Ageing-associated changes in transcriptional elongation influence longevity.
Animals
Humans
Mice
Rats
Aging
/ genetics
Insulin
/ metabolism
Longevity
/ genetics
RNA Polymerase II
/ genetics
Signal Transduction
Transcription Elongation, Genetic
Drosophila melanogaster
/ genetics
Caenorhabditis elegans
/ genetics
RNA, Circular
Somatomedins
Nucleosomes
Histones
Cell Division
Caloric Restriction
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
10
09
2019
accepted:
07
03
2023
medline:
28
4
2023
pubmed:
13
4
2023
entrez:
12
4
2023
Statut:
ppublish
Résumé
Physiological homeostasis becomes compromised during ageing, as a result of impairment of cellular processes, including transcription and RNA splicing
Identifiants
pubmed: 37046086
doi: 10.1038/s41586-023-05922-y
pii: 10.1038/s41586-023-05922-y
pmc: PMC10132977
doi:
Substances chimiques
Insulin
0
RNA Polymerase II
EC 2.7.7.-
RNA, Circular
0
Somatomedins
0
Nucleosomes
0
Histones
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
814-821Commentaires et corrections
Type : CommentIn
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Fritsch, C. et al. Genome-wide surveillance of transcription errors in response to genotoxic stress. Proc. Natl Acad. Sci. USA 118, e2004077118 (2021).
pubmed: 33443141
doi: 10.1073/pnas.2004077118
Bentley, D. L. Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 15, 163–175 (2014).
pubmed: 24514444
pmcid: 4304646
doi: 10.1038/nrg3662
Conaway, J. W. & Conaway, R. C. Transcription elongation and human disease. Annu. Rev. Biochem. 68, 301–319 (1999).
pubmed: 10872452
doi: 10.1146/annurev.biochem.68.1.301
Heintz, C. et al. Splicing factor 1 modulates dietary restriction and TORC1 pathway longevity in C. elegans. Nature 541, 102–106 (2017).
pubmed: 27919065
doi: 10.1038/nature20789
Rogalski, T. M., Bullerjahn, A. M. & Riddle, D. L. Lethal and amanitin-resistance mutations in the Caenorhabditis elegans ama-1 and ama-2 genes. Genetics 120, 409–422 (1988).
pubmed: 3197954
pmcid: 1203520
doi: 10.1093/genetics/120.2.409
Chen, Y., Chafin, D., Price, D. H. & Greenleaf, A. L. Drosophila RNA polymerase II mutants that affect transcription elongation. J. Biol. Chem. 271, 5993–5999 (1996).
pubmed: 8626382
doi: 10.1074/jbc.271.11.5993
Darnell, J. E. Variety in the level of gene control in eukaryotic cells. Nature 297, 365–371 (1982).
pubmed: 6176879
doi: 10.1038/297365a0
Vogel, C. & Marcotte, E. M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227–232 (2012).
pubmed: 22411467
pmcid: 3654667
doi: 10.1038/nrg3185
Liu, Y., Beyer, A. & Aebersold, R. On the dependency of cellular protein levels on mRNA abundance. Cell 165, 535–550 (2016).
pubmed: 27104977
doi: 10.1016/j.cell.2016.03.014
Saldi, T., Cortazar, M. A., Sheridan, R. M. & Bentley, D. L. Coupling of RNA polymerase II transcription elongation with pre-mRNA splicing. J. Mol. Biol. 428, 2623–2635 (2016).
pubmed: 27107644
pmcid: 4893998
doi: 10.1016/j.jmb.2016.04.017
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M. & Kroemer, G. The hallmarks of aging. Cell 153, 1194–1217 (2013).
pubmed: 23746838
pmcid: 3836174
doi: 10.1016/j.cell.2013.05.039
Vermulst, M. et al. Transcription errors induce proteotoxic stress and shorten cellular lifespan. Nat. Commun. 6, 8065 (2015).
pubmed: 26304740
doi: 10.1038/ncomms9065
Rangaraju, S. et al. Suppression of transcriptional drift extends C. elegans lifespan by postponing the onset of mortality. eLife 4, e08833 (2015).
pubmed: 26623667
pmcid: 4720515
doi: 10.7554/eLife.08833
Martinez-Jimenez, C. P. et al. Aging increases cell-to-cell transcriptional variability upon immune stimulation. Science 355, 1433–1436 (2017).
