The DNA damage repair protein Ku70 interacts with FOXO4 to coordinate a conserved cellular stress response

FASEB Journal

Volumn 24, Issue 11, 2010, Pages 4271-4280

  Brenkman, Arjan B ^a,b   Van Den Broek, Niels J F ^a,b   De Keizer, Peter L J ^a,d   Van Gent, Dik C ^c   Burgering, Boudewijn M T ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b Netherlands Metabolomics Center   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

Author keywords

Aging; Oxidative stress; p27kip1

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; HYDROGEN PEROXIDE; KU ANTIGEN; LUCIFERASE; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR FOXO4; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ARTICLE; CELL AGING; CELL CYCLE ARREST; CELL NUCLEUS; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CHEMICAL ANALYSIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DISSOCIATION CONSTANT; DNA DAMAGE; DNA REPAIR; EMBRYONIC STEM CELL; ENZYME ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LIFESPAN; MEDIATOR; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STOICHIOMETRY; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; WILD TYPE;

ANIMALS; ANTIGENS, NUCLEAR; CELL CYCLE; CELL LINE; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MULTIPROTEIN COMPLEXES; OXIDATIVE STRESS; STRESS, PHYSIOLOGICAL; TANDEM MASS SPECTROMETRY; TRANSCRIPTION FACTORS;

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 78649815977     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-158717     Document Type: Article

References (48)

