Regulation of Chk2 ubiquitination and signaling through autophosphorylation of serine 379

Molecular and Cellular Biology

Volumn 28, Issue 19, 2008, Pages 5874-5885

  Lovly, Christine M ^a,b   Yan, Ling ^a   Ryan, Christine E ^a   Takada, Saeko ^a,c   Piwnica Worms, Helen ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; COMPLEMENTARY DNA; ETOPOSIDE; PHOSPHOPEPTIDE; SERINE;

APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; CELL CYCLE ARREST; CELL STRAIN HEK293; DNA CONTENT; DNA STRAND BREAKAGE; EMBRYO; FAMILIAL CANCER; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; UBIQUITINATION; WESTERN BLOTTING;

CELL LINE; CULLIN PROTEINS; DNA DAMAGE; DNA REPAIR; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; SERINE; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 52649098505     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00821-08     Document Type: Article

References (57)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with Image J. Biophotonics Int. 11:36-42.
2. Ahn, J.-Y., X. Li, H. L. Davis, and C. E. Canman. 2002. Phosphorylation of threonine 68 promotes oligomerization and autophosphorylation of the Chk2 protein kinase via the Forkhead-associated (FHA) domain. J. Biol. Chem. 277:19389-19395.
3. Ahn, J.-Y., J. K. Schwarz, H. Piwnica-Worms, and C. E. Canman. 2000. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res. 60:5934-5936.
4. Bartek, J., and J. Lukas. 2001. Pathways governing G1/S transition and their response to DNA damage. FEBS Lett. 490:117-122.
5. Bartkova, J., J. Falck, E. Rajpert-De Meyts, N. E. Skakkebaek, J. Lukas, and J. Bartek. 2001. Chk2 tumour suppressor protein in human spermatogenesis and testicular germ-cell tumours. Oncogene 20:5897-5902.
6. Bell, D. W., J. M. Variey, T. E. Szydlo, D. H. Kang, C. R. Wahrer-Doke, K. E. Shannon, M. Lubratovich, S. J. Versellls, K. J. Isselbacher, J. F. Fraumeni, J. M. Birch, F. P. Li, J. E. Garber, and D. A. Haber. 1999. Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 286:2528-2531.
7. Brown, A., C.-H. Lee, J. K. Schwarz, N. Mitiku, D. Griffith, H. Piwnica-Worms, and J. H. Chung. 1999. A human Cds1-related kinase that functions downsteam of ATM in the cellular response to DNA damage. Proc. Natl. Acad. Sci. USA 96:3745-3750.
8. Chaturvedi, P., W. K. Eng, Y. Zhu, M. R. Mattern, R. Mishra, M. R. Hurle, X. Zhang, R. S. Annan, Q. Lu, L. F. Faucette, G. F. Scott, X. Li, S. A. Carr, R. K. Johnson, J. D. Winkler, and B.-B. S. Zhou. 1999. Mammalian Chk2 is a downstream effector of the ATM-dependent DNA damage checkpoint pathway. Oncogene 18:4047-4054.
9. Chehab, N. H., A. Malikzay, M. Appel, and T. D. Halazonetis. 2000. Chk2/hCds1 functions as a DNA damage checkpoint in G1 by stabilizing p53. Genes Dev. 14:278-288.
10. Chehab, N. H., A. Malikzay, E. S. Stavridi, and T. D. Halazonetis. 1999. Phosphorylation of Scr-20 mediates stabilization of human p53 in response to DNA damage. Proc. Natl. Acad. Sci. USA 96:13777-13782.
11. Chen, L., D. M. Gilkes, Y. Pan, W. S. Lane, and J. Chen. 2005. ATM and Chk2-dependent phosphorylation of MDMX contribute to p53 activation after DNA damage. EMBO J. 24:3411-3422.
12. Cullinan, S. B., J. D. Gordan, J. Jin, J. W. Harper, and J. A. Diehl. 2004. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol. Cell. Biol. 24:8477-8486.
13. Feldman, R. M. R., C. C. Correll, K. B. Kaplan, and R. J. Deshaies. 1997. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91:221-230.
14. Graves, P. R., L. Yu, J. K. Schwarz, J. Gales, E. A. Sausville, P. M. O'Connor, and H. Piwnica-Worms. 2000. The Chk1 protein kinase and the Cdc25C regulatory pathway are targets of the anticancer agent UCN-01. J. Biol. Chem. 275:5600-5605.
