ATR mediates a checkpoint at the nuclear envelope in response to mechanical stress

Cell

Volumn 158, Issue 3, 2014, Pages 633-646

  Kumar, Amit ^a   Mazzanti, Michele ^b   Mistrik, Martin ^c   Kosar, Martin ^d,e   Beznoussenko, Galina V ^a   Mironov, Alexandre A ^a   Garrè, Massimiliano ^a   Parazzoli, Dario ^a   Shivashankar, G V ^f   Scita, Giorgio ^a,b   Bartek, Jiri ^c,d,e   Foiani, Marco ^a,b  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c PALACKÝ UNIVERSITY   (Czech Republic)

^d DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^e INSTITUTE OF MATHEMATICS   (Czech Republic)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; ATM PROTEIN; ATR PROTEIN, HUMAN; ATR PROTEIN, MOUSE; CHECKPOINT KINASE 1; CHROMATIN; PROTEIN KINASE;

ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL NUCLEUS MEMBRANE; CHROMATIN CONDENSATION; DNA DAMAGE; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MECHANICAL STRESS; MECHANICAL TORSION; OSMOTIC STRESS; PRIORITY JOURNAL; PROPHASE; 3T3 CELL LINE; ANIMAL; CELL CYCLE CHECKPOINT; CHROMATIN; CYTOLOGY; FIBROBLAST; HELA CELL LINE; METABOLISM; MOUSE; OSMOSIS; TUMOR CELL LINE;

ANIMALS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CHROMATIN; FIBROBLASTS; HELA CELLS; HUMANS; MICE; NIH 3T3 CELLS; NUCLEAR ENVELOPE; OSMOSIS; PROTEIN KINASES; STRESS, MECHANICAL;

EID: 84905385420     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.05.046     Document Type: Article

References (69)

