The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
A MademoiseLLE domain binding platform links the key RNA transporter to endosomes
Open accessPublished version of a preprint
Abstract
Spatiotemporal expression can be achieved by transport and translation of mRNAs at defined subcellular sites. An emerging mechanism mediating mRNA trafficking is microtubule-dependent co-transport on shuttling endosomes. Although progress has been made in identifying various components of the endosomal mRNA transport machinery, a mechanistic understanding of how these RNA-binding proteins are connected to endosomes is still lacking. Here, we demonstrate that a flexible MademoiseLLE (MLLE) domain platform within RNA-binding protein Rrm4 of Ustilago maydis is crucial for endosomal attachment. Our structure/function analysis uncovered three MLLE domains at the C-terminus of Rrm4 with a functionally defined hierarchy. MLLE3 recognises two PAM2-like sequences of the adaptor protein Upa1 and is essential for endosomal shuttling of Rrm4. MLLE1 and MLLE2 are most likely accessory domains exhibiting a variable binding mode for interaction with currently unknown partners. Thus, endosomal attachment of the mRNA transporter is orchestrated by a sophisticated MLLE domain binding platform.
Overview
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
Verification
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Accurate prediction of protein structures and interactions using a 3-track network
Baek, M., DiMaio, F., Anishchenko, I., Dauparas, J., Ovchinnikov, S., Lee, G. R., Wang, J., Cong, Q., Kinch, L. N., Schaeffer, R. D., et al. (2021) · doi:10.1101/2021.06.14.448402 · Cited by 5,549
Flagged first, then by citations
Research works printed but not linked: 65
- M Mofatteh, 2017, SnapShot: Subcellular mRNA localization, Cell, 169, 178.e1, 10.1016/j.cell.2017.03.004 · DOI
- S Das, 2021, Intracellular mRNA transport and localized translation, Nat Rev Mol Cell Biol, 22, 483, 10.1038/s41580-021-00356-8 · DOI
- MS Fernandopulle, 2021, RNA transport and local translation in neurodevelopmental and neurodegenerative disease, Nature neuroscience
- D Niessing, 2018, mRNA transport in fungal top models, Wiley interdisciplinary reviews RNA, 9, e1453, 10.1002/wrna.1453 · DOI
- K Müntjes, 2021, Linking transport and translation of mRNAs with endosomes and mitochondria, EMBO reports
- S Baumann, 2012, Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes, J Cell Sci, 125, 2740
- L Tian, 2020, mRNA localization in plant cells, Plant Physiol, 182, 97, 10.1104/pp.19.00972 · DOI
- JM Cioni, 2019, Late endosomes act as mRNA translation platforms and sustain mitochondria in axons, Cell, 176, 56, 10.1016/j.cell.2018.11.030 · DOI
- YC Liao, 2019, RNA granules hitchhike on lysosomes for long-distance transport, using annexin A11 as a molecular tether, Cell, 179, 147, 10.1016/j.cell.2019.08.050 · DOI · Paper page
- D Quentin, 2021, Structure of the human FERRY Rab5 effector complex, bioRiv
- JS Schuhmacher, 2021, The novel Rab5 effector FERRY links early endosomes with the translation machinery, BioRiv
- L Tian, 2020, Zipcode RNA-binding proteins and membrane trafficking proteins cooperate to transport glutelin mRNAs in rice endosperm, Plant Cell, 32, 2566, 10.1105/tpc.20.00111 · DOI
- C Haag, 2015, Membrane-coupled mRNA trafficking in fungi, Annu Rev Microbiol, 69, 265, 10.1146/annurev-micro-091014-104242 · DOI
