The pentatricopeptide repeat protein Rmd9 recognizes the dodecameric element in the 3′-UTRs of yeast mitochondrial mRNAs
Open accessAbstract
comprise a dodecamer sequence element that confers RNA stability and 3'-end processing via an unknown mechanism. Here, we isolated the protein that binds the dodecamer and identified it as Rmd9, a factor that is known to stabilize yeast mitochondrial RNA. We show that Rmd9 associates with mRNA around dodecamer elements in vivo and that recombinant Rmd9 specifically binds the element in vitro. The crystal structure of Rmd9 bound to its dodecamer target reveals that Rmd9 belongs to the family of pentatricopeptide (PPR) proteins and uses a previously unobserved mode of specific RNA recognition. Rmd9 protects RNA from degradation by the mitochondrial 3'-exoribonuclease complex mtEXO in vitro, indicating that recognition and binding of the dodecamer element by Rmd9 confers stability to yeast mitochondrial mRNAs.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Purification of individual members of the PPR family (heterologously expressed) was possible mostly for abundant or ribosome-associated proteins, e.g. ScDmr1p or ScRmd9p.
“Purification of individual members of the PPR family (heterologously expressed) was possible mostly for abundant or ribosome-associated proteins, e.g. ScDmr1p (Puchta et al. 2010; Piątkowski and Golik 2020) or ScRmd9p (Hillen et al. 2021).”
From <i>Candida albicans</i> PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Hillen et al. 2021
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Sheldrick, G. M. (2007) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767307043930 · Cited by 87,861 · see citing works
Features and development of Coot
Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. D. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444910007493 · Cited by 27,510 · see citing works
<i>PHENIX</i> : a comprehensive Python-based system for macromolecular structure solution
Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., et al. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444909052925 · Cited by 23,716 · see citing works
PHENIX: a comprehensive Python-based system for macromolecular structure solution
Adams, P. D., Afonine, P. V., Bunkòczi, G., Chen, V. B., Davis, I., Echols, N., Headd, J. J., Hung, L., Kapral, G. J., Grosse‐Kunstleve, R. W., et al. (2012) · International Tables for Crystallography · doi:10.1107/97809553602060000865 · Cited by 7,334 · see citing works
Ashkenazy, H., Abadi, S., Martz, E., Chay, O., Mayrose, I., Pupko, T., & Ben-Tal, N. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw408 · Cited by 3,163 · see citing works
Transcriptome-wide Identification of RNA-Binding Protein and MicroRNA Target Sites by PAR-CLIP
Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jungkamp, A.-C., Munschauer, M., et al. (2010) · Cell · doi:10.1016/j.cell.2010.03.009 · Cited by 2,873 · see citing works
A Completely Reimplemented MPI Bioinformatics Toolkit with a New HHpred Server at its Core
Zimmermann, L., Stephens, A., Nam, S.-Z., Rau, D., Kübler, J., Lozajic, M., Gabler, F., Söding, J., Lupas, A. N., & Alva, V. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.12.007 · Cited by 2,522 · see citing works
Pentatricopeptide Repeat Proteins in Plants
Barkan, A., & Small, I. (2014) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050213-040159 · Cited by 1,035 · see citing works
The PPR motif – a TPR-related motif prevalent in plant organellar proteins
Small, I., & Peeters, N. M. (2000) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01520-0 · Cited by 839 · see citing works
Pentatricopeptide repeat proteins: a socket set for organelle gene expression
