A Tale of Loops and Tails: The Role of Intrinsically Disordered Protein Regions in R-Loop Recognition and Phase Separation Article Swipe
Leonardo G. Dettori
,
Diego Torrejon
,
Arijita Chakraborty
,
Arijit Dutta
,
Mohamed Mohamed
,
Csaba Papp
,
Vladimir A. Kuznetsov
,
Patrick Sung
,
Wenyi Feng
,
Alaji Bah
·
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.3389/fmolb.2021.691694
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.3389/fmolb.2021.691694
R-loops are non-canonical, three-stranded nucleic acid structures composed of a DNA:RNA hybrid, a displaced single-stranded (ss)DNA, and a trailing ssRNA overhang. R-loops perform critical biological functions under both normal and disease conditions. To elucidate their cellular functions, we need to understand the mechanisms underlying R-loop formation, recognition, signaling, and resolution. Previous high-throughput screens identified multiple proteins that bind R-loops, with many of these proteins containing folded nucleic acid processing and binding domains that prevent (e.g., topoisomerases), resolve (e.g., helicases, nucleases), or recognize (e.g., KH, RRMs) R-loops. However, a significant number of these R-loop interacting Enzyme and Reader proteins also contain long stretches of intrinsically disordered regions (IDRs). The precise molecular and structural mechanisms by which the folded domains and IDRs synergize to recognize and process R-loops or modulate R-loop-mediated signaling have not been fully explored. While studying one such modular R-loop Reader, the Fragile X Protein (FMRP), we unexpectedly discovered that the C-terminal IDR (C-IDR) of FMRP is the predominant R-loop binding site, with the three N-terminal KH domains recognizing the trailing ssRNA overhang. Interestingly, the C-IDR of FMRP has recently been shown to undergo spontaneous Liquid-Liquid Phase Separation (LLPS) assembly by itself or in complex with another non-canonical nucleic acid structure, RNA G-quadruplex. Furthermore, we have recently shown that FMRP can suppress persistent R-loops that form during transcription, a process that is also enhanced by LLPS via the assembly of membraneless transcription factories. These exciting findings prompted us to explore the role of IDRs in R-loop processing and signaling proteins through a comprehensive bioinformatics and computational biology study. Here, we evaluated IDR prevalence, sequence composition and LLPS propensity for the known R-loop interactome. We observed that, like FMRP, the majority of the R-loop interactome, especially Readers, contains long IDRs that are highly enriched in low complexity sequences with biased amino acid composition, suggesting that these IDRs could directly interact with R-loops, rather than being “mere flexible linkers” connecting the “functional folded enzyme or binding domains”. Furthermore, our analysis shows that several proteins in the R-loop interactome are either predicted to or have been experimentally demonstrated to undergo LLPS or are known to be associated with phase separated membraneless organelles. Thus, our overall results present a thought-provoking hypothesis that IDRs in the R-loop interactome can provide a functional link between R-loop recognition via direct binding and downstream signaling through the assembly of LLPS-mediated membrane-less R-loop foci. The absence or dysregulation of the function of IDR-enriched R-loop interactors can potentially lead to severe genomic defects, such as the widespread R-loop-mediated DNA double strand breaks that we recently observed in Fragile X patient-derived cells.
