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Enhancement of the seed-target recognition step in RNA silencing by a PIWI/MID domain protein.

<div class='caption-title'>Structure of AfPiwi in Complex with Duplex DNA</div>
<div class='caption-title'>Overview of Experimental Strategy</div>
<div class='caption-title'>Enhancement of the Seed-Target Interaction</div>
Parker JS, Parizotto EA, Wang M, Roe SM, Barford D
OpenAccess logo Mol Cell 33 204-14 (2009)
Cited: 89 times
EuropePMC logo PMID: 19187762

Abstract

Target recognition in RNA silencing is governed by the "seed sequence" of a guide RNA strand associated with the PIWI/MID domain of an Argonaute protein in RISC. Using a reconstituted in vitro target recognition system, we show that a model PIWI/MID domain protein confers position-dependent tightening and loosening of guide-strand-target interactions. Over the seed sequence, the interaction affinity is enhanced up to approximately 300-fold. Enhancement is achieved through a reduced entropy penalty for the interaction. In contrast, interactions 3' of the seed are inhibited. We quantified mismatched target recognition inside and outside the seed, revealing amplified discrimination at the third position in the seed mediated by the PIWI/MID domain. Thus, association of the guide strand with the PIWI/MID domain generates an enhanced affinity anchor site over the seed that can promote fidelity in target recognition and stabilize and guide the assembly of the active silencing complex.

Reviews - 2w42 mentioned but not cited (1)

  1. DNA interference and beyond: structure and functions of prokaryotic Argonaute proteins. Lisitskaya L, Aravin AA, Kulbachinskiy A. Nat Commun 9 5165 (2018)

Articles - 2w42 mentioned but not cited (5)

  1. Two novel PIWI families: roles in inter-genomic conflicts in bacteria and Mediator-dependent modulation of transcription in eukaryotes. Burroughs AM, Iyer LM, Aravind L. Biol Direct 8 13 (2013)
  2. Self-association of a highly charged arginine-rich cell-penetrating peptide. Tesei G, Vazdar M, Jensen MR, Cragnell C, Mason PE, Heyda J, Skepö M, Jungwirth P, Lund M. Proc Natl Acad Sci U S A 114 11428-11433 (2017)
  3. Local conformational changes in the DNA interfaces of proteins. Sunami T, Kono H. PLoS One 8 e56080 (2013)
  4. Prokaryotic Argonaute from Archaeoglobus fulgidus interacts with DNA as a homodimer. Golovinas E, Rutkauskas D, Manakova E, Jankunec M, Silanskas A, Sasnauskas G, Zaremba M. Sci Rep 11 4518 (2021)
  5. Structural basis for sequence-specific recognition of guide and target strands by the Archaeoglobus fulgidus Argonaute protein. Manakova E, Golovinas E, Pocevičiūtė R, Sasnauskas G, Grybauskas A, Gražulis S, Zaremba M. Sci Rep 13 6123 (2023)


Reviews citing this publication (22)