1. Greer, E. L., and Brunet, A. (2005) FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24, 7410-7425
2. Paik, J. H., Kollipara, R., Chu, G., Ji, H., Xiao, Y., Ding, Z., Miao, L., Tothova, Z., Horner, J. W., Carrasco, D. R., Jiang, S., Gilliland, D. G., Chin, L., Wong, W. H., Castrillon, D. H., and DePinho, R. A. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128, 309-323
3. Datta, S. R., Brunet, A., and Greenberg, M. E. (1999) Cellular survival: a play in three Akts. Genes Dev. 13, 2905-2927
4. Cantley, L. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
5. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J., and Greenberg, M. E. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868
6. Kops, G. J., de Ruiter, N. D., Vries-Smits, A. M., Powell, D. R., Bos, J. L., and Burgering, B. M. (1999) Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398, 630-634
7. Brownawell, A. M., Kops, G. J., Macara, I. G., and Burgering, B. M. (2001) Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol. Cell. Biol. 21, 3534-3546
8. Kops, G. J., Dansen, T. B., Polderman, P. E., Saarloos, I., Wirtz, K. W., Coffer, P. J., Huang, T. T., Bos, J. L., Medema, R. H., and Burgering, B. M. (2002) Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321
9. Brunet, A., Sweeney, L. B., Sturgill, J. F., Chua, K. F., Greer, P. L., Lin, Y., Tran, H., Ross, S. E., Mostoslavsky, R., Cohen, H. Y., Hu, L. S., Cheng, H. L., Jedrychowski, M. P., Gygi, S. P., Sinclair, D. A., Alt, F. W., and Greenberg, M. E. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303, 2011-2015
10. Essers, M. A., Weijzen, S., Vries-Smits, A. M., Saarloos, I., de Ruiter, N. D., Bos, J. L., and Burgering, B. M. (2004) FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J. 23, 4802-4812
11. Wang, M. C., Bohmann, D., and Jasper, H. (2005) JNK extends life span and limits growth by antagonizing cellular and organism- wide responses to insulin signaling. Cell 121, 115-125 (Pubitemid 40501172)
12. Oh, S. W., Mukhopadhyay, A., Svrzikapa, N., Jiang, F., Davis, R. J., and Tissenbaum, H. A. (2005) JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc. Natl. Acad. Sci. U. S. A. 102, 4494-4499
13. Wolff, S., and Dillin, A. (2006) The trifecta of aging in Caenorhabditis elegans. Exp. Gerontol. 41, 894-903
14. Kirkwood, T. B., and Austad, S. N. (2000) Why do we age? Nature 408, 233-238
15. Brunet, A. (2007) Aging and cancer: killing two birds with one worm. Nat. Genet. 39, 1306-1307
16. van der Horst. A., and Burgering, B. M. (2007) Stressing the role of FoxO proteins in lifespan and disease. Nat. Rev. Mol. Cell. Biol. 8, 440-450
17. Helleday, T., Lo, J., van Gent, D. C., and Engelward, B. P. (2007) DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst.) 6, 923-935 (Pubitemid 46880473)
18. Wyman, C., and Kanaar, R. (2006) DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40, 363-383 (Pubitemid 44956790)
19. Downs, J. A., and Jackson, S. P. (2004) A means to a DNA end: the many roles of Ku. Nat. Rev. Mol. Cell. Biol. 5, 367-378
20. Lieber, M. R., Ma, Y., Pannicke, U., and Schwarz, K. (2004) The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. DNA Repair (Amst.) 3, 817-826 (Pubitemid 39004089)
21. Van Gent, D. C., and van der Burg, M. (2007) Non-homologous end-joining, a sticky affair. Oncogene 26, 7731-7740
22. McColl, G., Vantipalli, M. C., and Lithgow, G. J. (2005) The C. elegans ortholog of mammalian Ku70, interacts with insulin-like signaling to modulate stress resistance and life span. FASEB J. 19, 1716-1718 (Pubitemid 41429540)
23. Brenkman, A. B., de Keizer, P. L. J., van den Broek, N. J. F., van der Groep, P., van Diest, P. J., van der Hoerst, A., Smits, A. M. M., and Burgering, B. M. T. (2008) The peptidyl-isomerase Pin1 regulates p27kip1 expression through inhibition of Forkhead box O tumor suppressors. Cancer Res. 68, 7597-7605
24. Mari, P. O., Florea, B. I., Persengiev, S. P., Verkaik, N. S., Bruggenwirth, H. T., Modesti, M., Giglia-Mari, G., Bezstarosti, K., Demmers, J. A., Luider, T. M., Houtsmuller, A. B., and van Gent, D. C. (2006) Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. U. S. A. 103, 18597-18602
25. Brenkman, A. B., de Keizer, P. L., van den Broek, N. J., Jochemsen, A. G., and Burgering, B. M. (2008) Mdm2 induces mono-ubiquitination of FOXO4. PLoS ONE 3, e2819
26. Medema, R. H., Kops, G. J., Bos, J. L., and Burgering, B. M. (2000) AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404, 782-787
27. Tuteja, R., and Tuteja, N. (2000) Ku autoantigen: a multifunctional DNA-binding protein. Crit. Rev. Biochem. Mol. Biol. 35, 1-33
28. Blier, P. R., Griffith, A. J., Craft, J., and Hardin, J. A. (1993) Binding of Ku protein to DNA. Measurement of affinity for ends and demonstration of binding to nicks. J. Biol. Chem. 268, 7594-7601
29. Lai, J. S., and Herr, W. (1992) Ethidium bromide provides a simple tool for identifying genuine DNA-independent protein associations. Proc. Natl. Acad. Sci. U. S. A. 89, 6958-6962
30. Gu, Y., Seidl, K. J., Rathbun, G. A., Zhu, C., Manis, J. P., van der Stoep, N., Davidson, L., Cheng, H. L., Sekiguchi, J. M., Frank, K., Stanhope-Baker, P., Schlissel, M. S., Roth, D. B., and Alt, F. W. (1997) Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7, 653-665
31. Zhu, C., Bogue, M. A., Lim, D. S., Hasty, P., and Roth, D. B. (1996) Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86, 379-389
32. Nussenzweig, A., Chen, C., da Costa Soares, V., Sanchez, M., Sokol, K., Nussenzweig, M. C., and Li, G. C. (1996) Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382, 551-555
33. Holcomb, V. B., Vogel, H., and Hasty, P. (2007) Deletion of Ku80 causes early aging independent of chronic inflammation and Rag-1-induced DSBs. Mech. Ageing Dev. 128, 601-608 (Pubitemid 350299043)
34. Li, H., Vogel, H., Holcomb, V. B., Gu, Y., and Hasty, P. (2007) Deletion of Ku70, Ku80, or both causes early aging without substantially increased cancer. Mol. Cell. Biol. 27, 8205-8214 (Pubitemid 350234234)
35. Vogel, H., Lim, D. S., Karsenty, G., Finegold, M., and Hasty, P. (1999) Deletion of Ku86 causes early onset of senescence in mice. Proc. Natl. Acad. Sci. U. S. A. 96, 10770-10775 (Pubitemid 29442219)
36. Li, G. C., Ouyang, H., Li, X., Nagasawa, H., Little, J. B., Chen, D. J., Ling, C. C., Fuks, Z., and Cordon-Cardo, C. (1998) Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol. Cell. 2, 1-8
37. Li, H., Choi, Y. J., Hanes, M. A., Marple, T., Vogel, H., and Hasty, P. (2009) Deleting Ku70 is milder than deleting Ku80 in p53-mutant mice and cells. Oncogene 28, 1875-1878
38. Hasty, P., Campisi, J., Hoeijmakers, J., van Steeg, H., and Vijg, J. (2003) Aging and genome maintenance: lessons from the mouse? Science 299, 1355-1359 (Pubitemid 36254641)
39. Schumacher, B., Garinis, G. A., and Hoeijmakers, J. H. (2008) Age to survive: DNA damage and aging. Trends Genet. 24, 77-85
40. Cohen, H. Y., Lavu, S., Bitterman, K. J., Hekking, B., Imahiyerobo, T. A., Miller, C., Frye, R., Ploegh, H., Kessler, B. M., and Sinclair, D. A. (2004) Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell. 13, 627-638
41. Van der Horst, A., Tertoolen, L. G., Vries-Smits, L. M., Frye, R. A., Medema, R. H., and Burgering, B. M. (2004) FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J. Biol. Chem. 279, 28873-28879
42. Van der Horst, A., de Vries-Smits, A. M., Brenkman, A. B., van Triest, M. H., van den Broek, N., Colland, F., Maurice, M. M., and Burgering, B. M. (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol. 8, 1064-1073
43. Yamagata, K., Daitoku, H., Takahashi, Y., Namiki, K., Hisatake, K., Kako, K., Mukai, H., Kasuya, Y., and Fukamizu, A. (2008) Arginine methylation of FOXO transcription factors inhibits their phosphorylation by Akt. Mol. Cell. 32, 221-231
44. Motta, M. C., Divecha, N., Lemieux, M., Kamel, C., Chen, D., Gu, W., Bultsma, Y., McBurney, M., and Guarente, L. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116, 551-563
45. Frescas, D., Valenti, L., and Accili, D. (2005) Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J. Biol. Chem. 280, 20589-20595 (Pubitemid 40776761)
46. Lei, H., and Quelle, F. W. (2009) FOXO transcription factors enforce cell cycle checkpoints and promote survival of hematopoietic cells after DNA damage. Mol. Cancer Res. 7, 1294-1303
47. Huang, H., Regan, K. M., Lou, Z., Chen, J., and Tindall, D. J. (2006) CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science 314, 294-297 (Pubitemid 44571973)
48. Fiaschi, T., Cozzi, G., Raugei, G., Formigli, L., Ramponi, G., and Chiarugi, P. (2006) Redox regulation of beta-actin during integrin-mediated cell adhesion. J. Biol. Chem. 281, 22983-22991 (Pubitemid 44242328)