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- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.3389/fmolb.2021.691694
- OA Status
- gold
- Cited By
- 34
- References
- 136
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W3169357026
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W3169357026Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.3389/fmolb.2021.691694Digital Object Identifier
- Title
-
A Tale of Loops and Tails: The Role of Intrinsically Disordered Protein Regions in R-Loop Recognition and Phase SeparationWork title
- Type
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articleOpenAlex work type
- Language
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enPrimary language
- Publication year
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2021Year of publication
- Publication date
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2021-06-10Full publication date if available
- Authors
-
Leonardo G. Dettori, Diego Torrejon, Arijita Chakraborty, Arijit Dutta, Mohamed Mohamed, Csaba Papp, Vladimir A. Kuznetsov, Patrick Sung, Wenyi Feng, Alaji BahList of authors in order
- Landing page
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https://doi.org/10.3389/fmolb.2021.691694Publisher landing page
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YesWhether a free full text is available
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goldOpen access status per OpenAlex
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https://doi.org/10.3389/fmolb.2021.691694Direct OA link when available
- Concepts
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Nucleic acid, RNA, DNA, Loop (graph theory), Biology, Biophysics, Helicase, Intrinsically disordered proteins, Chemistry, Cell biology, Biochemistry, Gene, Mathematics, CombinatoricsTop concepts (fields/topics) attached by OpenAlex
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34Total citation count in OpenAlex
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2025: 7, 2024: 6, 2023: 6, 2022: 11, 2021: 4Per-year citation counts (last 5 years)
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136Number of works referenced by this work
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.overall | 362 |
| abstract_inverted_index.perform | 22 |
| abstract_inverted_index.precise | 108 |
| abstract_inverted_index.present | 364 |
| abstract_inverted_index.prevent | 73 |
| abstract_inverted_index.process | 124, 220 |
| abstract_inverted_index.provide | 375 |
| abstract_inverted_index.regions | 105 |
| abstract_inverted_index.resolve | 76 |
| abstract_inverted_index.results | 363 |
| abstract_inverted_index.screens | 52 |
| abstract_inverted_index.several | 331 |
| abstract_inverted_index.through | 251, 388 |
| abstract_inverted_index.undergo | 184, 347 |
| abstract_inverted_index.“mere | 315 |
| abstract_inverted_index.(ss)DNA, | 15 |
| abstract_inverted_index.However, | 86 |
| abstract_inverted_index.Previous | 50 |
| abstract_inverted_index.R-loops, | 58, 311 |
| abstract_inverted_index.R-loops. | 85 |
| abstract_inverted_index.Readers, | 286 |
| abstract_inverted_index.analysis | 328 |
| abstract_inverted_index.assembly | 190, 229, 390 |
| abstract_inverted_index.cellular | 35 |
| abstract_inverted_index.composed | 7 |
| abstract_inverted_index.contains | 287 |
| abstract_inverted_index.critical | 23 |
| abstract_inverted_index.defects, | 413 |
| abstract_inverted_index.directly | 308 |
| abstract_inverted_index.enhanced | 224 |
| abstract_inverted_index.enriched | 293 |
| abstract_inverted_index.exciting | 235 |
| abstract_inverted_index.findings | 236 |
| abstract_inverted_index.flexible | 316 |
| abstract_inverted_index.function | 402 |
| abstract_inverted_index.interact | 309 |
| abstract_inverted_index.majority | 280 |
| abstract_inverted_index.modulate | 127 |
| abstract_inverted_index.multiple | 54 |
| abstract_inverted_index.observed | 275, 426 |
| abstract_inverted_index.prompted | 237 |
| abstract_inverted_index.proteins | 55, 63, 97, 250, 332 |
| abstract_inverted_index.recently | 180, 207, 425 |
| abstract_inverted_index.sequence | 264 |
| abstract_inverted_index.studying | 136 |
| abstract_inverted_index.suppress | 212 |
| abstract_inverted_index.trailing | 18, 171 |
| abstract_inverted_index.displaced | 13 |
| abstract_inverted_index.elucidate | 33 |
| abstract_inverted_index.evaluated | 261 |
| abstract_inverted_index.explored. | 134 |
| abstract_inverted_index.functions | 25 |