- J Béthune, 2019, Membrane-associated RNA-binding proteins orchestrate organelle-coupled translation Trends in cell biology, 29, 178
- P Becht, 2006, The RNA-binding protein Rrm4 is essential for polarity in Ustilago maydis and shuttles along microtubules, J Cell Sci, 119, 4964, 10.1242/jcs.03287 · DOI
- T Pohlmann, 2015, A FYVE zinc finger domain protein specifically links mRNA transport to endosome trafficking, eLife, 4, e06041, 10.7554/eLife.06041 · DOI
- S Baumann, 2014, Endosomal transport of septin mRNA and protein indicates local translation on endosomes and is required for correct septin filamentation, EMBO Rep, 15, 94, 10.1002/embr.201338037 · DOI
- S Zander, 2016, Endosomal assembly and transport of heteromeric septin complexes promote septin cytoskeleton formation, J Cell Sci, 129, 2778, 10.1242/jcs.182824 · DOI
- L Olgeiser, 2019, The key protein of endosomal mRNP transport Rrm4 binds translational landmark sites of cargo mRNAs, EMBO Rep, 20, e46588, 10.15252/embr.201846588 · DOI
- H Stenmark, 2002, The phosphatidylinositol 3-phosphate-binding FYVE finger, FEBS Lett, 513, 77, 10.1016/S0014-5793(01)03308-7 · DOI · Paper page
- M Albrecht, 2004, Survey on the PABC recognition motif PAM2, Biochem Biophys Res Commun, 316, 129, 10.1016/j.bbrc.2004.02.024 · DOI
- G Kozlov, 2004, Structural basis of ligand recognition by PABC, a highly specific peptide-binding domain found in poly(A)-binding protein and a HECT ubiquitin ligase, EMBO J, 23, 272, 10.1038/sj.emboj.7600048 · DOI
- M Jinek, 2010, Structural insights into the human GW182-PABC interaction in microRNA-mediated deadenylation, Nat Struct Mol Biol, 17, 238, 10.1038/nsmb.1768 · DOI
- DA Mangus, 1998, Pbp1p, a factor interacting with Saccharomyces cerevisiae poly(A)-binding protein, regulates polyadenylation, Molecular and cellular biology, 18, 7383, 10.1128/MCB.18.12.7383 · DOI
- DA Mangus, 2003, Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression, Genome Biol, 4, 223, 10.1186/gb-2003-4-7-223 · DOI
- G Kozlov, 2001, Structure and function of the C-terminal PABC domain of human poly(A)-binding protein, Proc Natl Acad Sci U S A, 98, 4409, 10.1073/pnas.071024998 · DOI
- RC Deo, 2001, X-ray structure of the human hyperplastic discs protein: an ortholog of the C-terminal domain of poly(A)-binding protein, Proc Natl Acad Sci U S A, 98, 4414, 10.1073/pnas.071552198 · DOI
- J Xie, 2014, The “tale” of poly(A) binding protein: the MLLE domain and PAM2-containing proteins, Biochim Biophys Acta, 1839, 1062, 10.1016/j.bbagrm.2014.08.001 · DOI
- G Kozlov, 2010, Molecular basis of eRF3 recognition by the MLLE domain of poly(A)-binding protein, PLoS One, 5, e10169, 10.1371/journal.pone.0010169 · DOI
- H Su, 2011, Mammalian hyperplastic discs homolog EDD regulates miRNA-mediated gene silencing, Mol Cell, 43, 97, 10.1016/j.molcel.2011.06.013 · DOI
- J Müller, 2019, Core components of endosomal mRNA transport are evolutionarily conserved in fungi, Fungal Genet Biol, 126, 12, 10.1016/j.fgb.2019.01.013 · DOI
- D Mulnaes, 2020, TopModel: template-based protein structure prediction at low sequence identity using top-down consensus and deep neural networks, J Chem Theory Comput, 16, 1953, 10.1021/acs.jctc.9b00825 · DOI
- D Mulnaes, 2018, TopScore: using deep neural networks and large diverse data sets for accurate protein model quality assessment, J Chem Theory Comput, 14, 6117, 10.1021/acs.jctc.8b00690 · DOI
