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Cell Cycle-Dependent Role of MRN at Dysfunctional Telomeres: ATM Signaling-Dependent Induction of Nonhomologous End Joining (NHEJ) in G1 and Resection-Mediated Inhibition of NHEJ in G2

Nadya DimitrovaThe Rockefeller University, 1230 York Avenue, New York, New York10065
&
Titia de LangeThe Rockefeller University, 1230 York Avenue, New York, New York10065Correspondence[email protected]
Pages 5552-5563 | Received 13 Apr 2009, Accepted 30 Jul 2009, Published online: 21 Mar 2023

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Raffaella Diotti & Diego Loayza. (2011) Shelterin complex and associated factors at human telomeres. Nucleus 2:2, pages 119-135.
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Articles from other publishers (76)

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Chris Wilson & John P Murnane. (2022) High-throughput screen to identify compounds that prevent or target telomere loss in human cancer cells. NAR Cancer 4:4.
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Moisés Ó. Fiesco-Roa, Benilde García-de Teresa, Paula Leal-Anaya, Renée van ‘t Hek, Talia Wegman-Ostrosky, Sara Frías & Alfredo Rodríguez. (2022) Fanconi anemia and dyskeratosis congenita/telomere biology disorders: Two inherited bone marrow failure syndromes with genomic instability. Frontiers in Oncology 12.
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Alex Penev, Marta Markiewicz-Potoczny, Agnel Sfeir & Eros Lazzerini Denchi. (2022) Stem cells at odds with telomere maintenance and protection. Trends in Cell Biology 32:6, pages 527-536.
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Mohammad Shoeb, Helen C.S. Meier & James M. Antonini. (2021) Telomeres in toxicology: Occupational health. Pharmacology & Therapeutics 220, pages 107742.
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Marta Markiewicz-Potoczny, Anastasia Lobanova, Anisha M. Loeb, Oktay Kirak, Teresa Olbrich, Sergio Ruiz & Eros Lazzerini Denchi. (2020) TRF2-mediated telomere protection is dispensable in pluripotent stem cells. Nature 589:7840, pages 110-115.
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Phil Ruis & Simon J. Boulton. (2021) The end protection problem—an unexpected twist in the tail. Genes & Development 35:1-2, pages 1-21.
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Ayse Basak Engin & Atilla Engin. 2021. Protein Kinase-mediated Decisions Between Life and Death. Protein Kinase-mediated Decisions Between Life and Death 71 100 .
Raneem Habib, Ryong Kim, Heidemarie Neitzel, Ilja Demuth, Krystyna Chrzanowska, Eva Seemanova, Renaldo Faber, Martin Digweed, Reinhard Voss, Kathrin Jäger, Karl Sperling & Michael Walter. (2020) Telomere attrition and dysfunction: a potential trigger of the progeroid phenotype in nijmegen breakage syndrome. Aging 12:12, pages 12342-12375.
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Inge de Krijger, Jaco van der Torre, Marieke H. Peuscher, Mathias Eder & Jacqueline J. L. Jacobs. (2020) H3K36 dimethylation by MMSET promotes classical non-homologous end-joining at unprotected telomeres. Oncogene 39:25, pages 4814-4827.
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Zachary Mirman & Titia de Lange. (2020) 53BP1: a DSB escort. Genes & Development 34:1-2, pages 7-23.
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Rekha Rai, Peili Gu, Cayla Broton, Chandan Kumar-Sinha, Yong Chen & Sandy Chang. (2019) The Replisome Mediates A-NHEJ Repair of Telomeres Lacking POT1-TPP1 Independently of MRN Function. Cell Reports 29:11, pages 3708-3725.e5.
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Susanna Stroik, Kevin Kurtz & Eric A Hendrickson. (2019) CtIP is essential for telomere replication. Nucleic Acids Research 47:17, pages 8927-8940.
Crossref
Titia de Lange. (2018) Shelterin-Mediated Telomere Protection. Annual Review of Genetics 52:1, pages 223-247.
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Cristina Espinosa-Diez, RaeAnna Wilson, Namita Chatterjee, Clayton Hudson, Rebecca Ruhl, Christina Hipfinger, Erin Helms, Omar F. Khan, Daniel G. Anderson & Sudarshan Anand. (2018) MicroRNA regulation of the MRN complex impacts DNA damage, cellular senescence, and angiogenic signaling. Cell Death & Disease 9:6.
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Chunyi Hu, Rekha Rai, Chenhui Huang, Cayla Broton, Juanjuan Long, Ying Xu, Jing Xue, Ming Lei, Sandy Chang & Yong Chen. (2017) Structural and functional analyses of the mammalian TIN2-TPP1-TRF2 telomeric complex. Cell Research 27:12, pages 1485-1502.