15. Hartwell, L. H., and M. B. Kastan. 1994. Cell cycle control and cancer. Science 266:1821-1828.
16. Hirao, A., A. Cheung, G. Duncan, P.-M. Girard, A. J. Elia, A. Wakeham, H. Okada, T. Sarkissian, J. A. Wong, T. Sakai, E.-d. Stanchina, R. G. Bristow, T. Suda, S. W. Lowe, P. A. Jeggo, S. J. Elledge, and T. W. Mak. 2002. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol. Cell. Biol. 22:6521-6532.
17. Hirao, A., Y. Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, H. Yoshida, D. Liu, S. J. Elledge, and T. W. Mak. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824-1827.
18. Huen, M. S., R. Grant, I. Manke, K. Minn, X. Yu, M. B. Yaffe, and J. Chen. 2007. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901-914.
19. Jack, M. T., R. A. Woo, A. Hirao, A. Cheung, T. W. Mak, and P. W. Lee. 2002. Chk2 is dispensable for p53-mediated G1 arrest but is required for a latent p53-mediated apoptotic response. Proc. Natl. Acad. Sci. USA 99:9825-9829.
20. Jackson, M. W., M. K. Agarwal, M. L. Agarwal, A. Agarwal, P. Stanhope-Baker, B. R. Williams, and G. R. Stark. 2004. Limited role of N-terminal phosphoserine residues in the activation of transcription by p53. Oncogene 23:4477-4487.
21. Johnson, E. S. 2002. Ubiquitin branches out. Nat. Cell Biol. 4:E295-E298.
22. Kass, E. M., J. Ahn, T. Tanaka, W. A. Freed-Pastor, S. Keezer, and C. Prives. 2007. Stability of checkpoint kinase 2 is regulated via phosphorylation at serine 456. J. Biol. Chem. 282:30311-30321.
23. King, J. B., J. Gross, H. Rohrs, C. M. Lovly, H. Piwnica-Worms, and R. R. Townsend. 2006. Mass-driven analysis for the characterization of protein phosphorylation - a study of the human Chk2 protein kinase. Anal. Chem. 78:2171-2181.
24. Kolas, N. K., J. R. Chapman, S. Nakada, J. Ylanko, R. Chahwan, F. D. Sweeney, S. Panier, M. Mendez, J. Wildenhain, T. M. Thomson, L. Pelletier, S. P. Jackson, and D. Durocher. 2007. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318:1637-1640.
25. Lee, C. H., and J. H. Chung. 2001. The hCds1 (Chk2)-FHA domain is essential for a chain of phosphorylation events on hCds1 that is induced by ionizing radiation. J. Biol. Chem. 276:30537-30541.
26. Lee, J. S., K. M. Collins, A. L. Brown, C. H. Lee, and J. H. Chung. 2000. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 404:201-204.
27. Lou, Z., K. Minter-Dykhouse, X. Wu, and J. Chen. 2003. MDC1 is coupled to activated Chk2 in mammalian DNA damage response pathways. Nature 421:957-960.
28. Lukas, C., J. Bartkova, L. Latella, J. Falck, N. Mailand, T. Schroeder, M. Sehested, J. Lukas, and J. Bartek. 2001. DNA damage-activated kinase Chk2 is independent of proliferation or differentiation yet correlates with tissue biology. Cancer Res. 61:4990-4993.
29. Lukas, C., J. Falck, J. Bartkova, J. Bartek, and J. Lukas. 2003. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5:255-260.
30. Mailand, N., S. Bekker-Jensen, H. Faustrup, F. Melander, J. Bartek, C. Lukas, and J. Lukas. 2007. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131:887-900.
31. Matsuoka, S., Huang, M., and S. J. Elledge. 1998. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282:1893-1897.
32. Matsuoka, S., G. Rotman, A. Ogawa, Y. Shiloh, K. Tamai, and S. J. Elledge. 2000. Ataxia telangiectasia-mutated phosphorytates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. USA 97:10389-10394.
33. Melchionna, R., X. B. Chen, A. Blasina, and C. H. McGowan. 2000. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2:762-705.
34. Ogg, S., B. Gabrielli, and H. Piwnica-Worms. 1994. Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. J. Biol. Chem. 269:30461-30469.
35. Ohta, T., J. J. Michel, A. J. Schottelius, and Y. Xiong. 1999. ROC1, a homolog of APC11, represents a family of cullin partners with an associated ubiquitin ligase activity. Mol. Cell 3:535-541.
