NMR- and circular dichroism-monitored lipid binding studies suggest a general role for the FATC domain as membrane anchor of phosphatidylinositol 3-kinase-related kinases (PIKK)

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 20046-20063

  Sommer, Lisa A M ^a   Schaad, Martin ^a,b   Dames, Sonja A ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b IQVIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC RESIDUES; C-TERMINAL REGIONS; MEMBRANE ANCHORS; MEMBRANE PROPERTIES; PHOSPHATIDYLINOSITOL; PROTEIN-PROTEIN INTERACTIONS; REDOX SENSITIVES; SECONDARY STRUCTURES;

BINDING ENERGY; CIRCULAR DICHROISM SPECTROSCOPY; ENZYMES; LIPIDS; PROTEINS;

MEMBRANES;

ATM PROTEIN; ATR PROTEIN; DNA DEPENDENT PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE RELATED KINASE; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE SMG 1; TRANSFORMATION TRANSCRIPTION DOMAIN ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DISULFIDE BOND; HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

BICELLE; LIPIDS; MEMBRANE BILAYER; MICELLE; NMR; PHOSPHOLIPID VESICLE; PIKK; PROTEIN CONFORMATION; PROTEIN-LIPID INTERACTIONS; PROTEIN-MEMBRANE INTERACTIONS;

CELL MEMBRANE; HUMANS; LIPIDS; MEMBRANES, ARTIFICIAL; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84880074658     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.467233     Document Type: Article

References (83)

