Translation initiation complex eIF4F is a therapeutic target for dual mTOR kinase inhibitors in non-Hodgkin lymphoma

Oncotarget

Volumn 6, Issue 11, 2015, Pages 9488-9501

  Demosthenous, Christos ^a   Han, Jing Jing ^a   Stenson, Mary J ^a   Maurer, Matthew J ^a   Wellik, Linda E ^a   Link, Brian ^b   Hege, Kristen ^c   Dogan, Ahmet ^d   Sotomayor, Eduardo ^e   Witzig, Thomas ^a   Gupta, Mamta ^a  

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c CELGENE CORPORATION   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

eIF4E; CC214 1; Dual mTOR inhibitors; Lymphoma; Translation initiation complex

Indexed keywords

CC 214 1; CYCLIN D3; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4F; INITIATION FACTOR 4G; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MYC PROTEIN; PROTEIN MCL 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; 6-(4-(1H-1,2,4-TRIAZOL-3-YL)PHENYL)-1-(2-(TETRAHYDRO-2H-PYRAN-4-YL)ETHYL)-1H-IMIDAZO(4,5-B)PYRAZIN-2(3H)-ONE; CAPPED RNA; CCND3 PROTEIN, HUMAN; EIF4EBP1 PROTEIN, HUMAN; EIF4G1 PROTEIN, HUMAN; IMIDAZOLE DERIVATIVE; MTOR PROTEIN, HUMAN; MYC PROTEIN, HUMAN; PHOSPHOPROTEIN; PROTEIN KINASE INHIBITOR; PYRAZINE DERIVATIVE; RNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TARGET OF RAPAMYCIN KINASE; TUMOR PROTEIN;

ADULT; ARTICLE; CAP DEPENDENT PROTEIN TRANSLATION; CELL GROWTH; COLONY FORMATION; CONTROLLED STUDY; EVENT FREE SURVIVAL; FEMALE; HUMAN; HUMAN TISSUE; LARGE CELL LYMPHOMA; MAJOR CLINICAL STUDY; MALE; MANTLE CELL LYMPHOMA CELL; NONHODGKIN LYMPHOMA; PROTEIN MODIFICATION; RNA TRANSLATION; TRANSLATION REGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; MOLECULARLY TARGETED THERAPY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; PROTEIN SYNTHESIS; RNA INTERFERENCE; TUMOR CELL LINE; TUMOR INVASION; TUMOR STEM CELL ASSAY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; CYCLIN D3; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTOR-4G; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; IMIDAZOLES; LYMPHOMA, LARGE B-CELL, DIFFUSE; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-MYC; PYRAZINES; RNA CAPS; RNA INTERFERENCE; RNA, NEOPLASM; RNA, SMALL INTERFERING; TOR SERINE-THREONINE KINASES; TUMOR STEM CELL ASSAY;

EID: 84928735563     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3378     Document Type: Article

