Concurrent inhibition of PI3K and mTORC1/mTORC2 overcomes resistance to rapamycin induced apoptosis by down-regulation of Mcl-1 in mantle cell lymphoma

International Journal of Cancer

Volumn 133, Issue 8, 2013, Pages 1813-1824

  Müller, Anja ^a   Zang, Chuanbing ^a   Chumduri, Cindrilla ^a   Dörken, Bernd ^a   Daniel, Peter T ^a   Scholz, Christian W ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

AKT; mantle cell lymphoma; Mcl 1; mTOR; PI3K; signaling

Indexed keywords

1 (1 CYANO 1 METHYLETHYL) 3 METHYL 8 (3 QUINOLINYL)IMIDAZO[4,5 C]QUINOLIN 2(1H,3H) ONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; BORTEZOMIB; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; OBATOCLAX; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAK; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN MCL 1; RAPAMYCIN; SMALL INTERFERING RNA;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL CULTURE; CANCER SURVIVAL; CELL DEATH; CELL PROLIFERATION; COCULTURE; CYTOSTASIS; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG POTENTIATION; ENZYME INHIBITION; HUMAN; INHIBITION KINETICS; MANTLE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION;

AKT; MANTLE CELL LYMPHOMA; MCL-1; MTOR; PI3K; SIGNALING;

AMINO ACID CHLOROMETHYL KETONES; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BCL-X PROTEIN; CASPASE INHIBITORS; CASPASES; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; CYCLIN D1; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; HUMANS; IMIDAZOLES; LYMPHOMA, MANTLE-CELL; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; PYRROLES; QUINOLINES; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84881558195     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28206     Document Type: Article

References (49)