pubmed: 28360329
pmcid: 5405862
doi: 10.1126/science.aah4115
Wada, Y. et al. A wave of nascent transcription on activated human genes. Proc. Natl Acad. Sci. USA 106, 18357–18361 (2009).
pubmed: 19826084
pmcid: 2761237
doi: 10.1073/pnas.0902573106
Ameur, A. et al. Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain. Nat. Struct. Mol. Biol. 18, 1435–1440 (2011).
pubmed: 22056773
doi: 10.1038/nsmb.2143
Singh, J. & Padgett, R. A. Rates of in situ transcription and splicing in large human genes. Nat. Struct. Mol. Biol. 16, 1128–1133 (2009).
pubmed: 19820712
pmcid: 2783620
doi: 10.1038/nsmb.1666
Fuchs, G. et al. 4sUDRB-seq: measuring genomewide transcriptional elongation rates and initiation frequencies within cells. Genome Biol. 15, R69 (2014).
pubmed: 24887486
pmcid: 4072947
doi: 10.1186/gb-2014-15-5-r69
Jonkers, I., Kwak, H. & Lis, J. T. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 3, e02407 (2014).
pubmed: 24843027
pmcid: 4001325
doi: 10.7554/eLife.02407
Veloso, A. et al. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications. Genome Res. 24, 896–905 (2014).
pubmed: 24714810
pmcid: 4032854
doi: 10.1101/gr.171405.113
Ori, A. et al. Integrated transcriptome and proteome analyses reveal organ-specific proteome deterioration in old rats. Cell Syst. 1, 224–237 (2015).
pubmed: 27135913
pmcid: 4802414
doi: 10.1016/j.cels.2015.08.012
Fong, N. et al. Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate. Genes Dev. 28, 2663–2676 (2014).
pubmed: 25452276
pmcid: 4248296
doi: 10.1101/gad.252106.114
Oesterreich, F. C. et al. Splicing of nascent RNA coincides with intron exit from RNA polymerase II. Cell 165, 372–381 (2016).
pubmed: 27020755
pmcid: 4826323
doi: 10.1016/j.cell.2016.02.045
de la Mata, M. et al. A slow RNA polymerase II affects alternative splicing in vivo. Mol. Cell 12, 525–532 (2003).
pubmed: 14536091
doi: 10.1016/j.molcel.2003.08.001
Ip, J. Y. et al. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res. 21, 390–401 (2011).
pubmed: 21163941
pmcid: 3044853
doi: 10.1101/gr.111070.110
Braunschweig, U. et al. Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res. 24, 1774–1786 (2014).
pubmed: 25258385
pmcid: 4216919
doi: 10.1101/gr.177790.114
Jung, H. et al. Intron retention is a widespread mechanism of tumor-suppressor inactivation. Nat. Genet. 47, 1242–1248 (2015).
pubmed: 26437032
doi: 10.1038/ng.3414
Aslanzadeh, V., Huang, Y., Sanguinetti, G. & Beggs, J. D. Transcription rate strongly affects splicing fidelity and cotranscriptionality in budding yeast. Genome Res. 28, 203–213 (2018).
pubmed: 29254943
pmcid: 5793784
doi: 10.1101/gr.225615.117
Leng, X. et al. Organismal benefits of transcription speed control at gene boundaries. EMBO Rep. 21, e49315 (2020).
pubmed: 32103605
pmcid: 7132196
doi: 10.15252/embr.201949315
Herzel, L., Straube, K. & Neugebauer, K. M. Long-read sequencing of nascent RNA reveals coupling among RNA processing events. Genome Res. 28, 1008–1019 (2018).
pubmed: 29903723
pmcid: 6028129
doi: 10.1101/gr.232025.117
Drexler, H. L., Choquet, K. & Churchman, L. S. Splicing kinetics and coordination revealed by direct nascent RNA sequencing through nanopores. Mol. Cell 77, 985–998.e8 (2020).
pubmed: 31839405
doi: 10.1016/j.molcel.2019.11.017
Mazin, P. et al. Widespread splicing changes in human brain development and aging. Mol. Syst. Biol. 9, 633 (2013).
pubmed: 23340839
pmcid: 3564255
doi: 10.1038/msb.2012.67
Tollervey, J. R. et al. Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res. 21, 1572–1582 (2011).
