Structural basis for RNA slicing by a plant Argonaute.
Journal
Nature structural & molecular biology
ISSN: 1545-9985
Titre abrégé: Nat Struct Mol Biol
Pays: United States
ID NLM: 101186374
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
received:
25
04
2022
accepted:
06
04
2023
medline:
21
6
2023
pubmed:
2
5
2023
entrez:
1
5
2023
Statut:
ppublish
Résumé
Argonaute (AGO) proteins use small RNAs to recognize transcripts targeted for silencing in plants and animals. Many AGOs cleave target RNAs using an endoribonuclease activity termed 'slicing'. Slicing by DNA-guided prokaryotic AGOs has been studied in detail, but structural insights into RNA-guided slicing by eukaryotic AGOs are lacking. Here we present cryogenic electron microscopy structures of the Arabidopsis thaliana Argonaute10 (AtAgo10)-guide RNA complex with and without a target RNA representing a slicing substrate. The AtAgo10-guide-target complex adopts slicing-competent and slicing-incompetent conformations that are unlike known prokaryotic AGO structures. AtAgo10 slicing activity is licensed by docking target (t) nucleotides t9-t13 into a surface channel containing the AGO endoribonuclease active site. A β-hairpin in the L1 domain secures the t9-t13 segment and coordinates t9-t13 docking with extended guide-target pairing. Results show that prokaryotic and eukaryotic AGOs use distinct mechanisms for achieving target slicing and provide insights into small interfering RNA potency.
Identifiants
pubmed: 37127820
doi: 10.1038/s41594-023-00989-7
pii: 10.1038/s41594-023-00989-7
doi:
Substances chimiques
Argonaute Proteins
0
RNA, Small Interfering
0
RNA, Plant
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
778-784Subventions
Organisme : NIGMS NIH HHS
ID : R35 GM127090
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM092740
Pays : United States
Organisme : NIH HHS
ID : S10 OD021634
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature America, Inc.
Références
Singh, A. et al. Plant small RNAs: advancement in the understanding of biogenesis and role in plant development. Planta 248, 545–558 (2018).
doi: 10.1007/s00425-018-2927-5
pubmed: 29968061
Bartel, D. P. Metazoan microRNAs. Cell 173, 20–51 (2018).
doi: 10.1016/j.cell.2018.03.006
pubmed: 29570994
pmcid: 6091663
Iwakawa, H. O. & Tomari, Y. Life of RISC: formation, action, and degradation of RNA-induced silencing complex. Mol. Cell 82, 30–43 (2022).
doi: 10.1016/j.molcel.2021.11.026
pubmed: 34942118
Zamore, P. D., Tuschl, T., Sharp, P. A. & Bartel, D. P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101, 25–33 (2000).
doi: 10.1016/S0092-8674(00)80620-0
pubmed: 10778853
Hu, B. et al. Therapeutic siRNA: state of the art. Signal Transduct. Target Ther. 5, 101 (2020).
doi: 10.1038/s41392-020-0207-x
pubmed: 32561705
pmcid: 7305320
Llave, C., Xie, Z., Kasschau, K. D. & Carrington, J. C. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053–2056 (2002).
doi: 10.1126/science.1076311
pubmed: 12242443
Allen, E., Xie, Z., Gustafson, A. M. & Carrington, J. C. MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221 (2005).
doi: 10.1016/j.cell.2005.04.004
pubmed: 15851028
Axtell, M. J., Jan, C., Rajagopalan, R. & Bartel, D. P. A two-hit trigger for siRNA biogenesis in plants. Cell 127, 565–577 (2006).
doi: 10.1016/j.cell.2006.09.032
pubmed: 17081978
Creasey, K. M. et al. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508, 411–415 (2014).
doi: 10.1038/nature13069
pubmed: 24670663
pmcid: 4074602
Sheng, G. et al. Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. Proc. Natl Acad. Sci. USA 111, 652–657 (2014).
doi: 10.1073/pnas.1321032111
pubmed: 24374628
Wang, Y. et al. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754–761 (2009).
doi: 10.1038/nature08434
pubmed: 19812667
pmcid: 2880917
Ober-Reynolds, B. et al. High-throughput biochemical profiling reveals functional adaptation of a bacterial Argonaute. Mol. Cell 82, 1329–1342 e1328 (2022).
doi: 10.1016/j.molcel.2022.02.026
pubmed: 35298909
pmcid: 9158488
Wang, Y. et al. Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456, 921–926 (2008).
doi: 10.1038/nature07666
pubmed: 19092929
pmcid: 2765400
Wang, Y., Sheng, G., Juranek, S., Tuschl, T. & Patel, D. J. Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209–213 (2008).
doi: 10.1038/nature07315
pubmed: 18754009
pmcid: 4689319
Wee, L. M., Flores-Jasso, C. F., Salomon, W. E. & Zamore, P. D. Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Cell 151, 1055–1067 (2012).
doi: 10.1016/j.cell.2012.10.036
pubmed: 23178124
pmcid: 3595543
Becker, W. R. et al. High-throughput analysis reveals rules for target RNA binding and cleavage by AGO2. Mol. Cell https://doi.org/10.1016/j.molcel.2019.06.012 (2019).
doi: 10.1016/j.molcel.2019.06.012
pubmed: 31324449
pmcid: 6823844
Niaz, S. The AGO proteins: an overview. Biol. Chem. 399, 525–547 (2018).
doi: 10.1515/hsz-2017-0329
pubmed: 29447113
Pourjafar-Dehkordi, D. & Zacharias, M. Binding-induced functional-domain motions in the Argonaute characterized by adaptive advanced sampling. PLoS Comput. Biol. 17, e1009625 (2021).
doi: 10.1371/journal.pcbi.1009625
pubmed: 34843451
pmcid: 8683029
Sheu-Gruttadauria, J., Xiao, Y., Gebert, L. F. & MacRae, I. J. Beyond the seed: structural basis for supplementary microRNA targeting by human Argonaute2. EMBO J. https://doi.org/10.15252/2Fembj.2018101153 (2019).
