دورية أكاديمية
أعرض في EDS

The CRTC-1 transcriptional domain is required for COMPASS complex-mediated longevity in C. elegans.

التفاصيل البيبلوغرافية
العنوان: The CRTC-1 transcriptional domain is required for COMPASS complex-mediated longevity in C. elegans.
المؤلفون: Silva-García CG; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA.; Center on the Biology of Aging, Brown University, Providence, RI, USA.; Department of Molecular Biology, Cell Biology, and Biochemistry, Brown University, Providence, RI, USA., Láscarez-Lagunas LI; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA, USA., Papsdorf K; Department of Genetics, Stanford University, Stanford, CA, USA., Heintz C; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Prabhakar A; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Morrow CS; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Pajuelo Torres L; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Sharma A; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Liu J; Harvard Chan Bioinformatics Core, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA., Colaiácovo MP; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA, USA., Brunet A; Department of Genetics, Stanford University, Stanford, CA, USA.; Glenn Center for the Biology of Aging, Stanford University, Stanford, CA, USA., Mair WB; Department of Molecular Metabolism, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA. wmair@hsph.harvard.edu.
المصدر: Nature aging [Nat Aging] 2023 Nov; Vol. 3 (11), pp. 1358-1371. Date of Electronic Publication: 2023 Nov 09.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group US Country of Publication: United States NLM ID: 101773306 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 2662-8465 (Electronic) Linking ISSN: 26628465 NLM ISO Abbreviation: Nat Aging Subsets: MEDLINE
أسماء مطبوعة: Original Publication: [New York] : Nature Publishing Group US, [2021]-
مواضيع طبية MeSH: Caenorhabditis elegans*/genetics , Longevity*/genetics, Animals ; Epigenesis, Genetic ; Histones/chemistry ; Transcription Factors/genetics
مستخلص: Loss of function during aging is accompanied by transcriptional drift, altering gene expression and contributing to a variety of age-related diseases. CREB-regulated transcriptional coactivators (CRTCs) have emerged as key regulators of gene expression that might be targeted to promote longevity. Here we define the role of the Caenorhabditis elegans CRTC-1 in the epigenetic regulation of longevity. Endogenous CRTC-1 binds chromatin factors, including components of the COMPASS complex, which trimethylates lysine 4 on histone H3 (H3K4me3). CRISPR editing of endogenous CRTC-1 reveals that the CREB-binding domain in neurons is specifically required for H3K4me3-dependent longevity. However, this effect is independent of CREB but instead acts via the transcription factor AP-1. Strikingly, CRTC-1 also mediates global histone acetylation levels, and this acetylation is essential for H3K4me3-dependent longevity. Indeed, overexpression of an acetyltransferase enzyme is sufficient to promote longevity in wild-type worms. CRTCs, therefore, link energetics to longevity by critically fine-tuning histone acetylation and methylation to promote healthy aging.
(© 2023. The Author(s).)
References: Corrales, G. M. & Alic, N. Evolutionary conservation of transcription factors affecting longevity. Trends Genet. 36, 373–382 (2020). (PMID: 10.1016/j.tig.2020.02.003)
Mair, W. et al. Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB. Nature 470, 404–408 (2011). (PMID: 21331044309890010.1038/nature09706)
Burkewitz, K. et al. Neuronal CRTC-1 governs systemic mitochondrial metabolism and lifespan via a catecholamine signal. Cell 160, 842–855 (2015). (PMID: 25723162439290910.1016/j.cell.2015.02.004)
Ravnskjaer, K. et al. Glucagon regulates gluconeogenesis through KAT2B- and WDR5-mediated epigenetic effects. J. Clin. Invest. 123, 4318–4328 (2013). (PMID: 24051374378453910.1172/JCI69035)
Liu, Y. et al. A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange. Nature 456, 269–273 (2008). (PMID: 18849969259766910.1038/nature07349)
Han, J. et al. The CREB coactivator CRTC2 controls hepatic lipid metabolism by regulating SREBP1. Nature 524, 243–246 (2015). (PMID: 2614708110.1038/nature14557)
Amelio, A. L., Caputi, M. & Conkright, M. D. Bipartite functions of the CREB co‐activators selectively direct alternative splicing or transcriptional activation. EMBO J. 28, 2733–2747 (2009). (PMID: 19644446275002510.1038/emboj.2009.216)
Escoubas, C. C., Silva-García, C. G. & Mair, W. B. Deregulation of CRTCs in aging and age-related disease risk. Trends Genet. 33, 303–321 (2017). (PMID: 28365140553689710.1016/j.tig.2017.03.002)
Conkright, M. D. et al. TORCs: transducers of regulated CREB activity. Mol. Cell 12, 413–423 (2003). (PMID: 1453608110.1016/j.molcel.2003.08.013)
Screaton, R. A. et al. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119, 61–74 (2004). (PMID: 1545408110.1016/j.cell.2004.09.015)
Szklarczyk, D. et al. STRING v11: protein–protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47, gky1131 (2018).