pubmed: 21846794
pmcid: 3202275
doi: 10.1101/gr.122226.111
Lee, B. P. et al. Changes in the expression of splicing factor transcripts and variations in alternative splicing are associated with lifespan in mice and humans. Aging Cell 15, 903–913 (2016).
pubmed: 27363602
pmcid: 5013025
doi: 10.1111/acel.12499
Pickrell, J. K., Pai, A. A., Gilad, Y. & Pritchard, J. K. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet. 6, e1001236 (2010).
pubmed: 21151575
pmcid: 3000347
doi: 10.1371/journal.pgen.1001236
Stepankiw, N., Raghavan, M., Fogarty, E. A., Grimson, A. & Pleiss, J. A. Widespread alternative and aberrant splicing revealed by lariat sequencing. Nucleic Acids Res. 43, 8488–8501 (2015).
pubmed: 26261211
pmcid: 4787815
doi: 10.1093/nar/gkv763
Li, Y. I. et al. Annotation-free quantification of RNA splicing using LeafCutter. Nat. Genet. 50, 151–158 (2018).
pubmed: 29229983
doi: 10.1038/s41588-017-0004-9
Mariotti, M., Kerepesi, C., Oliveros, W., Mele, M. & Gladyshev, V. N. Deterioration of the human transcriptome with age due to increasing intron retention and spurious splicing. Preprint at bioRxiv https://doi.org/10.1101/2022.03.14.484341 (2022).
Cocquerelle, C., Mascrez, B., Hétuin, D. & Bailleul, B. Mis-splicing yields circular RNA molecules. FASEB J. 7, 155–160 (1993).
pubmed: 7678559
doi: 10.1096/fasebj.7.1.7678559
Nigro, J. M. et al. Scrambled exons. Cell 64, 607–613 (1991).
pubmed: 1991322
doi: 10.1016/0092-8674(91)90244-S
Zhang, X.-O. et al. Complementary sequence-mediated exon circularization. Cell 159, 134–147 (2014).
pubmed: 25242744
doi: 10.1016/j.cell.2014.09.001
Zhang, Y. et al. The biogenesis of nascent circular RNAs. Cell Rep. 15, 611–624 (2016).
pubmed: 27068474
doi: 10.1016/j.celrep.2016.03.058
Venkatesh, S. & Workman, J. L. Histone exchange, chromatin structure and the regulation of transcription. Nat. Rev. Mol. Cell Biol. 16, 178–189 (2015).
pubmed: 25650798
doi: 10.1038/nrm3941
Jonkers, I. & Lis, J. T. Getting up to speed with transcription elongation by RNA polymerase II. Nat. Rev. Mol. Cell Biol. 16, 167–177 (2015).
pubmed: 25693130
pmcid: 4782187
doi: 10.1038/nrm3953
Jimeno-González, S. et al. Defective histone supply causes changes in RNA polymerase II elongation rate and cotranscriptional pre-mRNA splicing. Proc. Natl Acad. Sci. USA 112, 14840–14845 (2015).
pubmed: 26578803
pmcid: 4672771
doi: 10.1073/pnas.1506760112
Feser, J. et al. Elevated histone expression promotes life span extension. Mol. Cell 39, 724–735 (2010).
pubmed: 20832724
pmcid: 3966075
doi: 10.1016/j.molcel.2010.08.015
Hu, Z. et al. Nucleosome loss leads to global transcriptional up-regulation and genomic instability during yeast aging. Genes Dev. 28, 396–408 (2014).
pubmed: 24532716
pmcid: 3937517
doi: 10.1101/gad.233221.113
Hughes, A. L. & Rando, O. J. Mechanisms underlying nucleosome positioning in vivo. Annu. Rev. Biophys. 43, 41–63 (2014).
pubmed: 24702039
doi: 10.1146/annurev-biophys-051013-023114
Struhl, K. & Segal, E. Determinants of nucleosome positioning. Nat. Struct. Mol. Biol. 20, 267–273 (2013).
pubmed: 23463311
pmcid: 3740156
doi: 10.1038/nsmb.2506
Fitz, V. et al. Nucleosomal arrangement affects single-molecule transcription dynamics. Proc. Natl Acad. Sci. USA 113, 12733–12738 (2016).
pubmed: 27791062
pmcid: 5111697
doi: 10.1073/pnas.1602764113
Gossett, A. J. & Lieb, J. D. In vivo effects of histone H3 depletion on nucleosome occupancy and position in Saccharomyces cerevisiae. PLoS Genet. 8, e1002771 (2012).
