DNA damage induces the accumulation of tiam1 by blocking β-TrCP-dependent degradation

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15482-15494

  Zhu, Guixin ^a,b   Fan, Zhongyun ^a   Ding, Miao ^c   Mu, Libing ^a   Liang, Juan ^a   Ding, Yajie ^a   Fu, Yu ^a   Huang, Binlu ^a   Wu, Wei ^a  

^a TSINGHUA UNIVERSITY   (China)

^b Tsinghua University   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CHEMICAL ACTIVATION; DRUG THERAPY;

CHEMOTHERAPEUTIC DRUGS; DNA DAMAGES; UP-REGULATION;

DNA;

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; CAMPTOTHECIN; CASEIN KINASE I; CULLIN; DOXORUBICIN; F BOX PROTEIN; PROTEASOME; RAC1 PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN; STRESS ACTIVATED PROTEIN KINASE; T CELL LYMPHOMA INVASION AND METASTASIS 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA DAMAGE; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; T CELL LYMPHOMA; TUMOR CELL; UBIQUITINATION;

APOPTOSIS; C-JUN N-TERMINAL KINASE (JNK); CHEMOTHERAPY; DNA DAMAGE; E3 UBIQUITIN LIGASE; RAC1; TIAM1;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; CASEIN KINASE I; DNA DAMAGE; DOXORUBICIN; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HELA CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, NUDE; RAC1 GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION; UTERINE CERVICAL NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901712719     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.553388     Document Type: Article

References (59)

