journal, February 2005
- Hook, B.
- RNA, Vol. 11, Issue 2
Puf1p acts in combination with other yeast Puf proteins to control mRNA stability
journal, December 2007
- Ulbricht, R. J.; Olivas, W. M.
- RNA, Vol. 14, Issue 2
Yeast Mitochondrial Biogenesis: A Role for the PUF RNA-Binding Protein Puf3p in mRNA Localization
journal, June 2008
- Saint-Georges, Yann; Garcia, Mathilde; Delaveau, Thierry
- PLoS ONE, Vol. 3, Issue 6
Cell-free Formation of RNA Granules: Low Complexity Sequence Domains Form Dynamic Fibers within Hydrogels
journal, May 2012
- Kato, Masato; Han, Tina W.; Xie, Shanhai
- Cell, Vol. 149, Issue 4
Modular peptide binding: From a comparison of natural binders to designed armadillo repeat proteins
journal, February 2014
- Reichen, Christian; Hansen, Simon; Plückthun, Andreas
- Journal of Structural Biology, Vol. 185, Issue 2
Saccharomyces cerevisiae Mpt5p interacts with Sst2p and plays roles in pheromone sensitivity and recovery from pheromone arrest.
journal, June 1997
- Chen, T.; Kurjan, J.
- Molecular and Cellular Biology, Vol. 17, Issue 6
Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences
journal, January 2010
- Goecks, Jeremy; Nekrutenko, Anton; Taylor, James
- Genome Biology, Vol. 11, Issue 8
Manipulation of FASTQ data with Galaxy
journal, June 2010
- Blankenberg, D.; Gordon, A.; Von Kuster, G.
- Bioinformatics, Vol. 26, Issue 14
Fast gapped-read alignment with Bowtie 2
journal, March 2012
- Langmead, Ben; Salzberg, Steven L.
- Nature Methods, Vol. 9, Issue 4
Saccharomyces Genome Database: the genomics resource of budding yeast
journal, November 2011
- Cherry, J. M.; Hong, E. L.; Amundsen, C.
- Nucleic Acids Research, Vol. 40, Issue D1
YeastMine—an integrated data warehouse for Saccharomyces cerevisiae data as a multipurpose tool-kit
journal, January 2012
- Balakrishnan, Rama; Park, Julie; Karra, Kalpana
- Database, Vol. 2012
Ulp1-SUMO Crystal Structure and Genetic Analysis Reveal Conserved Interactions and a Regulatory Element Essential for Cell Growth in Yeast
journal, May 2000
- Mossessova, Elena; Lima, Christopher D.
- Molecular Cell, Vol. 5, Issue 5
[20] Processing of X-ray diffraction data collected in oscillation mode
book, January 1997
- Otwinowski, Zbyszek; Minor, Wladek
- Macromolecular Crystallography Part A, 307-326
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
Auto-Rickshaw : an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment
journal, March 2005
- Panjikar, Santosh; Parthasarathy, Venkataraman; Lamzin, Victor S.
- Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 4
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids
journal, May 2007
- Davis, I. W.; Leaver-Fay, A.; Chen, V. B.
- Nucleic Acids Research, Vol. 35, Issue Web Server
Engineering RNA sequence specificity of Pumilio repeats
journal, September 2006
- Cheong, C. -G.; Hall, T. M. T.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 37
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
A three-hybrid system to detect RNA-protein interactions in vivo.
journal, August 1996
- SenGupta, D. J.; Zhang, B.; Kraemer, B.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 16
PUF Protein-mediated Deadenylation Is Catalyzed by Ccr4p
journal, November 2006
- Goldstrohm, Aaron C.; Seay, Daniel J.; Hook, Brad A.