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Razan Charif, Christine Granotier-Beckers, Hélène Charlotte Bertrand, Joël Poupon, Evelyne Ségal-Bendirdjian, Marie-Paule Teulade-Fichou, François D. Boussin & Sophie Bombard. (2017) Association of a Platinum Complex to a G-Quadruplex Ligand Enhances Telomere Disruption. Chemical Research in Toxicology 30:8, pages 1629-1640.
Crossref
T K Pandita. (2016) Critical role of the POT1 OB domain in maintaining genomic stability. Oncogene 36:14, pages 1908-1910.
Crossref
Rekha Rai, Chunyi Hu, Cayla Broton, Yong Chen, Ming Lei & Sandy Chang. (2017) NBS1 Phosphorylation Status Dictates Repair Choice of Dysfunctional Telomeres. Molecular Cell 65:5, pages 801-817.e4.
Crossref
Marko Ivancich, Zachary Schrank, Luke Wojdyla, Brandon Leviskas, Adijan Kuckovic, Ankita Sanjali & Neelu Puri. (2017) Treating Cancer by Targeting Telomeres and Telomerase. Antioxidants 6:1, pages 15.
Crossref
Keiko Muraki & John P. Murnane. (2017) The DNA damage response at dysfunctional telomeres, and at interstitial and subtelomeric DNA double-strand breaks. Genes & Genetic Systems 92:3, pages 135-152.
Crossref
Yi Gong, Naofumi Handa, Stephen C. Kowalczykowski & Titia de Lange. (2017) PHF11 promotes DSB resection, ATR signaling, and HR. Genes & Development 31:1, pages 46-58.
Crossref
Eros Lazzerini-Denchi & Agnel Sfeir. (2016) Stop pulling my strings — what telomeres taught us about the DNA damage response. Nature Reviews Molecular Cell Biology 17:6, pages 364-378.
Crossref
Morgan Jones, Kamlesh Bisht, Sharon A. Savage, Jayakrishnan Nandakumar, Catherine E. Keegan & Ivan Maillard. (2016) The shelterin complex and hematopoiesis. Journal of Clinical Investigation 126:5, pages 1621-1629.
Crossref
Arthur J. Lustig. (2016) Hypothesis: Paralog Formation from Progenitor Proteins and Paralog Mutagenesis Spur the Rapid Evolution of Telomere Binding Proteins. Frontiers in Genetics 7.
Crossref
Deanna N. Edwards, Amrita Machwe, Li Chen, Vilhelm A. Bohr & David K. Orren. (2015) The DNA structure and sequence preferences of WRN underlie its function in telomeric recombination events. Nature Communications 6:1.
Crossref
Keiko Muraki, Limei Han, Douglas Miller & John P. Murnane. (2015) Processing by MRE11 is involved in the sensitivity of subtelomeric regions to DNA double-strand breaks. Nucleic Acids Research 43:16, pages 7911-7930.
Crossref
Vera Boersma, Nathalie Moatti, Sandra Segura-Bayona, Marieke H. Peuscher, Jaco van der Torre, Brigitte A. Wevers, Alexandre Orthwein, Daniel Durocher & Jacqueline J. L. Jacobs. (2015) MAD2L2 controls DNA repair at telomeres and DNA breaks by inhibiting 5′ end resection. Nature 521:7553, pages 537-540.
Crossref
Sophie Badie, Ana Rita Carlos, Cecilia Folio, Keiji Okamoto, Peter Bouwman, Jos Jonkers & Madalena Tarsounas. (2015) BRCA 1 and Ct IP promote alternative non‐homologous end‐joining at uncapped telomeres . The EMBO Journal 34:3, pages 410-424.
Crossref
Anthony J. Cesare. (2014) Mitosis, double strand break repair, and telomeres: A view from the end. BioEssays 36:11, pages 1054-1061.
Crossref
Ivana Rybanska-Spaeder, Rajib Ghosh & Sonia Franco. (2014) 53BP1 Mediates the Fusion of Mammalian Telomeres Rendered Dysfunctional by DNA-PKcs Loss or Inhibition. PLoS ONE 9:9, pages e108731.
Crossref
Deanna N. Edwards, David K. Orren & Amrita Machwe. (2014) Strand exchange of telomeric DNA catalyzed by the Werner syndrome protein (WRN) is specifically stimulated by TRF2. Nucleic Acids Research 42:12, pages 7748-7761.
Crossref
Maki Ohara, Yumi Funyu, Shunsuke Ebara, Yuki Sakamoto, Ryota Seki, Kenta Iijima, Akiko Ohishi, Junya Kobayashi, Kenshi Komatsu, Akira Tachibana & Hiroshi Tauchi. (2014) Mutations in the FHA-domain of ectopically expressed NBS1 lead to radiosensitization and to no increase in somatic mutation rates via a partial suppression of homologous recombination. Journal of Radiation Research 55:4, pages 690-698.