Greer, E. L. et al. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466, 383 (2010). (PMID: 20555324307500610.1038/nature09195)
Han, S. et al. Mono-unsaturated fatty acids link H3K4me3 modifiers to C. elegans lifespan. Nature 544, 185 (2017). (PMID: 28379943539127410.1038/nature21686)
Silva-García, C. G. & Mair, W. B. Confirming the pro-longevity effects of H3K4me3-deficient set-2 mutants in extending lifespan in C. elegans. Preprint at biorxiv https://doi.org/10.1101/2022.08.02.502497 (2022).
Kenyon, C., Chang, J., Gensch, E., Rudner, A. & Tabtiang, R. A C. elegans mutant that lives twice as long as wild type. Nature 366, 461–464 (1993). (PMID: 824715310.1038/366461a0)
Liu, G. & Sabatini, D. mTOR at the nexus of nutrition, growth, ageing and disease. Nat. Rev. Mol. Cell Biol. 21, 183–203 (2020). (PMID: 31937935710293610.1038/s41580-019-0199-y)
Dillin, A. et al. Rates of behavior and aging specified by mitochondrial function during development. Science 298, 2398–2401 (2002). (PMID: 1247126610.1126/science.1077780)
Ching, T.-T. & Hsu, A.-L. Solid plate-based dietary restriction in Caenorhabditis elegans. J. Vis. Exp. JoVE https://doi.org/10.3791/2701 (2011). (PMID: 10.3791/270121654629)
Zhang, Y. et al. Neuronal TORC1 modulates longevity via AMPK and cell nonautonomous regulation of mitochondrial dynamics in C. elegans. eLife 8, e49158 (2019). (PMID: 31411562671350910.7554/eLife.49158)
Luo, Q. et al. Mechanism of CREB recognition and coactivation by the CREB-regulated transcriptional coactivator CRTC2. Proc. Natl Acad. Sci. USA 109, 20865–20870 (2012). (PMID: 23213254352907610.1073/pnas.1219028109)
Yang, F. et al. An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442, 700–704 (2006). (PMID: 1679956310.1038/nature04942)
Hansen, M. et al. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6, 95–110 (2007). (PMID: 1726667910.1111/j.1474-9726.2006.00267.x)
Pan, K. Z. et al. Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6, 111–119 (2007). (PMID: 1726668010.1111/j.1474-9726.2006.00266.x)
Troemel, E. R. et al. p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2, e183 (2006). (PMID: 17096597163553310.1371/journal.pgen.0020183)
Iourgenko, V. et al. Identification of a family of cAMP response element-binding protein coactivators by genome-scale functional analysis in mammalian cells. Proc. Natl Acad. Sci. USA 100, 12147–12152 (2003). (PMID: 1450629021872710.1073/pnas.1932773100)
Canettieri, G. et al. The coactivator CRTC1 promotes cell proliferation and transformation via AP-1. Proc. Natl Acad. Sci. USA 106, 1445–1450 (2009). (PMID: 19164581263581010.1073/pnas.0808749106)
Wang, Y., Vera, L., Fischer, W. H. & Montminy, M. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 460, 534–537 (2009). (PMID: 19543265273092410.1038/nature08111)
Kwon, A. T., Arenillas, D. J., Hunt, R. W. & Wasserman, W. W. oPOSSUM-3: advanced analysis of regulatory motif over-representation across genes or ChIP–seq datasets. G3 2, 987–1002 (2012). (PMID: 22973536342992910.1534/g3.112.003202)
Sui, S. J. H., Fulton, D. L., Arenillas, D. J., Kwon, A. T. & Wasserman, W. W. oPOSSUM: integrated tools for analysis of regulatory motif over-representation. Nucleic Acids Res. 35, W245–W252 (2007). (PMID: 10.1093/nar/gkm427)
Sui, S. J. H. et al. oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res. 33, 3154–3164 (2005). (PMID: 10.1093/nar/gki624)
Burkewitz, K. et al. Atf-6 regulates lifespan through ER–mitochondrial calcium homeostasis. Cell Rep. 32, 108125 (2020). (PMID: 32905769803027210.1016/j.celrep.2020.108125)
Chinenov, Y. & Kerppola, T. K. Close encounters of many kinds: Fos–Jun interactions that mediate transcription regulatory specificity. Oncogene 20, 2438–2452 (2001). (PMID: 1140233910.1038/sj.onc.1204385)
Silva-García, C. G. et al. Single-copy knock-in loci for defined gene expression in Caenorhabditis elegans. G3 9, g3.400314.2019 (2019). (PMID: 10.1534/g3.119.400314)
Li, T. Y. et al. The transcriptional coactivator CBP/p300 is an evolutionarily conserved node that promotes longevity in response to mitochondrial stress. Nat. Aging 1, 165–178 (2021). (PMID: 33718883711689410.1038/s43587-020-00025-z)
Cohen, E. et al. Caenorhabditis elegans nicotinic acetylcholine receptors are required for nociception. Mol. Cell Neurosci. 59, 85–96 (2014). (PMID: 24518198425861010.1016/j.mcn.2014.02.001)
Rand, J. Acetylcholine. WormBook https://doi.org/10.1895/wormbook.1.131.1 (2007).