1. Keith, C. T., and Schreiber, S. L. (1995) PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science 270, 50-51
2. Lempiäinen, H., and Halazonetis, T. D. (2009) Emerging common themes in regulation of PIKKs and PI3Ks. EMBO J. 28, 3067-3073
3. Lovejoy, C. A., and Cortez, D. (2009) Common mechanisms of PIKK regulation. DNA Repair (Amst.) 8, 1004-1008
4. Ditch, S., and Paull, T. T. (2012) The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 37, 15-22
5. Flynn, R. L., and Zou, L. (2011) ATR: a master conductor of cellular responses to DNA replication stress. Trends Biochem. Sci. 36, 133-140
6. Kong, X., Shen, Y., Jiang, N., Fei, X., and Mi, J. (2011) Emerging roles of DNA-PK besides DNA repair. Cell. Signal. 23, 1273-1280
7. Krüger, A., and Ralser, M. (2011) ATM is a redox sensor linking genome stability and carbon metabolism. Sci. Signal. 4, pe17
8. Ju, J., Naura, A. S., Errami, Y., Zerfaoui, M., Kim, H., Kim, J. G., Abd Elmageed, Z. Y., Abdel-Mageed, A. B., Giardina, C., Beg, A. A., Smulson, M. E., and Boulares, A. H. (2010) Phosphorylation of p50 NF-κB at a single serine residue by DNA-dependent protein kinase is critical for VCAM-1 expression upon TNF treatment. J. Biol. Chem. 285, 41152-41160
9. Lucero, H., Gae, D., and Taccioli, G. E. (2003) Novel localization of the DNA-PK complex in lipid rafts: a putative role in the signal transduction pathway of the ionizing radiation response. J. Biol. Chem. 278, 22136-22143
10. Toulany, M., Lee, K. J., Fattah, K. R., Lin, Y. F., Fehrenbacher, B., Schaller, M., Chen, B. P., Chen, D. J., and Rodemann, H. P. (2012) Akt promotes post-irradiation survival of human tumor cells through initiation, progression, and termination of DNA-PKcs-dependent DNA double-strand break repair. Mol. Cancer Res. 10, 945-957
11. Grdzka, I., Sochanowicz, B., Brzóska, K., Wójciuk, G., Sommer, S., Wojewódzka, M., Gasińska, A., Degen, C., Jahreis, G., and Szumiel, I. (2013) Cis-9,trans-11-conjugated linoleic acid affects lipid raft composition and sensitizes human colorectal adenocarcinoma HT-29 cells to X-radiation. Biochim. Biophys. Acta 1830, 2233-2242
12. Watters, D., Khanna, K. K., Beamish, H., Birrell, G., Spring, K., Kedar, P., Gatei, M., Stenzel, D., Hobson, K., Kozlov, S., Zhang, N., Farrell, A., Ramsay, J., Gatti, R., and Lavin, M. (1997) Cellular localisation of the ataxiatelangiectasia (ATM) gene product and discrimination between mutated and normal forms. Oncogene 14, 1911-1921
13. Yan, J., Khanna, K. K., and Lavin, M. F. (2000) Defective radiation signal transduction in ataxia-telangiectasia cells. Int. J. Radiat. Biol. 76, 1025-1035
14. Masse, I., Molin, L., Mouchiroud, L., Vanhems, P., Palladino, F., Billaud, M., and Solari, F. (2008) A novel role for the SMG-1 kinase in lifespan and oxidative stress resistance in Caenorhabditis elegans. PloS One 3, e3354
15. Oliveira, V., Romanow, W. J., Geisen, C., Otterness, D. M., Mercurio, F., Wang, H. G., Dalton, W. S., and Abraham, R. T. (2008) A protective role for the human SMG-1 kinase against tumor necrosis factor-α-induced apoptosis. J. Biol. Chem. 283, 13174-13184
16. Morita, T., Yamashita, A., Kashima, I., Ogata, K., Ishiura, S., and 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
17. Wullschleger, S., Loewith, R., and Hall, M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484
18. Laplante, M., and Sabatini, D. M. (2012) mTOR signaling in growth control and disease. Cell 149, 274-293
19. Unno, A., Takada, I., Takezawa, S., Oishi, H., Baba, A., Shimizu, T., Tokita, A., Yanagisawa, J., and Kato, S. (2005) TRRAP as a hepatic coactivator of LXR and FXR function. Biochem. Biophys. Res. Commun. 327, 933-938
20. Herceg, Z., and Wang, Z. Q. (2005) Rendez-vous at mitosis: TRRAPed in the chromatin. Cell Cycle 4, 383-387
21. Robert, F., Hardy, S., Nagy, Z., Baldeyron, C., Murr, R., Déry, U., Masson, J. Y., Papadopoulo, D., Herceg, Z., and Tora, L. (2006) The transcriptional histone acetyltransferase cofactor TRRAP associates with theMRNrepair complex and plays a role in DNA double-strand break repair. Mol. Cell. Biol. 26, 402-412
22. Bosotti, R., Isacchi, A., and Sonnhammer, E. L. (2000) FAT: a novel domain in PIK-related kinases. Trends Biochem. Sci. 25, 225-227
23. Perry, J., and Kleckner, N. (2003) The ATRs, ATMs, and TORs are giant HEAT repeat proteins. Cell 112, 151-155
24. Knutson, B. A. (2010) Insights into the domain and repeat architecture of target of rapamycin. J. Struct. Biol. 170, 354-363
25. 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
26. Takahashi, T., Hara, K., Inoue, H., Kawa, Y., Tokunaga, C., Hidayat, S., Yoshino, K., Kuroda, Y., and 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
27. Hoke, S. M., Irina Mutiu, A., Genereaux, J., Kvas, S., Buck, M., Yu, M., Gloor, G. B., and Brandl, C. J. (2010) Mutational analysis of the C-terminal FATC domain of Saccharomyces cerevisiae Tra1. Curr. Genet. 56, 447-465
