A viral ADP-ribosyltransferase attaches RNA chains to host proteins.
ADP Ribose Transferases
/ metabolism
Bacteriophage T4
/ enzymology
Escherichia coli
/ genetics
NAD
/ metabolism
Ribosomal Proteins
/ chemistry
Viral Proteins
/ metabolism
Escherichia coli Proteins
/ chemistry
RNA
/ chemistry
Protein Biosynthesis
Gene Expression Regulation, Bacterial
Protein Processing, Post-Translational
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
04
06
2021
accepted:
12
07
2023
medline:
1
9
2023
pubmed:
17
8
2023
entrez:
16
8
2023
Statut:
ppublish
Résumé
The mechanisms by which viruses hijack the genetic machinery of the cells they infect are of current interest. When bacteriophage T4 infects Escherichia coli, it uses three different adenosine diphosphate (ADP)-ribosyltransferases (ARTs) to reprogram the transcriptional and translational apparatus of the host by ADP-ribosylation using nicotinamide adenine dinucleotide (NAD) as a substrate
Identifiants
pubmed: 37587340
doi: 10.1038/s41586-023-06429-2
pii: 10.1038/s41586-023-06429-2
pmc: PMC10468400
doi:
Substances chimiques
ADP Ribose Transferases
EC 2.4.2.-
NAD
0U46U6E8UK
Ribosomal Proteins
0
Viral Proteins
0
Escherichia coli Proteins
0
RNA
63231-63-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1054-1062Informations de copyright
© 2023. The Author(s).
Références
Tiemann, B. et al. ModA and ModB, two ADP-ribosyltransferases encoded by bacteriophage T4: catalytic properties and mutation analysis. J. Bacteriol. 186, 7262–7272 (2004).
pubmed: 15489438
pmcid: 523198
doi: 10.1128/JB.186.21.7262-7272.2004
Koch, T., Raudonikiene, A., Wilkens, K. & Rüger, W. Over expression, purification, and characterization of the ADP-ribosyltransferase (gpAlt) of bacteriophage T4: ADP-ribosylation of E. coli RNA polymerase modulates T4 “early” transcription. Gene Expr. 4, 253–264 (1995).
pubmed: 7787417
Cahová, H., Winz, M. L., Höfer, K., Nübel, G. & Jäschke, A. NAD captureSeq indicates NAD as a bacterial cap for a subset of regulatory RNAs. Nature 519, 374–377 (2015).
pubmed: 25533955
doi: 10.1038/nature14020
Chen, Y. G., Kowtoniuk, W. E., Agarwal, I., Shen, Y. & Liu, D. R. LC/MS analysis of cellular RNA reveals NAD-linked RNA. Nat. Chem. Biol. 5, 879–881 (2009).
pubmed: 19820715
pmcid: 2842606
doi: 10.1038/nchembio.235
Jiao, X. et al. 5′ End nicotinamide adenine dinucleotide cap in human cells promotes RNA decay through DXO-mediated deNADding. Cell 168, 1015–1027(2017).
pubmed: 28283058
pmcid: 5371429
doi: 10.1016/j.cell.2017.02.019
Fehr, A. R. et al. The impact of PARPs and ADP-ribosylation on inflammation and host–pathogen interactions. Genes Dev. 34, 341–359 (2020).
pubmed: 32029454
pmcid: 7050484
doi: 10.1101/gad.334425.119
Cohen, M. S. & Chang, P. Insights into the biogenesis, function, and regulation of ADP-ribosylation. Nat. Chem. Biol. 14, 236–243 (2018).
pubmed: 29443986
pmcid: 5922452
doi: 10.1038/nchembio.2568
Simon, N. C., Aktories, K. & Barbieri, J. T. Novel bacterial ADP-ribosylating toxins: structure and function. Nat. Rev. Microbiol. 12, 599–611 (2014).
pubmed: 25023120
pmcid: 5846498
doi: 10.1038/nrmicro3310
Lüscher, B. et al. ADP-ribosylation, a multifaceted posttranslational modification involved in the control of cell physiology in health and disease. Chem. Rev. 118, 1092–1136 (2018).
pubmed: 29172462
doi: 10.1021/acs.chemrev.7b00122
Morales-Filloy, H. G. et al. The 5′ NAD cap of RNAIII modulates toxin production in Staphylococcus aureus isolates. J. Bacteriol. 202, e00591-19 (2020).
pubmed: 31871032
pmcid: 7043667
doi: 10.1128/JB.00591-19
Frindert, J. et al. Identification, biosynthesis, and decapping of NAD-capped RNAs in B. subtilis. Cell Rep. 24, 1890–1901 (2018).
pubmed: 30110644
doi: 10.1016/j.celrep.2018.07.047
Ruiz-Larrabeiti, O. et al. NAD
Gomes-Filho, J. V. et al. Identification of NAD-RNAs and ADPR-RNA decapping in the archaeal model organisms Sulfolobus acidocaldarius and Haloferax volcanii. Preprint at bioRxiv https://doi.org/10.1101/2022.11.02.514978 (2022).
