Balestrini et al Defining ATM-independent Functions of the ... · Balestrini et al 1 Defining ATM-independent Functions of the Mre11 Complex with a Novel Mouse Model Alessia Balestrini1,
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
Balestrini et al
1
Defining ATM-independent Functions of the Mre11 Complex with a Novel Mouse
Model
Alessia Balestrini1, Laura Nicolas2, Katherine Yang-lott3,4, Olga A. Guryanova5,
Ross L. Levine5, Craig H. Bassing3,4, Jayanta Chaudhuri2, John H.J. Petrini1 *
1Molecular Biology Program, Sloan-Kettering Institute, New York, NY, USA
2 Immunology Program, Memorial Sloan Kettering Cancer Center, New York, NY, USA
3 Department of Pathology and Laboratory Medicine, Center for Childhood Cancer
Research, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, PA
4 Abramson Family Cancer Research Institute, Department of Pathology and Laboratory
Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA
5 Human Oncology and Pathogenesis Program, Leukemia Service, Department of
Medicine, Memorial Sloan-Kettering Cancer Center, New York, NY, USA
*Corresponding author: John H. J. Petrini, Memorial Sloan-Kettering Cancer Center,
1275 York Avenue, New York, NY 10065. Phone: 212-639-2927, Fax: 646-422-2062,
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
1. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40:179-204. 2. Stracker TH, Petrini JH. The MRE11 complex: starting from the ends. Nature reviews Molecular cell biology. 2011;12:90-103. 3. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer. 2003;3:155-68. 4. Stracker TH, Theunissen JW, Morales M, Petrini JH. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA repair. 2004;3:845-54. 5. Deriano L, Stracker TH, Baker A, Petrini JH, Roth DB. Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol Cell. 2009;34:13-25. 6. Saidi A, Li TL, Weih F, Concannon P, Wang ZQ. Dual Functions of Nbs1 in the Repair of DNA Breaks and Proliferation Ensure Proper V(D)J Recombination and T-Cell Development. Mol Cell Biol. 2010;30:5572-81. 7. Reina-San-Martin B, Nussenzweig MC, Nussenzweig A, Difilippantonio S. Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1. Proc Natl Acad Sci U S A. 2005;102:1590-5. 8. Williams BR, Mirzoeva OK, Morgan WF, Lin J, Dunnick W, Petrini JH. A murine model of Nijmegen breakage syndrome. Curr Biol. 2002;12:648-53. 9. Theunissen JW, Kaplan MI, Hunt PA, Williams BR, Ferguson DO, Alt FW, et al. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol Cell. 2003;12:1511-23. 10. Morales M, Theunissen JW, Kim CF, Kitagawa R, Kastan MB, Petrini JH. The Rad50S allele promotes ATM-dependent DNA damage responses and suppresses ATM deficiency: implications for the Mre11 complex as a DNA damage sensor. Genes Dev. 2005;19:3043-54. 11. Shiotani B, Nguyen HD, Hakansson P, Marechal A, Tse A, Tahara H, et al. Two distinct modes of ATR activation orchestrated by Rad17 and Nbs1. Cell reports. 2013;3:1651-62. 12. Duursma AM, Driscoll R, Elias JE, Cimprich KA. A role for the MRN complex in ATR activation via TOPBP1 recruitment. Mol Cell. 2013;50:116-22. 13. Flynn RL, Zou L. ATR: a master conductor of cellular responses to DNA replication stress. Trends Biochem Sci. 2011;36:133-40. 14. Lopez-Contreras AJ, Fernandez-Capetillo O. The ATR barrier to replication-born DNA damage. DNA repair. 2010;9:1249-55. 15. Zha S, Sekiguchi J, Brush JW, Bassing CH, Alt FW. Complementary functions of ATM and H2AX in development and suppression of genomic instability. Proc Natl Acad Sci U S A. 2008;105:9302-6. 16. Stadtfeld M, Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development. 2005;132:203-13. 17. Stavnezer J, Guikema JE, Schrader CE. Mechanism and regulation of class switch recombination. Annu Rev Immunol. 2008;26:261-92.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
18. Revy P, Buck D, le Deist F, de Villartay JP. The repair of DNA damages/modifications during the maturation of the immune system: lessons from human primary immunodeficiency disorders and animal models. Adv Immunol. 2005;87:237-95. 19. Helmink BA, Bredemeyer AL, Lee BS, Huang CY, Sharma GG, Walker LM, et al. MRN complex function in the repair of chromosomal Rag-mediated DNA double-strand breaks. J Exp Med. 2009;206:669-79. 20. Fehling HJ, Krotkova A, Saint-Ruf C, von Boehmer H. Crucial role of the pre-T-cell receptor alpha gene in development of alpha beta but not gamma delta T cells. Nature. 1995;375:795-8. 21. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 1992;68:869-77. 22. Gordon J, Millsum MJ, Guy GR, Ledbetter JA. Resting B lymphocytes can be triggered directly through the CDw40 (Bp50) antigen. A comparison with IL-4-mediated signaling. J Immunol. 1988;140:1425-30. 