Emerging common themes in regulation of PIKKs and PI3Ks

EMBO Journal

Volumn 28, Issue 20, 2009, Pages 3067-3073

  Lempiäinen, Harri ^a   Halazonetis, Thanos D ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

ATM; ATR; DNA PK; PI3K; PIKK

Indexed keywords

LIPID; PHOSPHATIDYLINOSITOL 3 KINASE;

CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; REGULATORY MECHANISM; REVIEW; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

ANIMALS; CELL CYCLE PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 70350324640     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.281     Document Type: Review

References (62)

1. Adami A, Garcia-Alvarez B, Arias-Palomo E, Barford D, Llorca O (2007) Structure of TOR and its complex with KOG1. Mol Cell 27: 509-516
2. Bader AG, Kang S, Vogt PK (2006) Cancer-specific mutations in PIK3CA are oncogenic in vivo. Proc Natl Acad Sci USA 103: 1475-1479
3. Ball HL, Myers JS, 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
4. Bosotti R, Isacchi A, Sonnhammer EL (2000) FAT: a novel domain in PIK-related kinases. Trends Biochem Sci 25: 225-227
5. Brunn GJ, Fadden P, Haystead TA, Lawrence Jr JC (1997) The mammalian target of rapamycin phosphorylates sites having a (Ser/Thr)-Pro motif and is activated by antibodies to a region near its COOH terminus. J Biol Chem 272: 32547-32550
6. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296: 1655-1657
7. Carpenter CL, Auger KR, Chanudhuri M, Yoakim M, Schaffhausen B, Shoelson S, Cantley LC (1993) Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J Biol Chem 268: 9478-9483
8. Cavalieri S, Funaro A, Porcedda P, Turinetto V, Migone N, Gatti RA, Brusco A (2006) ATM mutations in Italian families with ataxia telangiectasia include two distinct large genomic deletions. Hum Mutat 27: 10 61
9. Chen J, Zheng XF, Brown EJ, Schreiber SL (1995) Identification of an 11-kDa FKBP12-rapamycin-binding domain within the 289-kDa FKBP12-rapamycin- associated protein and characterization of a critical serine residue. Proc Natl Acad Sci USA 92: 4947-4951
10. Chiang GG, Abraham RT (2005) Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J Biol Chem 280: 25485-25490
11. Choi J, Chen J, Schreiber SL, Clardy J (1996) Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273: 239-242
12. Dames SA, Mulet JM, Rathgeb-Szabo K, Hall MN, Grzesiek S (2005) The solution structure of the FATC domain of the protein kinase target of rapamycin suggests a role for redox-dependent structural and cellular stability. J Biol Chem 280: 20558-20564
13. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC et al (2008) Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455: 1069-1075
14. Domin J, Waterfield MD (1997) Using structure to define the function of phosphoinositide 3-kinase family members. FEBS Lett 410: 91-95
15. Fang NY, Greiner TC, Weisenburger DD, Chan WC, Vose JM, Smith LM, Armitage JO, Mayer RA, Pike BL, Collins FS, Hacia JG (2003) Oligonucleotide microarrays demonstrate the highest frequency of ATM mutations in the mantle cell subtype of lymphoma. Proc Natl Acad Sci USA 100: 5372-5377
16. Greenman C, Stephens P, Smith R, Dalgliesh GL, Hunter C, Bignell G, Davies H, Teague J, Butler A, Stevens C, Edkins S, O?Meara S, Vastrik I, Schmidt EE, Avis T, Barthorpe S, Bhamra G, Buck G, Choudhury B, Clements J et al (2007) Patterns of somatic mutation in human cancer genomes. Nature 446: 153-158 (Pubitemid 46398669)
17. Gymnopoulos M, Elsliger MA, Vogt PK (2007) Rare cancer-specific mutations in PIK3CA show gain of function. Proc Natl Acad Sci USA 104: 5569-5574
18. Holz MK, Blenis J (2005) Identification of S6 kinase 1 as a novel mammalian target of rapamycin (mTOR)-phosphorylating kinase. J Biol Chem 280: 26089-26093
