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

Volumn 51, Issue 24, 2012, Pages 4909-4921

  Rodriguez Camargo, Diana C ^a   Link, Nina M ^b   Dames, Sonja A ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BICELLES; BINDING DOMAIN; BINDING STUDIES; BINDING SURFACE; CELLULAR GROWTH; CELLULAR MEMBRANES; CELLULAR SIGNALS; CONFORMATIONAL CHANGE; INHIBITOR COMPLEX; KINASE TARGETS; LIPID CONCENTRATION; LIPID SECOND MESSENGER; MEMBRANE PATCH; MEMBRANE-MIMETIC ENVIRONMENTS; MIMETICS; NEUROLOGICAL DISORDERS; PERIPHERAL MEMBRANES; PHOSPHATIDIC ACIDS; RAPAMYCIN; SECONDARY STRUCTURES; TUMOR FORMATION;

CELL MEMBRANES; LIPIDS; LIPOSOMES; MAMMALS; METABOLISM;

MEMBRANES;

LIPID; LIPOSOME; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE PROTEIN; PHOSPHATIDIC ACID; PROTEIN FKBP12; REGULATOR PROTEIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BIOMIMETICS; CELL MEMBRANE POTENTIAL; CIRCULAR DICHROISM; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME LOCALIZATION; HUMAN; MICELLE; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE;

CELL MEMBRANE; HUMANS; LIPOSOMES; MICELLES; MODELS, MOLECULAR; PHOSPHATIDIC ACIDS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SIROLIMUS; TACROLIMUS BINDING PROTEIN 1A; TOR SERINE-THREONINE KINASES;

EID: 84862555250     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3002133     Document Type: Article

References (68)

