162
Views
90
CrossRef citations to date
0
Altmetric
Article

Large FK506-Binding Proteins Shape the Pharmacology of Rapamycin

, , , &
Pages 1357-1367 | Received 22 May 2012, Accepted 19 Jan 2013, Published online: 20 Mar 2023

REFERENCES

  • Proud CG. 2011. mTOR signalling in health and disease. Biochem. Soc. Trans. 39:431–436.
  • Zoncu R, Efeyan A, Sabatini DM. 2011. mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12:21–35.
  • Vezina C, Kudelski A, Sehgal SN. 1975. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J. Antibiot. (Tokyo) 28:721–726.
  • Gaali S, Gopalakrishnan R, Wang Y, Kozany C, Hausch F. 2011. The chemical biology of immunophilin ligands. Curr. Med. Chem. 18:5355–5379.
  • Choo AY, Blenis J. 2009. Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 8:567–572.
  • Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098–1101.
  • Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. 2006. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22:159–168.
  • Lamming DW, Ye L, Katajisto P, Goncalves MD, Saitoh M, Stevens DM, Davis JG, Salmon AB, Richardson A, Ahima RS, Guertin DA, Sabatini DM, Baur JA. 2012. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335:1638–1643.
  • Araki K, Ellebedy AH, Ahmed R. 2011. TOR in the immune system. Curr. Opin. Cell Biol. 23:707–715.
  • Benjamin D, Colombi M, Moroni C, Hall MN. 2011. Rapamycin passes the torch: a new generation of mTOR inhibitors. Nat. Rev. Drug Discov. 10:868–880.
  • Bové J, Martinez-Vicente M, Vila M. 2011. Fighting neurodegeneration with rapamycin: mechanistic insights. Nat. Rev. Neurosci. 12:437–452.
  • Saunders RN, Metcalfe MS, Nicholson ML. 2001. Rapamycin in transplantation: a review of the evidence. Kidney Int. 59:3–16.
  • Kozany C, Marz A, Kress C, Hausch F. 2009. Fluorescent probes to characterise FK506-binding proteins. Chembiochem 10:1402–1410.
  • Bai X, Ma D, Liu A, Shen X, Wang QJ, Liu Y, Jiang Y. 2007. Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318:977–980.
  • Uhlenbrock K, Weiwad M, Wetzker R, Fischer G, Wittinghofer A, Rubio I. 2009. Reassessment of the role of FKBP38 in the Rheb/mTORC1 pathway. FEBS Lett. 583:965–970.
  • Pei H, Li L, Fridley BL, Jenkins GD, Kalari KR, Lingle W, Petersen G, Lou Z, Wang L. 2009. FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 16:259–266.
  • Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14:1296–1302.
  • Schalm SS, Blenis J. 2002. Identification of a conserved motif required for mTOR signaling. Curr. Biol. 12:632–639.
  • Vilella-Bach M, Nuzzi P, Fang Y, Chen J. 1999. The FKBP12-rapamycin-binding domain is required for FKBP12-rapamycin-associated protein kinase activity and G1 progression. J. Biol. Chem. 274:4266–4272.
  • Ikenoue T, Hong S, Inoki K. 2009. Monitoring mammalian target of rapamycin (mTOR) activity. Methods Enzymol. 452:165–180.
  • Sato T, Umetsu A, Tamanoi F. 2008. Characterization of the Rheb-mTOR signaling pathway in mammalian cells: constitutive active mutants of Rheb and mTOR. Methods Enzymol. 438:307–320.
  • Dubois S, Shou W, Haneline LS, Fleischer S, Waldmann TA, Muller JR. 2003. Distinct pathways involving the FK506-binding proteins 12 and 12.6 underlie IL-2- versus IL-15-mediated proliferation of T cells. Proc. Natl. Acad. Sci. U. S. A. 100:14169–14174.
  • Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67:235–242.
  • Leslie AGW. 1992. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallography, no. 26. Daresbury Laboratory, Warrington, UK.
  • Evans P. 2006. Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr. 62:72–82.
  • Liang J, Choi J, Clardy J. 1999. Refined structure of the FKBP12-rapamycin-FRB ternary complex at 2.2 A resolution. Acta Crystallogr. D Biol. Crystallogr. 55:736–744.
  • Perrakis A, Morris R, Lamzin VS. 1999. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 6:458–463.
  • Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486–501.
  • Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53:240–255.
  • Gerard M, Deleersnijder A, Daniels V, Schreurs S, Munck S, Reumers V, Pottel H, Engelborghs Y, Van den Haute C, Taymans JM, Debyser Z, Baekelandt V. 2010. Inhibition of FK506 binding proteins reduces alpha-synuclein aggregation and Parkinson's disease-like pathology. J. Neurosci. 30:2454–2463.
  • Banaszynski LA, Liu CW, Wandless TJ. 2005. Characterization of the FKBP.rapamycin.FRB ternary complex. J. Am. Chem. Soc. 127:4715–4721.
  • Waksman R, Ajani AE, Pichard AD, Torguson R, Pinnow E, Canos D, Satler LF, Kent KM, Kuchulakanti P, Pappas C, Gambone L, Weissman N, Abbott MC, Lindsay J. 2004. Oral rapamycin to inhibit restenosis after stenting of de novo coronary lesions: the Oral Rapamune to Inhibit Restenosis (ORBIT) study. J. Am. Coll. Cardiol. 44:1386–1392.
  • Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284:8023–8032.
  • Lawrence MC, Colman PM. 1993. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234:946–950.
  • Heitman J, Movva NR, Hall MN. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905–909.
  • 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. U. S. A. 92:4947–4951.
  • Hoeffer CA, Tang W, Wong H, Santillan A, Patterson RJ, Martinez LA, Tejada-Simon MV, Paylor R, Hamilton SL, Klann E. 2008. Removal of FKBP12 enhances mTOR-Raptor interactions, LTP, memory, and perseverative/repetitive behavior. Neuron 60:832–845.
  • Price RD, Yamaji T, Yamamoto H, Higashi Y, Hanaoka K, Yamazaki S, Ishiye M, Aramori I, Matsuoka N, Mutoh S, Yanagihara T, Gold BG. 2005. FK1706, a novel non-immunosuppressive immunophilin: neurotrophic activity and mechanism of action. Eur. J. Pharmacol. 509:11–19.
  • Gopalakrishnan R, Kozany C, Gaali S, Kress C, Hoogeland B, Bracher A, Hausch F. 2012. Evaluation of synthetic FK506 analogues as ligands for the FK506-binding proteins 51 and 52. J. Med. Chem. 55:4114–4122.
  • Gopalakrishnan R, Kozany C, Wang Y, Schneider S, Hoogeland B, Bracher A, Hausch F. 2012. Exploration of pipecolate sulfonamides as binders of the FK506-binding proteins 51 and 52. J. Med. Chem. 55:4123–4131.
  • Bastidas RJ, Shertz CA, Lee SC, Heitman J, Cardenas ME. 2012. Rapamycin exerts antifungal activity in vitro and in vivo against Mucor circinelloides via FKBP12-dependent inhibition of Tor. Eukaryot. Cell 11:270–281.
  • Cruz MC, Cavallo LM, Gorlach JM, Cox G, Perfect JR, Cardenas ME, Heitman J. 1999. Rapamycin antifungal action is mediated via conserved complexes with FKBP12 and TOR kinase homologs in Cryptococcus neoformans. Mol. Cell. Biol. 19:4101–4112.
  • Cruz MC, Goldstein AL, Blankenship J, Del Poeta M, Perfect JR, McCusker JH, Bennani YL, Cardenas ME, Heitman J. 2001. Rapamycin and less immunosuppressive analogs are toxic to Candida albicans and Cryptococcus neoformans via FKBP12-dependent inhibition of TOR. Antimicrob. Agents Chemother. 45:3162–3170.
  • Pemberton TJ. 2006. Identification and comparative analysis of sixteen fungal peptidyl-prolyl cis/trans isomerase repertoires. BMC Genomics 7:244. doi:10.1186/1471-2164-7-244.
  • Lam E, Martin MM, Timerman AP, Sabers C, Fleischer S, Lukas T, Abraham RT, O'Keefe SJ, O'Neill EA, Wiederrecht GJ. 1995. A novel FK506 binding protein can mediate the immunosuppressive effects of FK506 and is associated with the cardiac ryanodine receptor. J. Biol. Chem. 270:26511–26522.
  • Jiang W, Cazacu S, Xiang C, Zenklusen JC, Fine HA, Berens M, Armstrong B, Brodie C, Mikkelsen T. 2008. FK506 binding protein mediates glioma cell growth and sensitivity to rapamycin treatment by regulating NF-kappaB signaling pathway. Neoplasia 10:235–243.
  • Weiwad M, Edlich F, Kilka S, Erdmann F, Jarczowski F, Dorn M, Moutty MC, Fischer G. 2006. Comparative analysis of calcineurin inhibition by complexes of immunosuppressive drugs with human FK506 binding proteins. Biochemistry 45:15776–15784.
  • Hsu PP, Kang SA, Rameseder J, Zhang Y, Ottina KA, Lim D, Peterson TR, Choi Y, Gray NS, Yaffe MB, Marto JA, Sabatini DM. 2011. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332:1317–1322.
  • Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villen J, Kubica N, Hoffman GR, Cantley LC, Gygi SP, Blenis J. 2011. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332:1322–1326.
  • Liu J, Stevens PD, Gao T. 2011. mTOR-dependent regulation of PHLPP expression controls the rapamycin sensitivity in cancer cells. J. Biol. Chem. 286:6510–6520.
  • Yip CK, Murata K, Walz T, Sabatini DM, Kang SA. 2010. Structure of the human mTOR complex I and its implications for rapamycin inhibition. Mol. Cell 38:768–774.
  • Laplante M, Sabatini DM. 2012. mTOR signaling in growth control and disease. Cell 149:274–293.
  • Takai H, Xie Y, de Lange T, Pavletich NP. 2010. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev. 24:2019–2030.
  • Nigam SK, Jin YJ, Jin MJ, Bush KT, Bierer BE, Burakoff SJ. 1993. Localization of the FK506-binding protein, FKBP 13, to the lumen of the endoplasmic reticulum. Biochem. J. 294(Pt 2):511–515.
  • Jin YJ, Burakoff SJ. 1993. The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci. U. S. A. 90:7769–7773.
  • Baughman G, Wiederrecht GJ, Chang F, Martin MM, Bourgeois S. 1997. Tissue distribution and abundance of human FKBP51, and FK506-binding protein that can mediate calcineurin inhibition. Biochem. Biophys. Res. Commun. 232:437–443.
  • Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 101:6062–6067.
  • Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460:392–395.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.