The dimeric architecture of checkpoint kinases Mec1ATR and Tel1ATM reveal a common structural organization

Journal of Biological Chemistry

Volumn 291, Issue 26, 2016, Pages 13436-13447

  Sawicka, Marta ^a   Wanrooij, Paulina H ^b,c   Darbari, Vidya C ^a   Tannous, Elias ^b   Hailemariam, Sarem ^b   Bose, Daniel ^a,d   Makarova, Alena V ^b   Burgers, Peter M ^b   Zhang, Xiaodong ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERS; PROTEINS; YEAST;

DIMERIC ARCHITECTURE; ELONGATION FACTOR; HEAD-TO-HEAD DIMERS; PHOSPHATIDYLINOSITOL; PROTEIN PHOSPHATASE 2A; SEPARATE INTERFACES; STRUCTURAL INSIGHTS; STRUCTURAL ORGANIZATION;

ENZYMES;

ELONGATION FACTOR 3; HUNTINGTIN; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN DDC2; PROTEIN MEC1; PROTEIN SERINE THREONINE KINASE; PROTEIN TEL1; UNCLASSIFIED DRUG; ATM PROTEIN; ATM PROTEIN, HUMAN; ATR PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME STRUCTURE; GEL FILTRATION; HUMAN; IMAGE PROCESSING; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; CHEMISTRY; GENETICS; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; STRUCTURAL HOMOLOGY;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; HUMANS; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84975887007     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.708263     Document Type: Article

References (63)