Schmitz‐Linneweber, C., & Small, I. (2008) · Trends in Plant Science · doi:10.1016/j.tplants.2008.10.001 · Cited by 825 · see citing works
HKL2MAP: a graphical user interface for macromolecular phasing withSHELXprograms
Pape, T., & Schneider, T. R. (2004) · Journal of Applied Crystallography · doi:10.1107/s0021889804018047 · Cited by 743 · see citing works
Starting at the Beginning, Middle, and End: Translation Initiation in Eukaryotes
Sachs, A. B., Sarnow, P., & Hentze, M. W. (1997) · Cell · doi:10.1016/s0092-8674(00)80268-8 · Cited by 679 · see citing works
Ending the message: poly(A) signals then and nowPreprint
Proudfoot, N. J. (2011) · Genes & Development · doi:10.1101/gad.17268411 · Cited by 607 · see citing works
A Combinatorial Amino Acid Code for RNA Recognition by Pentatricopeptide Repeat Proteins
Barkan, A., Rojas, M., Fujii, S., Yap, A., Chong, Y. S., Bond, C. S., & Small, I. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002910 · Cited by 538 · see citing works
Structural basis for the modular recognition of single-stranded RNA by PPR proteins
Yin, P., Li, Q., Yan, C., Liu, Y., Liu, J., Yu, F., Wang, Z., Long, J., He, J., Wang, H., et al. (2013) · Nature · doi:10.1038/nature12651 · Cited by 338 · see citing works
Life and death in the cytoplasm: messages from the 3′ end
Wickens, M., Anderson, P., & Jackson, R. J. (1997) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(97)80132-3 · Cited by 332 · see citing works
Maignan, S., Guilloteau, J. P., Zhou, Q., Clément-Mella, C., & Mikol, V. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2002 · Cited by 277 · see citing works
An overview of pentatricopeptide repeat proteins and their applications
Manna, S. (2015) · Biochimie · doi:10.1016/j.biochi.2015.04.004 · Cited by 258 · see citing works
Transcriptome Surveillance by Selective Termination of Noncoding RNA Synthesis
Schulz, D., Schwalb, B., Kiesel, A., Baejen, C., Torkler, P., Gagneur, J., Söding, J., & Cramer, P. (2013) · Cell · doi:10.1016/j.cell.2013.10.024 · Cited by 219 · see citing works
Self-citationIdentification of RNA–protein interaction networks using PAR‐CLIP
Ascano, M., Hafner, M., Čekan, P., Gerstberger, S. C., & Tuschl, T. (2011) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1103 · Cited by 218 · see citing works
Shen, C., Zhang, D., Guan, Z., Liu, Y., Zhao, Y., Yang, Y., Wang, X., Wang, Q., Zhang, Q., Fan, S., et al. (2016) · Nature Communications · doi:10.1038/ncomms11285 · Cited by 156 · see citing works
MOBILITY OF AN HIV-1 INTEGRASE ACTIVE SITE LOOP IS CORRELATED WITH CATALYTIC ACTIVITY
Greenwald, J., Le, V. P., Butler, S. L., Bushman, F. D., & Choe, S. (1999) · Biochemistry · doi:10.1021/bi9907173 · Cited by 150 · see citing works
Delineation of pentatricopeptide repeat codes for target RNA prediction
Yan, J., Yao, Y., Hong, S., Yang, Y., Shen, C., Zhang, Q., Zhang, D., Zou, T., & Yin, P. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz075 · Cited by 149 · see citing works
Transcriptome Maps of mRNP Biogenesis Factors Define Pre-mRNA Recognition
Baejen, C., Torkler, P., Gressel, S., Essig, K., Söding, J., & Cramer, P. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.08.005 · Cited by 127 · see citing works
Self-citationPolyadenylation and nuclear export of mRNAs
Stewart, M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev118.005594 · Cited by 124 · see citing works
Organization of mitochondrial gene expression in two distinct ribosome-containing assemblies
Kehrein, K., Schilling, R., Möller-Hergt, B. V., Wurm, C. A., Jakobs, S., Lamkemeyer, T., Langer, T., & Ott, M. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.01.012 · Cited by 112 · see citing works
Processing of yeast mitochondrial messenger RNAs at a conserved dodecamer sequence.