| abstract_inverted_index.molecular | 109 |
| abstract_inverted_index.overhang. | 20, 173 |
| abstract_inverted_index.predicted | 339 |
| abstract_inverted_index.recognize | 81, 122 |
| abstract_inverted_index.separated | 357 |
| abstract_inverted_index.sequences | 297 |
| abstract_inverted_index.signaling | 129, 249, 387 |
| abstract_inverted_index.stretches | 101 |
| abstract_inverted_index.synergize | 120 |
| abstract_inverted_index.C-terminal | 152 |
| abstract_inverted_index.N-terminal | 166 |
| abstract_inverted_index.Separation | 188 |
| abstract_inverted_index.associated | 354 |
| abstract_inverted_index.biological | 24 |
| abstract_inverted_index.complexity | 296 |
| abstract_inverted_index.connecting | 318 |
| abstract_inverted_index.containing | 64 |
| abstract_inverted_index.discovered | 149 |
| abstract_inverted_index.disordered | 104 |
| abstract_inverted_index.downstream | 386 |
| abstract_inverted_index.especially | 285 |
| abstract_inverted_index.factories. | 233 |
| abstract_inverted_index.formation, | 45 |
| abstract_inverted_index.functional | 377 |
| abstract_inverted_index.functions, | 36 |
| abstract_inverted_index.helicases, | 78 |
| abstract_inverted_index.hypothesis | 367 |
| abstract_inverted_index.identified | 53 |
| abstract_inverted_index.linkers” | 317 |
| abstract_inverted_index.mechanisms | 42, 112 |
| abstract_inverted_index.persistent | 213 |
| abstract_inverted_index.processing | 68, 247 |
| abstract_inverted_index.propensity | 268 |
| abstract_inverted_index.signaling, | 47 |
| abstract_inverted_index.structural | 111 |
| abstract_inverted_index.structure, | 201 |
| abstract_inverted_index.structures | 6 |
| abstract_inverted_index.suggesting | 303 |
| abstract_inverted_index.underlying | 43 |
| abstract_inverted_index.understand | 40 |
| abstract_inverted_index.widespread | 417 |
| abstract_inverted_index.composition | 265 |
| abstract_inverted_index.conditions. | 31 |
| abstract_inverted_index.domains”. | 325 |
| abstract_inverted_index.interacting | 93 |
| abstract_inverted_index.interactome | 336, 373 |
| abstract_inverted_index.interactors | 406 |
| abstract_inverted_index.nucleases), | 79 |
| abstract_inverted_index.organelles. | 359 |
| abstract_inverted_index.potentially | 408 |
| abstract_inverted_index.predominant | 159 |
| abstract_inverted_index.prevalence, | 263 |
| abstract_inverted_index.recognition | 381 |
| abstract_inverted_index.recognizing | 169 |
| abstract_inverted_index.resolution. | 49 |
| abstract_inverted_index.significant | 88 |
| abstract_inverted_index.spontaneous | 185 |
| abstract_inverted_index.Furthermore, | 204, 326 |
| abstract_inverted_index.IDR-enriched | 404 |
| abstract_inverted_index.composition, | 302 |
| abstract_inverted_index.demonstrated | 345 |
| abstract_inverted_index.interactome, | 284 |
| abstract_inverted_index.interactome. | 273 |
| abstract_inverted_index.membraneless | 231, 358 |
| abstract_inverted_index.recognition, | 46 |
| abstract_inverted_index.unexpectedly | 148 |
| abstract_inverted_index.G-quadruplex. | 203 |
| abstract_inverted_index.LLPS-mediated | 392 |
| abstract_inverted_index.Liquid-Liquid | 186 |
| abstract_inverted_index.comprehensive | 253 |
| abstract_inverted_index.computational | 256 |
| abstract_inverted_index.dysregulation | 399 |
| abstract_inverted_index.intrinsically | 103 |
| abstract_inverted_index.membrane-less | 393 |
| abstract_inverted_index.non-canonical | 198 |
| abstract_inverted_index.transcription | 232 |
| abstract_inverted_index.“functional | 320 |
| abstract_inverted_index.Interestingly, | 174 |
| abstract_inverted_index.bioinformatics | 254 |
| abstract_inverted_index.experimentally | 344 |
| abstract_inverted_index.non-canonical, | 2 |
| abstract_inverted_index.three-stranded | 3 |
| abstract_inverted_index.transcription, | 218 |
| abstract_inverted_index.R-loop-mediated | 128, 418 |
| abstract_inverted_index.high-throughput | 51 |
| abstract_inverted_index.patient-derived | 430 |
| abstract_inverted_index.single-stranded | 14 |
| abstract_inverted_index.topoisomerases), | 75 |
| abstract_inverted_index.thought-provoking | 366 |
| cited_by_percentile_year.max | 99 |
| cited_by_percentile_year.min | 97 |
| corresponding_author_ids | https://openalex.org/A5086367121 |
| countries_distinct_count | 2 |
| institutions_distinct_count | 10 |
| corresponding_institution_ids | https://openalex.org/I20388574 |
| citation_normalized_percentile.value | 0.89385285 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | True |