Oligomerization-mediated activation of a short prokaryotic Argonaute.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Sep 2023
Historique:
received: 18 01 2023
accepted: 19 07 2023
medline: 8 9 2023
pubmed: 27 7 2023
entrez: 26 7 2023
Statut: ppublish

Résumé

Although eukaryotic and long prokaryotic Argonaute proteins (pAgos) cleave nucleic acids, some short pAgos lack nuclease activity and hydrolyse NAD(P)

Identifiants

pubmed: 37494956
doi: 10.1038/s41586-023-06456-z
pii: 10.1038/s41586-023-06456-z
doi:

Substances chimiques

Apoproteins 0
Argonaute Proteins 0
DNA 9007-49-2
NAD 0U46U6E8UK
RNA 63231-63-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

154-161

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM124320
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM138997
Pays : United States

Informations de copyright

© 2023. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Koopal, B., Mutte, S. K. & Swarts, D. C. A long look at short prokaryotic Argonautes. Trends Cell Biol. 33, 605–618 (2023).
Koopal, B. et al. Short prokaryotic Argonaute systems trigger cell death upon detection of invading DNA. Cell 185, 1471–1486 (2022).
doi: 10.1016/j.cell.2022.03.012 pubmed: 35381200 pmcid: 9097488
Swarts, D. C. et al. The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21, 743–753 (2014).
doi: 10.1038/nsmb.2879 pubmed: 25192263 pmcid: 4691850
Vaucheret, H. Plant ARGONAUTES. Trends Plant Sci. 13, 350–358 (2008).
doi: 10.1016/j.tplants.2008.04.007 pubmed: 18508405
Nakanishi, K. Anatomy of four human Argonaute proteins. Nucleic Acids Res. 50, 6618–6638 (2022).
doi: 10.1093/nar/gkac519 pubmed: 35736234 pmcid: 9262622
Peters, L. & Meister, G. Argonaute proteins: mediators of RNA silencing. Mol. Cell 26, 611–623 (2007).
doi: 10.1016/j.molcel.2007.05.001 pubmed: 17560368
Lisitskaya, L., Aravin, A. A. & Kulbachinskiy, A. DNA interference and beyond: structure and functions of prokaryotic Argonaute proteins. Nat. Commun. 9, 5165 (2018).
doi: 10.1038/s41467-018-07449-7 pubmed: 30514832 pmcid: 6279821
Ryazansky, S., Kulbachinskiy, A. & Aravin, A. A. The expanded universe of prokaryotic Argonaute proteins. mBio 9, e01935-18 (2018).
Kuzmenko, A. et al. DNA targeting and interference by a bacterial Argonaute nuclease. Nature 587, 632–637 (2020).
doi: 10.1038/s41586-020-2605-1 pubmed: 32731256
Swarts, D. C. et al. DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507, 258–261 (2014).
doi: 10.1038/nature12971 pubmed: 24531762 pmcid: 4697943
Zander, A. et al. Guide-independent DNA cleavage by archaeal Argonaute from Methanocaldococcus jannaschii. Nat. Microbiol. 2, 17034 (2017).
doi: 10.1038/nmicrobiol.2017.34 pubmed: 28319081
Li, W. et al. A programmable pAgo nuclease with RNA target preference from the psychrotolerant bacterium Mucilaginibacter paludis. Nucleic Acids Res. 50, 5226–5238 (2022).
doi: 10.1093/nar/gkac315 pubmed: 35524569 pmcid: 9122594
Swarts, D. C. et al. Argonaute of the archaeon Pyrococcus furiosus is a DNA-guided nuclease that targets cognate DNA. Nucleic Acids Res. 43, 5120–5129 (2015).
doi: 10.1093/nar/gkv415 pubmed: 25925567 pmcid: 4446448
Kuzmenko, A., Yudin, D., Ryazansky, S., Kulbachinskiy, A. & Aravin, A. A. Programmable DNA cleavage by Ago nucleases from mesophilic bacteria Clostridium butyricum and Limnothrix rosea. Nucleic Acids Res. 47, 5822–5836 (2019).
doi: 10.1093/nar/gkz379 pubmed: 31114878 pmcid: 6582412
Hegge, J. W. et al. DNA-guided DNA cleavage at moderate temperatures by Clostridium butyricum Argonaute. Nucleic Acids Res. 47, 5809–5821 (2019).
doi: 10.1093/nar/gkz306 pubmed: 31069393 pmcid: 6582352
Jolly, S. M. et al. Thermus thermophilus Argonaute functions in the completion of DNA replication. Cell 182, 1545–1559 (2020).
doi: 10.1016/j.cell.2020.07.036 pubmed: 32846159 pmcid: 7502556
Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D. K. & Aravin, A. A. Bacterial argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51, 594–605 (2013).
doi: 10.1016/j.molcel.2013.08.014 pubmed: 24034694
Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Comprehensive comparative-genomic analysis of type 2 toxin–antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4, 19 (2009).
doi: 10.1186/1745-6150-4-19 pubmed: 19493340 pmcid: 2701414
Burroughs, A. M., Ando, Y. & Aravind, L. New perspectives on the diversification of the RNA interference system: insights from comparative genomics and small RNA sequencing. Wiley Interdiscip. Rev. RNA 5, 141–181 (2014).
doi: 10.1002/wrna.1210 pubmed: 24311560
Zaremba, M. et al. Short prokaryotic Argonautes provide defence against incoming mobile genetic elements through NAD
doi: 10.1038/s41564-022-01239-0 pubmed: 36192537
Zeng, Z. et al. A short prokaryotic Argonaute activates membrane effector to confer antiviral defense. Cell Host Microbe 30, 930–943 (2022).
doi: 10.1016/j.chom.2022.04.015 pubmed: 35594868
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).
doi: 10.1126/science.1102514 pubmed: 15284453
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
Elkayam, E. et al. The structure of human argonaute-2 in complex with miR-20a. Cell 150, 100–110 (2012).
doi: 10.1016/j.cell.2012.05.017 pubmed: 22682761 pmcid: 3464090
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
Shi, Y. et al. Structural basis of SARM1 activation, substrate recognition, and inhibition by small molecules. Mol. Cell 82, 1643–1659 (2022).
doi: 10.1016/j.molcel.2022.03.007 pubmed: 35334231 pmcid: 9188649
Hogrel, G. et al. Cyclic nucleotide-induced helical structure activates a TIR immune effector. Nature 608, 808–812 (2022).
doi: 10.1038/s41586-022-05070-9 pubmed: 35948638
Morehouse, B. R. et al. Cryo-EM structure of an active bacterial TIR-STING filament complex. Nature 608, 803–807 (2022).
doi: 10.1038/s41586-022-04999-1 pubmed: 35859168 pmcid: 9402430
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
Miyoshi, T., Ito, K., Murakami, R. & Uchiumi, T. Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute. Nat. Commun. 7, 11846 (2016).
doi: 10.1038/ncomms11846 pubmed: 27325485 pmcid: 4919518
Frank, F., Sonenberg, N. & Nagar, B. Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818–822 (2010).
doi: 10.1038/nature09039 pubmed: 20505670
Potocnik, A. & Swarts, D. C. Short prokaryotic Argonaute system repurposed as a nucleic acid detection tool. Clin. Transl. Med. 12, e1059 (2022).
doi: 10.1002/ctm2.1059 pubmed: 36163630 pmcid: 9513045
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
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
Rosenthal, P. B. & Henderson, R. Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol. 333, 721–745 (2003).
doi: 10.1016/j.jmb.2003.07.013 pubmed: 14568533
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126–2132 (2004).
doi: 10.1107/S0907444904019158 pubmed: 15572765
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
doi: 10.1107/S0907444909052925 pubmed: 20124702 pmcid: 2815670
Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).
doi: 10.1002/pro.3330 pubmed: 29067766
The PyMOL Molecular Graphics System v.2.5 (Schrödinger, 2022).
Pettersen, E. F. et al. UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci. 30, 70–82 (2021).
doi: 10.1002/pro.3943 pubmed: 32881101