19. Huang CH, Mandelker D, Schmidt-Kittler O, Samuels Y, Velculescu VE, Kinzler KW, Vogelstein B, Gabelli SB, Amzel LM (2007) The structure of a human p110álpha/p85álpha complex elucidates the effects of oncogenic PI3Kalpha mutations. Science 318: 1744-1748
20. Ikenoue T, Kanai F, Hikiba Y, Obata T, Tanaka Y, Imamura J, Ohta M, Jazag A, Guleng B, Tateishi K, Asaoka Y, Matsumura M, Kawabe T, Omata M (2005) Functional analysis of PIK3CA gene mutations in human colorectal cancer. Cancer Res 65: 4562-4567
21. Isakoff SJ, Engelman JA, Irie HY, Luo J, Brachmann SM, Pearline RV, Cantley LC, Brugge JS (2005) Breast cancer-associated PIK3CA mutations are oncogenic in mammary epithelial cells. Cancer Res 65: 10992-11000
22. Jiang X, Sun Y, Chen S, Roy K, Price BD (2006) The FATC domains of PIKK proteins are functionally equivalent and participate in the Tip60-dependent activation of DNA-PKcs and ATM. J Biol Chem 281: 15741-15746
23. Kang S, Bader AG, Vogt PK (2005) Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic. Proc Natl Acad Sci USA 102: 802-807
24. Keith CT, Schreiber SL (1995) PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science 270: 50-51
25. Kumagai A, Lee J, Yoo HY, Dunphy WG (2006) TopBP1 activates the ATR-ATRIP complex. Cell 124: 943-955
26. Li A, Swift M (2000) Mutations at the ataxia-telangiectasia locus and clinical phenotypes of A-T patients. Am J Med Genet 92: 170-177
27. Llorca O, Rivera-Calzada A, Grantham J, Willison KR (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
28. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298: 1912-1934
29. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD (1998) The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94: 363-374
30. McMahon SB, Wood MA, Cole MD (2000) The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol Cell Biol 20: 556-562
31. Miled N, Yan Y, Hon WC, Perisic O, Zvelebil M, Inbar Y, Schneidman-Duhovny D, Wolfson HJ, Backer JM, Williams RL (2007) Mechanism of two classes of cancer mutations in the phosphoinositide 3-kinase catalytic subunit. Science 317: 239-242
32. Mordes DA, Glick GG, Zhao R, Cortez D (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev 22: 1478-1489
33. Morita T, Yamashita A, Kashima I, Ogata K, Ishiura S, Ohno S (2007) Distant N- and C-terminal domains are required for intrinsic kinase activity of SMG-1, a critical component of nonsense-mediated mRNA decay. J Biol Chem 282: 7799-7808
34. Nakada D, Hirano Y, Tanaka Y, 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
35. O?Driscoll M, Ruiz-Perez VL, Woods CG, Jeggo PA, Goodship JA (2003) A splicing mutation affecting expression of ataxia-telan-giectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat Genet 33: 497-501
36. Pacold ME, Suire S, Perisic O, Lara-Gonzalez S, Davis CT, Walker EH, Hawkins PT, Stephens L, Eccleston JF, Williams RL (2000) Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103: 931-943
37. Perry J, Kleckner N (2003) The ATRs, ATMs, and TORs are giant HEAT repeat proteins. Cell 112: 151-155
38. Peterson RT, Beal PA, Comb MJ, Schreiber SL (2000) FKBP12-rapamycin- associated protein (FRAP) autophosphorylates at ser-ine 2481 under translationally repressive conditions. J Biol Chem 275: 7416-7423
39. Rivera-Calzada A, Maman JD, Spagnolo L, Pearl LH, Llorca O (2005) Three-dimensional structure and regulation of the DNA-dependent protein kinase catalytic subunit (DNA-PKcs). Structure 13: 243-255
40. Samuels Y, Diaz Jr LA, Schmidt-Kittler O, Cummins JM, Delong L, Cheong I, Rago C, Huso DL, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE (2005) Mutant PIK3CA promotes cell growth and invasion of human cancer cells. Cancer Cell 7: 561-573
41. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, Yan H, Gazdar A, Powell SM, Riggins GJ, Willson JK, Markowitz S, Kinzler KW, Vogelstein B, Velculescu VE (2004) High frequency of mutations of the PIK3CA gene in human cancers. Science 304: 554 (Pubitemid 38541907)
42. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, Tagle DA, Smith S, Uziel T, Sfez S, Ashkenazi M, Pecker I, Frydman M, Harnik R, Patanjali SR, Simmons A, Clines GA,
43. Sartiel A, Gatti RA, Chessa L et al (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268: 1749-1753
44. Sekulic A, Hudson CC, Homme JL, Yin P, Otterness DM, Karnitz LM, Abraham RT (2000) A direct linkage between the phospho-inositide 3-kinase-AKT signaling pathway and the mammalian target of rapamycin in mitogen-stimulated and transformed cells. Cancer Res 60: 3504-3513
45. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168
46. Spagnolo L, Rivera-Calzada A, Pearl LH, 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
47. Stan R, McLaughlin MM, Cafferkey R, Johnson RK, Rosenberg M, Livi GP (1994) Interaction between FKBP12-rapamycin and TOR involves a conserved serine residue. J Biol Chem 269: 32027-32030
48. Stephens LR, Eguinoa A, Erdjument-Bromage H, Lui M, Cooke F, Coadwell J, Smrcka AS, Thelen M, Cadwallader K, Tempst P, Hawkins PT (1997) The G beta gamma sensitivity of a PI3K is dependent upon a tightly associated adaptor, p101. Cell 89: 105-114
49. Sun Y, Jiang X, Chen S, Fernandes N, Price BD (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 102: 13182-13187
50. Sun Y, Xu Y, Roy K, Price BD (2007) DNA damage-induced acetyla-tion of lysine 3016 of ATM activates ATM kinase activity. Mol Cell Biol 27: 8502-8509
51. Takahashi T, Hara K, Inoue H, Kawa Y, Tokunaga C, Hidayat S, Yoshino K, Kuroda Y, Yonezawa K (2000) Carboxyl-terminal region conserved among phosphoinositide-kinase-related kinases is indispensable for mTOR function in vivo and in vitro. Genes Cells 5: 765-775
52. van der Burg M, Ijspeert H, Verkaik NS, Turul T, Wiegant WW, Morotomi-Yano K, Mari PO, Tezcan I, Chen DJ, Zdzienicka MZ, van Dongen JJ, van Gent DC (2009) A DNA-PKcs mutation in a radiosensitive T-B- SCID patient inhibits Artemis activation and nonhomologous end-joining. J Clin Invest 119: 91-98
53. Vogt PK, Kang S, Elsliger MA, Gymnopoulos M (2007) Cancer-specific mutations in phosphatidylinositol 3-kinase. Trends Biochem Sci 32: 342-349
54. Walker EH, Perisic O, Ried C, Stephens L, Williams RL (1999) Structural insights into phosphoinositide 3-kinase catalysis and signalling. Nature 402: 313-320
55. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124: 471-484
56. Yamashita A, Kashima I, Ohno S (2005) The role of SMG-1 in nonsense-mediated mRNA decay. Biochim Biophys Acta 1754: 305-315
57. You Z, Chahwan C, Bailis J, Hunter T, Russell P (2005) ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol Cell Biol 25: 5363-5379
58. Yu J, Wjasow C, Backer JM (1998a) Regulation of the p85/ p110alpha phosphatidylinositol 3'-kinase. Distinct roles for the n-terminal and c-terminal SH2 domains. J Biol Chem 273: 30199-30203
59. Yu J, Zhang Y, McIlroy J, Rordorf-Nikolic T, Orr GA, Backer JM (1998b) Regulation of the p85/p110 phosphatidylinositol 3'-kinase: stabilization and inhibition of the p110alpha catalytic sub-unit by the p85 regulatory subunit. Mol Cell Biol 18: 1379-1387
60. Zhao JJ, Liu Z, Wang L, Shin E, Loda MF, Roberts TM (2005) The oncogenic properties of mutant p110álpha and p110beta phosphatidylinositol 3-kinases in human mammary epithelial cells. Proc Natl Acad Sci USA 102: 18443-18448
61. Zhao L, Vogt PK (2008) Class I PI3K in oncogenic cellular transformation. Oncogene 27: 5486-5496
62. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548