1. Wullschleger, S., Loewith, R., and Hall, M. N. (2006) TOR signaling in growth and metabolism. Cell 124, 471-484. (Pubitemid 43199434)
2. Jacinto, E., and Hall, M. N. (2003) Tor signalling in bugs, brain and brawn. Nat. Rev. Mol. Cell Biol. 4, 117-126. (Pubitemid 36172695)
3. Araki, K., Ellebedy, A. H., and Ahmed, R. (2011) TOR in the immune system. Curr. Opin. Cell Biol. 23, 707-715.
4. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A., Crespo, J. L., Bonenfant, D., Oppliger, W., Jenoe, P., and Hall, M. N. (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10, 457-468. (Pubitemid 35284167)
5. Dazert, E., and Hall, M. N. (2011) mTOR signaling in disease. Curr. Opin. Cell Biol. 23, 744-755.
6. De Virgilio, C., and Loewith, R. (2006) Cell growth control: Little eukaryotes make big contributions. Oncogene 25, 6392-6415. (Pubitemid 44582284)
7. Corradetti, M. N., and Guan, K. L. (2006) Upstream of the mammalian target of rapamycin: Do all roads pass through mTOR? Oncogene 25, 6347-6360. (Pubitemid 44582281)
8. Guertin, D. A., and Sabatini, D. M. (2007) Defining the role of mTOR in cancer. Cancer Cell 12, 9-22. (Pubitemid 47001784)
9. Guertin, D. A., and Sabatini, D. M. (2005) An expanding role for mTOR in cancer. Trends Mol. Med. 11, 353-361. (Pubitemid 41080576)
10. Tee, A. R., and Blenis, J. (2005) mTOR, translational control and human disease. Semin. Cell Dev. Biol. 16, 29-37. (Pubitemid 40126874)
11. Choo, A. Y., and Blenis, J. (2006) TORgeting oncogene addiction for cancer therapy. Cancer Cell 9, 77-79. (Pubitemid 43202658)
12. Bjornsti, M. A., and Houghton, P. J. (2004) The TOR pathway: A target for cancer therapy. Nat. Rev. Cancer 4, 335-348.
13. Jacinto, E., Loewith, R., Schmidt, A., Lin, S., Ruegg, M. A., Hall, A., and Hall, M. N. (2004) Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 6, 1122-1128. (Pubitemid 39468014)
14. Sarbassov, D. D., Ali, S. M., Sengupta, S., Sheen, J. H., Hsu, P. P., Bagley, A. F., Markhard, A. L., and Sabatini, D. M. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168.
15. Andrade, M. A., and Bork, P. (1995) HEAT repeats in the Huntington's disease protein. Nat. Genet. 11, 115-116.
16. Bosotti, R., Isacchi, A., and Sonnhammer, E. L. (2000) FAT: A novel domain in PIK-related kinases. Trends Biochem. Sci. 25, 225-227. (Pubitemid 30236217)
17. 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.
18. 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. (Pubitemid 40776757)
19. Dames, S. A. (2010) Structural basis for the association of the redox-sensitive target of rapamycin FATC domain with membrane-mimetic micelles. J. Biol. Chem. 285, 7766-7775.
20. 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. (Pubitemid 38044883)
21. 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. (Pubitemid 32002117)
22. Wedaman, K. P., Reinke, A., Anderson, S., Yates, J., III, McCaffery, J. M., and Powers, T. (2003) Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14, 1204-1220.
23. 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.
24. Withers, D. J., Ouwens, D. M., Nave, B. T., van der Zon, G. C., Alarcon, C. M., Cardenas, M. E., Heitman, J., Maassen, J. A., and Shepherd, P. R. (1997) Expression, enzyme activity, and subcellular localization of mammalian target of rapamycin in insulin-responsive cells. Biochem. Biophys. Res. Commun. 241, 704-709. (Pubitemid 28036721)
25. 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.
26. 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. (Pubitemid 34966765)
27. Zinzalla, V., Stracka, D., Oppliger, W., and Hall, M. N. (2011) Activation of mTORC2 by association with the ribosome. Cell 144, 757-768.
28. Saci, A., Cantley, L. C., and Carpenter, C. L. (2011) Rac1 regulates the activity of mTORC1 and mTORC2 and controls cellular size. Mol. Cell 42, 50-61.
29. 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.
30. 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. (Pubitemid 350098994)
31. 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. (Pubitemid 33101594)
32. Selvy, P. E., Lavieri, R. R., Lindsley, C. W., and Brown, H. A. (2011) Phospholipase D: Enzymology, functionality, and chemical modulation. Chem. Rev. 111, 6064-6119.
33. Ha, S. H., Kim, D. H., Kim, I. S., Kim, J. H., Lee, M. N., Lee, H. J., Kim, J. H., Jang, S. K., Suh, P. G., and Ryu, S. H. (2006) PLD2 forms a functional complex with mTOR/raptor to transduce mitogenic signals. Cell. Signalling 18, 2283-2291. (Pubitemid 44636169)
34. Foster, D. A. (2009) Phosphatidic acid signaling to mTOR: Signals for the survival of human cancer cells. Biochim. Biophys. Acta 1791, 949-955.
35. Sun, Y., Fang, Y., Yoon, M. S., Zhang, C., Roccio, M., Zwartkruis, F. J., Armstrong, M., Brown, H. A., and Chen, J. (2008) Phospholipase D1 is an effector of Rheb in the mTOR pathway. Proc. Natl. Acad. Sci. U.S.A. 105, 8286-8291. (Pubitemid 351904748)
36. Zhang, C., Wendel, A. A., Keogh, M. R., Harris, T. E., Chen, J., and Coleman, R. A. (2012) Glycerolipid signals alter mTOR complex 2 (mTORC2) to diminish insulin signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 1667-1672.