Sheu-Gruttadauria, J. et al. Structural basis for target-directed microRNA degradation. Mol. Cell https://doi.org/10.1016/j.molcel.2019.06.019 (2019).
doi: 10.1016/j.molcel.2019.06.019
pubmed: 31353209
pmcid: 6754277
Nakanishi, K., Weinberg, D. E., Bartel, D. P. & Patel, D. J. Structure of yeast Argonaute with guide RNA. Nature 486, 368–374 (2012).
doi: 10.1038/nature11211
pubmed: 22722195
pmcid: 3853139
Schirle, N. T. & MacRae, I. J. The crystal structure of human Argonaute2. Science 336, 1037–1040 (2012).
doi: 10.1126/science.1221551
pubmed: 22539551
pmcid: 3521581
Nakanishi, K. et al. Eukaryote-specific insertion elements control human ARGONAUTE slicer activity. Cell Rep. 3, 1893–1900 (2013).
doi: 10.1016/j.celrep.2013.06.010
pubmed: 23809764
pmcid: 3757560
Park, M. S. et al. Human Argonaute3 has slicer activity. Nucleic Acids Res. 45, 11867–11877 (2017).
doi: 10.1093/nar/gkx916
pubmed: 29040713
pmcid: 5714244
Park, M. S. et al. Multidomain convergence of argonaute during RISC assembly correlates with the formation of internal water clusters. Mol. Cell 75, 725–740 e726 (2019).
doi: 10.1016/j.molcel.2019.06.011
pubmed: 31324450
pmcid: 6707842
Faehnle, C. R., Elkayam, E., Haase, A. D., Hannon, G. J. & Joshua-Tor, L. The making of a slicer: activation of human Argonaute-1. Cell Rep. 3, 1901–1909 (2013).
doi: 10.1016/j.celrep.2013.05.033
pubmed: 23746446
pmcid: 3769929
Elbashir, S. M., Lendeckel, W. & Tuschl, T. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 15, 188–200 (2001).
doi: 10.1101/gad.862301
pubmed: 11157775
pmcid: 312613
Nowotny, M., Gaidamakov, S. A., Crouch, R. J. & Yang, W. Crystal structures of RNase H bound to an RNA/DNA hybrid: substrate specificity and metal-dependent catalysis. Cell 121, 1005–1016 (2005).
doi: 10.1016/j.cell.2005.04.024
pubmed: 15989951
Schirle, N. T., Sheu-Gruttadauria, J. & MacRae, I. J. Structural basis for microRNA targeting. Science 346, 608–613 (2014).
doi: 10.1126/science.1258040
pubmed: 25359968
pmcid: 4313529
Schwarz, D. S. et al. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115, 199–208 (2003).
doi: 10.1016/S0092-8674(03)00759-1
pubmed: 14567917
Khvorova, A., Reynolds, A. & Jayasena, S. D. Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209–216 (2003).
doi: 10.1016/S0092-8674(03)00801-8
pubmed: 14567918
Ameres, S. L., Martinez, J. & Schroeder, R. Molecular basis for target RNA recognition and cleavage by human RISC. Cell 130, 101–112 (2007).
doi: 10.1016/j.cell.2007.04.037
pubmed: 17632058
Reynolds, A. et al. Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326–330 (2004).
doi: 10.1038/nbt936
pubmed: 14758366
Suloway, C. et al. Automated molecular microscopy: the new Leginon system. J. Struct. Biol. 151, 41–60 (2005).
doi: 10.1016/j.jsb.2005.03.010
pubmed: 15890530
Kimanius, D., Forsberg, B. O., Scheres, S. H. & Lindahl, E. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife https://doi.org/10.7554/eLife.18722 (2016).
Zhang, K. Gctf: real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016).
doi: 10.1016/j.jsb.2015.11.003
pubmed: 26592709
pmcid: 4711343
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
doi: 10.1038/nmeth.4169
pubmed: 28165473
Tan, Y. Z. et al. Addressing preferred specimen orientation in single-particle cryo-EM through tilting. Nat. Methods 14, 793–796 (2017).
doi: 10.1038/nmeth.4347
pubmed: 28671674
pmcid: 5533649
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
doi: 10.1038/nmeth.4193
pubmed: 28250466
pmcid: 5494038
Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95–102 (2009).
doi: 10.1016/j.jsb.2009.01.002
pubmed: 19263523
pmcid: 2775544
Goddard, T. D., Huang, C. C. & Ferrin, T. E. Visualizing density maps with UCSF Chimera. J. Struct. Biol. 157, 281–287 (2007).
doi: 10.1016/j.jsb.2006.06.010
pubmed: 16963278
Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
doi: 10.1002/jcc.20084
pubmed: 15264254
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. Sect. D 66, 486–501 (2010).
doi: 10.1107/S0907444910007493
Liebschner, D. et al. Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix. Acta Crystallogr. Sect. D 75, 861–877 (2019).
Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545–W549 (2010).
doi: 10.1093/nar/gkq366
pubmed: 20457744
pmcid: 2896194