Cited by 246

Structural Basis for Target-Directed MicroRNA Degradation

Sheu-Gruttadauria, Jessica, Pawlica, Paulina, Klum, Shannon M., Wang, Sonia, Yario, Therese A., Schirle Oakdale, Nicole T., Steitz, Joan A., MacRae, Ian J.·2019·Molecular Cell

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.molcel.2019.06.019

Cites

4 of 4 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • TDMD may promote dissociation of the 3' end of the miRNA from the Argonaute protein, thereby exposing the 3' end to modifications that lead to miRNA degradation.

    “TDMD may promote dissociation of the 3′ end of the miRNA from the Argonaute protein, thereby exposing the 3′ end to modifications that lead to miRNA degradation (Sheu‐Gruttadauria et al., 2019; Yang et al., 2020).”

    From microRNA strand selection: Unwinding the rules (2021) · cites this paper as Sheu-Gruttadauria et al., 2019

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

Flagged first, then by citations

Research works printed but not linked: 69

  1. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta crystallographica Section D, Biological crystallography 66, 213– 221. 20124702 PMC2815670
  2. Ameres SL, Horwich MD, Hung JH, Xu J, Ghildiyal M, Weng Z, and Zamore PD (2010). Target RNA-directed trimming and tailing of small silencing RNAs. Science 328, 1534– 1539. 20558712 PMC2902985
  3. Ameres SL, Hung JH, Xu J, Weng Z, and Zamore PD (2011). Target RNA-directed tailing and trimming purifies the sorting of endo-siRNAs between the two Drosophila Argonaute proteins. RNA 17, 54– 63. 21106652 PMC3004066
  4. Baccarini A, Chauhan H, Gardner TJ, Jayaprakash AD, Sachidanandam R, and Brown BD (2011). Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Current biology: CB 21, 369– 376. 21353554 PMC3088433
  5. Bartel DP (2018). Metazoan MicroRNAs. Cell 173, 20– 51. 29570994 PMC6091663
  6. Bitetti A, Mallory AC, Golini E, Carrieri C, Carreno Gutierrez H, Perlas E, Perez-Rico YA, Tocchini-Valentini GP, Enright AJ, Norton WHJ, (2018). MicroRNA degradation by a conserved target RNA regulates animal behavior. Nature structural & molecular biology 25, 244– 251. 29483647
  7. Cazalla D, Yario T, and Steitz JA (2010). Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328, 1563– 1566. 20558719 PMC3075239
  8. Crooks GE, Hon G, Chandonia JM, and Brenner SE (2004). WebLogo: a sequence logo generator. Genome research 14, 1188– 1190. 15173120 PMC419797
  9. D’Ambrogio A, Gu W, Udagawa T, Mello CC, and Richter JD (2012). Specific miRNA stabilization by Gld2-catalyzed monoadenylation. Cell Rep 2, 1537– 1545. 23200856 PMC3534910
  10. de la Mata M, Gaidatzis D, Vitanescu M, Stadler MB, Wentzel C, Scheiffele P, Filipowicz W, and Grosshans H (2015). Potent degradation of neuronal miRNAs induced by highly complementary targets. EMBO reports 16, 500– 511. 25724380 PMC4388616
  11. De N, Young L, Lau PW, Meisner NC, Morrissey DV, and Macrae IJ (2013). Highly Complementary Target RNAs Promote Release of Guide RNAs from Human Argonaute2. Molecular cell 50, 344– 355. 23664376 PMC3746828
  12. Desvignes T, Batzel P, Berezikov E, Eilbeck K, Eppig JT, McAndrews MS, Singer A, and Postlethwait JH (2015). miRNA Nomenclature: A View Incorporating Genetic Origins, Biosynthetic Pathways, and Sequence Variants. Trends in genetics: TIG 31, 613– 626. 26453491 PMC4639415
  13. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, and Gingeras TR (2013). STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15– 21. 23104886 PMC3530905
  14. Duffy EE, Rutenberg-Schoenberg M, Stark CD, Kitchen RR, Gerstein MB, and Simon MD (2015). Tracking Distinct RNA Populations Using Efficient and Reversible Covalent Chemistry. Molecular cell 59, 858– 866. 26340425 PMC4560836