Crossref
Cristina Bartocci, Jolene K. Diedrich, Iliana Ouzounov, Julia Li, Andrea Piunti, Diego Pasini, John R. YatesIIIIII & Eros Lazzerini Denchi. (2014) Isolation of Chromatin from Dysfunctional Telomeres Reveals an Important Role for Ring1b in NHEJ-Mediated Chromosome Fusions. Cell Reports 7:4, pages 1320-1332.
Crossref
Grace Shim, Michelle Ricoul, William M. Hempel, Edouard I. Azzam & Laure Sabatier. (2014) Crosstalk between telomere maintenance and radiation effects: A key player in the process of radiation-induced carcinogenesis. Mutation Research/Reviews in Mutation Research 760, pages 1-17.
Crossref
Michal Zimmermann & Titia de Lange. (2014) 53BP1: pro choice in DNA repair. Trends in Cell Biology 24:2, pages 108-117.
Crossref
Mária Štorcelová, Marián Vicián, Richard Reis, Michal Zeman & Iveta Herichová. (2013) Expression of cell cycle regulatory factors hus1, gadd45a, rb1, cdkn2a and mre11a correlates with expression of clock gene per2 in human colorectal carcinoma tissue. Molecular Biology Reports 40:11, pages 6351-6361.
Crossref
B Bojovic, H-Y Ho, J Wu & D L Crowe. (2012) Stem cell expansion during carcinogenesis in stem cell-depleted conditional telomeric repeat factor 2 null mutant mice. Oncogene 32:43, pages 5156-5166.
Crossref
Yang Wang, Norman Sharpless & Sandy Chang. (2013) p16INK4a protects against dysfunctional telomere–induced ATR-dependent DNA damage responses. Journal of Clinical Investigation 123:10, pages 4489-4501.
Crossref
Yong Woo Lee & Woo Taek Kim. (2013) Telomerase-Dependent 3′ G-Strand Overhang Maintenance Facilitates GTBP1-Mediated Telomere Protection from Misplaced Homologous Recombination  . The Plant Cell 25:4, pages 1329-1342.
Crossref
Peili Gu, Wei Deng, Ming Lei & Sandy Chang. (2013) Single strand DNA binding proteins 1 and 2 protect newly replicated telomeres. Cell Research 23:5, pages 705-719.
Crossref
Keiko Muraki, Limei Han, Douglas Miller & John P. Murnane. (2013) The Role of ATM in the Deficiency in Nonhomologous End-Joining near Telomeres in a Human Cancer Cell Line. PLoS Genetics 9:3, pages e1003386.
Crossref
Hugo Almeida & Miguel Godinho Ferreira. (2013) Spontaneous telomere to telomere fusions occur in unperturbed fission yeast cells. Nucleic Acids Research 41:5, pages 3056-3067.
Crossref
Francisca Lottersberger, Anne Bothmer, Davide F. Robbiani, Michel C. Nussenzweig & Titia de Lange. (2013) Role of 53BP1 oligomerization in regulating double-strand break repair. Proceedings of the National Academy of Sciences 110:6, pages 2146-2151.
Crossref
Clara Correia Reis, Sílvia Batista & Miguel Godinho Ferreira. (2012) The fission yeast MRN complex tethers dysfunctional telomeres for NHEJ repair. The EMBO Journal 31:24, pages 4576-4586.
Crossref
Agnel Sfeir. (2012) Telomeres at a glance. Journal of Cell Science 125:18, pages 4173-4178.
Crossref
Peng Wu, Hiroyuki Takai & Titia de Lange. (2012) Telomeric 3′ Overhangs Derive from Resection by Exo1 and Apollo and Fill-In by POT1b-Associated CST. Cell 150:1, pages 39-52.
Crossref
Tracy T. Chow, Yong Zhao, Sabrina S. Mak, Jerry W. Shay & Woodring E. Wright. (2012) Early and late steps in telomere overhang processing in normal human cells: the position of the final RNA primer drives telomere shortening. Genes & Development 26:11, pages 1167-1178.
Crossref
Jason A. Stewart, Mary F. Chaiken, Feng Wang & Carolyn M. Price. (2012) Maintaining the end: Roles of telomere proteins in end-protection, telomere replication and length regulation. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 730:1-2, pages 12-19.
Crossref
Hossein Mozdarani. (2012) Biological Complexities in Radiation Carcinogenesis and Cancer Radiotherapy: Impact of New Biological Paradigms. Genes 3:1, pages 90-114.
Crossref
Lucie Najdekrova & Jiri Siroky. (2012) NBS1 plays a synergistic role with telomerase in the maintenance of telomeres in Arabidopsis thaliana. BMC Plant Biology 12:1, pages 167.