- J Munoz-Escobar, 2015, The MLLE domain of the ubiquitin ligase UBR5 binds to its catalytic domain to regulate substrate binding, The Journal of biological chemistry, 290, 22841, 10.1074/jbc.M115.672246 · DOI
- G Kozlov, 2010, Molecular determinants of PAM2 recognition by the MLLE domain of poly(A)-binding protein, J Mol Biol, 397, 397, 10.1016/j.jmb.2010.01.032 · DOI
- G Tria, 2015, Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering, IUCrJ, 207, 10.1107/S205225251500202X · DOI
- PV Konarev, 2003, PRIMUS: a Windows PC-based system for small-angle scattering data analysis, J Appl Crystallogr, 36, 1277, 10.1107/S0021889803012779 · DOI
- K Müntjes, 2020, Establishing polycistronic expression in the model microorganism Ustilago maydis, Front Microbiol, 11, 1384, 10.3389/fmicb.2020.01384 · DOI
- S Mattijssen, 2021, LARP1 and LARP4: up close with PABP for mRNA 3’ poly(A) protection and stabilization, RNA Biol, 18, 259, 10.1080/15476286.2020.1868753 · DOI
- A Brachmann, 2001, Identification of genes in the bW/bE regulatory cascade in Ustilago maydis, Mol Microbiol, 42, 1047, 10.1046/j.1365-2958.2001.02699.x · DOI
- S Jankowski, 2019, The multi PAM2 protein Upa2 functions as novel core component of endosomal mRNA transport, EMBO Rep, 24, e47381, 10.15252/embr.201847381 · DOI
- R Yang, 2011, La-related protein 4 binds poly(A), interacts with the poly(A)-binding protein MLLE domain via a variant PAM2w motif, and can promote mRNA stability, Mol Cell Biol, 31, 542, 10.1128/MCB.01162-10 · DOI
- C Grimm, 2020, Crystal structure of a variant PAM2 motif of LARP4B bound to the MLLE domain of PABPC1, Biomol, 10
- NS Lim, 2006, Comparative peptide binding studies of the PABC domains from the ubiquitin-protein isopeptide ligase HYD and poly(A)-binding protein. Implications for HYD function, The Journal of biological chemistry, 281, 14376, 10.1074/jbc.M600307200 · DOI
- IB Schäfer, 2019, Molecular bsis for poly(A) RNP architecture and recognition by the Pan2-Pan3 deadenylase, Cell, 177, 1619, 10.1016/j.cell.2019.04.013 · DOI
- R Sawazaki, 2018, Characterization of the multimeric structure of poly(A)-binding protein on a poly(A) tail, Sci Rep., 8, 1455, 10.1038/s41598-018-19659-6 · DOI
- L Tian, 2018, RNA-binding protein RBP-P is required for glutelin and prolamine mRNA localization in rice endosperm cells, Plant Cell, 30, 2529, 10.1105/tpc.18.00321 · DOI
- A Brachmann, 2004, A reverse genetic approach for generating gene replacement mutants in Ustilago maydis, Mol Gen Genom, 272, 216, 10.1007/s00438-004-1047-z · DOI
- M Terfrüchte, 2014, Establishing a versatile Golden Gate cloning system for genetic engineering in fungi, Fungal Genet Biol, 62, 1, 10.1016/j.fgb.2013.10.012 · DOI
- G Loubradou, 2001, A homologue of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis, Mol Microbiol, 40, 719, 10.1046/j.1365-2958.2001.02424.x · DOI
- FW Studier, 2005, Protein production by auto-induction in high density shaking cultures, Protein Expr Purif, 41, 207, 10.1016/j.pep.2005.01.016 · DOI
- A Abts, 2013, NisC binds the FxLx motif of the nisin leader peptide, Biochemistry, 52, 5387, 10.1021/bi4008116 · DOI
- AJ Weiler, 2021, Novel intracellular phospholipase B from Pseudomonas aeruginosa with activity towards endogenous phospholipids affects biofilm assembly, bioRiv