1. P.S. Aguilar, and D. de Mendoza Control of fatty acid desaturation: a mechanism conserved from bacteria to humans Mol. Microbiol. 62 2006 1507 1514
2. G.K. Alderton, H. Joenje, R. Varon, A.D. Børglum, P.A. Jeggo, and M. O'Driscoll Seckel syndrome exhibits cellular features demonstrating defects in the ATR-signalling pathway Hum. Mol. Genet. 13 2004 3127 3138
3. C.J. Bakkenist, and M.B. Kastan DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation Nature 421 2003 499 506
4. J. Beaudouin, D. Gerlich, N. Daigle, R. Eils, and J. Ellenberg Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina Cell 108 2002 83 96
5. D. Berchtold, M. Piccolis, N. Chiaruttini, I. Riezman, H. Riezman, A. Roux, T.C. Walther, and R. Loewith Plasma membrane stress induces relocalization of Slm proteins and activation of TORC2 to promote sphingolipid synthesis Nat. Cell Biol. 14 2012 542 547
6. R. Bermejo, A. Kumar, and M. Foiani Preserving the genome by regulating chromatin association with the nuclear envelope Trends Cell Biol. 22 2012 465 473
7. R. Bermejo, M.S. Lai, and M. Foiani Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription Mol. Cell 45 2012 710 718
8. R. Bermejo, Y. Doksani, T. Capra, Y.M. Katou, H. Tanaka, K. Shirahige, and M. Foiani Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation Genes Dev. 21 2007 1921 1936
9. R. Bermejo, T. Capra, R. Jossen, A. Colosio, C. Frattini, W. Carotenuto, A. Cocito, Y. Doksani, H. Klein, and B. Gómez-González et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores Cell 146 2011 233 246
10. M. Blasius, J.V. Forment, N. Thakkar, S.A. Wagner, C. Choudhary, and S.P. Jackson A phospho-proteomic screen identifies substrates of the checkpoint kinase Chk1 Genome Biol. 12 2011 R78
11. C.A. Bourgeois, D. Hemon, and M. Bouteille Structural relationship between the nucleolus and the nuclear envelope J. Ultrastruct. Res. 68 1979 328 340
12. E.J. Brown, and D. Baltimore Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance Genes Dev. 17 2003 615 628
13. A.M. Casper, P. Nghiem, M.F. Arlt, and T.W. Glover ATR regulates fragile site stability Cell 111 2002 779 789
14. R.S. Cha, and N. Kleckner ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones Science 297 2002 602 606
15. D.E. Comings Arrangement of chromatin in the nucleus Hum. Genet. 53 1980 131 143
16. D.S. Dimitrova, and D.M. Gilbert The spatial position and replication timing of chromosomal domains are both established in early G1 phase Mol. Cell 4 1999 983 993
17. D.S. Dimitrova, I.T. Todorov, T. Melendy, and D.M. Gilbert Mcm2, but not RPA, is a component of the mammalian early G1-phase prereplication complex J. Cell Biol. 146 1999 709 722
18. A.M. Duursma, R. Driscoll, J.E. Elias, and K.A. Cimprich A role for the MRN complex in ATR activation via TOPBP1 recruitment Mol. Cell 50 2013 116 122
19. J.M. Enserink, M.B. Smolka, H. Zhou, and R.D. Kolodner Checkpoint proteins control morphogenetic events during DNA replication stress in Saccharomyces cerevisiae J. Cell Biol. 175 2006 729 741
20. P. Friedl, K. Wolf, and J. Lammerding Nuclear mechanics during cell migration Curr. Opin. Cell Biol. 23 2011 55 64
21. K. Fujikawa-Yamamoto, and S. Odashima Effects of hydroxyurea on the phagocytosis of microspheres in V79 cells Cell Struct. Funct. 14 1989 485 493
22. G. Gerlitz, and M. Bustin Efficient cell migration requires global chromatin condensation J. Cell Sci. 123 2010 2207 2217
23. A. Grinthal, I. Adamovic, B. Weiner, M. Karplus, and N. Kleckner PR65, the HEAT-repeat scaffold of phosphatase PP2A, is an elastic connector that links force and catalysis Proc. Natl. Acad. Sci. USA 107 2010 2467 2472
24. N. Hashash, A.L. Johnson, and R.S. Cha Topoisomerase II- and condensin-dependent breakage of MEC1ATR-sensitive fragile sites occurs independently of spindle tension, anaphase, or cytokinesis PLoS Genet. 8 2012 e1002978
25. S.H. Hu, J.X. Chen, J.P. Butler, and N. Wang Prestress mediates force propagation into the nucleus Biochem. Biophys. Res. Commun. 329 2005 423 428
26. S.P. Jackson, and J. Bartek The DNA-damage response in human biology and disease Nature 461 2009 1071 1078
27. A. Krämer, N. Mailand, C. Lukas, R.G. Syljuåsen, C.J. Wilkinson, E.A. Nigg, J. Bartek, and J. Lukas Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase Nat. Cell Biol. 6 2004 884 891
28. B.E. Kremer, L.A. Adang, and I.G. Macara Septins regulate actin organization and cell-cycle arrest through nuclear accumulation of NCK mediated by SOCS7 Cell 130 2007 837 850
29. N. Kudo, B. Wolff, T. Sekimoto, E.P. Schreiner, Y. Yoneda, M. Yanagida, S. Horinouchi, and M. Yoshida Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1 Exp. Cell Res. 242 1998 540 547
30. D. Kültz, and D. Chakravarty Hyperosmolality in the form of elevated NaCl but not urea causes DNA damage in murine kidney cells Proc. Natl. Acad. Sci. USA 98 2001 1999 2004
31. A. Kumar, M. Marqués, and A.C. Carrera Phosphoinositide 3-kinase activation in late G1 is required for c-Myc stabilization and S phase entry Mol. Cell. Biol. 26 2006 9116 9125
32. A. Kumar, O. Fernandez-Capetillo, and A.C. Carrera Nuclear phosphoinositide 3-kinase beta controls double-strand break DNA repair Proc. Natl. Acad. Sci. USA 107 2010 7491 7496
33. A. Kumar, J. Redondo-Muñoz, V. Perez-García, I. Cortes, M. Chagoyen, and A.C. Carrera Nuclear but not cytosolic phosphoinositide 3-kinase beta has an essential function in cell survival Mol. Cell. Biol. 31 2011 2122 2133
34. H.S. Kweon, G.V. Beznoussenko, M. Micaroni, R.S. Polishchuk, A. Trucco, O. Martella, D. Di Giandomenico, P. Marra, A. Fusella, and A. Di Pentima et al. Golgi enzymes are enriched in perforated zones of golgi cisternae but are depleted in COPI vesicles Mol. Biol. Cell 15 2004 4710 4724