1. Polo, S. E., and Jackson, S. P. (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433
2. Sperka, T., Wang, J., and Rudolph, K. L. (2012) DNA damage checkpoints in stem cells, ageing and cancer. Nat. Rev. Mol. Cell Biol. 13, 579-590
3. Harper, J. W., and Elledge, S. J. (2007) The DNA damage response: ten years after. Mol. Cell 28, 739-745
4. Deng, Y., Ren, X., Yang, L., Lin, Y., and Wu, X. (2003) A JNK-dependent pathway is required for TNF α-induced apoptosis. Cell 115, 61-70
5. Dhanasekaran, D. N., and Reddy, E. P. (2008) JNK signaling in apoptosis. Oncogene 27, 6245-6251
6. Liu, J., and Lin, A. (2005) Role of JNK activation in apoptosis: a doubleedged sword. Cell Res. 15, 36-42
7. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., and Greenberg, M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331
8. Xu, Z., Maroney, A. C., Dobrzanski, P., Kukekov, N. V., and Greene, L. A. (2001) The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol. Cell Biol. 21, 4713-4724
9. Xu, Z., Kukekov, N. V., and Greene, L. A. (2003)POSHacts as a scaffold for a multiprotein complex that mediates JNK activation in apoptosis. EMBO J. 22, 252-261
10. Shirokawa, J. M., Elisei, R., Knauf, J. A., Hara, T., Wang, J., Saavedra, H. I., and Fagin, J. A. (2000) Conditional apoptosis induced by oncogenic Ras in thyroid cells. Mol. Endocrinol. 14, 1725-1738
11. Suárez, Y., González-Santiago, L., Zarich, N., Dávalos, A., Aranda, J. F., Alonso, M. A., Lasunción, M. A., Rojas, J. M., and Muñoz, A. (2006) Plitidepsin cellular binding and Rac1/JNK pathway activation depend on membrane cholesterol content. Mol. Pharmacol. 70, 1654-1663
12. Nethe, M., and Hordijk, P. L. (2010) The role of ubiquitylation and degradation in RhoGTPase signalling. J. Cell Sci. 123, 4011-4018
13. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
14. Oberoi-Khanuja, T. K., and Rajalingam, K. (2012) IAPs as E3 ligases of Rac1: shaping the move. Small GTPases 3, 131-136
15. Torrino, S., Visvikis, O., Doye, A., Boyer, L., Stefani, C., Munro, P., Bertoglio, J., Gacon, G., Mettouchi, A., and Lemichez, E. (2011) The E3 ubiquitin- ligase HACE1 catalyzes the ubiquitylation of active Rac1. Dev. Cell 21, 959-965
16. Habets, G. G., Scholtes, E. H., Zuydgeest, D., van der Kammen, R. A., Stam, J. C., Berns, A., and Collard, J. G. (1994) Identification of an invasioninducing gene, Tiam-1, that encodes a protein with homology to GDPGTP exchangers for Rho-like proteins. Cell 77, 537-549
17. Malliri, A., van der Kammen, R. A., Clark, K., van der Valk, M., Michiels, F., and Collard, J. G. (2002) Mice deficient in the Rac activator Tiam1 are resistant to Ras-induced skin tumours. Nature 417, 867-871
18. Minard, M. E., Ellis, L. M., and Gallick, G. E. (2006) Tiam1 regulates cell adhesion, migration and apoptosis in colon tumor cells. Clin. Exp. Metastasis 23, 301-313
19. Minard, M. E., Kim, L. S., Price, J. E., and Gallick, G. E. (2004) The role of the guanine nucleotide exchange factor Tiam1 in cellular migration, invasion, adhesion and tumor progression. Breast Cancer Res. Treat. 84, 21-32
20. Woodcock, S. A., Rooney, C., Liontos, M., Connolly, Y., Zoumpourlis, V., Whetton, A. D., Gorgoulis, V. G., and Malliri, A. (2009) SRC-induced disassembly of adherens junctions requires localized phosphorylation and degradation of the Rac activator Tiam1. Mol. Cell 33, 639-653
21. Schmidt, A., and Hall, A. (2002) Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16, 1587-1609
22. Mertens, A. E., Roovers, R. C., and Collard, J. G. (2003) Regulation of Tiam1-Rac signalling. FEBS Lett. 546, 11-16
23. Rygiel, T. P., Mertens, A. E., Strumane, K., van der Kammen, R., and Collard, J. G. (2008) The Rac activator Tiam1 prevents keratinocyte apoptosis by controlling ROS-mediated ERK phosphorylation. J. Cell Sci. 121, 1183-1192
24. Cao-Hong, Shibayama-Imazu, T., Masuda, Y., Shinki, T., Nakajo, S., and Nakaya, K. (2007) Involvement of Tiam1 in apoptosis induced by bufalin in HeLa cells. Anticancer Res. 27, 245-249
25. Nitiss, J. L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer 9, 338-350
26. Hertzberg, R. P., Caranfa, M. J., and Hecht, S. M. (1989) On the mechanism of topoisomerase I inhibition by camptothecin: evidence for binding to an enzyme-DNA complex. Biochemistry 28, 4629-4638
27. Fuchs, S. Y., Spiegelman, V. S., and Kumar, K. G. (2004) The many faces of β-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 23, 2028-2036
28. Cardozo, T., and Pagano, M. (2004) The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751
29. Frescas, D., and Pagano, M. (2008) Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 8, 438-449
30. Lau, A. W., Fukushima, H., and Wei, W. (2012) The Fbw7 and β-TRCP E3 ubiquitin ligases and their roles in tumorigenesis. Front Biosci. 17, 2197-2212
31. Winston, J. T., Strack, P., Beer-Romero, P., Chu, C. Y., Elledge, S. J., and Harper, J. W. (1999) The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev. 13, 270-283
32. Inuzuka, H., Tseng, A., Gao, D., Zhai, B., Zhang, Q., Shaik, S., Wan, L., Ang, X. L., Mock, C., Yin, H., Stommel, J. M., Gygi, S., Lahav, G., Asara, J., Xiao, Z. X., Kaelin, W. G., Jr., Harper, J. W., and Wei, W. (2010) Phosphorylation by casein kinase I promotes the turnover of theMdm2oncoprotein via the SCF (β-TRCP) ubiquitin ligase. Cancer Cell 18, 147-159
