#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

ALC1/eIF4A1-mediated regulation of CtIP mRNA stability controls DNA end resection


Autoři: Fernando Mejías-Navarro aff001;  Guillermo Rodríguez-Real aff001;  Javier Ramón aff001;  Rosa Camarillo aff001;  Pablo Huertas aff001
Působiště autorů: Department of Genetics, University of Seville, Sevilla, Spain aff001;  Centro Andaluz de Biología Molecular y Medicina Regenerativa-CABIMER, Universidad de Sevilla-CSIC-Universidad Pablo de Olavide, Sevilla, Spain aff002
Vyšlo v časopise: ALC1/eIF4A1-mediated regulation of CtIP mRNA stability controls DNA end resection. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008787
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008787

Souhrn

During repair of DNA double-strand breaks, resection of DNA ends influences how these lesions will be repaired. If resection is activated, the break will be channeled through homologous recombination; if not, it will be simply ligated using the non-homologous end-joining machinery. Regulation of resection relies greatly on modulating CtIP, which can be done by modifying: i) its interaction partners, ii) its post-translational modifications, or iii) its cellular levels, by regulating transcription, splicing and/or protein stability/degradation. Here, we have analyzed the role of ALC1, a chromatin remodeler previously described as an integral part of the DNA damage response, in resection. Strikingly, we found that ALC1 affects resection independently of chromatin remodeling activity or its ability to bind damaged chromatin. In fact, it cooperates with the RNA-helicase eIF4A1 to help stabilize the most abundant splicing form of CtIP mRNA. This function relies on the presence of a specific RNA sequence in the 5′ UTR of CtIP. Therefore, we describe an additional layer of regulation of CtIP—at the level of mRNA stability through ALC1 and eIF4A1.

Klíčová slova:

Cell cycle and cell division – DNA damage – Chromatin – Messenger RNA – Non-homologous end joining – Recombinase polymerase amplification – Small interfering RNAs – Surgical resection


Zdroje

1. Ciccia A, Elledge SJ. The DNA Damage Response: Making It Safe to Play with Knives. Mol Cell. 2010;40: 179–204. doi: 10.1016/j.molcel.2010.09.019 20965415

2. Davis AJA, Chen DDJ. DNA double strand break repair via non-homologous end-joining. Transl Cancer Res. 2013;2: 130–143. doi: 10.3978/j.issn.2218-676X.2013.04.02 24000320

3. Jasin M, Rothstein R. Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol. 2013;5. doi: 10.1101/cshperspect.a012740 24097900

4. Huertas P. DNA resection in eukaryotes: Deciding how to fix the break. Nat Struct Mol Biol. 2010;17: 11–16. doi: 10.1038/nsmb.1710 20051983

5. Symington LS. Mechanism and regulation of DNA end resection in eukaryotes. Crit Rev Biochem Mol Biol. 2016;51: 195–212. doi: 10.3109/10409238.2016.1172552 27098756

6. Makharashvili N, Paull TT. CtIP: A DNA damage response protein at the intersection of DNA metabolism. DNA Repair (Amst). 2015;32: 75–81. doi: 10.1016/j.dnarep.2015.04.016 25957490

7. Liu F, Lee W. CtIP Activates Its Own and Cyclin D1 Promoters via the E2F / RB Pathway during G 1 / S Progression. Mol Cell Biol. 2006;26: 3124–3134. doi: 10.1128/MCB.26.8.3124-3134.2006 16581787

8. Zhang F, Tang H, Jiang Y, Mao Z. The transcription factor GATA3 is required for homologous recombination repair by regulating CtIP expression. Oncogene. 2017;36: 5168–5176. doi: 10.1038/onc.2017.127 28481869

9. Hühn D, Kousholt AN, Sørensen CS, Sartori AA. MiR-19, a component of the oncogenic miR-17∼92 cluster, targets the DNA-end resection factor CtIP. Oncogene. 2015;34: 3977–3984. doi: 10.1038/onc.2014.329 25308476

10. Hashimoto M, Iwabuchi K, Isono M, Matsui T, Matsunaga T, Wakasugi M, et al. Aquarius is required for proper CtIP expression and homologous recombination repair. Sci Rep. 2017;7: 1–11. doi: 10.1038/s41598-016-0028-x 28127051

