Autophosphorylation of ataxia-telangiectasia mutated is regulated by protein phosphatase 2A

EMBO Journal

Volumn 23, Issue 22, 2004, Pages 4451-4461

  Goodarzi, Aaron A ^a   Jonnalagadda, Jyoti C ^b   Douglas, Pauline ^a   Young, David ^b   Ye, Ruiqiong ^a   Moorhead, Greg B G ^a   Lees Miller, Susan P ^a   Khanna, Kum Kum ^b  

^a UNIVERSITY OF CALGARY   (Canada)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

ATM; Autophosphorylation; Okadaic acid; Protein phosphatase

Indexed keywords

ATM PROTEIN; DNA; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 2A;

ARTICLE; AUTOPHOSPHORYLATION; CELL DAMAGE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DISSOCIATION; DNA STRAND BREAKAGE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME MECHANISM; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; IONIZING RADIATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ATAXIA TELANGIECTASIA; CATALYTIC DOMAIN; CELL CYCLE PROTEINS; CELL LINE; COMET ASSAY; DNA-BINDING PROTEINS; ENZYME INHIBITORS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GENE DELETION; GENE EXPRESSION REGULATION; GENES, DOMINANT; GREEN FLUORESCENT PROTEINS; HUMANS; HYDRAZINES; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; SERINE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

ATAXIA; ATAXIA TELANGIECTASIA;

EID: 10044225999     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600455     Document Type: Article

References (39)