pubmed: 22737086
pmcid: 3380831
doi: 10.1371/journal.pgen.1002771
Oberdoerffer, P. An age of fewer histones. Nat. Cell Biol. 12, 1029–1031 (2010).
pubmed: 21045802
doi: 10.1038/ncb1110-1029
Sural, S., Liang, C.-Y., Wang, F.-Y., Ching, T.-T. & Hsu, A.-L. HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity. Sci. Adv. 6, eaaz4452 (2020).
pubmed: 33087356
pmcid: 7577724
doi: 10.1126/sciadv.aaz4452
Lu, Y.-X. et al. A TORC1–histone axis regulates chromatin organisation and non-canonical induction of autophagy to ameliorate ageing. eLife 10, e62233 (2021).
pubmed: 33988501
pmcid: 8186904
doi: 10.7554/eLife.62233
Mason, P. B. & Struhl, K. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol. Cell 17, 831–840 (2005).
pubmed: 15780939
doi: 10.1016/j.molcel.2005.02.017
Saldi, T., Riemondy, K., Erickson, B. & Bentley, D. L. Alternative RNA structures formed during transcription depend on elongation rate and modify RNA processing. Mol. Cell 81, 1789–1801.e5 (2021).
pubmed: 33631106
pmcid: 8052309
doi: 10.1016/j.molcel.2021.01.040
Miller, T. E. et al. Transcription elongation factors represent in vivo cancer dependencies in glioblastoma. Nature 547, 355–359 (2017).
pubmed: 28678782
pmcid: 5896562
doi: 10.1038/nature23000
Bushnell, D. A., Cramer, P. & Kornberg, R. D. Structural basis of transcription: α-amanitin–RNA polymerase II cocrystal at 2.8 Å resolution. Proc. Natl Acad. Sci. USA 99, 1218–1222 (2002).
pubmed: 11805306
pmcid: 122170
doi: 10.1073/pnas.251664698
Bowman, E. A., Riddle, D. L. & Kelly, W. Amino acid substitutions in the Caenorhabditis elegans RNA polymerase II large subunit AMA-1/RPB-1 that result in α-amanitin resistance and/or reduced function. G3 (Bethesda) 1, 411–416 (2011).
pubmed: 22384351
doi: 10.1534/g3.111.000968
Stroustrup, N. et al. The Caenorhabditis elegans lifespan machine. Nat. Methods 10, 665–670 (2013).
pubmed: 23666410
pmcid: 3865717
doi: 10.1038/nmeth.2475
Greenleaf, A. L., Borsett, L. M., Jiamachello, P. F. & Coulter, D. E. α-Amanitin-resistant D. melanogaster with an altered RNA polymerase II. Cell 18, 613–622 (1979).
pubmed: 117900
doi: 10.1016/0092-8674(79)90116-8
Grönke, S., Clarke, D.-F., Broughton, S., Andrews, T. D. & Partridge, L. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6, e1000857 (2010).
pubmed: 20195512
pmcid: 2829060
doi: 10.1371/journal.pgen.1000857
Hahn, O. et al. Dietary restriction protects from age-associated DNA methylation and induces epigenetic reprogramming of lipid metabolism. Genome Biol. 18, 56 (2017).
pubmed: 28351387
pmcid: 5370449
doi: 10.1186/s13059-017-1187-1
Weigelt, C. M. et al. An insulin-sensitive circular RNA that regulates lifespan in Drosophila. Mol. Cell 79, 268–279.e5 (2020).
pubmed: 32592682
pmcid: 7318944
doi: 10.1016/j.molcel.2020.06.011
Selman, C. et al. Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J. 22, 807–818 (2008).
pubmed: 17928362
doi: 10.1096/fj.07-9261com
Melnik, S. et al. Isolation of the protein and RNA content of active sites of transcription from mammalian cells. Nat. Protoc. 11, 553–565 (2016).
pubmed: 26914315
doi: 10.1038/nprot.2016.032
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Gerstner, J. R. et al. Removal of unwanted variation reveals novel patterns of gene expression linked to sleep homeostasis in murine cortex. BMC Genomics 17, 727 (2016).
pubmed: 27801296
pmcid: 5088519
doi: 10.1186/s12864-016-3065-8
Liberzon, A. et al. The Molecular Signatures Database hallmark gene set collection. Cell Syst. 1, 417–425 (2015).
