دورية أكاديمية

Tunable DNMT1 degradation reveals DNMT1/DNMT3B synergy in DNA methylation and genome organization.

التفاصيل البيبلوغرافية
العنوان: Tunable DNMT1 degradation reveals DNMT1/DNMT3B synergy in DNA methylation and genome organization.
المؤلفون: Scelfo A; Institut Curie, PSL Research University, Sorbonne Université, CNRS, UMR 144 , Paris, France., Barra V; Institut Curie, PSL Research University, Sorbonne Université, CNRS, UMR 144 , Paris, France.; Department of Biological, Chemical and Pharmaceutical Sciences and Technologies, University of Palermo, Palermo, Italy., Abdennur N; Program in Bioinformatics and Integrative Biology, UMass Chan Medical School , Worcester, MA, USA.; Department of Systems Biology, UMass Chan Medical School, Worcester, MA, USA.; Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology , Cambridge, MA, USA., Spracklin G; Department of Systems Biology, UMass Chan Medical School, Worcester, MA, USA.; Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology , Cambridge, MA, USA., Busato F; Centre National de Recherche en Génomique Humaine, CEA-Institut de Biologie François Jacob, Université Paris-Saclay , Evry, France., Salinas-Luypaert C; Institut Curie, PSL Research University, Sorbonne Université, CNRS, UMR 144 , Paris, France., Bonaiti E; Institut Curie, PSL Research University, Sorbonne Université, CNRS, UMR 144 , Paris, France., Velasco G; Université de Paris Cité, CNRS UMR 7216 , Paris, France., Bonhomme F; Epigenetic Chemical Biology, Institut Pasteur, CNRS UMR n°3523 Chem4Life, Université Paris Cité , Paris, France., Chipont A; Cytometry Platform, Institut Curie , Paris, France., Tijhuis AE; European Research Institute for the Biology of Ageing, University Groningen, University Medical Center Groningen , Groningen, Netherlands., Spierings DCJ; European Research Institute for the Biology of Ageing, University Groningen, University Medical Center Groningen , Groningen, Netherlands., Guérin C; Cytometry Platform, Institut Curie , Paris, France.; Université Paris Cité, INSERM , Paris, France., Arimondo P; Epigenetic Chemical Biology, Institut Pasteur, CNRS UMR n°3523 Chem4Life, Université Paris Cité , Paris, France., Francastel C; Université de Paris Cité, CNRS UMR 7216 , Paris, France., Foijer F; European Research Institute for the Biology of Ageing, University Groningen, University Medical Center Groningen , Groningen, Netherlands., Tost J; Centre National de Recherche en Génomique Humaine, CEA-Institut de Biologie François Jacob, Université Paris-Saclay , Evry, France., Mirny L; Institute for Medical Engineering and Sciences, Massachusetts Institute of Technology , Cambridge, MA, USA.; Department of Physics, Massachusetts Institute of Technology, Cambridge, MA, USA., Fachinetti D; Institut Curie, PSL Research University, Sorbonne Université, CNRS, UMR 144 , Paris, France.
المصدر: The Journal of cell biology [J Cell Biol] 2024 Apr 01; Vol. 223 (4). Date of Electronic Publication: 2024 Feb 20.
نوع المنشور: Journal Article; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Rockefeller University Press Country of Publication: United States NLM ID: 0375356 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1540-8140 (Electronic) Linking ISSN: 00219525 NLM ISO Abbreviation: J Cell Biol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: New York : Rockefeller University Press
مواضيع طبية MeSH: DNA Methylation* , Epigenomics* , DNA (Cytosine-5-)-Methyltransferase 1*/genetics , DNA Methyltransferase 3A*/genetics, Humans ; Cell Division ; Heterochromatin/genetics ; Cell Line
مستخلص: DNA methylation (DNAme) is a key epigenetic mark that regulates critical biological processes maintaining overall genome stability. Given its pleiotropic function, studies of DNAme dynamics are crucial, but currently available tools to interfere with DNAme have limitations and major cytotoxic side effects. Here, we present cell models that allow inducible and reversible DNAme modulation through DNMT1 depletion. By dynamically assessing whole genome and locus-specific effects of induced passive demethylation through cell divisions, we reveal a cooperative activity between DNMT1 and DNMT3B, but not of DNMT3A, to maintain and control DNAme. We show that gradual loss of DNAme is accompanied by progressive and reversible changes in heterochromatin, compartmentalization, and peripheral localization. DNA methylation loss coincides with a gradual reduction of cell fitness due to G1 arrest, with minor levels of mitotic failure. Altogether, this system allows DNMTs and DNA methylation studies with fine temporal resolution, which may help to reveal the etiologic link between DNAme dysfunction and human disease.