  15. Elbarbary RA, Miyoshi K, Myers JR, Du P, Ashton JM, Tian B, and Maquat LE (2017). Tudor-SN-mediated endonucleolytic decay of human cell microRNAs promotes G1/S phase transition. Science 356, 859– 862. 28546213 PMC5551500
  16. Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, and Tuschl T (2001). Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. The EMBO journal 20, 6877– 6888. 11726523 PMC125328
  17. Emsley P, Lohkamp B, Scott WG, and Cowtan K (2010). Features and development of Coot. Acta crystallographica Section D, Biological crystallography 66, 486– 501. 20383002 PMC2852313
  18. Faehnle CR, Elkayam E, Haase AD, Hannon GJ, and Joshua-Tor L (2013). The making of a slicer: activation of human Argonaute-1. Cell Rep 3, 1901– 1909. 23746446 PMC3769929
  19. Fan XC, Myer VE, and Steitz JA (1997). AU-rich elements target small nuclear RNAs as well as mRNAs for rapid degradation. Genes & development 11, 2557– 2568. 9334320 PMC316563
  20. Flores-Jasso CF, Salomon WE, and Zamore PD (2013). Rapid and specific purification of Argonaute-small RNA complexes from crude cell lysates. RNA 19, 271– 279. 23249751 PMC3543083
  21. Fuchs Wightman F, Giono LE, Fededa JP, and de la Mata M (2018). Target RNAs Strike Back on MicroRNAs. Frontiers in Genetics 9. PMC6175985 30333855
  22. Gebert LFR, and MacRae IJ (2018). Regulation of microRNA function in animals. Nature reviews Molecular cell biology. PMC6546304 30108335
  23. Ghini F, Rubolino C, Climent M, Simeone I, Marzi MJ, and Nicassio F (2018). Endogenous transcripts control miRNA levels and activity in mammalian cells by target-directed miRNA degradation. Nature communications 9, 3119. PMC6081425 30087332
  24. Guo YE, Riley KJ, Iwasaki A, and Steitz JA (2014). Alternative capture of noncoding RNAs or protein-coding genes by herpesviruses to alter host T cell function. Molecular cell 54, 67– 79. 24725595 PMC4039351
  25. Hafner M, Renwick N, Brown M, Mihailovic A, Holoch D, Lin C, Pena JT, Nusbaum JD, Morozov P, Ludwig J, (2011). RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. RNA 17, 1697– 1712. 21775473 PMC3162335
  26. Hauptmann J, Dueck A, Harlander S, Pfaff J, Merkl R, and Meister G (2013). Turning catalytically inactive human Argonaute proteins into active slicer enzymes. Nature structural & molecular biology. 23665583
  27. Horman SR, Janas MM, Litterst C, Wang B, Macrae IJ, Sever MJ, Morrissey DV, Graves P, Luo B, Umesalma S, (2013). Akt-Mediated Phosphorylation of Argonaute 2 Downregulates Cleavage and Upregulates Translational Repression of MicroRNA Targets. Molecular cell 50, 356– 367. 23603119 PMC3654076
  28. Hur JK, Zinchenko MK, Djuranovic S, and Green R (2013). Regulation of Argonaute Slicer Activity by Guide RNA 3′ End Interactions with the N-terminal Lobe. The Journal of biological chemistry 288, 7829– 7840. 23329841 PMC3597821
  29. Jo MH, Shin S, Jung SR, Kim E, Song JJ, and Hohng S (2015). Human Argonaute 2 Has Diverse Reaction Pathways on Target RNAs. Molecular cell 59, 117– 124. 26140367
  30. Kabsch W (2010). Xds. Acta crystallographica Section D, Biological crystallography 66, 125– 132. 20124692 PMC2815665
  31. Katoh K, Misawa K, Kuma K, and Miyata T (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30, 3059– 3066. 12136088 PMC135756
  32. Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T, and Suzuki T (2009). Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes & development 23, 433– 438. 19240131 PMC2648654
  33. Kawamata T, Seitz H, and Tomari Y (2009). Structural determinants of miRNAs for RISC loading and slicer-independent unwinding. Nature structural & molecular biology 16, 953– 960. 19684602