36. Ohta, T., and Y. Xiong. 2001. Phosphorylation- and Skp1-independent in vitro ubiquitination of E2F1 by multiple ROC-cullin ligases. Cancer Res. 61:1347-1353.
37. Pereg, Y., S. Lam, A. Teunisse, S. Biton, E. Meulmeester, L. Mittelman, G. Buscemi, K. Okamoto, Y. Taya, Y. Shiloh, and A. G. Jochemsen. 2006. Differential roles of ATM- and Chk2-mediated phosphorylations of Hdmx in response to DNA damage. Mol. Cell. Biol. 26:6819-6831.
38. Petroski, M. D., and R. J. Deshaies. 2005. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6:9-20.
39. Pickart, C. M. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-533.
40. Pickart, C. M. 2001. Ubiquitin enters the new millennium. Mol. Cell 8:499-504.
41. Schwarz, J. K., C. M. Lovly, and H. Piwnica-Worms. 2003. Regulation of the Chk2 protein kinase by oligomerization-mediated cis- and trans-phosphorylation. Mol. Cancer Res. 1:598-609.
42. Shieh, S. Y., J. Ahn, K. Tamai, Y. Taya, and C. Prives. 2000. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:289-300.
43. Shirogane, T., J. Jin, X. L. Ang, and J. W. Harper. 2005. SCFbeta-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem. 280:26803-26872.
44. Skowyra, D., K. L. Craig, M. Tyers, S. J. Elledge, and J. W. Harper. 1997. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209-219.
45. Stevens, C., L. Smith, and N. B. La Thangue. 2003. Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol. 5:401-409.
46. Takai, H., K. Naka, Y. Ohada, M. Watanabe, N. Harada, S. Saito, C. W. Anderson, E. Appella, M. Nakanishi, H. Suzuki, K. Nagashima, H. Sawa, K. Ikeda, and N. Motoyama. 2002. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21:5195-5205.
47. Urist, M., T. Tanaka, M. V. Poyurovsky, and C. Prives. 2004. p73 induction after DNA damage is regulated by checkpoint kinases Chk1 and Chk2. Genes Dev. 18:3041-3054.
48. van der Geer, P., and T. Hunter. 1994. Phosphopeptide mapping and phosphoamino acid analysis by electrophoresis and chromatography on thin-layer cellulose plates. Electrophoresis 15:544-554.
49. Wang, B., and S. J. Elledge. 2007. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. USA 104:20759-20763.
50. Wang, B., S. Matsuoka, B. A. Ballif, D. Zhang, A. Smogorzewska, S. P. Gygi, and S. J. Elledge. 2007. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316:1194-1198.
51. Wu, X., and J. Chen. 2003. Autophosphorylation of checkpoint kinase 2 at serine 516 is required for radiation-induced apoptosis. J. Biol. Chem. 278:36163-36168.
52. Wu, Z., J. Earle, S. Saito, C. W. Anderson, E. Appella, and Y. Xu. 2002. Mutation of mouse p53 S23 and the response to DNA damage. Mol. Cell. Biol. 22:2441-2449.
53. Xu, X., L. M. Tsvetkov, and D. F. Stern. 2002. Chk2 activation and phosphorylation-dependent oligomerization. Mol. Cell. Biol. 22:4419-4432.
54. Yang, S., C. Kuo, J. E. Bisi, and M. K. Kim. 2002. PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/Chk2. Nat. Cell Biol. 4:865-870.
55. Zhang, D., K. Zaugg, T. W. Mak, and S. J. Elledge. 2006. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126:529-542.
56. Zheng, N., B. A. Schulman, L. Song, J. J. Miller, P. D. Jeffrey, P. Wang, C. Chu, D. M. Koepp, S. J. Elledge, M. Pagano, R. C. Conaway, J. W. Conaway, J. W. Harper, and N. P. Pavletich. 2002. Structure of the Cull-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. Nature 416:703-709.
57. Zhou, B. B., P. Chaturvedi, K. Spring, S. P. Scott, R. A. Johanson, R. Mishra, M. R. Mattern, J. D. Winkler, and K. K. Khanna. 2000. Caffeine abolishes the mammalian G(2)/M DNA damage checkpoint by inhibiting ataxia-telangiectasia-mutated kinase activity. J. Biol. Chem. 275:10342-10348.