A requirement for polymerized actin in DNA double-strand break repair

Nucleus (United States)

Volumn 3, Issue 4, 2012, Pages 384-395

  Andrin, Christi ^a   McDonald, Darin ^b   Attwood, Kathleen M ^c   Rodrigue, Amélie ^d   Ghosh, Sunita ^b   Mirzayans, Razmik ^b   Masson, Jean Yves ^d   Dellaire, Graham ^c,e   Hendzel, Michael J ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b CROSS CANCER INSTITUTE   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

^d UNIVERSITÉ LAVAL   (Canada)

^e Beatrice Hunter Cancer Research Institute   (Canada)

Author keywords

DNA damage; DSB repair; Ku70; Ku80; Nuclear actin; Polymeric actin

Indexed keywords

ACTIN; CELL DNA; CHECKPOINT KINASE 2; CYTOCHALASIN D; DOUBLE STRANDED DNA; HISTONE H2AX; KU ANTIGEN; MUTANT PROTEIN; CELL NUCLEUS ANTIGEN; DNA BINDING PROTEIN; GREEN FLUORESCENT PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEUROBLASTOMA CELL; OSTEOSARCOMA CELL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; BINDING SITE; CELL NUCLEUS; CHEMISTRY; DNA DAMAGE; HELA CELL LINE; METABOLISM; POLYMERIZATION; TUMOR CELL LINE;

ACTINS; ANTIGENS, NUCLEAR; BINDING SITES; CELL LINE, TUMOR; CELL NUCLEUS; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; POLYMERIZATION;

EID: 84863853737     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.21055     Document Type: Article

References (53)