- Journal of Biological Chemistry, Vol. 282, Issue 1
Phagocytosis-like cell engulfment by a planctomycete bacterium
journal, December 2019
- Shiratori, Takashi; Suzuki, Shigekatsu; Kakizawa, Yukako
- Nature Communications, Vol. 10, Issue 1
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
YeastMine--an integrated data warehouse for Saccharomyces cerevisiae data as a multipurpose tool-kit.
text, January 2012
- Balakrishnan, Rama; Park, Julie; Karra, Kalpana
- Apollo - University of Cambridge Repository
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids
text, January 2007
- B., Chen, Vincent; C., Richardson, David; S., Richardson, Jane
- The University of North Carolina at Chapel Hill University Libraries
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
Modular peptide binding: from a comparison of natural binders to designed armadillo repeat proteins
text, January 2014
- Reichen, Christian; Hansen, Simon; Plückthun, Andreas
- Elsevier
Works referencing / citing this record:
Protein-RNA networks revealed through covalent RNA marks
journal, November 2015
- Lapointe, Christopher P.; Wilinski, Daniel; Saunders, Harriet A. J.
- Nature Methods, Vol. 12, Issue 12
Recurrent rewiring and emergence of RNA regulatory networks
journal, March 2017
- Wilinski, Daniel; Buter, Natascha; Klocko, Andrew D.
- Proceedings of the National Academy of Sciences, Vol. 114, Issue 14
Multiple Puf proteins regulate the stability of ribosome biogenesis transcripts
journal, September 2018
- Fischer, Anthony D.; Olivas, Wendy M.
- RNA Biology, Vol. 15, Issue 9
Nop9 binds the central pseudoknot region of 18S rRNA
journal, January 2017
- Wang, Bing; Ye, Keqiong
- Nucleic Acids Research
Expanding RNA binding specificity and affinity of engineered PUF domains
journal, February 2018
- Zhao, Yang-Yang; Mao, Miao-Wei; Zhang, Wen-Jing
- Nucleic Acids Research, Vol. 46, Issue 9
Distinct RNA-binding modules in a single PUF protein cooperate to determine RNA specificity
journal, July 2019
- Qiu, Chen; Dutcher, Robert C.; Porter, Douglas F.
- Nucleic Acids Research
Regulation of LRG1 expression by RNA‐binding protein Puf5 in the budding yeast cell wall integrity pathway
journal, October 2018
- Viet, Nguyen Thi Minh; Duy, Duong Long; Saito, Kazuhiro
- Genes to Cells, Vol. 23, Issue 12
The PUF binding landscape in metazoan germ cells
journal, May 2016
- Prasad, Aman; Porter, Douglas F.; Kroll-Conner, Peggy L.
- RNA, Vol. 22, Issue 7
Toward Identifying Subnetworks from FBF Binding Landscapes in Caenorhabditis Spermatogenic or Oogenic Germlines
journal, November 2018
- Porter, Douglas F.; Prasad, Aman; Carrick, Brian H.
- G3: Genes|Genomes|Genetics, Vol. 9, Issue 1
Drosophila Nanos acts as a molecular clamp that modulates the RNA-binding and repression activities of Pumilio
journal, August 2016
- Weidmann, Chase A.; Qiu, Chen; Arvola, René M.
- eLife, Vol. 5
Context-dependent deposition and regulation of mRNAs in P-bodies
journal, January 2018
- Wang, Congwei; Schmich, Fabian; Srivatsa, Sumana
- eLife, Vol. 7
RNA-binding proteins distinguish between similar sequence motifs to promote targeted deadenylation by Ccr4-Not
journal, January 2019
- Webster, Michael W.; Stowell, James AW; Passmore, Lori A.
- eLife, Vol. 8
Engineering a conserved RNA regulatory protein repurposes its biological function in vivo
journal, January 2019
- Bhat, Vandita D.; McCann, Kathleen L.; Wang, Yeming
- eLife, Vol. 8
A crystal structure of a collaborative RNA regulatory complex reveals mechanisms to refine target specificity
journal, August 2019
- Qiu, Chen; Bhat, Vandita D.; Rajeev, Sanjana
- eLife, Vol. 8
Context-dependent deposition and regulation of mRNAs in P-bodies
text, January 2018
- Wang, Congwei; Schmich, Fabian; Srivatsa, Sumana
- eLife Sciences Publications
Context-dependent deposition and regulation of mRNAs in P-bodies
text, January 2018
- Wang, Congwei; Schmich, Fabian; Srivatsa, Sumana
- ETH Zurich