  1. Regulation of mRNA translation and stability by microRNAs. Fabian MR, Sonenberg N, Filipowicz W. Annu Rev Biochem 79 351-379 (2010)
  2. RNA-guided genetic silencing systems in bacteria and archaea. Wiedenheft B, Sternberg SH, Doudna JA. Nature 482 331-338 (2012)
  3. Diversifying microRNA sequence and function. Ameres SL, Zamore PD. Nat Rev Mol Cell Biol 14 475-488 (2013)
  4. Molecular mechanisms of RNA interference. Wilson RC, Doudna JA. Annu Rev Biophys 42 217-239 (2013)
  5. PIWI-interacting RNAs: small RNAs with big functions. Ozata DM, Gainetdinov I, Zoch A, O'Carroll D, Zamore PD. Nat Rev Genet 20 89-108 (2019)
  6. Identification and consequences of miRNA-target interactions--beyond repression of gene expression. Hausser J, Zavolan M. Nat Rev Genet 15 599-612 (2014)
  7. The evolutionary journey of Argonaute proteins. Swarts DC, Makarova K, Wang Y, Nakanishi K, Ketting RF, Koonin EV, Patel DJ, van der Oost J. Nat Struct Mol Biol 21 743-753 (2014)
  8. Exploring chemical modifications for siRNA therapeutics: a structural and functional outlook. Shukla S, Sumaria CS, Pradeepkumar PI. ChemMedChem 5 328-349 (2010)
  9. RNA-based recognition and targeting: sowing the seeds of specificity. Gorski SA, Vogel J, Doudna JA. Nat Rev Mol Cell Biol 18 215-228 (2017)
  10. Influenza virus non-structural protein NS1: interferon antagonism and beyond. Marc D. J Gen Virol 95 2594-2611 (2014)
  11. Eukaryotic Argonautes come into focus. Kuhn CD, Joshua-Tor L. Trends Biochem Sci 38 263-271 (2013)
  12. Structural Foundations of RNA Silencing by Argonaute. Sheu-Gruttadauria J, MacRae IJ. J Mol Biol 429 2619-2639 (2017)
  13. Concise review: The Piwi-piRNA axis: pivotal beyond transposon silencing. Bamezai S, Rawat VP, Buske C. Stem Cells 30 2603-2611 (2012)
  14. Evaluation and control of miRNA-like off-target repression for RNA interference. Seok H, Lee H, Jang ES, Chi SW. Cell Mol Life Sci 75 797-814 (2018)
  15. Mechanisms of MicroRNAs in Atherosclerosis. Schober A, Weber C. Annu Rev Pathol 11 583-616 (2016)
  16. Analysis of the roles of HIV-derived microRNAs. Narayanan A, Kehn-Hall K, Bailey C, Kashanchi F. Expert Opin Biol Ther 11 17-29 (2011)
  17. A prokaryotic twist on argonaute function. Willkomm S, Zander A, Gust A, Grohmann D. Life (Basel) 5 538-553 (2015)
  18. The AGO proteins: an overview. Niaz S. Biol Chem 399 525-547 (2018)
  19. Anatomy of four human Argonaute proteins. Nakanishi K. Nucleic Acids Res 50 6618-6638 (2022)
  20. Functional Features and Current Applications of the RNA-Targeting Type VI CRISPR-Cas Systems. Perčulija V, Lin J, Zhang B, Ouyang S. Adv Sci (Weinh) 8 2004685 (2021)
  21. Conformational Dynamics of Ago-Mediated Silencing Processes. Willkomm S, Restle T. Int J Mol Sci 16 14769-14785 (2015)
  22. PiRNA pathway in the cardiovascular system: a novel regulator of cardiac differentiation, repair and regeneration. Zhou Y, Fang Y, Dai C, Wang Y. J Mol Med (Berl) 99 1681-1690 (2021)

Articles citing this publication (61)