1. Ali A, Zhang J, Bao S, Liu I, Otterness D, Dean NM, Abraham RT, Wang XF (2004) Requirement of protein phosphatase 5 in DNA-damage-induced ATM activation. Genes Dev 18: 249-254
2. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506
3. Bakkenist CJ, Kastan MB (2004) Phosphatases join kinases in DNA-damage response pathways. Trends Cell Biol 14: 339341
4. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, Smorodinsky NI, Prives C, Reiss Y, Shiloh Y, Ziv Y (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281: 1674-1677
5. Borthwick EB, Zeke T, Prescott AR, Cohen PT (2001) Nuclear localization of protein phosphatase 5 is dependent on the carboxy-terminal region. FEBS Lett 491: 279-284
6. Bruno S, Ardelt B, Skierski JS, Traganos F, Darzynkiewicz Z (1992) Different effects of staurosporine, an inhibitor of protein kinases, on the cell cycle and chromatin structure of normal and leukemic lymphocytes. Cancer Res 52: 470-473
7. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1677-1679
8. Cedervall B, Wong R, Albright N, Dynlacht J, Lambin P, Dewey WC (1995) Methods for the quantification of DNA double-strand breaks determined from the distribution of DNA fragment sizes measured by pulsed-field gel electrophoresis. Radiat Res 143: 8-16
9. Chan DW, Son SC, Block W, Ye R, Khanna KK, Wold MS, Douglas P, Goodarzi AA, Pelley J, Taya Y, Lavin MF, Lees-Miller SP (2000) Purification and characterization of ATM from human placenta. A manganese-dependent, wortmannin-sensitive serine/threonine protein kinase. J Biol Chem 275: 7803-7810
10. Cohen PT (1997) Novel protein serine/threonine phosphatases: variety is the spice of life. Trends Biochem Sci 22: 245-251
11. Cohen PT (2002) Protein phosphatase 1-targeted in many directions. J Cell Sci 115: 241-256
12. Douglas P, Moorhead GB, Ye R, Lees-Miller SP (2001) Protein phosphatases regulate DNA-dependent protein kinase activity. J Biol Chem 276: 18992-18998
13. Douglas P, Sapkota GP, Morrice N, Yu Y, Goodarzi AA, Merkle D, Meek K, Alessi DR, Lees-Miller SP (2002) Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem J 368: 243-251
14. Evans DR, Myles T, Hofsteenge J, Hemmings BA (1999) Functional expression of human PP2Ac in yeast permits the identification of novel C-terminal and dominant-negative mutant forms. J Biol Chem 274: 24038-24046
15. Goodarzi AA, Block WD, Lees-Miller SP (2003) The role of ATM and ATR in DNA damage-induced cell cycle control. Prog Cell Cycle Res 5: 393-411
16. Goodarzi AA, Lees-Miller SP (2004) Biochemical characterization of the ataxia-telangiectasia mutated (ATM) protein from human cells. DNA Repair (Amst) 3: 753-767
17. Guo CY, Brautigan DL, Larner JM (2002) ATM-dependent dissociation of B55 regulatory subunit from nuclear PP2A in response to ionizing radiation. J Biol Chem 277: 4839-4844
18. Hastie CJ, Cohen PT (1998) Purification of protein phosphatase 4 catalytic subunit: inhibition by the antitumour drug fostriecin and other tumour suppressors and promoters. FEBS Lett 431: 357-361
19. Honkanen RE, Golden T (2002) Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr Med Chem 9: 2055-2075
20. Huang X, Honkanen RE (1998) Molecular cloning, expression, and characterization of a novel human serine/threonine protein phosphatase, PP7, that is homologous to Drosophila retinal degeneration C gene product (rdgC). J Biol Chem 273: 1462-1468
21. Janssens V, Goris J (2001) Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem J 353: 417-439
22. Khanna KK, Keating KE, Kozlov S, Scott S, Gatei M, Hobson K, Taya Y, Gabrielli B, Chan D, Lees-Miller SP, Lavin MF (1998) ATM associates with and phosphorylates p53: mapping the region of interaction. Nat Genet 20: 398-400
23. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB (2004) Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev 18: 1423-1438
24. Kloeker S, Reed R, McConnell JL, Chang D, Tran K, Westphal RS, Law BK, Colbran RJ, Kamoun M, Campbell KS, Wadzinski BE (2003) Parallel purification of three catalytic subunits of the protein serine/threonine phosphatase 2A family (PP2A(C), PP4(C), and PP6(C)) and analysis of the interaction of PP2A(C) with alpha4 protein. Protein Expr Purif 31: 19-33
25. Kozlov S, Gueven N, Keating K, Ramsay J, Lavin MF (2003) ATP activates ATM in vitro: importance of autophosphorylation. J Biol Chem 278: 9309-9317
26. Kuhne M, Riballo E, Rief N, Rothkamm K, Jeggo PA, Lobrich M (2004) A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res 64: 500-508
27. Kurz EU, Lees Miller SP (2004) DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst) 3: 889-900
28. Lee JH, Paull TT (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304: 93-96
29. MacKintosh C, Moorhead GBG (1999) Assay and purification of protein serine/threonine phosphatases. In Protein Phosphorylation: A Practical Approach, Hardie DG (ed) pp 153-181. Oxford: Oxford University Press
30. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM (2003) Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 81: 123-129
31. Rothkamm K, Lobrich M (2003) Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc Natl Acad Sci USA 100: 5057-5062
32. Ruiz de Almodovar JM, Steel GG, Whitaker SJ, McMillan TJ (1994) A comparison of methods for calculating DNA double-strand break induction frequency in mammalian cells by pulsed-field gel electrophoresis. Int J Radiat Biol 65: 641-649
33. Sarkaria JN, Tibbetts RS, Busby EC, Kennedy AP, Hill DE, Abraham RT (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res 58: 4375-4382
34. Schmidt KN, Traenckner EB, Meier B, Baeuerle PA (1995) Induction of oxidative stress by okadaic acid is required for activation of transcription factor NF-kappa B. J Biol Chem 270: 27136-27142
35. Shackelford RE, Innes CL, Sieber SO, Heinloth AN, Leadon SA, Paules RS (2001) The Ataxia telangiectasia gene product is required for oxidative stress-induced G1 and G2 checkpoint function in human fibroblasts. J Biol Chem 276: 21951-21959
36. Stubbs MD, Tran HT, Atwell AJ, Smith CS, Olson D, Moorhead GB (2001) Purification and properties of Arabidopsis thaliana type 1 protein phosphatase (PP1). Biochim Biophys Acta 1550: 52-63
37. Wechsler T, Chen BP, Harper R, Morotomi-Yano K, Huang BC, Meek K, Cleaver JE, Chen DJ, Wabl M (2004) DNA-PKcs function regulated specifically by protein phosphatase 5. Proc Natl Acad Sci USA 101: 1247-1252
38. Ye R, Goodarzi AA, Kurz EU, Saito S, Higashimoto Y, Lavin MF, Appella E, Anderson CW, Lees-Miller SP (2004) The isoflavonoids genistein and quercetin activate different stress signaling pathways as shown by analysis of site-specific phosphorylation of ATM, p53 and histone H2AX. DNA Repair (Amst) 3: 235-244
39. Zhang N, Chen P, Khanna KK, Scott S, Gatei M, Kozlov S, Watters D, Spring K, Yen T, Lavin MF (1997) Isolation of full-length ATM cDNA and correction of the ataxia-telangiectasia cellular phenotype. Proc Natl Acad Sci USA 94: 8021-8026