1. McKinnon PJ, Caldecott KW. DNA strand break repair and human genetic disease. Annu Rev Genomics Hum Genet 2007; 8:37-55; PMID:17887919; http://dx.doi.org/10.1146/annurev.genom.7.080505.115648.
2. Phillips ER, McKinnon PJ. DNA double-strand break repair and development. Oncogene 2007; 26:7799-808; PMID:18066093; http://dx.doi.org/10.1038/sj.onc.1210877.
3. Wyman C, Kanaar R. DNA double-strand break repair: all's well that ends well. Annu Rev Genet 2006; 40:363-83; PMID:16895466; http://dx.doi.org/10.1146/annurev.genet.40.110405.090451.
4. Shrivastav M, De Haro LP, NickoloffJA. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008; 18:134-47; PMID:18157161; http://dx.doi. org/10.1038/cr.2007.111.
5. Bettinger BT, Gilbert DM, Amberg DC. Actin up in the nucleus. Nat Rev Mol Cell Biol 2004; 5:410-5; PMID:15122354; http://dx.doi.org/10.1038/nrm1370.
6. Blessing CA, Ugrinova GT, Goodson HV. Actin and ARPs: action in the nucleus. Trends Cell Biol 2004; 14:435-42; PMID:15308210; http://dx.doi. org/10.1016/j.tcb.2004.07.009.
7. Cruz JR, de la Torre C, Moreno Diaz de la Espina S. Nuclear actin in plants. Cell Biol Int 2007; PMID:18155933.
8. Pederson T, Aebi U. Nuclear actin extends, with no contraction in sight. Mol Biol Cell 2005; 16:5055-60; PMID:16148048; http://dx.doi.org/10.1091/mbc. E05-07-0656.
9. Olave IA, Reck-Peterson SL, Crabtree GR. Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem 2002; 71:755-81; PMID:12045110; http://dx.doi.org/10.1146/annurev. biochem.71.110601.135507.
10. Miralles F, Visa N. Actin in transcription and transcription regulation. Curr Opin Cell Biol 2006; 18:261-6; PMID:16687246; http://dx.doi.org/10.1016/j. ceb.2006.04.009.
11. Percipalle P, Visa N. Molecular functions of nuclear actin in transcription. J Cell Biol 2006; 172:967-71; PMID:16549500; http://dx.doi.org/10.1083/jcb.200512083.
12. Hofmann WA, Stojiljkovic L, Fuchsova B, Vargas GM, Mavrommatis E, Philimonenko V, et al. Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol 2004; 6:1094-101; PMID:15502823; http://dx.doi. org/10.1038/ncb1182.
13. Hu P, Wu S, Hernandez N. A role for beta-actin in RNA polymerase III transcription. Genes Dev 2004; 18:3010-5; PMID:15574586; http://dx.doi. org/10.1101/gad.1250804.
14. Kukalev A, Nord Y, Palmberg C, Bergman T, Percipalle P. Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol 2005; 12:238-44; PMID:15711563; http://dx.doi. org/10.1038/nsmb904.
15. Philimonenko VV, Zhao J, Iben S, Dingová H, Kyselá K, Kahle M, et al. Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol 2004; 6:1165-72; PMID:15558034; http://dx.doi.org/10.1038/ncb1190.
16. Percipalle P, Fomproix N, Kylberg K, Miralles F, Bjorkroth B, Daneholt B, et al. An actin-ribonucleoprotein interaction is involved in transcription by RNA polymerase II. Proc Natl Acad Sci USA 2003; 100:6475-80; PMID:12743363; http://dx.doi. org/10.1073/pnas.1131933100.
17. Fomproix N, Percipalle P. An actin-myosin complex on actively transcribing genes. Exp Cell Res 2004; 294:140-8; PMID:14980509; http://dx.doi. org/10.1016/j.yexcr.2003.10.028.
18. Chen M, Shen X. Nuclear actin and actin-related proteins in chromatin dynamics. Curr Opin Cell Biol 2007; 19:326-30; PMID:17467255; http://dx.doi. org/10.1016/j.ceb.2007.04.009.
19. Meagher RB, Kandasamy MK, Deal RB, McKinney EC. Actin-related proteins in chromatin-level control of the cell cycle and developmental transitions. Trends Cell Biol 2007; 17:325-32; PMID:17643304; http://dx.doi.org/10.1016/j.tcb.2007.06.001.
20. Zhao K, Wang W, Rando OJ, Xue Y, Swiderek K, Kuo A, et al. Rapid and phosphoinositol-dependent binding of the SWI/SNF-like BAF complex to chromatin after T lymphocyte receptor signaling. Cell 1998; 95:625-36; PMID:9845365; http://dx.doi.org/10.1016/S0092-8674(00)81633-5.
21. Pederson T. As functional nuclear actin comes into view, is it globular, filamentous or both? J Cell Biol 2008; 180:1061-4; PMID:18347069; http://dx.doi. org/10.1083/jcb.200709082.
22. Pederson T, Aebi U. Actin in the nucleus: what form and what for? J Struct Biol 2002; 140:3-9; PMID:12490148; http://dx.doi.org/10.1016/S1047-8477(02)00528-2.
23. Hofmann WA, de Lanerolle P. Nuclear actin: to polymerize or not to polymerize. J Cell Biol 2006; 172:495-6; PMID:16476772; http://dx.doi.org/10.1083/jcb.200601095.
24. Jockusch BM, Schoenenberger CA, Stetefeld J, Aebi U. Tracking down the different forms of nuclear actin. Trends Cell Biol 2006; 16:391-6; PMID:16828286; http://dx.doi.org/10.1016/j.tcb.2006.06.006.
25. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003; 113:329-42; PMID:12732141; http://dx.doi.org/10.1016/S0092-8674(03)00278-2.
26. Posern G, Sotiropoulos A, Treisman R. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol Biol Cell 2002; 13:4167-78; PMID:12475943; http://dx.doi. org/10.1091/mbc.02-05-0068.
27. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 2007; 316:1749-52; PMID:17588931; http://dx.doi. org/10.1126/science.1141084.
28. Posern G, Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol 2006; 16:588-96; PMID:17035020; http://dx.doi.org/10.1016/j.tcb.2006.09.008.
29. Stern S, Debre E, Stritt C, Berger J, Posern G, Knöll B. A nuclear actin function regulates neuronal motility by serum response factor-dependent gene transcription. J Neurosci 2009; 29:4512-8; PMID:19357276; http://dx.doi.org/10.1523/JNEUROSCI.0333-09.2009.