Walters, R. W. et al. Identification of NAD
pubmed: 28031484
doi: 10.1073/pnas.1619369114
Zhang, Y. et al. Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast. Nat. Commun. 11, 5508 (2020).
pubmed: 33139726
pmcid: 7606564
doi: 10.1038/s41467-020-19326-3
Wang, J. et al. Quantifying the RNA cap epitranscriptome reveals novel caps in cellular and viral RNA. Nucleic Acids Res. 47, e130 (2019).
pubmed: 31504804
pmcid: 6847653
doi: 10.1093/nar/gkz751
Zhang, H. et al. NAD tagSeq reveals that NAD
pubmed: 31142650
pmcid: 6575590
doi: 10.1073/pnas.1903683116
Wang, Y. et al. NAD
pubmed: 31142655
pmcid: 6575598
doi: 10.1073/pnas.1903682116
Dong, H. et al. NAD
pubmed: 35648362
doi: 10.1007/s11427-021-2113-7
Wolfram-Schauerte, M. & Höfer, K. NAD-capped RNAs – a redox cofactor meets RNA. Trends Biochem. Sci. 48, 142–155 (2022).
pubmed: 36068130
doi: 10.1016/j.tibs.2022.08.004
Höfer, K. & Jäschke, A,. Epitranscriptomics: RNA modifications in Bacteria and Archaea. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.RWR-0015-2017 (2018).
doi: 10.1128/microbiolspec.RWR-0015-2017
pubmed: 29916347
Miller, E. S. et al. Bacteriophage T4 genome. Microbiol. Mol. Biol. Rev. 67, 86–156 (2003).
pubmed: 12626685
pmcid: 150520
doi: 10.1128/MMBR.67.1.86-156.2003
Rohrer, H., Zillig, W. & Mailhammer, R. ADP-ribosylation of DNA-dependent RNA polymerase of Escherichia coli by an NAD
pubmed: 173540
doi: 10.1111/j.1432-1033.1975.tb20995.x
Depping, R., Lohaus, C., Meyer, H. E. & Rüger, W. The mono-ADP-ribosyltransferases Alt and ModB of bacteriophage T4: target proteins identified. Biochem. Biophys. Res. Commun. 335, 1217–1223 (2005).
pubmed: 16112649
doi: 10.1016/j.bbrc.2005.08.023
Skórko, R., Zillig, W., Rohrer, H., Fujiki, H. & Mailhammer, R. Purification and properties of the NAD
pubmed: 199442
doi: 10.1111/j.1432-1033.1977.tb11783.x
Tiemann, B., Depping, R. & Rüger, W. Overexpression, purification, and partial characterization of ADP-ribosyltransferases ModA and ModB of bacteriophage T4. Gene Expr. 8, 187–196 (1999).
pubmed: 10634320
Rankin, P. W., Jacobson, E. L., Benjamin, R. C., Moss, J. & Jacobson, M. K. Quantitative studies of inhibitors of ADP-ribosylation in vitro and in vivo. J. Biol. Chem. 264, 4312–4317 (1989).
pubmed: 2538435
doi: 10.1016/S0021-9258(18)83741-3
Goelz, S. & Steitz, J. A. Escherichia coli ribosomal protein S1 recognizes two sites in bacteriophage Qβ RNA. J. Biol. Chem. 252, 5177–5179 (1977).
pubmed: 328498
doi: 10.1016/S0021-9258(19)63326-0
Cervantes-Laurean, D., Jacobson, E. L. & Jacobson, M. K. Glycation and glycoxidation of histones by ADP-ribose. J. Biol. Chem. 271, 10461–10469 (1996).
pubmed: 8631841
doi: 10.1074/jbc.271.18.10461
Kramer, K. et al. Photo-cross-linking and high-resolution mass spectrometry for assignment of RNA-binding sites in RNA-binding proteins. Nat. Methods 11, 1064–1070 (2014).
pubmed: 25173706
pmcid: 6485471
doi: 10.1038/nmeth.3092
Gehrig, P. M. et al. Gas-phase fragmentation of ADP-ribosylated peptides: arginine-specific side-chain losses and their implication in database searches. J. Am. Soc. Mass. Spectrom. 32, 157–168 (2021).