Osinga, K. A., de Vries, E., van der Horst, G. T. J., & Tabak, H. F. (1984) · The EMBO Journal · doi:10.1002/j.1460-2075.1984.tb01892.x · Cited by 112 · see citing works
Chapter 10 RNA Polyadenylation and Decay in Mitochondria and Chloroplasts
Schuster, G., & Stern, D. B. (2009) · Progress in molecular biology and translational science · doi:10.1016/s0079-6603(08)00810-6 · Cited by 108 · see citing works
Structural basis for RNA recognition by a dimeric PPR-protein complex
Ke, J., Chen, R. Z., Ban, T., Zhou, X. E., Gu, X., Tan, M. H. E., Chen, C., Kang, Y., Brunzelle, J. S., Zhu, J.-K., et al. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2710 · Cited by 103 · see citing works
Mitochondrial poly(A) polymerase and polyadenylation
Chang, J., & Tong, L. (2011) · Biochimica et Biophysica Acta · doi:10.1016/j.bbagrm.2011.10.012 · Cited by 98 · see citing works
The Mitochondrial RNA Landscape of Saccharomyces cerevisiae
Turk, E. M., Das, V., Seibert, R., & Andrulis, E. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078105 · Cited by 75 · see citing works
Origins of transcripts of the yeast mitochondrial var 1 gene.
Zassenhaus, H. P., Martin, N. C., & Butow, R. A. (1984) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)91116-6 · Cited by 69 · see citing works
Molecular connectivity of mitochondrial gene expression and OXPHOS biogenesis
Singh, A. P., Salvatori, R., Aftab, W., Kohler, A., Carlström, A., Forne, I., Imhof, A., & Ott, M. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.07.024 · Cited by 65 · see citing works
Lipinski, K. A., Puchta, O., Surendranath, V., Kudla, M., & Golik, P. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr120 · Cited by 62 · see citing works
Ban, T., Ke, J., Chen, R., Gu, X., Tan, M. H. E., Zhou, X. E., Kang, Y., Melcher, K., Zhu, J., & Xu, H. E. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.496828 · Cited by 61 · see citing works
Yeast PPR proteins, watchdogs of mitochondrial gene expression
Herbert, C. J., Golik, P., & Bonnefoy, N. (2013) · RNA Biology · doi:10.4161/rna.25392 · Cited by 54 · see citing works
Organization and processing of the mitochondrial oxi3/oli2 multigenic transcript in yeast
Simon, M., & Faye, G. (1984) · Molecular and General Genetics MGG · doi:10.1007/bf00328059 · Cited by 54 · see citing works
RNA polyadenylation and its consequences in prokaryotes
Hajnsdorf, E., & Kaberdin, V. R. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0166 · Cited by 54 · see citing works
Małecki, M., Jedrzejczak, R. P., Stępień, P. P., & Golik, P. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.06.074 · Cited by 51 · see citing works
Nouet, C., Bourens, M., Hlaváček, O., Marsy, S., Lemaire, C., & Dujardin, G. (2006) · Genetics · doi:10.1534/genetics.106.063883 · Cited by 51 · see citing works
RNA Polyadenylation in Prokaryotes and Organelles; Different Tails Tell Different Tales
Slomovic, S., Portnoy, V., Liveanu, V., et al. (2006) · Critical Reviews in Plant Sciences · doi:10.1080/07352680500391337 · Cited by 50 · see citing works
RNA-stabilization factors in chloroplasts of vascular plants
Manavski, N., Schmid, L., & Meurer, J. (2018) · Essays in Biochemistry · doi:10.1042/ebc20170061 · Cited by 50 · see citing works
The role of a conserved dodecamer sequence in yeast mitochondrial gene expression
Butow, R. A., Zhu, H., Perlman, P. S., & Conrad-Webb, H. (1989) · Genome · doi:10.1139/g89-134 · Cited by 45 · see citing works
Williams, E. H., Butler, C. A., Bonnefoy, N., & Fox, T. D. (2006) · Genetics · doi:10.1534/genetics.106.064576 · Cited by 40 · see citing works
Min, J., & Zassenhaus, H. P. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.4167-4173.1993 · Cited by 34 · see citing works
Hofmann, T. J., Min, J., & Zassenhaus, H. P. (1993) · Yeast · doi:10.1002/yea.320091205 · Cited by 34 · see citing works
5′ and 3′ modifications controlling RNA degradation: from safeguards to executioners
Gagliardi, D., & Dziembowski, A. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0160 · Cited by 31 · see citing works
RNA degradation in yeast and human mitochondria.