(© 2024 Scelfo et al.)
References: Trends Genet. 2021 Nov;37(11):1012-1027. (PMID: 34120771)
Genes Cancer. 2011 Jun;2(6):607-17. (PMID: 21941617)
Cancer Res. 2017 Apr 15;77(8):1854-1867. (PMID: 28130225)
Nat Methods. 2012 Mar 04;9(4):357-9. (PMID: 22388286)
Cancer Res. 2006 Jan 15;66(2):682-92. (PMID: 16423997)
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14412-7. (PMID: 10588719)
Nat Commun. 2019 Nov 7;10(1):5069. (PMID: 31699985)
Genome Biol. 2016 May 31;17(1):115. (PMID: 27246460)
Science. 2009 Oct 9;326(5950):289-93. (PMID: 19815776)
Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11797-801. (PMID: 7527544)
Nat Cancer. 2021 Oct;2(10):1002-1017. (PMID: 34790902)
Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9209-14. (PMID: 11481484)
Nat Rev Genet. 2005 Aug;6(8):597-610. (PMID: 16136652)
Cell Rep. 2021 Sep 21;36(12):109722. (PMID: 34551299)
Biochim Biophys Acta Mol Basis Dis. 2017 Feb;1863(2):518-528. (PMID: 27919711)
Epigenetics. 2020 Mar;15(3):272-282. (PMID: 31509087)
Cell. 2014 Dec 18;159(7):1665-80. (PMID: 25497547)
J Biol Chem. 2005 Jan 7;280(1):64-72. (PMID: 15509558)
Nature. 2002 Apr 4;416(6880):552-6. (PMID: 11932749)
Mol Cell. 2019 Jun 6;74(5):1037-1052.e7. (PMID: 31029542)
Cell. 2013 Apr 25;153(3):692-706. (PMID: 23602152)
Nat Genet. 2005 Aug;37(8):853-62. (PMID: 16007088)
Cell. 2016 Sep 22;167(1):233-247.e17. (PMID: 27662091)
Nature. 1986 May 15-21;321(6067):209-13. (PMID: 2423876)
Nat Rev Mol Cell Biol. 2019 Oct;20(10):590-607. (PMID: 31399642)
Hum Mol Genet. 1995;4 Spec No:1751-5. (PMID: 8541875)
PLoS Genet. 2012 Jun;8(6):e1002750. (PMID: 22761581)
Mol Cell. 2013 Feb 21;49(4):645-56. (PMID: 23352454)
Curr Biol. 2003 Jul 15;13(14):1192-200. (PMID: 12867029)
Nature. 2008 Aug 7;454(7205):766-70. (PMID: 18600261)
Genome Res. 2015 Jun;25(6):918-25. (PMID: 25883319)
Biochim Biophys Acta. 2014 Dec;1839(12):1362-72. (PMID: 24560929)
Sci Rep. 2023 Apr 27;13(1):6874. (PMID: 37106015)
Nat Genet. 2007 Mar;39(3):391-6. (PMID: 17322882)
Clin Epigenetics. 2018 Feb 9;10:17. (PMID: 29449903)
Nucleic Acids Res. 1997 Jun 15;25(12):2532-4. (PMID: 9171110)
Nat Commun. 2021 Sep 29;12(1):5711. (PMID: 34588447)
J Mol Biol. 2001 Jun 22;309(5):1189-99. (PMID: 11399088)
Hum Mol Genet. 2018 Jul 15;27(14):2409-2424. (PMID: 29659838)
Gigascience. 2021 Feb 16;10(2):. (PMID: 33590861)
Nature. 1983 Jan 6;301(5895):89-92. (PMID: 6185846)
Nat Struct Mol Biol. 2021 Jul;28(7):594-603. (PMID: 34140676)
Nature. 2000 Apr 27;404(6781):1003-7. (PMID: 10801130)
Nat Rev Genet. 2007 Apr;8(4):272-85. (PMID: 17363976)
Nat Struct Mol Biol. 2023 Jan;30(1):38-51. (PMID: 36550219)
J Cell Biol. 2007 May 7;177(3):401-11. (PMID: 17485486)
Trends Genet. 2000 Sep;16(9):418-20. (PMID: 10973072)
Bioinformatics. 2014 Feb 01;30(3):428-30. (PMID: 24336642)
Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):6796-9. (PMID: 25368180)
Epigenetics. 2011 Nov;6(11):1373-7. (PMID: 22048250)
Biol Cell. 2023 Jan;115(1):e2200023. (PMID: 36117150)
Methods Mol Biol. 2019;1896:159-190. (PMID: 30474848)
PLoS One. 2007 Nov 07;2(11):e1136. (PMID: 17989773)
Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):976-81. (PMID: 16418264)
J Biol Chem. 1948 Aug;175(1):315-32. (PMID: 18873306)
Nat Methods. 2009 Dec;6(12):917-22. (PMID: 19915560)
Nature. 2011 May 5;473(7345):43-9. (PMID: 21441907)
Genome Res. 2017 Apr;27(4):533-544. (PMID: 28232479)
Nucleic Acids Res. 2017 Jul 27;45(13):7655-7665. (PMID: 28472485)
Curr Opin Cell Biol. 2014 Jun;28:54-60. (PMID: 24690547)
Mol Cell Biol. 2013 Nov;33(21):4321-33. (PMID: 24001767)
J Cell Biol. 2007 Feb 26;176(5):565-71. (PMID: 17312023)
Proc Natl Acad Sci U S A. 2012 Dec 4;109(49):E3350-7. (PMID: 23150568)
Nat Genet. 2001 Jan;27(1):31-9. (PMID: 11137995)
Cell Rep. 2016 Apr 5;15(1):210-218. (PMID: 27052166)
Proc Natl Acad Sci U S A. 2007 Oct 16;104(42):16546-51. (PMID: 17923676)
Proc Natl Acad Sci U S A. 2006 Sep 19;103(38):14080-5. (PMID: 16963560)
Eur J Biochem. 2002 Oct;269(20):4981-4. (PMID: 12383256)
J Biol Chem. 2011 May 27;286(21):18347-53. (PMID: 21454628)
Nat Rev Genet. 2012 May 29;13(7):484-92. (PMID: 22641018)
Mol Cell Biol. 2008 Jan;28(2):752-71. (PMID: 17991895)
Oncotarget. 2016 Jul 19;7(29):46545-46556. (PMID: 27356740)
Science. 2011 Sep 2;333(6047):1300-3. (PMID: 21778364)
Genome Biol. 2012 Jun 15;13(6):R44. (PMID: 22703947)
Mol Cell Biol. 2002 Jan;22(2):480-91. (PMID: 11756544)
Epigenetics Chromatin. 2015 Jul 21;8:24. (PMID: 26195987)
Nat Methods. 2012 Oct;9(10):999-1003. (PMID: 22941365)
Genome Biol. 2013 Sep 24;14(9):r105. (PMID: 24063430)
Methods Mol Biol. 2018;1832:223-241. (PMID: 30073530)
ACS Omega. 2019 Aug 01;4(8):13250-13259. (PMID: 31460452)
Nat Protoc. 2017 Dec;12(12):2478-2492. (PMID: 29120462)
J Am Chem Soc. 2010 Feb 17;132(6):1782-3. (PMID: 20095602)
Bioinformatics. 2017 Dec 15;33(24):3982-3984. (PMID: 28961746)
Nat Commun. 2022 Nov 21;13(1):7130. (PMID: 36414620)
معلومات مُعتمدة: Centre National de la Recherche Scientifique; Institut Curie; AIRC; Fondation ARC pour la recherche sur le cancer; 800924 Marie Skłodowska-Curie Actions
المشرفين على المادة: 0 (Heterochromatin)
EC 2.1.1.37 (DNMT1 protein, human)
0 (DNMT3A protein, human)
EC 2.1.1.37 (DNA (Cytosine-5-)-Methyltransferase 1)
EC 2.1.1.37 (DNA Methyltransferase 3A)
تواريخ الأحداث: Date Created: 20240220 Date Completed: 20240221 Latest Revision: 20240228
رمز التحديث: 20240228
مُعرف محوري في PubMed: PMC10876481
DOI: 10.1083/jcb.202307026
PMID: 38376465
قاعدة البيانات: MEDLINE
الوصف
تدمد:1540-8140
DOI:10.1083/jcb.202307026