Mathews, E. A., Mullen, G. P., Hodgkin, J., Duerr, J. S. & Rand, J. B. Genetic interactions between UNC-17/VAChT and a novel transmembrane protein in Caenorhabditis elegans. Genetics 192, 1315–1325 (2012). (PMID: 23051648351214110.1534/genetics.112.145771)
Bradshaw, P. C. Acetyl-CoA metabolism and histone acetylation in the regulation of aging and lifespan. Antioxidants 10, 572 (2021). (PMID: 33917812806815210.3390/antiox10040572)
Halestrap, A. P. The monocarboxylate transporter family—structure and functional characterization. IUBMB Life 64, 1–9 (2012). (PMID: 2213130310.1002/iub.573)
Tasoulas, J., Rodon, L., Kaye, F. J., Montminy, M. & Amelio, A. L. Adaptive transcriptional responses by CRTC coactivators in cancer. Trends Cancer 5, 111–127 (2019). (PMID: 30755304968290210.1016/j.trecan.2018.12.002)
Greer, E. L. et al. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479, 365–371 (2011). (PMID: 22012258336812110.1038/nature10572)
Caron, M. et al. Loss of SET1/COMPASS methyltransferase activity reduces lifespan and fertility in Caenorhabditis elegans. Life Sci. Alliance https://doi.org/10.1101/2021.06.07.447374 (2021).
Giblin, W., Skinner, M. E. & Lombard, D. B. Sirtuins: guardians of mammalian healthspan. Trends Genet. 30, 271–286 (2014). (PMID: 24877878407791810.1016/j.tig.2014.04.007)
Kaeberlein, M., McVey, M. & Guarente, L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Gene Dev. 13, 2570–2580 (1999). (PMID: 1052140131707710.1101/gad.13.19.2570)
Rogina, B. & Helfand, S. L. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl Acad. Sci. USA 101, 15998–16003 (2004). (PMID: 1552038452875210.1073/pnas.0404184101)
Tissenbaum, H. A. & Guarente, L. Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410, 227–230 (2001). (PMID: 1124208510.1038/35065638)
Kanfi, Y. et al. The sirtuin SIRT6 regulates lifespan in male mice. Nature 483, 218–221 (2012). (PMID: 2236754610.1038/nature10815)
Ikeda, T., Uno, M., Honjoh, S. & Nishida, E. The MYST family histone acetyltransferase complex regulates stress resistance and longevity through transcriptional control of DAF‐16/FOXO transcription factors. EMBO Rep. 18, 1716–1726 (2017). (PMID: 28794203562386810.15252/embr.201743907)
Yu, R. et al. Inactivating histone deacetylase HDA promotes longevity by mobilizing trehalose metabolism. Nat. Commun. 12, 1981 (2021). (PMID: 33790287801257310.1038/s41467-021-22257-2)
Wang, Y.-L., Faiola, F., Xu, M., Pan, S. & Martinez, E. Human ATAC is a GCN5/PCAF-containing acetylase complex with a novel NC2-like histone fold module that interacts with the TATA-binding protein. J. Biol. Chem. 283, 33808–33815 (2008). (PMID: 18838386259071110.1074/jbc.M806936200)
Beurton, F. et al. Physical and functional interaction between SET1/COMPASS complex component CFP-1 and a Sin3S HDAC complex in C. elegans. Nucleic Acids Res. 47, 11164–11180 (2019). (PMID: 31602465686839810.1093/nar/gkz880)
Cai, Y. et al. Subunit composition and substrate specificity of a MOF-containing histone acetyltransferase distinct from the male-specific lethal (MSL) complex. J. Biol. Chem. 285, 4268–4272 (2010). (PMID: 2001885210.1074/jbc.C109.087981)
Lee, T. W., David, H. S., Engstrom, A. K., Carpenter, B. S. & Katz, D. J. Repressive H3K9me2 protects lifespan against the transgenerational burden of COMPASS activity in C. elegans. eLife 8, e48498 (2019). (PMID: 31815663729934610.7554/eLife.48498)
Boon, R., Silveira, G. G. & Mostoslavsky, R. Nuclear metabolism and the regulation of the epigenome. Nat. Metabolism 2, 1190–1203 (2020). (PMID: 10.1038/s42255-020-00285-4)
Paix, A., Folkmann, A., Rasoloson, D. & Seydoux, G. High efficiency, homology-directed genome editing in Caenorhabditis elegans using CRISPR–Cas9 ribonucleoprotein complexes. Genetics 201, 47–54 (2015). (PMID: 26187122456627510.1534/genetics.115.179382)
Evans, T. Transformation and microinjection. WormBook https://doi.org/10.1895/wormbook.1.108.1 (2006). (PMID: 10.1895/wormbook.1.108.1)
Weir, H. J. et al. Dietary restriction and AMPK increase lifespan via mitochondrial network and peroxisome remodeling. Cell Metab. 26, 884–896.e5 (2017). (PMID: 29107506571893610.1016/j.cmet.2017.09.024)
bcbio. bcbio-nextgen https://bcbio-nextgen.readthedocs.org/en/latest/.