  1. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Garcia DM, Baek D, Shin C, Bell GW, Grimson A, Bartel DP. Nat Struct Mol Biol 18 1139-1146 (2011)
  2. Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Frank F, Sonenberg N, Nagar B. Nature 465 818-822 (2010)
  3. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Wang Y, Juranek S, Li H, Sheng G, Wardle GS, Tuschl T, Patel DJ. Nature 461 754-761 (2009)
  4. RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, Barendregt A, Westphal W, Heck AJ, Boekema EJ, Dickman MJ, Doudna JA. Proc Natl Acad Sci U S A 108 10092-10097 (2011)
  5. Structures of the RNA-guided surveillance complex from a bacterial immune system. Wiedenheft B, Lander GC, Zhou K, Jore MM, Brouns SJJ, van der Oost J, Doudna JA, Nogales E. Nature 477 486-489 (2011)
  6. An alternative mode of microRNA target recognition. Chi SW, Hannon GJ, Darnell RB. Nat Struct Mol Biol 19 321-327 (2012)
  7. Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Wee LM, Flores-Jasso CF, Flores-Jasso CF, Salomon WE, Zamore PD. Cell 151 1055-1067 (2012)
  8. Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. Ghildiyal M, Xu J, Seitz H, Weng Z, Zamore PD. RNA 16 43-56 (2010)
  9. Structure of yeast Argonaute with guide RNA. Nakanishi K, Weinberg DE, Bartel DP, Patel DJ. Nature 486 368-374 (2012)
  10. Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Grosswendt S, Filipchyk A, Manzano M, Klironomos F, Schilling M, Herzog M, Gottwein E, Rajewsky N. Mol Cell 54 1042-1054 (2014)
  11. miRNA-target chimeras reveal miRNA 3'-end pairing as a major determinant of Argonaute target specificity. Moore MJ, Scheel TK, Luna JM, Park CY, Fak JJ, Nishiuchi E, Rice CM, Darnell RB. Nat Commun 6 8864 (2015)
  12. Single-Molecule Imaging Reveals that Argonaute Reshapes the Binding Properties of Its Nucleic Acid Guides. Salomon WE, Jolly SM, Moore MJ, Zamore PD, Serebrov V. Cell 162 84-95 (2015)
  13. A Dynamic Search Process Underlies MicroRNA Targeting. Chandradoss SD, Schirle NT, Szczepaniak M, MacRae IJ, Joo C. Cell 162 96-107 (2015)
  14. Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Sheng G, Zhao H, Wang J, Rao Y, Tian W, Swarts DC, van der Oost J, Patel DJ, Wang Y. Proc Natl Acad Sci U S A 111 652-657 (2014)
  15. Crystal structure of the MID-PIWI lobe of a eukaryotic Argonaute protein. Boland A, Huntzinger E, Schmidt S, Izaurralde E, Weichenrieder O. Proc Natl Acad Sci U S A 108 10466-10471 (2011)
  16. Crystal structure and ligand binding of the MID domain of a eukaryotic Argonaute protein. Boland A, Tritschler F, Heimstädt S, Izaurralde E, Weichenrieder O. EMBO Rep 11 522-527 (2010)
  17. A bacterial Argonaute with noncanonical guide RNA specificity. Kaya E, Doxzen KW, Knoll KR, Wilson RC, Strutt SC, Kranzusch PJ, Doudna JA. Proc Natl Acad Sci U S A 113 4057-4062 (2016)
  18. The initial uridine of primary piRNAs does not create the tenth adenine that Is the hallmark of secondary piRNAs. Wang W, Yoshikawa M, Han BW, Izumi N, Tomari Y, Weng Z, Zamore PD. Mol Cell 56 708-716 (2014)
  19. Argonaute proteins. Cenik ES, Zamore PD. Curr Biol 21 R446-9 (2011)
  20. High-Throughput Analysis Reveals Rules for Target RNA Binding and Cleavage by AGO2. Becker WR, Ober-Reynolds B, Jouravleva K, Jolly SM, Zamore PD, Greenleaf WJ. Mol Cell 75 741-755.e11 (2019)
  21. A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Pandey SP, Minesinger BK, Kumar J, Walker GC. Nucleic Acids Res 39 4691-4708 (2011)
  22. Guide-bound structures of an RNA-targeting A-cleaving CRISPR-Cas13a enzyme. Knott GJ, East-Seletsky A, Cofsky JC, Holton JM, Charles E, O'Connell MR, Doudna JA. Nat Struct Mol Biol 24 825-833 (2017)