pubmed: 33140951
doi: 10.1021/jasms.0c00040
Winz, M. -L. et al. Capture and sequencing of NAD-capped RNA sequences with NAD captureSeq. Nat. Protoc. 12, 122–149 (2017).
pubmed: 27977022
doi: 10.1038/nprot.2016.163
Tao, P., Wu, X., Tang, W.-C., Zhu, J. & Rao, V. Engineering of bacteriophage T4 genome using CRISPR-Cas9. ACS Synth. Biol. 6, 1952–1961 (2017).
pubmed: 28657724
pmcid: 5771229
doi: 10.1021/acssynbio.7b00179
Zhang, H. et al. Use of NAD tagSeq II to identify growth phase-dependent alterations in E. coli RNA NAD
pubmed: 33782135
pmcid: 8040648
doi: 10.1073/pnas.2026183118
Bird, J. G. et al. The mechanism of RNA 5′ capping with NAD
pubmed: 27383794
pmcid: 4961592
doi: 10.1038/nature18622
Bycroft, M., Hubbard, T. J. P., Proctor, M., Freund, S. M. V. & Murzin, A. G. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88, 235–242 (1997).
pubmed: 9008164
doi: 10.1016/S0092-8674(00)81844-9
Bennett, B. D. et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593–599 (2009).
pubmed: 19561621
pmcid: 2754216
doi: 10.1038/nchembio.186
Wolfram-Schauerte, M., Pozhydaieva, N., Viering, M., Glatter, T. & Höfer, K. Integrated omics reveal time-resolved insights into T4 phage infection of E. coli on proteome and transcriptome levels. Viruses 14, 2502 (2022).
pubmed: 36423111
pmcid: 9697503
doi: 10.3390/v14112502
Diedrich, G. et al. Ribosomal protein L2 is involved in the association of the ribosomal subunits, tRNA binding to A and P sites and peptidyl transfer. EMBO J. 19, 5241–5250 (2000).
pubmed: 11013226
pmcid: 302109
doi: 10.1093/emboj/19.19.5241
Nakagawa, A. et al. The three-dimensional structure of the RNA-binding domain of ribosomal protein L2; a protein at the peptidyl transferase center of the ribosome. EMBO J. 18, 1459–1467 (1999).
pubmed: 10075918
pmcid: 1171235
doi: 10.1093/emboj/18.6.1459
Hentze, M. W., Castello, A., Schwarzl, T. & Preiss, T. A brave new world of RNA-binding proteins. Nat. Rev. Mol. Cell Biol. 19, 327–341 (2018).
pubmed: 29339797
doi: 10.1038/nrm.2017.130
Drygin, Y. F. Natural covalent complexes of nucleic acids and proteins: some comments on practice and theory on the path from well-known complexes to new ones. Nucleic Acids Res. 26, 4791–4796 (1998).
pubmed: 9776736
pmcid: 147930
doi: 10.1093/nar/26.21.4791
Ibba, M. & Söll, D. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69, 617–650 (2000).
pubmed: 10966471
doi: 10.1146/annurev.biochem.69.1.617
Rekosh, D. M. K., Russell, W. C., Bellet, A. J. D. & Robinson, A. J. Identification of a protein linked to the ends of adenovirus DNA. Cell 11, 283–295 (1977).
pubmed: 196758
doi: 10.1016/0092-8674(77)90045-9
Rothberg, P. G., Harris, T. J. R., Nomoto, A. & Wimmer, E. O
pubmed: 217003
pmcid: 336222
doi: 10.1073/pnas.75.10.4868
Uzan, M. & Miller, E. S. Post-transcriptional control by bacteriophage T4: mRNA decay and inhibition of translation initiation. Virol. J 7, 360 (2010).
pubmed: 21129205
pmcid: 3014915
doi: 10.1186/1743-422X-7-360
Ke, Y., Zhang, J., Lv, X., Zeng, X. & Ba, X. Novel insights into PARPs in gene expression: regulation of RNA metabolism. Cell. Mol. Life Sci. 76, 3283–3299 (2019).
pubmed: 31055645
pmcid: 6697709
doi: 10.1007/s00018-019-03120-6
Otten, E. G. et al. Ubiquitylation of lipopolysaccharide by RNF213 during bacterial infection. Nature 594, 111–116 (2021).
pubmed: 34012115
pmcid: 7610904
doi: 10.1038/s41586-021-03566-4
Flynn, R. A. et al. Small RNAs are modified with N-glycans and displayed on the surface of living cells. Cell 184, 3109–3124 (2021).
