Home entertainment Structural insights into RNA cleavage by PIWI Argonaute

Structural insights into RNA cleavage by PIWI Argonaute

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  • Ozata, D. M., Gainetdinov, I., Zoch, A., O’Carroll, D. & Zamore, P. D. PIWI-interacting RNAs: small RNAs with big functions. Nat. Rev. Genet. 20, 89–108 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wang, X., Ramat, A., Simonelig, M. & Liu, M. F. Emerging roles and functional mechanisms of PIWI-interacting RNAs. Nat. Rev. Mol. Cell Biol. https://doi.org/10.1038/s41580-022-00528-0 (2023).

  • Matsumoto, N. et al. Crystal structure of silkworm PIWI-clade Argonaute Siwi bound to piRNA. Cell 167, 484–497.e9 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Anzelon, T. A. et al. Structural basis for piRNA targeting. Nature 597, 285–289 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li, Z. et al. Mammalian PIWI–piRNA–target complexes reveal features for broad and efficient target silencing. Nat. Struct. Mol. Biol. https://doi.org/10.1038/s41594-024-01287-6 (2024).

  • Arif, A. et al. GTSF1 accelerates target RNA cleavage by PIWI-clade Argonaute proteins. Nature 608, 618–625 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Meister, G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. https://doi.org/10.1038/nrg3462 (2013).

  • Aravin, A. et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203–207 (2006).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Girard, A., Sachidanandam, R., Hannon, G. J. & Carmell, M. A. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442, 199–202 (2006).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Grivna, S. T., Beyret, E., Wang, Z. & Lin, H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev. 20, 1709–1714 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Aravin, A. A., Sachidanandam, R., Girard, A., Fejes-Toth, K. & Hannon, G. J. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316, 744–747 (2007).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Lewis, S. H. et al. Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-017-0403-4 (2018).

  • Schnettler, E. et al. Knockdown of piRNA pathway proteins results in enhanced semliki forest virus production in mosquito cells. J. Gen. Virol. 94, 1680–1689 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Morazzani, E. M., Wiley, M. R., Murreddu, M. G., Adelman, Z. N. & Myles, K. M. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog. 8, e1002470 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Miesen, P., Girardi, E. & Van Rij, R. P. Distinct sets of PIWI proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucleic Acids Res. 43, 6545–6556 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yu, T. et al. The piRNA response to retroviral invasion of the koala genome. Cell https://doi.org/10.1016/j.cell.2019.09.002 (2019).

  • Brennecke, J. et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128, 1089–1103 (2007).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Gunawardane, L. S. et al. A slicer-mediated mechanism for repeat-associated siRNA 5′ end formation in Drosophila. Science https://doi.org/10.1126/science.1140494 (2007).

  • Wu, P. H. et al. The evolutionarily conserved piRNA-producing locus pi6 is required for male mouse fertility. Nat. Genet. 52, 728–739 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Goh, W. S. S. et al. PiRNA-directed cleavage of meiotic transcripts regulates spermatogenesis. Genes Dev. https://doi.org/10.1101/gad.260455.115 (2015).

  • Vourekas, A. et al. Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat. Struct. Mol. Biol. 19, 773–781 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, P. et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 25, 193–207 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Ohtani, H. et al. DmGTSF1 is necessary for Piwi-piRISC-mediated transcriptional transposon silencing in the Drosophila ovary. Genes Dev. 27, 1656–1661 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Dönertas, D., Sienski, G. & Brennecke, J. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev. 27, 1693–1705 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yoshimura, T. et al. Mouse GTSF 1 is an essential factor for secondary pi RNA biogenesis. EMBO Rep. https://doi.org/10.15252/embr.201642054 (2018).