  34. Kim B, Ha M, Loeff L, Chang H, Simanshu DK, Li S, Fareh M, Patel DJ, Joo C, and Kim VN (2015). TUT7 controls the fate of precursor microRNAs by using three different uridylation mechanisms. The EMBO journal 34, 1801– 1815. 25979828 PMC4516432
  35. Kleaveland B, Shi CY, Stefano J, and Bartel DP (2018). A Network of Noncoding Regulatory RNAs Acts in the Mammalian Brain. Cell. PMC6559361 29887379
  36. Klum SM, Chandradoss SD, Schirle NT, Joo C, and MacRae IJ (2017). Helix-7 in Argonaute2 shapes the microRNA seed region for rapid target recognition. The EMBO journal. PMC5753032 28939659
  37. Klum SM, Chandradoss SD, Schirle NT, Joo C, and MacRae IJ (2018). Helix-7 in Argonaute2 shapes the microRNA seed region for rapid target recognition. The EMBO journal 37, 75– 88. 28939659 PMC5753032
  38. Kwak PB, and Tomari Y (2012). The N domain of Argonaute drives duplex unwinding during RISC assembly. Nature structural & molecular biology. 22233755
  39. Lee S, Song J, Kim S, Kim J, Hong Y, Kim Y, Kim D, Baek D, and Ahn K (2013). Selective degradation of host MicroRNAs by an intergenic HCMV noncoding RNA accelerates virus production. Cell host & microbe 13, 678– 690. 23768492
  40. Lerner EA, Lerner MR, Janeway CA Jr., and Steitz JA (1981). Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proceedings of the National Academy of Sciences of the United States of America 78, 2737– 2741. 6789322 PMC319432
  41. Libri V, Helwak A, Miesen P, Santhakumar D, Borger JG, Kudla G, Grey F, Tollervey D, and Buck AH (2012). Murine cytomegalovirus encodes a miR-27 inhibitor disguised as a target. Proceedings of the National Academy of Sciences of the United States of America 109, 279– 284. 22184245 PMC3252920
  42. Ma JB, Ye K, and Patel DJ (2004). Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318– 322. 15152257 PMC4700412
  43. Marcinowski L, Tanguy M, Krmpotic A, Radle B, Lisnic VJ, Tuddenham L, Chane-Woon-Ming B, Ruzsics Z, Erhard F, Benkartek C, (2012). Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS pathogens 8, e1002510. 22346748 PMC3276556
  44. Marzi MJ, Ghini F, Cerruti B, de Pretis S, Bonetti P, Giacomelli C, Gorski MM, Kress T, Pelizzola M, Muller H, (2016). Degradation dynamics of microRNAs revealed by a novel pulse-chase approach. Genome research 26, 554– 565. 26821571 PMC4817778
  45. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, and Read RJ (2007). Phaser crystallographic software. J Appl Crystallogr 40, 658– 674. 19461840 PMC2483472
  46. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, and Tuschl T (2004). Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Molecular cell 15, 185– 197. 15260970
  47. Nakanishi K, Ascano M, Gogakos T, Ishibe-Murakami S, Serganov AA, Briskin D, Morozov P, Tuschl T, and Patel DJ (2013). Eukaryote-specific insertion elements control human ARGONAUTE slicer activity. Cell Rep 3, 1893– 1900. 23809764 PMC3757560
  48. Nakel K, Bonneau F, Eckmann CR, and Conti E (2015). Structural basis for the activation of the C. elegans noncanonical cytoplasmic poly(A)-polymerase GLD-2 by GLD-3. Proceedings of the National Academy of Sciences of the United States of America 112, 8614– 8619. 26124149 PMC4507228
  49. Neilsen CT, Goodall GJ, and Bracken CP (2012). IsomiRs--the overlooked repertoire in the dynamic microRNAome. Trends in genetics: TIG 28, 544– 549. 22883467
  50. Pall GS, and Hamilton AJ (2008). Improved northern blot method for enhanced detection of small RNA. Nat Protoc 3, 1077– 1084. 18536652
  51. Park JH, Shin SY, and Shin C (2017). Non-canonical targets destabilize microRNAs in human Argonautes. Nucleic acids research 45, 1569– 1583. 28119422 PMC5389725
  52. Pawlica P, Moss WN, and Steitz JA (2016). Host miRNA degradation by Herpesvirus saimiri small nuclear RNA requires an unstructured interacting region. RNA 22, 1181– 1189. 27335146 PMC4931111