28. Jiang, X., Sun, Y., Chen, S., Roy, K., and Price, B. D. (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
29. Dames, S. A., Mulet, J. M., Rathgeb-Szabo, K., Hall, M. N., and 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
30. Dames, S. A. (2010) Structural basis for the association of the redoxsensitive target of rapamycin FATC domain with membrane-mimetic micelles. J. Biol. Chem. 285, 7766-7775
31. Berchtold, D., and Walther, T. C. (2009) TORC2 plasma membrane localization is essential for cell viability and restricted to a distinct domain. Mol. Biol. Cell 20, 1565-1575
32. Drenan, R. M., Liu, X., Bertram, P. G., and Zheng, X. F. (2004) FKBP12- rapamycin-associated protein or mammalian target of rapamycin (FRAP/mTOR) localization in the endoplasmic reticulum and the Golgi apparatus. J. Biol. Chem. 279, 772-778
33. Kunz, J., Schneider, U., Howald, I., Schmidt, A., and Hall, M. N. (2000) HEAT repeats mediate plasma membrane localization of Tor2p in yeast. J. Biol. Chem. 275, 37011-37020
34. Zhang, X., Shu, L., Hosoi, H., Murti, K. G., and Houghton, P. J. (2002) Predominant nuclear localization of mammalian target of rapamycin in normal and malignant cells in culture. J. Biol. Chem. 277, 28127-28134
35. Zinzalla, V., Stracka, D., Oppliger, W., and Hall, M. N. (2011) Activation of mTORC2 by association with the ribosome. Cell 144, 757-768
36. Zhang, L., Tie, Y., Tian, C., Xing, G., Song, Y., Zhu, Y., Sun, Z., and He, F. (2006) CKIP-1 recruits nuclear ATM partially to the plasma membrane through interaction with ATM. Cell. Signal. 18, 1386-1395
37. Huth, J. R., Bewley, C. A., Jackson, B. M., Hinnebusch, A. G., Clore, G. M., and Gronenborn, A. M. (1997) Design of an expression system for detecting folded protein domains and mapping macromolecular interactions by NMR. Protein Sci. 6, 2359-2364
38. Koenig, B. W., Rogowski, M., and Louis, J. M. (2003) A rapid method to attain isotope labeled small soluble peptides for NMR studies. J. Biomol. NMR 26, 193-202
39. Sommer, L. A., Meier, M. A., and Dames, S. A. (2012) A fast and simple method for probing the interaction of peptides and proteins with lipids and membrane-mimetics using GB1 fusion proteins and NMR spectroscopy. Protein Sci. 21, 1566-1570
40. Stafford, R. E., Fanni, T., and Dennis, E. A. (1989) Interfacial properties and critical micelle concentration of lysophospholipids. Biochemistry 28, 5113-5120
41. Weschayanwiwat, P., Scamehorn, J. F., and Reilly, P. J. (2005) Surfactant properties of low molecular weight phospholipids. J. Surfactants Deterg. 8, 65-72
42. Tausk, R. J., Karmiggelt, J., Oudshoorn, C., and Overbeek, J. T. (1974) Physical chemical studies of short-chain lecithin homologues. I. Influence of the chain length of the fatty acid ester and of electrolytes on the critical micelle concentration. Biophys. Chem. 1, 175-183
43. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293
44. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352
45. Vuister, G. W., and Bax, A. (1993) Quantitative J correlation: a new approach for measuring homonuclear three-bond J (HNH) coupling constants in 15N-enriched proteins. J. Am. Chem. Soc. 115, 7772-7777
46. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., and Sykes, B. D. (1995) 1H, 13C, and 15N random coil NMR chemical shifts of the common amino acids. I. Investigations of nearest-neighbor effects. J. Biomol. NMR 5, 67-81
47. Schanda, P., Kupce, E., and Brutscher, B. (2005) SOFAST-HMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J. Biomol. NMR 33, 199-211
48. Wimley, W. C., and White, S. H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3, 842-848
49. Liu, W., and Caffrey, M. (2006) Interactions of tryptophan, tryptophan peptides, and tryptophan alkyl esters at curved membrane interfaces. Biochemistry 45, 11713-11726
50. Lazaridis, T., Mallik, B., and Chen, Y. (2005) Implicit solvent simulations of DPC micelle formation. J. Phys. Chem. B 109, 15098-15106
51. Tieleman, D. P., van der Spoel, D., and Berendsen, H. J. C. (2000) Molecular dynamics simulations of dodecylphosphocholine micelles at three different aggregate sizes: Micellar structure and chain relaxation. J. Phys. Chem. B 104, 6380-6388
52. Whiles, J. A., Deems, R., Vold, R. R., and Dennis, E. A. (2002) Bicelles in structure-function studies of membrane-associated proteins. Bioorg. Chem. 30, 431-442
53. Tausk, R. J., van Esch, J., Karmiggelt, J., Voordouw, G., and Overbeek, J. T. (1974) Physical chemical studies of short-chain lecithin homologues. II. Micellar weights of dihexanoyl-and diheptanoyllecithin. Biophys. Chem. 1, 184-203
54. Seewald, M. J., Pichumani, K., Stowell, C., Tibbals, B. V., Regan, L., and Stone, M. J. (2000) The role of backbone conformational heat capacity in protein stability: temperature dependent dynamics of the B1 domain of streptococcal protein G. Protein Sci. 9, 1177-1193