Auteurs

Zhangfei Shen (Z)

Department of Biological Chemistry and Pharmacology, The Ohio State University, Columbus, OH, USA.
Comprehensive Cancer Center and Center for Cancer Metabolism, The Ohio State University, Columbus, OH, USA.

Xiao-Yuan Yang (XY)

Department of Biological Chemistry and Pharmacology, The Ohio State University, Columbus, OH, USA.
Comprehensive Cancer Center and Center for Cancer Metabolism, The Ohio State University, Columbus, OH, USA.
The Ohio State Biochemistry Program, The Ohio State University, Columbus, OH, USA.

Shiyu Xia (S)

Divison of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, USA.

Wei Huang (W)

Department of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, OH, USA.

Derek J Taylor (DJ)

Department of Pharmacology, Case Western Reserve University School of Medicine, Cleveland, OH, USA.
Department of Biochemistry, Case Western Reserve University School of Medicine, Cleveland, OH, USA.

Kotaro Nakanishi (K)

Department of Chemistry and Biochemistry, The Ohio State University, Columbus, OH, USA.

Tian-Min Fu (TM)

Department of Biological Chemistry and Pharmacology, The Ohio State University, Columbus, OH, USA. Fu.978@osu.edu.
Comprehensive Cancer Center and Center for Cancer Metabolism, The Ohio State University, Columbus, OH, USA. Fu.978@osu.edu.
The Ohio State Biochemistry Program, The Ohio State University, Columbus, OH, USA. Fu.978@osu.edu.

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