  53. Rajappa-Titu L, Suematsu T, Munoz-Tello P, Long M, Demir O, Cheng KJ, Stagno JR, Luecke H, Amaro RE, Aphasizheva I, (2016). RNA Editing TUTase 1: structural foundation of substrate recognition, complex interactions and drug targeting. Nucleic acids research 44, 10862– 10878. 27744351 PMC5159558
  54. Reuter JS, and Mathews DH (2010). RNAstructure: software for RNA secondary structure prediction and analysis. BMC bioinformatics 11, 129. 20230624 PMC2984261
  55. Robinson MD, McCarthy DJ, and Smyth GK (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139– 140. 19910308 PMC2796818
  56. Ruegger S, and Grosshans H (2012). MicroRNA turnover: when, how, and why. Trends Biochem Sci 37, 436– 446. 22921610
  57. Salomon WE, Jolly SM, Moore MJ, Zamore PD, and Serebrov V (2015). Single-Molecule Imaging Reveals that Argonaute Reshapes the Binding Properties of Its Nucleic Acid Guides. Cell 162, 84– 95. 26140592 PMC4503223
  58. Schirle NT, and MacRae IJ (2012). The crystal structure of human Argonaute2. Science 336, 1037– 1040. 22539551 PMC3521581
  59. Schirle NT, Sheu-Gruttadauria J, and MacRae IJ (2014). Structural basis for microRNA targeting. Science 346, 608– 613. 25359968 PMC4313529
  60. Sheu-Gruttadauria J, Xiao Y, Gebert LF, and MacRae IJ (2019). Beyond the seed: structural basis for supplementary microRNA targeting by human Argonaute2. The EMBO journal, e101153. PMC6600645 31268608
  61. Song J, Song J, Mo B, and Chen X (2015). Uridylation and adenylation of RNAs. Sci China Life Sci 58, 1057– 1066. 26563174 PMC5089844
  62. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, and Patel DJ (2008). Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921– 926. 19092929 PMC2765400
  63. Wang Y, Juranek S, Li H, Sheng G, Wardle GS, Tuschl T, and Patel DJ (2009). Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754– 761. 19812667 PMC2880917
  64. Wee LM, Flores-Jasso CF, Salomon WE, and Zamore PD (2012). Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Cell 151, 1055– 1067. 23178124 PMC3595543
  65. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, (2011). Overview of the CCP4 suite and current developments. Acta crystallographica Section D, Biological crystallography 67, 235– 242. 21460441 PMC3069738
  66. Wu M, Reuter M, Lilie H, Liu Y, Wahle E, and Song H (2005). Structural insight into poly(A) binding and catalytic mechanism of human PARN. The EMBO journal 24, 4082– 4093. 16281054 PMC1356309
  67. Xie J, Ameres SL, Friedline R, Hung JH, Zhang Y, Xie Q, Zhong L, Su Q, He R, Li M, (2012). Long-term, efficient inhibition of microRNA function in mice using rAAV vectors. Nature methods 9, 403– 409. 22388288 PMC3420816
  68. Zeng Y, Sankala H, Zhang X, and Graves PR (2008). Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. The Biochemical journal 413, 429– 436. 18476811
  69. Zhuang F, Fuchs RT, Sun Z, Zheng Y, and Robb GB (2012). Structural bias in T4 RNA ligase-mediated 3′-adapter ligation. Nucleic Acids Res 40, e54. 22241775 PMC3326334

Cited by

Sorted by citations

Authors
Sheu-Gruttadauria, J., Pawlica, P., Klum, S. M., Wang, S., Yario, T. A., Schirle Oakdale, N. T., Steitz, J. A., & MacRae, I. J.
Venue
Molecular Cell
Publisher
Elsevier BV
Published
2019-09
Volume
75
Issue
6
Pages
1243-1255.e7
ISSN
1097-2765
Cited by
246
References
4
Language
en
Funders
  • U.S. Department of Energy (DE-AC02-76SF00515)
  • National Cancer Institute (CA016038)
  • American Cancer Society (PF-18-1124-01-RMC)
  • American Heart Association
  • National Institutes of Health
  • National Institute of General Medical Sciences (K99GM129412, DE-AC02-06CH11357, GM127090, P41GM103393, GM104475, GM115649)
  • Howard Hughes Medical Institute

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