1. Abraham, R. T. (2004) PI 3-kinase related kinases: "big" players in stress-induced signaling pathways. DNA Repair 3, 883-887
2. Lempiäinen, H., and Halazonetis, T. D. (2009) Emerging common themes in regulation of PIKKs and PI3Ks. EMBO J. 28, 3067-3073
3. Llorca, O., Rivera-Calzada, A., Grantham, J., and Willison, K. R. (2003) Electron microscopy and 3D reconstructions reveal that human ATM kinase uses an arm-like domain to clamp around double-stranded DNA. Oncogene 22, 3867-3874
4. Lau, W. C., Li, Y., Liu, Z., Gao, Y., Zhang, Q., and Huen, M. S. (2016) Structure of the human dimeric ATM kinase. Cell Cycle 15, 1117-1124
5. Boskovic, J., Rivera-Calzada, A., Maman, J. D., Chacón, P., Willison, K. R., Pearl, L. H., and Llorca, O. (2003) Visualization of DNA-induced conformational changes in the DNA repair kinase DNA-PKcs. EMBO J. 22, 5875-5882
6. Spagnolo, L., Rivera-Calzada, A., Pearl, L. H., and Llorca, O. (2006) Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol. Cell 22, 511-519
7. Rivera-Calzada, A., Maman, J. D., Spagnolo, L., Pearl, L. H., and Llorca, O. (2005) Three-dimensional structure and regulation of the DNA-dependent protein kinase catalytic subunit (DNA-PKcs). Structure 13, 243-255
8. Williams, D. R., Lee, K. J., Shi, J., Chen, D. J., and Stewart, P. L. (2008) Cryo-EM structure of the DNA-dependent protein kinase catalytic subunit at subnanometer resolution reveals α helices and insight into DNA binding. Structure 16, 468-477
9. Arias-Palomo, E., Yamashita, A., Fernández, I. S., Núñez-Ramírez, R., Bamba, Y., Izumi, N., Ohno, S., and Llorca, O. (2011) The nonsense-mediated mRNA decay SMG-1 kinase is regulated by large-scale conformational changes controlled by SMG-8. Genes Dev. 25, 153-164
10. Melero, R., Uchiyama, A., Castaño, R., Kataoka, N., Kurosawa, H., Ohno, S., Yamashita, A., and Llorca, O. (2014) Structures of SMG1-UPFs complexes: SMG1 contributes to regulate UPF2-dependent activation of UPF1 in NMD. Structure 22, 1105-1119
11. Deniaud, A., Karuppasamy, M., Bock, T., Masiulis, S., Huard, K., Garzoni, F., Kerschgens, K., Hentze, M. W., Kulozik, A. E., Beck, M., Neu-Yilik, G., and Schaffitzel, C. (2015) A network of SMG-8, SMG-9 and SMG-1 C-terminal insertion domain regulates UPF1 substrate recruitment and phosphorylation. Nucleic Acids Res. 43, 7600-7611
12. Yip, C. K., Murata, K., Walz, T., Sabatini, D. M., and Kang, S. A. (2010) Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol. Cell 38, 768-774
13. Gaubitz, C., Oliveira, T. M., Prouteau, M., Leitner, A., Karuppasamy, M., Konstantinidou, G., Rispal, D., Eltschinger, S., Robinson, G. C., Thore, S., Aebersold, R., Schaffitzel, C., and Loewith, R. (2015) Molecular basis of the rapamycin insensitivity of target of rapamycin complex 2. Mol. Cell 58, 977-988
14. Sibanda, B. L., Chirgadze, D. Y., and Blundell, T. L. (2010) Crystal structure of DNA-PKcs reveals a large open-ring cradle comprised of HEAT repeats. Nature 463, 118-121
15. Yang, H., Rudge, D. G., Koos, J. D., Vaidialingam, B., Yang, H. J., and Pavletich, N. P. (2013) mTOR kinase structure, mechanism and regulation. Nature 497, 217-223
16. Aylett, C. H., Sauer, E., Imseng, S., Boehringer, D., Hall, M. N., Ban, N., and Maier, T. (2016) Architecture of human mTOR complex 1. Science 351, 48-52
17. Bakkenist, C. J., and Kastan, M. B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421, 499-506
18. Morrow, D. M., Tagle, D. A., Shiloh, Y., Collins, F. S., and Hieter, P. (1995) TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1. Cell 82, 831-840
19. Sun, Z., Fay, D. S., Marini, F., Foiani, M., and Stern, D. F. (1996) Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev. 10, 395-406
20. Lydall, D., Nikolsky, Y., Bishop, D. K., and Weinert, T. (1996) A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature 383, 840-843
21. Santocanale, C., and Diffley, J. F. (1998) A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395, 615-618
22. Sanchez, Y., Desany, B. A., Jones, W. J., Liu, Q., Wang, B., and Elledge, S. J. (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271, 357-360
23. Sanchez, Y., Bachant, J., Wang, H., Hu, F., Liu, D., Tetzlaff, M., and Elledge, S. J. (1999) Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286, 1166-1171
24. Paciotti, V., Lucchini, G., Plevani, P., and Longhese, M. P. (1998) Mec1p is essential for phosphorylation of the yeast DNA damage checkpoint protein Ddc1p, which physically interacts with Mec3p. EMBO J. 17, 4199-4209
25. Brush, G. S., Morrow, D. M., Hieter, P., and Kelly, T. J. (1996) The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc. Natl. Acad. Sci. U.S.A. 93, 15075-15080
26. Flott, S., Kwon, Y., Pigli, Y. Z., Rice, P. A., Sung, P., and Jackson, S. P. (2011) Regulation of Rad51 function by phosphorylation. EMBO Rep. 12, 833-839
27. Mills, K. D., Sinclair, D. A., and Guarente, L. (1999) MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell 97, 609-620
28. Moser, B. A., Chang, Y. T., Kosti, J., and Nakamura, T. M. (2011) Tel1ATM and Rad3ATR kinases promote Ccq1-Est1 interaction to maintain telomeres in fission yeast. Nat. Struct. Mol. Biol. 18, 1408-1413
29. Zou, L., and Elledge, S. J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548