pubmed: 34004145
pmcid: 9097497
doi: 10.1016/j.cell.2021.04.023
Tsuge, H. et al. Structural basis of actin recognition and arginine ADP-ribosylation by Clostridium perfringens ι-toxin. Proc Natl Acad. Sci. USA 105, 7399–7404 (2008).
pubmed: 18490658
pmcid: 2387182
doi: 10.1073/pnas.0801215105
Beckert, B. et al. Structure of a hibernating 100S ribosome reveals an inactive conformation of the ribosomal protein S1. Nat. Microbiol. 3, 1115–1121 (2018).
pubmed: 30177741
doi: 10.1038/s41564-018-0237-0
Höfer, K., Abele, F., Schlotthauer, J. & Jäschke, A. Synthesis of 5′-NAD-capped RNA. Bioconjug. Chem. 27, 874–877 (2016).
pubmed: 26942556
doi: 10.1021/acs.bioconjchem.6b00072
Ladner, C. L., Yang, J., Turner, R. J. & Edwards, R. A. Visible fluorescent detection of proteins in polyacrylamide gels without staining. Anal. Biochem. 326, 13–20 (2004).
pubmed: 14769330
doi: 10.1016/j.ab.2003.10.047
Hsia, J. A. et al. Amino acid-specific ADP-ribosylation. Sensitivity to hydroxylamine of [cysteine(ADP-ribose)]protein and [arginine(ADP-ribose)]protein linkages. J. Biol. Chem. 260, 16187–16191 (1985).
pubmed: 3934172
doi: 10.1016/S0021-9258(17)36219-1
McDonald, L. J., Wainschel, L. A., Oppenheimer, N. J. & Moss, J. Amino acid-specific ADP-ribosylation: structural characterization and chemical differentiation of ADP-ribose-cysteine adducts formed nonenzymatically and in a pertussis toxin-catalyzed reaction. Biochemistry 31, 11881–11887 (1992).
pubmed: 1445918
doi: 10.1021/bi00162a029
Silberklang, M., Gillum, A. M. & Rajbhandary, U. L. The use of nuclease P
pubmed: 202925
pmcid: 343228
doi: 10.1093/nar/4.12.4091
Abplanalp, J. et al. Proteomic analyses identify ARH3 as a serine mono-ADP-ribosylhydrolase. Nat. Commun. 8, 2055 (2017).
pubmed: 29234005
pmcid: 5727137
doi: 10.1038/s41467-017-02253-1
Banasik, M., Komura, H., Shimoyama, M. & Ueda, K. Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transferase. J. Biol. Chem. 267, 1569–1575 (1992).
pubmed: 1530940
doi: 10.1016/S0021-9258(18)45983-2
MacLean, B. et al. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966–968 (2010).
pubmed: 20147306
pmcid: 2844992
doi: 10.1093/bioinformatics/btq054
Wolfram-Schauerte, M. et al. RNAylomeSeq data analysis from “A viral ADP-ribosyltransferase attaches RNA chains to host proteins” (v.1.0). Zenodo https://doi.org/10.5281/zenodo.7977386 (2023).
Dell’Aquila, G. et al. Mobilization and cellular distribution of phosphate in the diatom Phaeodactylum tricornutum. Front. Plant Sci. 11, 579 (2020).
pubmed: 32582227
pmcid: 7283521
doi: 10.3389/fpls.2020.00579
Gibson, B. A., Conrad, L. B., Huang, D. & Kraus, W. L. Generation and characterization of recombinant antibody-like ADP-ribose binding proteins. Biochemistry 56, 6305–6316 (2017).
pubmed: 29053245
doi: 10.1021/acs.biochem.7b00670
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844
pmcid: 8371605
doi: 10.1038/s41586-021-03819-2
Qureshi, N. S., Bains, J. K., Sreeramulu, S., Schwalbe, H. & Fürtig, B. Conformational switch in the ribosomal protein S1 guides unfolding of structured RNAs for translation initiation. Nucleic Acids Res. 46, 10917–10929 (2018).
pubmed: 30124944
pmcid: 6237739
Di Tommaso, P. et al. T–Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res. 39, W13–W17 (2011).
pubmed: 21558174
pmcid: 3125728
doi: 10.1093/nar/gkr245
Watson, Z. L. et al. Structure of the bacterial ribosome at 2 Å resolution. eLife 9, e60482 (2020).
pubmed: 32924932
pmcid: 7550191
doi: 10.7554/eLife.60482