pubmed: 26771021
pmcid: 4707969
doi: 10.1016/j.cels.2015.12.004
Durinck, S. et al. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21, 3439–3440 (2005).
pubmed: 16082012
doi: 10.1093/bioinformatics/bti525
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11, 1650–1667 (2016).
pubmed: 27560171
pmcid: 5032908
doi: 10.1038/nprot.2016.095
Karolchik, D. et al. The UCSC Table Browser data retrieval tool. Nucleic Acids Res. 32, D493–D496 (2004).
pubmed: 14681465
pmcid: 308837
doi: 10.1093/nar/gkh103
Cui, P. et al. A comparison between ribo-minus RNA-sequencing and polyA-selected RNA-sequencing. Genomics 96, 259–265 (2010).
pubmed: 20688152
doi: 10.1016/j.ygeno.2010.07.010
Caudron-Herger, M., Cook, P. R., Rippe, K. & Papantonis, A. Dissecting the nascent human transcriptome by analysing the RNA content of transcription factories. Nucleic Acids Res. 43, e95 (2015).
pubmed: 25897132
pmcid: 4538806
doi: 10.1093/nar/gkv390
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Methods 5, 621–628 (2008).
pubmed: 18516045
doi: 10.1038/nmeth.1226
Gray, J. M. et al. SnapShot-seq: a method for extracting genome-wide, in vivo mRNA dynamics from a single total RNA sample. PLoS ONE 9, e89673 (2014).
pubmed: 24586954
pmcid: 3935918
doi: 10.1371/journal.pone.0089673
Fuchs, G. et al. Simultaneous measurement of genome-wide transcription elongation speeds and rates of RNA polymerase II transition into active elongation with 4sUDRB-seq. Nat. Protoc. 10, 605–618 (2015).
pubmed: 25811895
doi: 10.1038/nprot.2015.035
Lusser, A. et al. in The Eukaryotic RNA Exosome: Methods and Protocols (eds LaCava, J. & Vaňáčová, Š.) 191–211 (Springer, 2020).
Lindenbaum, P. JVarkit: java-based utilities for Bioinformatics. figshare https://doi.org/10.6084/m9.figshare.1425030.v1 (2015).
Essers, P. et al. Reduced insulin/insulin-like growth factor signaling decreases translation in Drosophila and mice. Sci. Rep. 6, 30290 (2016).
pubmed: 27452396
pmcid: 4959029
doi: 10.1038/srep30290
Hwang, T. et al. Dynamic regulation of RNA editing in human brain development and disease. Nat. Neurosci. 19, 1093–1099 (2016).
pubmed: 27348216
doi: 10.1038/nn.4337
Diermeier, S. et al. TNFα signalling primes chromatin for NF-κB binding and induces rapid and widespread nucleosome repositioning. Genome Biol. 15, 536 (2014).
pubmed: 25608606
pmcid: 4268828
doi: 10.1186/s13059-014-0536-6
Flores, O. & Orozco, M. nucleR: a package for non-parametric nucleosome positioning. Bioinformatics 27, 2149–2150 (2011).
pubmed: 21653521
doi: 10.1093/bioinformatics/btr345
Zhao, S. et al. PiggyBac transposon vectors: the tools of the human gene encoding. Transl Lung Cancer Res. 5, 120–125 (2016).
Adachi, K. et al. Esrrb unlocks silenced enhancers for reprogramming to naive pluripotency. Cell Stem Cell 23, 266–275.e6 (2018).
pubmed: 29910149
doi: 10.1016/j.stem.2018.05.020
Dimri, G. P. et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl Acad. Sci. USA 92, 9363–9367 (1995).
pubmed: 7568133
pmcid: 40985
doi: 10.1073/pnas.92.20.9363
Zirkel, A. et al. HMGB2 loss upon senescence entry disrupts genomic organization and induces CTCF clustering across cell types. Mol. Cell 70, 730–744.e6 (2018).
pubmed: 29706538
doi: 10.1016/j.molcel.2018.03.030
Berridge, M. V. & Tan, A. S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303, 474–482 (1993).
pubmed: 8390225
doi: 10.1006/abbi.1993.1311
Sepp, K. J., Schulte, J. & Auld, V. J. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev. Biol. 238, 47–63 (2001).
pubmed: 11783993
doi: 10.1006/dbio.2001.0411