30. Kiseleva E, Drummond SP, Goldberg MW, Rutherford SA, Allen TD, Wilson KL. Actin-and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J Cell Sci 2004; 117:2481-90; PMID:15128868; http://dx.doi. org/10.1242/jcs.01098.
31. McDonald D, Carrero G, Andrin C, de Vries G, Hendzel MJ. Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J Cell Biol 2006; 172:541-52; PMID:16476775; http://dx.doi. org/10.1083/jcb.200507101.
32. Ye J, Zhao J, Hoffmann-Rohrer U, Grummt I. Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev 2008; 22:322-30; PMID:18230700; http://dx.doi. org/10.1101/gad.455908.
33. Gieni RS, Hendzel MJ. Actin dynamics and functions in the interphase nucleus: moving toward an understanding of nuclear polymeric actin. Biochem Cell Biol 2009; 87:283-306; PMID:19234542; http://dx.doi. org/10.1139/O08-133.
34. Gettemans J, Van Impe K, Delanote V, Hubert T, Vandekerckhove J, De Corte V. Nuclear actin-binding proteins as modulators of gene transcription. Traffic 2005; 6:847-57; PMID:16138899; http://dx.doi. org/10.1111/j.1600-0854.2005.00326.x.
35. Wu X, Yoo Y, Okuhama NN, Tucker PW, Liu G, Guan JL. Regulation of RNA-polymerase-II-dependent transcription by N-WASP and its nuclear-binding partners. Nat Cell Biol 2006; 8:756-63; PMID:16767080; http://dx.doi.org/10.1038/ncb1433.
36. Zuchero JB, Coutts AS, Quinlan ME, Thangue NB, Mullins RD. p53-cofactor JMY is a multifunctional actin nucleation factor. Nat Cell Biol 2009; 11:451-9; PMID:19287377; http://dx.doi.org/10.1038/ncb1852.
37. Roadcap DW, Bear JE. Double JMY: making actin fast. Nat Cell Biol 2009; 11:375-6; PMID:19337319; http://dx.doi.org/10.1038/ncb0409-375.
38. Coutts AS, Boulahbel H, Graham A, La Thangue NB. Mdm2 targets the p53 transcription cofactor JMY for degradation. EMBO Rep 2007; 8:84-90; PMID:17170761; http://dx.doi.org/10.1038/sj.embor.7400855.
39. Ono S, Abe H, Obinata T. Stimulus-dependent disorganization of actin filaments induced by overexpression of cofilin in C2 myoblasts. Cell Struct Funct 1996; 21:491-9; PMID:9078407; http://dx.doi.org/10.1247/csf.21.491.
40. Yahara I, Aizawa H, Moriyama K, Iida K, Yonezawa N, Nishida E, et al. A role of cofilin/destrin in reorganization of actin cytoskeleton in response to stresses and cell stimuli. Cell Struct Funct 1996; 21:421-4; PMID:9118250; http://dx.doi.org/10.1247/csf.21.421.
41. Lee YJ, Sheu TJ, Keng PC. Enhancement of radiosensitivity in H1299 cancer cells by actin-associated protein cofilin. Biochem Biophys Res Commun 2005; 335:286-91; PMID:16061204; http://dx.doi. org/10.1016/j.bbrc.2005.07.073.
42. Andrin C, Hendzel MJ. F-actin-dependent insolubility of chromatin-modifying components. J Biol Chem 2004; 279:25017-23; PMID:15082715; http://dx.doi. org/10.1074/jbc.M401805200.
43. Feldmann E, Schmiemann V, Goedecke W, Reichenberger S, Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res 2000; 28:2585-96; PMID:10871410; http://dx.doi. org/10.1093/nar/28.13.2585.
44. Pfeiffer P, Feldmann E, Odersky A, Kuhfittig-Kulle S, Goedecke W. Analysis of DNA double-strand break repair by nonhomologous end joining in cell-free extracts from mammalian cells. Methods Mol Biol 2005; 291:351-71; PMID:15502235.
45. Mirzayans R, Severin D, Murray D. Relationship between DNA double-strand break rejoining and cell survival after exposure to ionizing radiation in human fibroblast strains with differing ATM/p53 status: implications for evaluation of clinical radiosensitivity. Int J Radiat Oncol Biol Phys 2006; 66:1498-505; PMID:17126209; http://dx.doi.org/10.1016/j. ijrobp.2006.08.064.
46. Ismail IH, Nyström S, Nygren J, Hammarsten O. Activation of ataxia telangiectasia mutated by DNA strand break-inducing agents correlates closely with the number of DNA double strand breaks. J Biol Chem 2005; 280:4649-55; PMID:15546858; http://dx.doi. org/10.1074/jbc.M411588200.
47. Verkaik NS, Esveldt-van Lange RE, van Heemst D, Brüggenwirth HT, Hoeijmakers JH, Zdzienicka MZ, et al. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. Eur J Immunol 2002; 32:701-9; PMID:11870614; http://dx.doi. org/10.1002/1521-4141(200203)32:3<701::AIDIMMU701>3.0.CO;2-T.
48. Posern G, Miralles F, Guettler S, Treisman R. Mutant actins that stabilise F-actin use distinct mechanisms to activate the SRF coactivator MAL. EMBO J 2004; 23:3973-83; PMID:15385960; http://dx.doi. org/10.1038/sj.emboj.7600404.
49. Mari PO, Florea BI, Persengiev SP, Verkaik NS, Brüggenwirth HT, Modesti M, et al. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc Natl Acad Sci USA 2006; 103:18597-602; PMID:17124166; http://dx.doi.org/10.1073/pnas.0609061103.
50. Uematsu N, Weterings E, Yano K, Morotomi-Yano K, Jakob B, Taucher-Scholz G, et al. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J Cell Biol 2007; 177:219-29; PMID:17438073; http://dx.doi.org/10.1083/jcb.200608077.
51. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 2006; 31:402-10; PMID:16774833; http://dx.doi.org/10.1016/j. tibs.2006.05.004.
52. 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; PMID:17713585; http://dx.doi.org/10.1139/O07-069.
53. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, et al. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007; 9:675-82; PMID:17486118; http://dx.doi.org/10.1038/ncb1591.