Crossref
Zeenia Kaul, Anthony J Cesare, Lily I Huschtscha, Axel A Neumann & Roger R Reddel. (2011) Five dysfunctional telomeres predict onset of senescence in human cells. EMBO reports 13:1, pages 52-59.
Crossref
Raghav Chawla, Sophie Redon, Christina Raftopoulou, Harry Wischnewski, Sarantis Gagos & Claus M Azzalin. (2011) Human UPF1 interacts with TPP1 and telomerase and sustains telomere leading-strand replication. The EMBO Journal 30:19, pages 4047-4058.
Crossref
Angela T. Noon & Aaron A. Goodarzi. (2011) 53BP1-mediated DNA double strand break repair: Insert bad pun here. DNA Repair 10:10, pages 1071-1076.
Crossref
Marieke H. Peuscher & Jacqueline J. L. Jacobs. (2011) DNA-damage response and repair activities at uncapped telomeres depend on RNF8. Nature Cell Biology 13:9, pages 1139-1145.
Crossref
Shahzad Bhatti, Sergei Kozlov, Ammad Ahmad Farooqi, Ali Naqi, Martin Lavin & Kum Kum Khanna. (2011) ATM protein kinase: the linchpin of cellular defenses to stress. Cellular and Molecular Life Sciences 68:18, pages 2977-3006.
Crossref
Travis H. Stracker & John H. J. Petrini. (2011) The MRE11 complex: starting from the ends. Nature Reviews Molecular Cell Biology 12:2, pages 90-103.
Crossref
Gareth J. Williams, Susan P. Lees-Miller & John A. Tainer. (2010) Mre11–Rad50–Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair 9:12, pages 1299-1306.
Crossref
Brandon J. Lamarche, Nicole I. Orazio & Matthew D. Weitzman. (2010) The MRN complex in double-strand break repair and telomere maintenance. FEBS Letters 584:17, pages 3682-3695.
Crossref
Suzanne S. Chan & Sandy Chang. (2010) Defending the end zone: Studying the players involved in protecting chromosome ends. FEBS Letters 584:17, pages 3773-3778.
Crossref
Momchil D Vodenicharov, Nancy Laterreur & Raymund J Wellinger. (2010) Telomere capping in non-dividing yeast cells requires Yku and Rap1. The EMBO Journal 29:17, pages 3007-3019.
Crossref
Rekha Rai, Hong Zheng, Hua He, Ying Luo, Asha Multani, Phillip B Carpenter & Sandy Chang. (2010) The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. The EMBO Journal 29:15, pages 2598-2610.
Crossref
Peng Wu, Megan van Overbeek, Sean Rooney & Titia de Lange. (2010) Apollo Contributes to G Overhang Maintenance and Protects Leading-End Telomeres. Molecular Cell 39:4, pages 606-617.
Crossref
Yung C Lam, Shamima Akhter, Peili Gu, Jing Ye, Anaïs Poulet, Marie-Josèphe Giraud-Panis, Susan M Bailey, Eric Gilson, Randy J Legerski & Sandy Chang. (2010) SNMIB/Apollo protects leading-strand telomeres against NHEJ-mediated repair. The EMBO Journal 29:13, pages 2230-2241.
Crossref
Sylvie Lantuejoul, Christophe Raynaud, Dimitri Salameire, Sylvie Gazzeri, Denis Moro-Sibilot, Jean-Charles Soria, Christian Brambilla & Elizabeth Brambilla. (2010) Telomere Maintenance and DNA Damage Responses during Lung Carcinogenesis. Clinical Cancer Research 16:11, pages 2979-2988.
Crossref
Gaëlle Pennarun, Françoise Hoffschir, Deborah Revaud, Christine Granotier, Laurent R. Gauthier, Patrick Mailliet, Denis S. Biard & François D. Boussin. (2010) ATR contributes to telomere maintenance in human cells. Nucleic Acids Research 38:9, pages 2955-2963.
Crossref
Anthony J. Cesare & Roger R. Reddel. (2010) Alternative lengthening of telomeres: models, mechanisms and implications. Nature Reviews Genetics 11:5, pages 319-330.
Crossref
Agnieszka Rupnik, Noel F. Lowndes & Muriel Grenon. (2009) MRN and the race to the break. Chromosoma 119:2, pages 115-135.
Crossref
Roderick J. O'Sullivan & Jan Karlseder. (2010) Telomeres: protecting chromosomes against genome instability. Nature Reviews Molecular Cell Biology 11:3, pages 171-181.
Crossref
Michael S.Y. Huen & Junjie Chen. (2010) Assembly of checkpoint and repair machineries at DNA damage sites. Trends in Biochemical Sciences 35:2, pages 101-108.
Crossref

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