37. Toschi, A., Lee, E., Xu, L., Garcia, A., Gadir, N., and Foster, D. A. (2009) Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: Competition with rapamycin. Mol. Cell. Biol. 29, 1411-1420.
38. Veverka, V., Crabbe, T., Bird, I., Lennie, G., Muskett, F. W., Taylor, R. J., and Carr, M. D. (2007) 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. (Pubitemid 351158903)
39. Dames, S. A. (2008) A fast and simple method to prepare the FKBP-rapamycin binding domain of human target of rapamycin for NMR binding assays. Protein Expression Purif. 59, 31-37.
40. Schanda, P., Kupce, E., and Brutscher, B. (2005) SOFASTHMQC experiments for recording two-dimensional heteronuclear correlation spectra of proteins within a few seconds. J. Biomol. NMR 33, 199-211. (Pubitemid 43118574)
41. 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.
42. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352.
43. Veverka, V., Lennie, G., Crabbe, T., Bird, I., Taylor, R. J., and Carr, M. D. (2006) NMR assignment of the mTOR domain responsible for rapamycin binding. J. Biomol. NMR 36 (Suppl. 1), 3. (Pubitemid 46909560)
44. Stafford, R. E., Fanni, T., and Dennis, E. A. (1989) Interfacial properties and critical micelle concentration of lysophospholipids. Biochemistry 28, 5113-5120. (Pubitemid 19162760)
45. 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. (Pubitemid 38114298)
46. Ahn, H. C., Juranic, N., Macura, S., and Markley, J. L. (2006) Three-dimensional structure of the water-insoluble protein crambin in dodecylphosphocholine micelles and its minimal solvent-exposed surface. J. Am. Chem. Soc. 128, 4398-4404.
47. Losonczi, J. A., Olejniczak, E. T., Betz, S. F., Harlan, J. E., Mack, J., and Fesik, S. W. (2000) NMR studies of the anti-apoptotic protein Bcl-xL in micelles. Biochemistry 39, 11024-11033.
48. Dames, S. A., Junemann, A., Sass, H. J., Schonichen, 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.
49. Weschayanwiwat, P., Scamehorn, J., and Reilly, P. (2005) Surfactant properties of low molecular weight phospholipids. J. Surfactants Deterg. 8, 65-72. (Pubitemid 41042106)
50. 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.
51. Hauser, H. (2000) Short-chain phospholipids as detergents. Biochim. Biophys. Acta 1508, 164-181.
52. Odagaki, Y., and Clardy, J. (1997) Structural basis for peptidomimicry by the effector element of rapamycin. J. Am. Chem. Soc. 119, 10253-10254. (Pubitemid 27478826)
53. Choi, J., Chen, J., Schreiber, S. L., and Clardy, J. (1996) Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273, 239-242. (Pubitemid 26285890)
54. Moravcevic, K., Oxley, C. L., and Lemmon, M. A. (2012) Conditional Peripheral Membrane Proteins: Facing up to Limited Specificity. Structure 20, 15-27.
55. Banaszynski, L. A., Liu, C. W., and Wandless, T. J. (2005) Characterization of the FKBP·rapamycin·FRB ternary complex. J. Am. Chem. Soc. 127, 4715-4721.
56. Bhat, V., McDonald, C. B., Mikles, D. C., Deegan, B. J., Seldeen, K. L., Bates, M. L., and Farooq, A. (2012) Ligand Binding and Membrane Insertion Compete with Oligomerization of the BclXL Apoptotic Repressor. J. Mol. Biol. 416, 57-77.
57. Bogner, C., Leber, B., and Andrews, D. W. (2010) Apoptosis: Embedded in membranes. Curr. Opin. Cell Biol. 22, 845-851.
58. Yeung, T., Ozdamar, B., Paroutis, P., and Grinstein, S. (2006) Lipid metabolism and dynamics during phagocytosis. Curr. Opin. Cell Biol. 18, 429-437. (Pubitemid 44016055)
59. Xian, W., and Janmey, P. A. (2002) Dissecting the gelsolin- polyphosphoinositide interaction and engineering of a polyphosphoinositide- sensitive gelsolin C-terminal half protein. J. Mol. Biol. 322, 755-771.
60. McMahon, L. P., Choi, K. M., Lin, T. A., Abraham, R. T., and Lawrence, J. C., Jr. (2002) The rapamycin-binding domain governs substrate selectivity by the mammalian target of rapamycin. Mol. Cell. Biol. 22, 7428-7438.
61. Frias, M. A., Thoreen, C. C., Jaffe, J. D., Schroder, W., Sculley, T., Carr, S. A., and Sabatini, D. M. (2006) mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr. Biol. 16, 1865-1870. (Pubitemid 44354144)
62. Zimmerberg, J., and Kozlov, M. M. (2006) How proteins produce cellular membrane curvature. Nat. Rev. Mol. Cell Biol. 7, 9-19. (Pubitemid 43361568)
63. Kam, Y., and Exton, J. H. (2004) Role of phospholipase D1 in the regulation of mTOR activity by lysophosphatidic acid. FASEB J. 18, 311-319. (Pubitemid 38186250)
64. Xu, L., Salloum, D., Medlin, P. S., Saqcena, M., Yellen, P., Perrella, B., and Foster, D. A. (2011) Phospholipase D mediates nutrient input to mammalian target of rapamycin complex 1 (mTORC1). J. Biol. Chem. 286, 25477-25486.
65. Young, B. P., Shin, J. J., Orij, R., Chao, J. T., Li, S. C., Guan, X. L., Khong, A., Jan, E., Wenk, M. R., Prinz, W. A., Smits, G. J., and Loewen, C. J. (2010) Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 329, 1085-1088.
66. Dechant, R., Binda, M., Lee, S. S., Pelet, S., Winderickx, J., and Peter, M. (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J. 29, 2515-2526.
67. Olsson, M. H. M., Søndergaard, C. R., Rostkowski, M., and Jensen, J. H. (2011) PROPKA3: Consistent Treatment of Internal and Surface Residues in Empirical pKa Predictions. J. Chem. Theory Comput. 7, 525-537.
68. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 29-32, 51-55.