11. Steger M, Murina O, Hühn D, Ferretti LP, Walser R, Hänggi K, et al. Prolyl isomerase PIN1 regulates DNA double-strand break repair by counteracting DNA end resection. Mol Cell. 2013;50: 333–343. doi: 10.1016/j.molcel.2013.03.023 23623683

12. Lafranchi L, de Boer HR, de Vries EG, Ong S, Sartori AA, van Vugt MA. APC/C C dh1 controls CtIP stability during the cell cycle and in response to DNA damage. EMBO J. 2014;33: 2860–2879. doi: 10.15252/embj.201489017 25349192

13. Huertas P, Jackson SP. Human CtIP Mediates Cell Cycle Control of DNA End Resection and Double Strand Break Repair. J Biol Chem. 2009;284: 9558–9565. doi: 10.1074/jbc.M808906200 19202191

14. Soria-Bretones I, Cepeda-García C, Checa-Rodriguez C, Heyer V, Reina-San-Martin B, Soutoglou E, et al. DNA end resection requires constitutive sumoylation of CtIP by CBX4. Nat Commun. 2017;8. doi: 10.1038/s41467-017-00183-6 28740167

15. Peterson SE, Li Y, Wu-Baer F, Chait BT, Baer R, Yan H, et al. Activation of DSB Processing Requires Phosphorylation of CtIP by ATR. Mol Cell. 2013;49: 657–667. doi: 10.1016/j.molcel.2012.11.020 23273981

16. Yu X, Fu S, Lai M, Baer R, Chen J. BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev. 2006;20: 1721–1726. doi: 10.1101/gad.1431006 16818604

17. Yu X, Chen J. DNA Damage-Induced Cell Cycle Checkpoint Control Requires CtIP, a Phosphorylation-Dependent Binding Partner of BRCA1 C-Terminal Domains DNA Damage-Induced Cell Cycle Checkpoint Control Requires CtIP, a Phosphorylation-Dependent Binding Partner of BRCA1. Mol Cell Biol. 2004;24: 9478–9486. doi: 10.1128/MCB.24.21.9478-9486.2004 15485915

18. Cejka P. DNA end resection: Nucleases team up with the right partners to initiate homologous recombination. J Biol Chem. 2015;290: 22931–22938. doi: 10.1074/jbc.R115.675942 26231213

19. Dantuma NP, van Attikum H. Spatiotemporal regulation of posttranslational modifications in the DNA damage response. EMBO J. 2015;35: 6–23. doi: 10.15252/embj.201592595 26628622

20. Ahel D, Hořejší Z, Wiechens N, Polo SEE, Garcia-Wilson E, Ahel I, et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science (80-). 2009;325: 1240–1243. doi: 10.1126/science.1177321 19661379

21. Sellou H, Lebeaupin T, Chapuis C, Smith R, Hegele A, Singh HR, et al. The poly(ADP-ribose)-dependent chromatin remodeler Alc1 induces local chromatin relaxation upon DNA damage. Mol Biol Cell. 2016;27: 3791–3799. doi: 10.1091/mbc.E16-05-0269 27733626

22. Li Y, Chen L, Chan THM, Liu M, Kong K, Qiu J, et al. SPOCK1 Is Regulated by CHD1L and Blocks Apoptosis and Promotes HCC Cell Invasiveness and Metastasis in Mice. Gastroenterology. 2013;144: 179–191.e4. doi: 10.1053/j.gastro.2012.09.042 23022495

23. Chan THM, Chen L, Liu M, Hu L, Zheng BJ, Poon VKM, et al. Translationally controlled tumor protein induces mitotic defects and chromosome missegregation in hepatocellular carcinoma development. Hepatology. 2012;55: 491–505. doi: 10.1002/hep.24709 21953552

24. Ma N-F, Hu L, Fung JM, Xie D, Zheng B-J, Chen L, et al. Isolation and characterization of a novel oncogene, amplified in liver cancer 1, within a commonly amplified region at 1q21 in hepatocellular carcinoma. Hepatology. 2008;47: 503–510. doi: 10.1002/hep.22072 18023026

25. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells service XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. 1999; 2633–2638.

26. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008;4. doi: 10.1371/journal.pgen.1000110 18584027

27. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol. 2004;24: 9305–16. doi: 10.1128/MCB.24.21.9305-9316.2004 15485900

28. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999;13: 2633–8. doi: 10.1101/gad.13.20.2633 10541549

29. Huertas P, Cruz-Garcia A. Single Molecule Analysis of Resection Tracks. 2018. pp. 147–154.

30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25: 402–408. doi: 10.1006/meth.2001.1262 11846609

31. Varis A, Salmela AL, Kallio MJ. Cenp-F (mitosin) is more than a mitotic marker. Chromosoma. 2006;115: 288–295. doi: 10.1007/s00412-005-0046-0 16565862

32. Cruz-García A, López-Saavedra A, Huertas P. BRCA1 accelerates CtIP-ediated DNA-end resection. Cell Rep. 2014;9: 451–459. doi: 10.1016/j.celrep.2014.08.076 25310973

33. Zimmermann M, De Lange T. 53BP1: Pro choice in DNA repair. Trends Cell Biol. 2014;24: 108–117. doi: 10.1016/j.tcb.2013.09.003 24094932

34. López-Saavedra A, Gómez-Cabello D, Domínguez-Sánchez MS, Mejías-Navarro F, Fernández-Ávila MJ, Dinant C, et al. A genome-wide screening uncovers the role of CCAR2 as an antagonist of DNA end resection. Nat Commun. 2016;7. doi: 10.1038/ncomms12364 27503537

35. Wolfe AL, Singh K, Zhong Y, Drewe P, Rajasekhar VK, Sanghvi VR, et al. RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature. 2014;513: 65–70. doi: 10.1038/nature13485 25079319

36. Modelska A, Turro E, Russell R, Beaton J, Sbarrato T, Spriggs K, et al. The malignant phenotype in breast cancer is driven by eIf4A1-mediated changes in the translational landscape. Cell Death Dis. 2015;6: 1–12. doi: 10.1038/cddis.2014.542 25611378

37. Wong AK, Ormonde PA, Pero R, Chen Y, Lian L, Salada G, et al. Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene. 1998;17: 2279–2285. doi: 10.1038/sj.onc.1202150 9811458

38. Chen L, Nievera CJ, Lee AYL, Wu X. Cell cycle-dependent complex formation of BRCA1·CtIP·MRN is important for DNA double-strand break repair. J Biol Chem. 2008;283: 7713–7720. doi: 10.1074/jbc.M710245200 18171670

39. Prados-Carvajal R, López-Saavedra A, Cepeda-García C, Jimeno S, Huertas P. Multiple roles of the splicing complex SF3B in DNA end resection and homologous recombination. DNA Repair (Amst). 2018;66–67: 11–23. doi: 10.1016/j.dnarep.2018.04.003 29705135

40. Muto A, Sugihara Y, Shibakawa M, Oshima K, Matsuda T, Nadano D. The mRNA-binding protein Serbp1 as an auxiliary protein associated with mammalian cytoplasmic ribosomes. Cell Biochem Funct. 2018;36: 312–322. doi: 10.1002/cbf.3350 30039520

41. Ahn J-W, Kim S, Na W, Baek S-J, Kim J-H, Min K, et al. SERBP1 affects homologous recombination-mediated DNA repair by regulation of CtIP translation during S phase. Nucleic Acids Res. 2015;43: 6321–6333. doi: 10.1093/nar/gkv592 26068472

42. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, et al. Human CtIP promotes DNA end resection. Nature. 2007;450: 509–514. doi: 10.1038/nature06337 17965729

43. Dungrawala H, Rose KL, Bhat KP, Mohni KN, Glick GG, Couch FB, et al. The Replication Checkpoint Prevents Two Types of Fork Collapse without Regulating Replisome Stability. Mol Cell. 2015;59: 998–1010. doi: 10.1016/j.molcel.2015.07.030 26365379

44. Yeo JE, Lee EH, Hendrickson EA, Sobeck A. CtIP mediates replication fork recovery in a FANCD2-regulated manner. Hum Mol Genet. 2014;23: 3695–3705. doi: 10.1093/hmg/ddu078 24556218

45. Przetocka S, Porro A, Bolck HA, Walker C, Lezaja A, Trenner A, et al. CtIP-Mediated Fork Protection Synergizes with BRCA1 to Suppress Genomic Instability upon DNA Replication Stress. Mol Cell. 2018;72: 568–582.e6. doi: 10.1016/j.molcel.2018.09.014 30344097


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 5
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Halitóza
Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#