  23. How to slice: snapshots of Argonaute in action. Parker JS. Silence 1 3 (2010)
  24. Structural and mechanistic insights into an archaeal DNA-guided Argonaute protein. Willkomm S, Oellig CA, Zander A, Restle T, Keegan R, Grohmann D, Schneider S. Nat Microbiol 2 17035 (2017)
  25. Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute. Miyoshi T, Ito K, Murakami R, Uchiumi T. Nat Commun 7 11846 (2016)
  26. Functional specialization of Piwi proteins in Paramecium tetraurelia from post-transcriptional gene silencing to genome remodelling. Bouhouche K, Gout JF, Kapusta A, Bétermier M, Meyer E. Nucleic Acids Res 39 4249-4264 (2011)
  27. Mechanism of microRNA-target interaction: molecular dynamics simulations and thermodynamics analysis. Wang Y, Li Y, Ma Z, Yang W, Ai C. PLoS Comput Biol 6 e1000866 (2010)
  28. SKI2 mediates degradation of RISC 5'-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis. Branscheid A, Marchais A, Schott G, Lange H, Gagliardi D, Andersen SU, Voinnet O, Brodersen P. Nucleic Acids Res 43 10975-10988 (2015)
  29. Optochemical control of RNA interference in mammalian cells. Govan JM, Young DD, Lusic H, Liu Q, Lively MO, Deiters A. Nucleic Acids Res 41 10518-10528 (2013)
  30. Helix-7 in Argonaute2 shapes the microRNA seed region for rapid target recognition. Klum SM, Chandradoss SD, Schirle NT, Joo C, MacRae IJ. EMBO J 37 75-88 (2018)
  31. Programmable DNA cleavage by Ago nucleases from mesophilic bacteria Clostridium butyricum and Limnothrix rosea. Kuzmenko A, Yudin D, Ryazansky S, Kulbachinskiy A, Aravin AA. Nucleic Acids Res 47 5822-5836 (2019)
  32. The Expanded Universe of Prokaryotic Argonaute Proteins. Ryazansky S, Kulbachinskiy A, Aravin AA. mBio 9 e01935-18 (2018)
  33. Mature miRNAs form secondary structure, which suggests their function beyond RISC. Belter A, Gudanis D, Rolle K, Piwecka M, Gdaniec Z, Naskręt-Barciszewska MZ, Barciszewski J. PLoS One 9 e113848 (2014)
  34. An interplay of miRNA abundance and target site architecture determines miRNA activity and specificity. Brancati G, Großhans H. Nucleic Acids Res 46 3259-3269 (2018)
  35. The conformation of microRNA seed regions in native microRNPs is prearranged for presentation to mRNA targets. Lambert NJ, Gu SG, Zahler AM. Nucleic Acids Res 39 4827-4835 (2011)
  36. Gene silencing activity of siRNA molecules containing phosphorodithioate substitutions. Yang X, Sierant M, Janicka M, Peczek L, Martinez C, Hassell T, Li N, Li X, Wang T, Nawrot B. ACS Chem Biol 7 1214-1220 (2012)
  37. Regulation of Argonaute slicer activity by guide RNA 3' end interactions with the N-terminal lobe. Hur JK, Zinchenko MK, Djuranovic S, Green R. J Biol Chem 288 7829-7840 (2013)
  38. Short prokaryotic Argonaute systems trigger cell death upon detection of invading DNA. Koopal B, Potocnik A, Mutte SK, Aparicio-Maldonado C, Lindhoud S, Vervoort JJM, Brouns SJJ, Swarts DC. Cell 185 1471-1486.e19 (2022)
  39. Structural basis for piRNA targeting. Anzelon TA, Chowdhury S, Hughes SM, Xiao Y, Lander GC, MacRae IJ. Nature 597 285-289 (2021)
  40. Expansion of genes encoding piRNA-associated argonaute proteins in the pea aphid: diversification of expression profiles in different plastic morphs. Lu HL, Tanguy S, Rispe C, Gauthier JP, Walsh T, Gordon K, Edwards O, Tagu D, Chang CC, Jaubert-Possamai S. PLoS One 6 e28051 (2011)
  41. Structural and biochemical insights into 2'-O-methylation at the 3'-terminal nucleotide of RNA by Hen1. Mui Chan C, Zhou C, Brunzelle JS, Huang RH. Proc Natl Acad Sci U S A 106 17699-17704 (2009)