55. Walsh, J. D., Meier, K., Ishima, R., and Gronenborn, A. M. (2010) NMR studies on domain diffusion and alignment in modular GB1 repeats. Biophys. J. 99, 2636-2646
56. Dames, S. A., Junemann, A., Sass, H. J., Schönichen, A., Stopschinski, B. E., Grzesiek, S., Faix, J., and Geyer, M. (2011) Structure, dynamics, lipid binding, and physiological relevance of the putative GTPase-binding domain of Dictyostelium formin C. J. Biol. Chem. 286, 36907-36920
57. Farrow, N. A., Zhang, O., Forman-Kay, J. D., and Kay, L. E. (1997) Characterization of the backbone dynamics of folded and denatured states of an SH3 domain. Biochemistry 36, 2390-2402
58. Sun, Y., Jiang, X., Chen, S., Fernandes, N., and Price, B. D. (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. U.S.A. 102, 13182-13187
59. 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
60. Fang, Y., Vilella-Bach, M., Bachmann, R., Flanigan, A., and Chen, J. (2001) Phosphatidic acid-mediated mitogenic activation of mTOR signaling. Science 294, 1942-1945
61. Foster, D. A. (2009) Phosphatidic acid signaling to mTOR: signals for the survival of human cancer cells. Biochim. Biophys. Acta 1791, 949-955
62. Veverka, V., Crabbe, T., Bird, I., Lennie, G., Muskett, F. W., Taylor, R. J., and Carr, M. D. (2008) Structural characterization of the interaction of mTOR with phosphatidic acid and a novel class of inhibitor: compelling evidence for a central role of the FRB domain in small molecule-mediated regulation of mTOR. Oncogene 27, 585-595
63. Rodriguez Camargo, D. C., Link, N. M., and Dames, S. A. (2012) The FKBP-rapamycin binding domain of human TOR undergoes strong conformational changes in the presence of membrane mimetics with and without the regulator phosphatidic acid. Biochemistry 51, 4909-4921
64. Chen, R. Q., Yang, Q. K., Chen, Y. L., Oliveira, V. A., Dalton, W. S., Fearns, C., and Lee, J. D. (2009) Kinome siRNA screen identifies SMG-1 as a negative regulator of hypoxia-inducible factor-1α in hypoxia. J. Biol. Chem. 284, 16752-16758
65. González-Estévez, C., Felix, D. A., Smith, M. D., Paps, J., Morley, S. J., James, V., Sharp, T. V., and Aboobaker, A. A. (2012) SMG-1 andmTORC1 act antagonistically to regulate response to injury and growth in planarians. PLoS Genet. 8, e1002619
66. Spagnolo, L., Rivera-Calzada, A., Pearl, L. H., and Llorca, O. (2006) Threedimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol. Cell 22, 511-519
67. 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
68. Adami, A., García-Alvarez, B., Arias-Palomo, E., Barford, D., and Llorca, O. (2007) Structure of TOR and its complex with KOG1. Mol. Cell 27, 509-516
69. Myers, G. A., Gacek, D. A., Peterson, E. M., Fox, C. B., and Harris, J. M. (2012) Microscopic rates of peptide-phospholipid bilayer interactions from single-molecule residence times. J. Am. Chem. Soc. 134, 19652-19660
70. Lange, O. F., Lakomek, N. A., Farès, C., Schröder, G. F., Walter, K. F., Becker, S., Meiler, J., Grubmüller, H., Griesinger, C., and de Groot, B. L. (2008) Recognition dynamics up to microseconds revealed from an RDCderived ubiquitin ensemble in solution. Science 320, 1471-1475
71. Sun, H., Greathouse, D. V., Andersen, O. S., and Koeppe, R. E., 2nd. (2008) The preference of tryptophan for membrane interfaces: insights from Nmethylation of tryptophans in gramicidin channels. J. Biol. Chem. 283, 22233-22243
72. Kutateladze, T. G., Capelluto, D. G., Ferguson, C. G., Cheever, M. L., Kutateladze, A. G., Prestwich, G. D., and Overduin, M. (2004) Multivalent mechanism of membrane insertion by the FYVE domain. J. Biol. Chem. 279, 3050-3057
73. Buerger, C., DeVries, B., and Stambolic, V. (2006) Localization of Rheb to the endomembrane is critical for its signaling function. Biochem. Biophys. Res. Commun. 344, 869-880
74. Bai, X., Ma, D., Liu, A., Shen, X., Wang, Q. J., Liu, Y., and Jiang, Y. (2007) Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318, 977-980
75. Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L., Nada, S., and Sabatini, D. M. (2010) Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141, 290-303
76. Guo, Z., Kozlov, S., Lavin, M. F., Person, M. D., and Paull, T. T. (2010) ATM activation by oxidative stress. Science 330, 517-521
77. Wouters, B. G., and Koritzinsky, M. (2008) Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat. Rev. Cancer 8, 851-864
78. Chen, B. P., Li, M., and Asaithamby, A. (2012) New insights into the roles of ATM and DNA-PKcs in the cellular response to oxidative stress. Cancer Lett. 327, 103-110
79. Pan, Y., Nishida, Y., Wang, M., and Verdin, E. (2012) Metabolic regulation, mitochondria and the life-prolonging effect of rapamycin: a mini-review. Gerontology 58, 524-530
80. Dazert, E., and Hall, M. N. (2011) mTOR signaling in disease. Curr. Opin. Cell Biol. 23, 744-755
81. 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
82. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308
83. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31, 1647-1651