1. Jares P, Colomer D, Campo E,. Genetic and molecular pathogenesis of mantle cell lymphoma: perspectives for new targeted therapeutics. Nat Rev Cancer 2007; 7: 750-62.
2. Bodrug SE, Warner BJ, Bath ML, Lindeman GJ, Harris AW, Adams JM,. Cyclin D1 transgene impedes lymphocyte maturation and collaborates in lymphomagenesis with the myc gene. EMBO J 1994; 13: 2124-30.
3. Stilgenbauer S, Schaffner C, Winkler D, Ott G, Leupolt E, Bentz M, Moller P, Muller-Hermelink HK, James MR, Lichter P, Dohner H,. The ATM gene in the pathogenesis of mantle-cell lymphoma. Ann Oncol 2000; 11 (Suppl 1): 127-30.
4. Diehl JA, Cheng M, Roussel MF, Sherr CJ,. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12: 3499-511.
5. Rosenwald IB, Kaspar R, Rousseau D, Gehrke L, Leboulch P, Chen JJ, Schmidt EV, Sonenberg N, London IM,. Eukaryotic translation initiation factor 4E regulates expression of cyclin D1 at transcriptional and post-transcriptional levels. J Biol Chem 1995; 270: 21176-80.
6. Jacinto E, Facchinetti V, Liu D, Soto N, Wei S, Jung SY, Huang Q, Qin J, Su B,. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 2006; 127: 125-37.
7. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM,. Active-site inhibitors of mTOR target rapamycin-resistant outputs of mTORC1 and mTORC2. PLoS Biol 2009; 7: e38.
8. Hsieh AC, Costa M, Zollo O, Davis C, Feldman ME, Testa JR, Meyuhas O, Shokat KM, Ruggero D,. Genetic dissection of the oncogenic mTOR pathway reveals druggable addiction to translational control via 4EBP-eIF4E. Cancer Cell 2010; 17: 249-61.
9. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME,. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91: 231-41.
10. Rahmani M, Anderson A, Habibi JR, Crabtree TR, Mayo M, Harada H, Ferreira-Gonzalez A, Dent P, Grant S,. The BH3-only protein Bim plays a critical role in leukemia cell death triggered by concomitant inhibition of the PI3K/Akt and MEK/ERK1/2 pathways. Blood 2009; 114: 4507-16.
11. Coloff JL, Mason EF, Altman BJ, et al. Akt requires glucose metabolism to suppress puma expression and prevent apoptosis of leukemic T cells. J Biol Chem 2011; 286: 5921-33.
12. Pugazhenthi S, Nesterova A, Sable C, Heidenreich KA, Boxer LM, Heasley LE, Reusch JE,. Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein. J Biol Chem 2000; 275: 10761-6.
13. Maurer U, Charvet C, Wagman AS, Dejardin E, Green DR,. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 2006; 21: 749-60.
14. Longo PG, Laurenti L, Gobessi S, Sica S, Leone G, Efremov DG,. The Akt/Mcl-1 pathway plays a prominent role in mediating antiapoptotic signals downstream of the B-cell receptor in chronic lymphocytic leukemia B cells. Blood 2008; 111: 846-55.
15. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, Huang DC,. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 2005; 19: 1294-305.
16. Gillissen B, Essmann F, Hemmati PG, Richter A, Oztop I, Chinnadurai G, Dorken B, Daniel PT,. Mcl-1 determines the Bax dependency of Nbk/Bik-induced apoptosis. J Cell Biol 2007; 179: 701-15.
17. Akgul C,. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci 2009; 66: 1326-36.
18. Puthalakath H, Villunger A, O'Reilly LA, Beaumont JG, Coultas L, Cheney RE, Huang DC, Strasser A,. Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 2001; 293: 1829-32.
19. Wiegmans AP, Alsop AE, Bots M, Cluse LA, Williams SP, Banks KM, Ralli R, Scott CL, Frenzel A, Villunger A, Johnstone RW,. Deciphering the molecular events necessary for synergistic tumor cell apoptosis mediated by the histone deacetylase inhibitor vorinostat and the BH3 mimetic ABT-737. Cancer Res 2011; 71: 3603-15.
20. Choi J, Chen J, Schreiber SL, Clardy J,. Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 1996; 273: 239-42.
21. Hess G, Herbrecht R, Romaguera J, et al. Phase III study to evaluate temsirolimus compared with investigator's choice therapy for the treatment of relapsed or refractory mantle cell lymphoma. J Clin Oncol 2009; 27: 3822-9.
22. Maira SM, Stauffer F, Brueggen J, et al. Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Therapeut 2008; 7: 1851-63.
23. Essmann F, Wieder T, Otto A, Muller EC, Dorken B, Daniel PT,. GDP dissociation inhibitor D4-GDI (Rho-GDI 2), but not the homologous rho-GDI 1, is cleaved by caspase-3 during drug-induced apoptosis. Biochem J 2000; 346 (Pt 3): 777-83.
24. Wieder T, Prokop A, Bagci B, Essmann F, Bernicke D, Schulze-Osthoff K, Dorken B, Schmalz HG, Daniel PT, Henze G,. Piceatannol, a hydroxylated analog of the chemopreventive agent resveratrol, is a potent inducer of apoptosis in the lymphoma cell line BJAB and in primary, leukemic lymphoblasts. Leukemia 2001; 15: 1735-42.
25. Rudelius M, Pittaluga S, Nishizuka S, Pham TH, Fend F, Jaffe ES, Quintanilla-Martinez L, Raffeld M,. Constitutive activation of Akt contributes to the pathogenesis and survival of mantle cell lymphoma. Blood 2006; 108: 1668-76.