33. Margottin, F., Bour, S. P., Durand, H., Selig, L., Benichou, S., Richard, V., Thomas, D., Strebel, K., and Benarous, R. (1998) A novel human WD protein, h-β TrCp, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1, 565-574
34. Liang, J., Fu, Y., Cruciat, C. M., Jia, S., Wang, Y., Tong, Z., Tao, Q., Ingelfinger, D., Boutros, M., Meng, A., Niehrs, C., and Wu, W. (2011) Transmembrane protein 198 promotes LRP6 phosphorylation and Wnt signaling activation. Mol. Cell Biol. 31, 2577-2590
35. Zhu, G., Wang, Y., Huang, B., Liang, J., Ding, Y., Xu, A., and Wu, W. (2012) A Rac1/PAK1 cascade controls β-catenin activation in colon cancer cells. Oncogene 31, 1001-1012
36. Seki, A., Coppinger, J. A., Du, H., Jang, C. Y., Yates, J. R., 3rd, and Fang, G. (2008) Plk1- and β-TrCP-dependent degradation of Bora controls mitotic progression. J. Cell Biol. 181, 65-78
37. Mailand, N., Bekker-Jensen, S., Bartek, J., and Lukas, J. (2006) Destruction of Claspin by SCFβTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol. Cell 23, 307-318
38. Malliri, A., van Es, S., Huveneers, S., and Collard, J. G. (2004) The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions. J. Biol. Chem. 279, 30092-30098
39. Habas, R., and He, X. (2006) Activation of Rho and Rac by Wnt/frizzled signaling. Methods Enzymol. 406, 500-511
40. Petroski, M. D., and Deshaies, R. J. (2005) Function and regulation of Cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20
41. Wu, G., Xu, G., Schulman, B. A., Jeffrey, P. D., Harper, J. W., and Pavletich, N. P. (2003) Structure of a β-TrCP1-Skp1-β-catenin complex: destruction motif binding and lysine specificity of the SCF ( β-TrCP1) ubiquitin ligase. Mol. Cell 11, 1445-1456
42. Marin, O., Bustos, V. H., Cesaro, L., Meggio, F., Pagano, M. A., Antonelli, M., Allende, C. C., Pinna, L. A., and Allende, J. E. (2003) A noncanonical sequence phosphorylated by casein kinase 1 in β-catenin may play a role in casein kinase 1 targeting of important signaling proteins. Proc. Natl. Acad. Sci. U.S.A. 100, 10193-10200
43. Rena, G., Bain, J., Elliott, M., and Cohen, P. (2004) D4476, a cell-permeant inhibitor of CK1, suppresses the site-specific phosphorylation and nuclear exclusion of FOXO1a. EMBO Rep. 5, 60-65
44. Hordijk, P. L., ten Klooster, J. P., van der Kammen, R. A., Michiels, F., Oomen, L. C., and Collard, J. G. (1997) Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278, 1464-1466
45. Kawazoe, N., Watabe, M., Masuda, Y., Nakajo, S., and Nakaya, K. (1999) Tiam1 is involved in the regulation of bufalin-induced apoptosis in human leukemia cells. Oncogene 18, 2413-2421
46. Michiels, F., Stam, J. C., Hordijk, P. L., van der Kammen, R. A., Ruuls-Van Stalle, L., Feltkamp, C. A., and Collard, J. G. (1997) Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation. J. Cell Biol. 137, 387-398
47. Tournier, C., Hess, P., Yang, D. D., Xu, J., Turner, T. K., Nimnual, A., Bar-Sagi, D., Jones, S. N., Flavell, R. A., and Davis, R. J. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870-874
48. van Leeuwen, F. N., van der Kammen, R. A., Habets, G. G., and Collard, J. G. (1995) Oncogenic activity of Tiam1 and Rac1 in NIH3T3 cells. Oncogene 11, 2215-2221
49. Kadara, H., Tahara, E., Kim, H. J., Lotan, D., Myers, J., and Lotan, R. (2008) Involvement of Rac in fenretinide-induced apoptosis. Cancer Res. 68, 4416-4423
50. Kang, M. A., So, E. Y., Simons, A. L., Spitz, D. R., and Ouchi, T. (2012)DNA damage induces reactive oxygen species generation through the H2AXNox1/ Rac1 pathway. Cell Death Dis. 3, e249
51. Mayr, M., Hu, Y., Hainaut, H., and Xu, Q. (2002) Mechanical stress-induced DNA damage and rac-p38MAPK signal pathways mediate p53-dependent apoptosis in vascular smooth muscle cells. FASEB J. 16, 1423-1425
52. Alsheich-Bartok, O., Haupt, S., Alkalay-Snir, I., Saito, S., Appella, E., and Haupt, Y. (2008) PML enhances the regulation of p53 by CK1 in response to DNA damage. Oncogene 27, 3653-3661
53. Santos, J. A., Logarinho, E., Tapia, C., Allende, C. C., Allende, J. E., and Sunkel, C. E. (1996) The casein kinase 1α gene of Drosophila melanogaster is developmentally regulated and the kinase activity of the protein induced by DNA damage. J. Cell Sci. 109, 1847-1856
54. Wang, Z., Inuzuka, H., Zhong, J., Fukushima, H., Wan, L., Liu, P., and Wei, W. (2012) DNA damage-induced activation of ATM promotes β-TRCP-mediated Mdm2 ubiquitination and destruction. Oncotarget 3, 1026-1035
55. Kanemori, Y., Uto, K., and Sagata, N. (2005) β-TrCP recognizes a previously undescribed nonphosphorylated destruction motif in Cdc25A and Cdc25B phosphatases. Proc. Natl. Acad. Sci. U.S.A. 102, 6279-6284
56. Shirogane, T., Jin, J., Ang, X. L., and Harper, J. W. (2005) SCFβ-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem. 280, 26863-26872
57. Cegielska, A., Gietzen, K. F., Rivers, A., and Virshup, D. M. (1998) Autoinhibition of casein kinase I∈ (CKI∈) is relieved by protein phosphatases and limited proteolysis. J. Biol. Chem. 273, 1357-1364
58. Graves, P. R., and Roach, P. J. (1995) Role of COOH-terminal phosphorylation in the regulation of casein kinase Iδ. J. Biol. Chem. 270, 21689-21694
59. Zhao, B., Li, L., Tumaneng, K., Wang, C. Y., and Guan, K. L. (2010) A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF (β-TRCP). Genes Dev. 24, 72-85