FastQC. Babraham Bioinformatics http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013). (PMID: 2310488610.1093/bioinformatics/bts635)
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017). (PMID: 28263959560014810.1038/nmeth.4197)
Soneson, C., Love, M. I. & Robinson, M. D. Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Research 4, 1521 (2015). (PMID: 2692522710.12688/f1000research.7563.1)
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). (PMID: 25516281430204910.1186/s13059-014-0550-8)
Yu, G., Wang, L.-G., Han, Y. & He, Q.-Y. clusterProfiler: an R Package for comparing biological themes among gene clusters. Omics J. Integr. Biol. 16, 284–287 (2012). (PMID: 10.1089/omi.2011.0118)
Lascarez-Lagunas, L. I., Herruzo, E., Grishok, A., San-Segundo, P. A. & Colaiácovo, M. P. DOT-1.1-dependent H3K79 methylation promotes normal meiotic progression and meiotic checkpoint function in C. elegans. PLoS Genet. 16, e1009171 (2020). (PMID: 33104701764409410.1371/journal.pgen.1009171)
Rappsilber, J., Ishihama, Y. & Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 75, 663–670 (2003). (PMID: 1258549910.1021/ac026117i)
Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008). (PMID: 1902991010.1038/nbt.1511)
Cox, J. et al. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794–1805 (2011). (PMID: 2125476010.1021/pr101065j)
Angeles-Albores, D., Lee, R. Y. N., Chan, J. & Sternberg, P. W. Tissue enrichment analysis for C. elegans genomics. BMC Bioinf. 17, 366 (2016). (PMID: 10.1186/s12859-016-1229-9)
Papsdorf, K. et al. Lipid droplets and peroxisomes are co-regulated to drive lifespan extension in response to mono-unsaturated fatty acids. Nat. Cell Biol. 25, 672–684 (2023). (PMID: 371277151018547210.1038/s41556-023-01136-6)
Heintz, C. et al. Splicing factor 1 modulates dietary restriction and TORC1 pathway longevity in C. elegans. Nature 541, 102 (2017). (PMID: 2791906510.1038/nature20789)
Barrett, T. et al. NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res. 41, D991–D995 (2013). (PMID: 2319325810.1093/nar/gks1193)
Okuda, S. et al. jPOSTrepo: an international standard data repository for proteomes. Nucleic Acids Res. 45, D1107–D1111 (2016). (PMID: 27899654521056110.1093/nar/gkw1080)
معلومات مُعتمدة: R00 AG065508 United States AG NIA NIH HHS; R01 AG059595 United States AG NIA NIH HHS; R01 GM072551 United States GM NIGMS NIH HHS; R01 AG051954 United States AG NIA NIH HHS; R01 AG067106 United States AG NIA NIH HHS; K99 AG065508 United States AG NIA NIH HHS; R01 AG044346 United States AG NIA NIH HHS; R01 AG054201 United States AG NIA NIH HHS
المشرفين على المادة: 0 (Histones)
0 (Transcription Factors)
0 (CRTC-1 protein, C elegans)
تواريخ الأحداث: Date Created: 20231109 Date Completed: 20231117 Latest Revision: 20240210
رمز التحديث: 20240210
مُعرف محوري في PubMed: PMC10645585
DOI: 10.1038/s43587-023-00517-8
PMID: 37946042
قاعدة البيانات: MEDLINE
الوصف
تدمد:2662-8465
DOI:10.1038/s43587-023-00517-8