26. Dal Col J, Zancai P, Terrin L, et al. Distinct functional significance of Akt and mTOR constitutive activation in mantle cell lymphoma. Blood 2008; 111: 5142-51.
27. Asnaghi L, Calastretti A, Bevilacqua A, D'Agnano I, Gatti G, Canti G, Delia D, Capaccioli S, Nicolin A,. Bcl-2 phosphorylation and apoptosis activated by damaged microtubules require mTOR and are regulated by Akt. Oncogene 2004; 23: 5781-91.
28. Wu LX, La Rose J, Chen L, Neale C, Mak T, Okkenhaug K, Wange R, Rottapel R,. CD28 regulates the translation of Bcl-xL via the phosphatidylinositol 3-kinase/mammalian target of rapamycin pathway. J Immunol 2005; 174: 180-94.
29. Mills JR, Hippo Y, Robert F, et al. mTORC1 promotes survival through translational control of Mcl-1. Proc Natl Acad Sci USA 2008; 105: 10853-8.
30. Rizzatti EG, Falcao RP, Panepucci RA, Proto-Siqueira R, Anselmo-Lima WT, Okamoto OK, Zago MA,. Gene expression profiling of mantle cell lymphoma cells reveals aberrant expression of genes from the PI3K-AKT, WNT and TGFbeta signalling pathways. Br J Haematol 2005; 130: 516-26.
31. Smith SM, van Besien K, Karrison T, et al. Temsirolimus has activity in non-mantle cell non-Hodgkin's lymphoma subtypes: The University of Chicago phase II consortium. J Clin Oncol 2010; 28: 4740-6.
32. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM,. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005; 307: 1098-101.
33. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM,. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006; 22: 159-68.
34. Moser BA, Dennis PB, Pullen N, Pearson RB, Williamson NA, Wettenhall RE, Kozma SC, Thomas G,. Dual requirement for a newly identified phosphorylation site in p70s6k. Mol Cell Biol 1997; 17: 5648-55.
35. Saitoh M, Pullen N, Brennan P, Cantrell D, Dennis PB, Thomas G,. Regulation of an activated S6 kinase 1 variant reveals a novel mammalian target of rapamycin phosphorylation site. J Biol Chem 2002; 277: 20104-12.
36. Ayuso MI, Hernandez-Jimenez M, Martin ME, Salinas M, Alcazar A,. New hierarchical phosphorylation pathway of the translational repressor eIF4E-binding protein 1 (4E-BP1) in ischemia-reperfusion stress. J Biol Chem 2010; 285: 34355-63.
37. Tamburini J, Green AS, Bardet V, Chapuis N, Park S, Willems L, Uzunov M, Ifrah N, Dreyfus F, Lacombe C, Mayeux P, Bouscary D,. Protein synthesis is resistant to rapamycin and constitutes a promising therapeutic target in acute myeloid leukemia. Blood 2009; 114: 1618-27.
38. Chapuis N, Tamburini J, Green AS, et al. Dual inhibition of PI3K and mTORC1/2 signaling by NVP-BEZ235 as a new therapeutic strategy for acute myeloid leukemia. Clin Cancer Res 2010; 16: 5424-35.
39. Qi XJ, Wildey GM, Howe PH,. Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem 2006; 281: 813-23.
40. Brachmann SM, Hofmann I, Schnell C, Fritsch C, Wee S, Lane H, Wang S, Garcia-Echeverria C, Maira SM,. Specific apoptosis induction by the dual PI3K/mTor inhibitor NVP-BEZ235 in HER2 amplified and PIK3CA mutant breast cancer cells. Proc Natl Acad Sci USA 2009; 106: 22299-304.
41. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC,. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998; 282: 1318-21.
42. Wei LH, Kuo ML, Chen CA, Chou CH, Cheng WF, Chang MC, Su JL, Hsieh CY,. The anti-Apoptotic role of interleukin-6 in human cervical cancer is mediated by up-regulation of Mcl-1 through a PI 3-K/Akt pathway. Oncogene 2001; 20: 5799-809.
43. Zhai D, Jin C, Satterthwait AC, Reed JC,. Comparison of chemical inhibitors of antiapoptotic Bcl-2-family proteins. Cell Death Different 2006; 13: 1419-21.
44. van Delft MF, Wei AH, Mason KD, et al. The BH3 mimetic ABT-737 targets selective Bcl-2 proteins and efficiently induces apoptosis via Bak/Bax if Mcl-1 is neutralized. Cancer Cell 2006; 10: 389-99.
45. Touzeau C, Dousset C, Bodet L, Gomez-Bougie P, Bonnaud S, Moreau A, Moreau P, Pellat-Deceunynk C, Amiot M, Le Gouill S,. ABT-737 induces apoptosis in mantle cell lymphoma cells with a Bcl-2high/Mcl-1low profile and synergizes with other antineoplastic agents. Clin Cancer Res 2011; 17: 5973-81.
46. Perez-Galan P, Roue G, Villamor N, Campo E, Colomer D,. The BH3-mimetic GX15-070 synergizes with bortezomib in mantle cell lymphoma by enhancing Noxa-mediated activation of Bak. Blood 2007; 109: 4441-9.
47. Chen R, Chubb S, Cheng T, Hawtin RE, Gandhi V, Plunkett W,. Responses in mantle cell lymphoma cells to SNS-032 depend on the biological context of each cell line. Cancer Res 2010; 70: 6587-97.
48. Gomez-Bougie P, Wuilleme-Toumi S, Menoret E, Trichet V, Robillard N, Philippe M, Bataille R, Amiot M,. Noxa up-regulation and Mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res 2007; 67: 5418-24.
49. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence JC, Jr, Abraham RT,. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J 1996; 15: 5256-67.