  • Chang, T. H. et al. Maelstrom represses canonical polymerase II transcription within bi-directional piRNA clusters in Drosophila melanogaster. Mol. Cell 73, 291–303.e6 (2019).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Xiol, J. et al. RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts. Cell 157, 1698–1711 (2014).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Dai, S. et al. A family of C. elegans VASA homologs control Argonaute pathway specificity and promote transgenerational silencing. Cell Rep. 40, 111265 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Saxe, J. P., Chen, M., Zhao, H. & Lin, H. Tdrkh is essential for spermatogenesis and participates in primary piRNA biogenesis in the germline. EMBO J. 32, 1869–1885 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Wei, H. et al. piRNA loading triggers MIWI translocation from the intermitochondrial cement to chromatoid body during mouse spermatogenesis. Nat. Commun. 15, 2343 (2024).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Song, J. J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of argonaute and its implications for RISC slicer activity. Science 305, 1434–1437 (2004).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • 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).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 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).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Wang, Y. et al. Nucleation, propagation and cleavage of target RNAs in Ago silencing complexes. Nature 461, 754–761 (2009).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Schirle, N. T. & MacR, I. J. The crystal structure of human Argonaute2. Science 336, 1037–1040 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Elkayam, E. et al. The structure of human argonaute-2 in complex with miR-20a. Cell 150, 100–110 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Nakanishi, K., Weinberg, D. E., Bartel, D. P. & Patel, D. J. Structure of yeast Argonaute with guide RNA. Nature 486, 368–374 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Schirle, N. T., Sheu-Gruttadauria, J. & MacRae, I. J. Structural basis for microRNA targeting. Science 346, 608–613 (2014).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Klum, S. M., Chandradoss, S. D., Schirle, N. T., Joo, C. & MacRae, I. J. Helix‐7 in Argonaute2 shapes the microRNA seed region for rapid target recognition. EMBO J. 37, 75–88 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Sheu-Gruttadauria, J. et al. Structural basis for target-directed microRNA degradation. Mol. Cell 75, 1243–1255.e7 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Gainetdinov, I. et al. Relaxed targeting rules help PIWI proteins silence transposons. Nature 619, 394–402 (2023).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yuan, Y. R. et al. Crystal structure of A. aeolicus Argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19, 405–419 (2005).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Parker, J. S., Roe, S. M. & Barford, D. Crystal structure of a PIWI protein suggests mechanisms for siRNA recognition and slicer activity. EMBO J. 23, 4727–4737 (2004).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Xiao, Y., Maeda, S., Otomo, T. & MacRae, I. J. Structural basis for RNA slicing by a plant Argonaute. Nat. Struct. Mol. Biol. 30, 778–784 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Nakanishi, K. et al. Eukaryote-specific insertion elements control human ARGONAUTE Slicer activity. Cell Rep. 3, 1893–1900 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Chen, K. et al. Gtsf1 is essential for proper female sex determination and transposon silencing in the silkworm, Bombyx mori. PLoS Genet. 16, e1009194 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yoshimura, T. et al. Gtsf1/Cue110, a gene encoding a protein with two copies of a CHHC Zn-finger motif, is involved in spermatogenesis and retrotransposon suppression in murine testes. Dev. Biol. 335, 216–227 (2009).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Muerdter, F. et al. A genome-wide RNAi screen draws a genetic framework for transposon control and primary piRNA biogenesis in drosophila. Mol. Cell 50, 736–748 (2013).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Almeida, M. V. et al. GTSF‐1 is required for formation of a functional RNA‐dependent RNA Polymerase complex in Caenorhabditis elegans. EMBO J. 37, e99325 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sheu‐Gruttadauria, J., Xiao, Y., Gebert, L. F. & MacRae, I. J. Beyond the seed: structural basis for supplementary micro RNA targeting by human Argonaute2. EMBO J. 38, e101153 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 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).

    Article 
    ADS 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Yamaguchi, S. et al. Crystal structure of Drosophila Piwi. Nat. Commun. 11, 858 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Park, M. S. et al. Human Argonaute3 has slicer activity. Nucleic Acids Res. 45, 11867–11877 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 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.e6 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Gainetdinov, I. et al. Terminal modification, sequence, length, and PIWI-protein identity determine piRNA stability. Mol. Cell 81, 4826–4842.e8 (2021).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • 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).

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Scheres, S. H. W. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Wang, N. et al. Structural basis of human monocarboxylate transporter 1 inhibition by anti-cancer drug candidates. Cell 184, 370–383.e13 (2021).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D. Biol. Crystallogr. https://doi.org/10.1107/S0907444904019158 (2004).

  • Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D. Biol. Crystallogr. https://doi.org/10.1107/S0907444909052925 (2010).

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

  • Varadi, M. et al. AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 50, D439–D444 (2022).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar 

  • Abramson, J. et al. Accurate structure prediction of biomolecular interactions with AlphaFold 3. Nature 630, 493–500 (2024).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar 

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