23. Franco S, Gostissa M, Zha S, Lombard DB, Murphy MM, Zarrin AA, et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol Cell. 2006;21:201-14. 24. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 2000;14:1448-59. 25. Anantha RW, Vassin VM, Borowiec JA. Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J Biol Chem. 2007;282:35910-23. 26. Brown EJ, Baltimore D. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev. 2003;17:615-28. 27. Casper AM, Nghiem P, Arlt MF, Glover TW. ATR regulates fragile site stability. Cell. 2002;111:779-89. 28. Durkin SG, Arlt MF, Howlett NG, Glover TW. Depletion of CHK1, but not CHK2, induces chromosomal instability and breaks at common fragile sites. Oncogene. 2006;25:4381-8. 29. Krummel KA, Denison SR, Calhoun E, Phillips LA, Smith DI. The common fragile site FRA16D and its associated gene WWOX are highly conserved in the mouse at Fra8E1. Genes Chromosomes Cancer. 2002;34:154-67. 30. Varon R, Vissinga C, Platzer M, Cerosaletti KM, Chrzanowska KH, Saar K, et al. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell. 1998;93:467-76. 31. Xie A, Kwok A, Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nature structural & molecular biology. 2009;16:814-8. 32. Rass E, Grabarz A, Plo I, Gautier J, Bertrand P, Lopez BS. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nature structural & molecular biology. 2009;16:819-24. 33. Chapman JR, Barral P, Vannier JB, Borel V, Steger M, Tomas-Loba A, et al. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell. 2013;49:858-71. 34. Deng Y, Guo X, Ferguson DO, Chang S. Multiple roles for MRE11 at uncapped telomeres. Nature. 2009;460:914-8.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
35. Dinkelmann M, Spehalski E, Stoneham T, Buis J, Wu Y, Sekiguchi JM, et al. Multiple functions of MRN in end-joining pathways during isotype class switching. Nature structural & molecular biology. 2009;16:808-13. 36. Williams RS, Williams JS, Tainer JA. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem Cell Biol. 2007;85:509-20. 37. Stiff T, Reis C, Alderton GK, Woodbine L, O'Driscoll M, Jeggo PA. Nbs1 is required for ATR-dependent phosphorylation events. EMBO J. 2004. 38. Gupta GP, Vanness K, Barlas A, Manova-Todorova KO, Wen YH, Petrini JH. The Mre11 complex suppresses oncogene-driven breast tumorigenesis and metastasis. Mol Cell. 2013;52:353-65. 39. Brown EJ, Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000;14:397-402. 40. Al-Ahmadie H, Iyer G, Hohl M, Asthana S, Inagaki A, Schultz N, et al. Synthetic Lethality in ATM-Deficient RAD50-Mutant Tumors Underlies Outlier Response to Cancer Therapy. Cancer discovery. 2014;4:1014-21. 41. Theunissen JW, Petrini JH. Methods for studying the cellular response to DNA damage: influence of the Mre11 complex on chromosome metabolism. Methods Enzymol. 2006;409:251-84. 42. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol. 1998;72:8463-71. 43. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science. 2002;295:868-72. 44. Lee-Theilen M, Matthews AJ, Kelly D, Zheng S, Chaudhuri J. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nature structural & molecular biology. 2011;18:75-9. 45. Nowak U, Matthews AJ, Zheng S, Chaudhuri J. The splicing regulator PTBP2 interacts with the cytidine deaminase AID and promotes binding of AID to switch-region DNA. Nature immunology. 2011;12:160-6. 46. Ehrenstein MR, Rada C, Jones AM, Milstein C, Neuberger MS. Switch junction sequences in PMS2-deficient mice reveal a microhomology-mediated mechanism of Ig class switch recombination. Proc Natl Acad Sci U S A. 2001;98:14553-8. 47. Hasham MG, Snow KJ, Donghia NM, Branca JA, Lessard MD, Stavnezer J, et al. Activation-induced cytidine deaminase-initiated off-target DNA breaks are detected and resolved during S phase. J Immunol. 2012;189:2374-82. 48. Bassing CH, Suh H, Ferguson DO, Chua KF, Manis J, Eckersdorff M, et al. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell. 2003;114:359-70. 49. Stracker TH, Couto SS, Cordon-Cardo C, Matos T, Petrini JH. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol Cell. 2008;31:21-32. 50. Chaudhuri J, Tian M, Khuong C, Chua K, Pinaud E, Alt FW. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature. 2003;422:726-30.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281
Published OnlineFirst November 4, 2015.Mol Cancer Res Alessia Balestrini, Laura Nicolas, Katherine Yang-lott, et al. with a Novel Mouse ModelDefining ATM-independent Functions of the Mre11 Complex
Updated version
10.1158/1541-7786.MCR-15-0281doi:
Access the most recent version of this article at:
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 4, 2015; DOI: 10.1158/1541-7786.MCR-15-0281