Szczęsny, R., Borowski, L. S., Malecki, M., Wojcik, M. A., Stepien, P., & Golik, P. (2012) · Biochimica et Biophysica Acta · doi:10.1016/j.bbagrm.2011.11.010 · Cited by 30 · see citing works
Markov, D. A., Savkina, M. V., Anikin, M., Campo, M. D., Ecker, K., Lambowitz, A. M., Gnore, J. P. D., & McAllister, W. T. (2009) · Yeast · doi:10.1002/yea.1672 · Cited by 30 · see citing works
Self-citationoli1 Transcripts in wild type and in a cytoplasmic “petite” mutant of yeast.
Thalenfeld, B. E., Bonitz, S. G., Nóbrega, F. G., et al. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)43819-1 · Cited by 29 · see citing works
Liu, X., Zhang, H., Wang, X., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024227 · Cited by 26 · see citing works
Rażew, M., Warkocki, Z., Taube, M., Kolondra, A., Czarnocki-Cieciura, M., Nowak, E., Labedzka-Dmoch, K., Kawińska, A., Piątkowski, J., Golik, P., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02570-5 · Cited by 26 · see citing works
Min, J., & Zassenhaus, H. P. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.7.4167 · Cited by 19 · see citing works
Jones, J. L., Hofmann, K., Cowan, A. T., Temiakov, D., Cramer, P., & Anikin, M. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.005355 · Cited by 18 · see citing works
Self-citationLi, H., & Zassenhaus, H. P. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1085 · Cited by 17 · see citing works
Structure of SRP14 from theSchizosaccharomyces pombesignal recognition particle
Brooks, M., Ravelli, R. B. G., McCarthy, A. A., Strub, K., & Cusack, S. (2009) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444909005484 · Cited by 12 · see citing works
Li, H., & Zassenhaus, H. P. (2000) · Current Genetics · doi:10.1007/s002940000117 · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [8]Schuster G., Stern D., RNA polyadenylation and decay in mitochondria and chloroplasts. Prog. Mol. Biol. Transl. Sci. 85, 393–422 (2009). [DOI] [PubMed] [Google Scholar]
- [52]Brooks M. A., Ravelli R. B., McCarthy A. A., Strub K., Cusack S., Structure of SRP14 from the Schizosaccharomyces pombe signal recognition particle. Acta Crystallogr. D Biol. Crystallogr. 65, 421–433 (2009). [DOI] [PubMed] [Google Scholar]
Cited by
Sorted by citations
Golik, P. (2024) · IUBMB Life · doi:10.1002/iub.2779 · Cited by 9 · see citing works
Wenda, J. M., Drzewicka, K., Mulica, P., Tetaud, E., di Rago, J. P., Golik, P., & Łabędzka-Dmoch, K. (2024) · GENETICS · doi:10.1093/genetics/iyae124 · Cited by 2 · see citing works
- Authors
- Hillen, H. S., Markov, D. A., Wojtas, I. D., Hofmann, K. B., Lidschreiber, M., Cowan, A. T., Jones, J. L., Temiakov, D., Cramer, P., & Anikin, M.
- Affiliations
- Universitätsmedizin Göttingen (DE)
- Rowan University (US)
- Max Planck Institute for Biophysical Chemistry (DE)
- Thomas Jefferson University (US)
- Corresponding author
- Cramer, Patrick
- Anikin, Michael
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2021-04-05
- Volume
- 118
- Issue
- 15
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC8054023
- OpenAlex
- W3143899700
- Cited by
- 21
- References
- 57
- Citations by year
- 2026: 5 · 2024: 7 · 2023: 6 · 2022: 3
- FWCI
- 1.26
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DORA PSI (Paul Scherrer Institute) (submittedVersion)
- Funders
- New Jersey Health Foundation (PC127-13)
- HHS | National Institutes of Health (R35 GM131832)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- pentatricopeptide repeat proteins, 3' untranslated region, RNA-binding proteins, 3' end processing, Saccharomyces cerevisiae, RNA degradation
- MeSH terms
- Protein Domains, Membrane Proteins, Protein Binding, RNA, Messenger, Saccharomyces cerevisiae, 3' Untranslated Regions, Saccharomyces cerevisiae Proteins, Genes, Mitochondrial, Nucleotide Motifs
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