35. A. Mammoto, T. Mammoto, and D.E. Ingber Mechanosensitive mechanisms in transcriptional regulation J. Cell Sci. 125 2012 3061 3073
36. A.J. Maniotis, C.S. Chen, and D.E. Ingber Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure Proc. Natl. Acad. Sci. USA 94 1997 849 854
37. R.P. Martins, J.D. Finan, F. Guilak, and D.A. Lee Mechanical regulation of nuclear structure and function Annu. Rev. Biomed. Eng. 14 2012 431 455
38. M. Marqués, A. Kumar, A.M. Poveda, S. Zuluaga, C. Hernandez, S. Jackson, P. Pasero, and A.C. Carrera Specific function of phosphoinositide 3-kinase beta in the control of DNA replication Proc. Natl. Acad. Sci. USA 106 2009 7525 7530
39. S. Matsuoka, B.A. Ballif, A. Smogorzewska, E.R. McDonald 3rd, K.E. Hurov, J. Luo, C.E. Bakalarski, Z. Zhao, N. Solimini, and Y. Lerenthal et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage Science 316 2007 1160 1166
40. A. Mazumder, T. Roopa, A. Basu, L. Mahadevan, and G.V. Shivashankar Dynamics of chromatin decondensation reveals the structural integrity of a mechanically prestressed nucleus Biophys. J. 95 2008 3028 3035
41. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature 438 2005 590 596
42. K. Mekhail, and D. Moazed The nuclear envelope in genome organization, expression and stability Nat. Rev. Mol. Cell Biol. 11 2010 317 328
43. A.A. Mironov, and G.V. Beznoussenko Correlative microscopy: a potent tool for the study of rare or unique cellular and tissue events J. Microsc. 235 2009 308 321
44. A.A. Mironov, and G.V. Beznoussenko Correlative light-electron microscopy a potent tool for the imaging of rare or unique cellular and tissue events and structures Methods Enzymol. 504 2012 201 219
45. M. Murga, S. Bunting, M.F. Montaña, R. Soria, F. Mulero, M. Cañamero, Y. Lee, P.J. McKinnon, A. Nussenzweig, and O. Fernandez-Capetillo A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging Nat. Genet. 41 2009 891 898
46. P. Nghiem, P.K. Park, Y. Kim, C. Vaziri, and S.L. Schreiber ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation Proc. Natl. Acad. Sci. USA 98 2001 9092 9097
47. M. O'Driscoll, V.L. Ruiz-Perez, C.G. Woods, P.A. Jeggo, and J.A. Goodship A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome Nat. Genet. 33 2003 497 501
48. C. Ostlund, T. Sullivan, C.L. Stewart, and H.J. Worman Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins Biochemistry 45 2006 1374 1382
49. J. Perry, and N. Kleckner The ATRs, ATMs, and TORs are giant HEAT repeat proteins Cell 112 2003 151 155
50. R.S. Polishchuk, E.V. Polishchuk, and A.A. Mironov Coalescence of Golgi fragments in microtubule-deprived living cells Eur. J. Cell Biol. 78 1999 170 185
51. A.C. Rowat, J. Lammerding, and J.H. Ipsen Mechanical properties of the cell nucleus and the effect of emerin deficiency Biophys. J. 91 2006 4649 4664
52. Y.Y. Shevelyov, and D.I. Nurminsky The nuclear lamina as a gene-silencing hub Curr. Issues Mol. Biol. 14 2012 27 38
53. G.V. Shivashankar Mechanosignaling to the cell nucleus and gene regulation Annu. Rev. Biophys. 40 2011 361 378
54. D.N. Simon, and K.L. Wilson The nucleoskeleton as a genome-associated dynamic 'network of networks' Nat. Rev. Mol. Cell Biol. 12 2011 695 708
55. J.M. Sogo, M. Lopes, and M. Foiani Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects Science 297 2002 599 602
56. R.S. Tibbetts, D. Cortez, K.M. Brumbaugh, R. Scully, D. Livingston, S.J. Elledge, and R.T. Abraham Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress Genes Dev. 14 2000 2989 3002
57. L.I. Toledo, M. Murga, R. Zur, R. Soria, A. Rodriguez, S. Martinez, J. Oyarzabal, J. Pastor, J.R. Bischoff, and O. Fernandez-Capetillo A cell-based screen identifies ATR inhibitors with synthetic lethal properties for cancer-associated mutations Nat. Struct. Mol. Biol. 18 2011 721 727
58. L.I. Toledo, M. Altmeyer, M.B. Rask, C. Lukas, D.H. Larsen, L.K. Povlsen, S. Bekker- Jensen, N. Mailand, J. Bartek, and J. Lukas ATR prohibits replication catastrophe by preventing global exhaustion of RPA Cell 155 2013 1088 1103
59. B.D. Towbin, P. Meister, and S.M. Gasser The nuclear envelope - a scaffold for silencing? Curr. Opin. Genet. Dev. 19 2009 180 186
60. V.M. Vassin, R.W. Anantha, E. Sokolova, S. Kanner, and J.A. Borowiec Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress J. Cell Sci. 122 2009 4070 4080
61. L. Vigh, H. Nakamoto, J. Landry, A. Gomez-Munoz, J.L. Harwood, and I. Horvath Membrane regulation of the stress response from prokaryotic models to mammalian cells Ann. N Y Acad. Sci. 1113 2007 40 51
62. J.C. Wang Cellular roles of DNA topoisomerases: a molecular perspective Nat. Rev. Mol. Cell Biol. 3 2002 430 440
63. N. Wang, J.D. Tytell, and D.E. Ingber Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus Nat. Rev. Mol. Cell Biol. 10 2009 75 82
64. X. Wang, L. Zou, T. Lu, S. Bao, K.E. Hurov, W.N. Hittelman, S.J. Elledge, and L. Li Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress Mol. Cell 23 2006 331 341
65. D. Wilsker, E. Petermann, T. Helleday, and F. Bunz Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control Proc. Natl. Acad. Sci. USA 105 2008 20752 20757
66. K. Wolf, and P. Friedl Mapping proteolytic cancer cell-extracellular matrix interfaces Clin. Exp. Metastasis 26 2009 289 298
67. S. Zhang, P. Hemmerich, and F. Grosse Centrosomal localization of DNA damage checkpoint proteins J. Cell. Biochem. 101 2007 451 465
68. X.H. Zhang, C. Zhao, and Z.A. Ma The increase of cell-membranous phosphatidylcholines containing polyunsaturated fatty acid residues induces phosphorylation of p53 through activation of ATR J. Cell Sci. 120 2007 4134 4143
69. L. Zou, and S.J. Elledge Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes Science 300 2003 1542 1548