- DJ Slotboom, 2008, Static light scattering to characterize membrane proteins in detergent solution, Methods, 46, 73, 10.1016/j.ymeth.2008.06.012 · DOI
- W. Kabsch, 2014, Processing of X-ray snapshots from crystals in random orientations, Acta Crystallogr D Biol Crystallogr, 70, 2204, 10.1107/S1399004714013534 · DOI
- PV Afonine, 2012, Towards automated crystallographic structure refinement with phenix.refine, Acta Crystallogr D Biol Crystallogr, 68, 352, 10.1107/S0907444912001308 · DOI · Paper page
- P Emsley, 2004, Coot: model-building tools for molecular graphics, Acta Crystallogr D Biol Crystallogr, 60, 2126, 10.1107/S0907444904019158 · DOI · Paper page
- P Pernot, 2013, Upgraded ESRF BM29 beamline for SAXS on macromolecules in solution., J Synchrotron Radiat., 20, 660, 10.1107/S0909049513010431 · DOI
- K Manalastas-Cantos, 2021, ATSAS 3.0: expanded functionality and new tools for small-angle scattering data analysis, J Appl Crystallogr, 54, 343, 10.1107/S1600576720013412 · DOI
- A Guinier, 1939, Small-angle X-ray diffraction: application to the study of ultramicroscopic phenomena, Ann Phys, 11, 161, 10.1051/anphys/193911120161 · DOI
- DI Svergun, 1992, Determination of the regularization parameter in indirect-transform methods using perceptual criteria, J Appl Crystallogr, 25, 495, 10.1107/S0021889892001663 · DOI
- D Mulnaes, 2021, TopSuite Web Server: A Meta-Suite for Deep-Learning-Based Protein Structure and Quality Prediction, Journal of chemical information and modeling, 61, 548, 10.1021/acs.jcim.0c01202 · DOI
- E Valentini, 2015, SASBDB, a repository for biological small-angle scattering data, Nucleic Acids Res, 43, D357, 10.1093/nar/gku1047 · DOI
- AG Kikhney, 2020, SASBDB: Towards an automatically curated and validated repository for biological scattering data, Protein science: a publication of the Protein Society, 29, 66, 10.1002/pro.3731 · DOI
- S Baumann, 2016, Methods in Cell Biol: Septins, 143
Metadata
- Authors
- Devan, S.-K., Schott-Verdugo, S., Müntjes, K., Bismar, L., Reiners, J., Hachani, E., Schmitt, L., Höppner, A., Smits, S. H., Gohlke, H., & Feldbrügge, M.
- Affiliations
- Cluster of Excellence on Plant Sciences (DE)
- Heinrich Heine University Düsseldorf (DE)
- Forschungszentrum Jülich (DE)
- Corresponding author
- Devan, Senthil-Kumar
- Müntjes, Kira
- Bismar, Lilli
- Reiners, Jens
- Hachani, Eymen
- Schmitt, Lutz
- Smits, Sander HJ
- Gohlke, Holger
- Feldbrügge, Michael
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2022-06-21
- Volume
- 18
- Issue
- 6
- Pages
- e1010269
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC9249222
- OpenAlex
- W4283265868
- Cited by
- 8
- References
- 2
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 3
- FWCI
- 0.57
- Type
- journal article
- Language
- en
- Update notices
- new_version (2022-07-01)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Deutsche Forschungsgemeinschaft (EXC-2048/1 - Project ID 39068111, Project-ID 267205415 – SFB 1208 A09, Project-ID 267205415 – SFB 1208 A03, Project-ID 267205415 – SFB 1208 A01, 417919780; INST 208/740-1 FUGG INST 208/761-1 FUGG)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- RNA-binding proteins, Ustilago maydis, structure-function analysis
- MeSH terms
- Fungal Proteins, Oligopeptides, Endosomes, RNA, RNA, Messenger, Ustilago, RNA-Binding Proteins, Membrane Transport Proteins, Toll-Like Receptor 2, Toll-Like Receptor 9
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