  42. Design of siRNA Therapeutics from the Molecular Scale. Angart P, Vocelle D, Chan C, Walton SP. Pharmaceuticals (Basel) 6 440-468 (2013)
  43. Complex role of microRNAs in HTLV-1 infections. Sampey GC, Van Duyne R, Currer R, Das R, Narayanan A, Kashanchi F. Front Genet 3 295 (2012)
  44. Sinorhizobium meliloti YbeY is an endoribonuclease with unprecedented catalytic features, acting as silencing enzyme in riboregulation. Saramago M, Peregrina A, Robledo M, Matos RG, Hilker R, Serrania J, Becker A, Arraiano CM, Jiménez-Zurdo JI. Nucleic Acids Res 45 1371-1391 (2017)
  45. Tertiary structure-based analysis of microRNA-target interactions. Gan HH, Gunsalus KC. RNA 19 539-551 (2013)
  46. Kinetic analysis of the effects of target structure on siRNA efficiency. Chen J, Zhang W. J Chem Phys 137 225102 (2012)
  47. Research Support, Non-U.S. Gov't The true core of RNA silencing revealed. Sasaki HM, Tomari Y. Nat Struct Mol Biol 19 657-660 (2012)
  48. Assembly and analysis of eukaryotic Argonaute-RNA complexes in microRNA-target recognition. Gan HH, Gunsalus KC. Nucleic Acids Res 43 9613-9625 (2015)
  49. Defining the seed sequence of the Cas12b CRISPR-Cas effector complex. Jain I, Minakhin L, Mekler V, Sitnik V, Rubanova N, Severinov K, Semenova E. RNA Biol 16 413-422 (2019)
  50. A Hyperthermophilic Argonaute From Ferroglobus placidus With Specificity on Guide Binding Pattern. Guo X, Sun Y, Chen L, Huang F, Liu Q, Feng Y. Front Microbiol 12 654345 (2021)
  51. A structural view of microRNA-target recognition. Leoni G, Tramontano A. Nucleic Acids Res 44 e82 (2016)
  52. Transcriptional Gene Silencing (TGS) via the RNAi Machinery in HIV-1 Infections. Sampey GC, Guendel I, Das R, Jaworski E, Klase Z, Narayanan A, Kehn-Hall K, Kashanchi F. Biology (Basel) 1 339-369 (2012)
  53. Structural and functional analyses reveal the contributions of the C- and N-lobes of Argonaute protein to selectivity of RNA target cleavage. Dayeh DM, Kruithoff BC, Nakanishi K. J Biol Chem 293 6308-6325 (2018)
  54. Prokaryotic Argonaute Proteins as a Tool for Biotechnology. Kropocheva EV, Lisitskaya LA, Agapov AA, Musabirov AA, Kulbachinskiy AV, Esyunina DM. Mol Biol 56 854-873 (2022)
  55. Effects of the PIWI/MID domain of Argonaute protein on the association of miRNAi's seed base with the target. Wang Z, Wang Y, Liu T, Wang Y, Zhang W. RNA 25 620-629 (2019)
  56. High-throughput biochemical profiling reveals functional adaptation of a bacterial Argonaute. Ober-Reynolds B, Becker WR, Jouravleva K, Jolly SM, Zamore PD, Greenleaf WJ. Mol Cell 82 1329-1342.e8 (2022)
  57. Single base mismatches in the mRNA target site allow specific seed region-mediated off-target binding of siRNA targeting human coagulation factor 7. Ravon M, Berrera M, Ebeling M, Certa U. RNA Biol 9 87-97 (2012)
  58. 3D Modeling of Non-coding RNA Interactions. Singh KP, Gupta S. Adv Exp Med Biol 1385 281-317 (2022)
  59. A tiny loop in the Argonaute PIWI domain tunes small RNA seed strength. Xiao Y, Liu TM, MacRae IJ. EMBO Rep 24 e55806 (2023)
  60. Profiling the Mismatch Tolerance of Argonaute 2 through Deep Sequencing of Sliced Polymorphic Viral RNAs. Theotokis PI, Usher L, Kortschak CK, Schwalbe E, Moschos SA. Mol Ther Nucleic Acids 9 22-33 (2017)
  61. Determining the defining lengths between mature microRNAs/small interfering RNAs and tinyRNAs. Sim G, Kehling AC, Park MS, Divoky C, Zhang H, Malhotra N, Secor J, Nakanishi K. Sci Rep 13 19761 (2023)


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