30. Rivera-Calzada, A., Lopez-Perrote, A., Melero, R., Boskovic, J., Munoz-Hernandez, H., Martino, F., and Llorca, O. (2015) Structure and assembly of the PI3K-like protein kinases (PIKKs) revealed by electron microscopy. AIMS Biophys. 2, 36-57
31. Mordes, D. A., Glick, G. G., Zhao, R., and Cortez, D. (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev. 22, 1478-1489
32. Seidel, J. J., Anderson, C. M., and Blackburn, E. H. (2008) A novel Tel1/ATM N-terminal motif, TAN, is essential for telomere length maintenance and a DNA damage response. Mol. Cell. Biol. 28, 5736-5746
33. Paciotti, V., Clerici, M., Lucchini, G., and Longhese, M. P. (2000) The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14, 2046-2059
34. Rouse, J., and Jackson, S. P. (2000) LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19, 5801-5812
35. Wakayama, T., Kondo, T., Ando, S., Matsumoto, K., and Sugimoto, K. (2001) Pie1, a protein interacting with Mec1, controls cell growth and checkpoint responses in Saccharomyces cerevisiae. Mol. Cell. Biol. 21, 755-764
36. Ball, H. L., Myers, J. S., and Cortez, D. (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell 16, 2372-2381
37. Ball, H. L., and Cortez, D. (2005) ATRIP oligomerization is required for ATR-dependent checkpoint signaling. J. Biol. Chem. 280, 31390-31396
38. Itakura, E., Sawada, I., and Matsuura, A. (2005) Dimerization of the ATRIP protein through the coiled-coil motif and its implication to the maintenance of stalled replication forks. Mol. Biol. Cell 16, 5551-5562
39. Mordes, D. A., Nam, E. A., and Cortez, D. (2008) Dpb11 activates the Mec1-Ddc2 complex. Proc. Natl. Acad. Sci. U.S.A. 105, 18730-18734
40. Ball, H. L., Ehrhardt, M. R., Mordes, D. A., Glick, G. G., Chazin, W. J., and Cortez, D. (2007) Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol. 27, 3367-3377
41. Nakada, D., Hirano, Y., Tanaka, Y., and Sugimoto, K. (2005) Role of the C terminus of Mec1 checkpoint kinase in its localization to sites of DNA damage. Mol. Biol. Cell 16, 5227-5235
42. Sun, Y., Xu, Y., Roy, K., and Price, B. D. (2007) DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity. Mol. Cell. Biol. 27, 8502-8509
43. Liu, S., Shiotani, B., Lahiri, M., Maréchal, A., Tse, A., Leung, C. C., Glover, J. N., Yang, X. H., and Zou, L. (2011) ATR autophosphorylation as a molecular switch for checkpoint activation. Mol. Cell 43, 192-202
44. Lee, J. H., and Paull, T. T. (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304, 93-96
45. Navadgi-Patil, V. M., and Burgers, P. M. (2009) A tale of two tails: activation of DNA damage checkpoint kinase Mec1/ATR by the 9-1-1 clamp and by Dpb11/TopBP1. DNA Repair 8, 996-1003
46. Pfander, B., and Diffley, J. F. (2011) Dpb11 coordinates Mec1 kinase activation with cell cycle-regulated Rad9 recruitment. EMBO J. 30, 4897-4907
47. Kumar, S., and Burgers, P. M. (2013) Lagging strand maturation factor Dna2 is a component of the replication checkpoint initiation machinery. Genes Dev. 27, 313-321
48. Navadgi-Patil, V. M., and Burgers, P. M. (2008) Yeast DNA replication protein Dpb11 activates the Mec1/ATR checkpoint kinase. J. Biol. Chem. 283, 35853-35859
49. 2/M checkpoint. J. Biol. Chem. 286, 40999-41007
50. Guo, Z., Kozlov, S., Lavin, M. F., Person, M. D., and Paull, T. T. (2010) ATM activation by oxidative stress. Science 330, 517-521
51. Majka, J., Niedziela-Majka, A., and Burgers, P. M. (2006) The checkpoint clamp activates Mec1 kinase during initiation of the DNA damage checkpoint. Mol. Cell 24, 891-901
52. Ludtke, S. J., Baldwin, P. R., and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97
53. Tang, G., Peng, L., Baldwin, P. R., Mann, D. S., Jiang, W., Rees, I., and Ludtke, S. J. (2007) EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46
54. Mindell, J. A., and Grigorieff, N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347
55. van Heel, M., Harauz, G., Orlova, E. V., Schmidt, R., and Schatz, M. (1996) A new generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24
56. Scheres, S. H. (2012) RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530
57. Scheres, S. H., and Chen, S. (2012) Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853-854
58. Shaikh, T. R., Gao, H., Baxter, W. T., Asturias, F. J., Boisset, N., Leith, A., and Frank, J. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc 3, 1941-1974
59. Scheres, S. H. (2012) A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406-418
60. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
61. Paciotti, V., Clerici, M., Scotti, M., Lucchini, G., and Longhese, M. P. (2001) Characterization of mec1 kinase-deficient mutants and of new hypomorphic mec1 alleles impairing subsets of the DNA damage response pathway. Mol. Cell. Biol. 21, 3913-3925
62. Chan, D. W., Chen, B. P., Prithivirajsingh, S., Kurimasa, A., Story, M. D., Qin, J., and Chen, D. J. (2002) Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16, 2333-2338
63. Soliman, G. A., Acosta-Jaquez, H. A., Dunlop, E. A., Ekim, B., Maj, N. E., Tee, A. R., and Fingar, D. C. (2010) mTOR Ser-2481 autophosphorylation monitors mTORC-specific catalytic activity and clarifies rapamycin mechanism of action. J. Biol. Chem. 285, 7866-7879