References (41)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64:9-29.
2. Grzmil M, Hemmings BA. Translation regulation as a therapeutic target in cancer. Cancer Res. 2012; 72:3891-3900.
3. Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nat Rev Cancer. 2010; 10:254-266.
4. Li BD, McDonald JC, Nassar R, De Benedetti A. Clinical outcome in stage I to III breast carcinoma and eIF4E overexpression. Ann Surg. 1998; 227:756-756l. discussion 761-753.
5. Graff JR, Konicek BW, Lynch RL, Dumstorf CA, Dowless MS, McNulty AM, Parsons SH, Brail LH, Colligan BM, Koop JW, Hurst BM, Deddens JA, Neubauer BL, Stancato LF, Carter HW, Douglass LE, et al. eIF4E activation is commonly elevated in advanced human prostate cancers and significantly related to reduced patient survival. Cancer research. 2009; 69:3866-3873.
6. Issaenko OA, Bitterman PB, Polunovsky VA, Dahlberg PS. Cap-dependent mRNA translation and the ubiquitin-proteasome system cooperate to promote ERBB2-dependent esophageal cancer phenotype. Cancer gene therapy. 2012; 19:609-618.
7. Avdulov S, Li S, Michalek V, Burrichter D, Peterson M, Perlman DM, Manivel JC, Sonenberg N, Yee D, Bitterman PB, Polunovsky VA. Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer cell. 2004; 5:553-563.
8. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes & development. 2004; 18:1926-1945.
9. Witzig TE, Geyer SM, Ghobrial I, Inwards DJ, Fonseca R, Kurtin P, Ansell SM, Luyun R, Flynn PJ, Morton RF, Dakhil SR, Gross H, Kaufmann SH. Phase II trial of singleagent temsirolimus (CCI-779) for relapsed mantle cell lymphoma. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2005; 23:5347-5356.
10. Hess G, Herbrecht R, Romaguera J, Verhoef G, Crump M, Gisselbrecht C, Laurell A, Offner F, Strahs A, Berkenblit A, Hanushevsky O, Clancy J, Hewes B, Moore L, Coiffier B. 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; 27:3822-3829.
11. Gupta M, Ansell SM, Novak AJ, Kumar S, Kaufmann SH, Witzig TE. Inhibition of histone deacetylase overcomes rapamycin-mediated resistance in diffuse large B-cell lymphoma by inhibiting Akt signaling through mTORC2. Blood. 2009; 114:2926-2935.
12. Zaytseva YY, Valentino JD, Gulhati P, Evers BM. mTOR inhibitors in cancer therapy. Cancer Lett. 2012; 319:1-7.
13. Gupta M, Hendrickson AE, Yun SS, Han JJ, Schneider PA, Koh BD, Stenson MJ, Wellik LE, Shing JC, Peterson KL, Flatten KS, Hess AD, Smith BD, Karp JE, Barr S, Witzig TE, et al. Dual mTORC1/mTORC2 inhibition diminishes Akt activation and induces Puma-dependent apoptosis in lymphoid malignancies. Blood. 2012; 119:476-487.
14. Culjkovic B, Topisirovic I, Borden KL. Controlling gene expression through RNA regulons: the role of the eukaryotic translation initiation factor eIF4E. Cell Cycle. 2007; 6:65-69.
15. De Benedetti A, Harris AL. eIF4E expression in tumors: its possible role in progression of malignancies. Int J Biochem Cell Biol. 1999; 31:59-72.
16. Rosenwald IB, Chen JJ, Wang S, Savas L, London IM, Pullman J. Upregulation of protein synthesis initiation factor eIF-4E is an early event during colon carcinogenesis. Oncogene. 1999; 18:2507-2517.
17. Wang S, Rosenwald IB, Hutzler MJ, Pihan GA, Savas L, Chen JJ, Woda BA. Expression of the eukaryotic translation initiation factors 4E and 2alpha in non-Hodgkin's lymphomas. The American journal of pathology. 1999; 155:247-255.
18. Anthony B, Carter P, De Benedetti A. Overexpression of the proto-oncogene/translation factor 4E in breast-carcinoma cell lines. Int J Cancer. 1996; 65:858-863.
19. Flowers A, Chu QD, Panu L, Meschonat C, Caldito G, Lowery-Nordberg M, Li BD. Eukaryotic initiation factor 4E overexpression in triple-negative breast cancer predicts a worse outcome. Surgery. 2009; 146:220-226.
20. Kodali D, Rawal A, Ninan MJ, Patel MR, Mesa H, Knapp D, Schnitzer B, Kratzke RA, Gupta P. Expression and phosphorylation of eukaryotic translation initiation factor 4E binding protein 1 in B-cell lymphomas and reactive lymphoid tissues. Archives of pathology & laboratory medicine. 2011; 135:365-371.
21. Ansell SM, Tang H, Kurtin PJ, Koenig PA, Inwards DJ, Shah K, Ziesmer SC, Feldman AL, Rao R, Gupta M, Erlichman C, Witzig TE. Temsirolimus and rituximab in patients with relapsed or refractory mantle cell lymphoma:a phase 2 study. Lancet Oncol. 2011; 12:361-368.
22. Graff JR, Konicek BW, Vincent TM, Lynch RL, Monteith D, Weir SN, Schwier P, Capen A, GoodeRL, Dowless MS, Chen Y, Zhang H, Sissons S, Cox K, McNulty AM, Parsons SH, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. The Journal of clinical investigation. 2007; 117:2638-2648.
23. Kimball SR, Horetsky RL, Jefferson LS. Implication of eIF2B rather than eIF4E in the regulation of global protein synthesis by amino acids in L6 myoblasts. J Biol Chem. 1998; 273:30945-30953.
24. Yanagiya A, Suyama E, Adachi H, Svitkin YV, Aza-Blanc P, Imataka H, Mikami S, Martineau Y, Ronai ZA, Sonenberg N. Translational homeostasis via the mRNA capbinding protein, eIF4E. Molecular cell. 2012; 46:847-858.
25. Li Y, Fan S, Koo J, Yue P, Chen ZG, Owonikoko TK, Ramalingam SS, Khuri FR, Sun SY. Elevated expression of eukaryotic translation initiation factor 4E is associated with proliferation, invasion and acquired resistance to erlotinib in lung cancer. Cancer biology & therapy. 2012; 13:272-280.
26. Soni A, Akcakanat A, Singh G, Luyimbazi D, Zheng Y, Kim D, Gonzalez-Angulo A, Meric-Bernstam F. eIF4E knockdown decreases breast cancer cell growth without activating Akt signaling. Mol Cancer Ther. 2008; 7:1782-1788.
27. Kentsis A, Topisirovic I, Culjkovic B, Shao L, Borden KL. Ribavirin suppresses eIF4E-mediated oncogenic transformation by physical mimicry of the 7-methyl guanosine mRNA cap. Proc Natl Acad Sci U S A. 2004; 101:18105-18110.
28. Assouline S, Culjkovic B, Cocolakis E, Rousseau C, Beslu N, Amri A, Caplan S, Leber B, Roy DC, Miller WH Jr., Borden KL. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood. 2009; 114:257-260.
29. Ma XM, Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol. 2009; 10:307-318.
30. Dutton A, Reynolds GM, Dawson CW, Young LS, Murray PG. Constitutive activation of phosphatidyl-inositide 3 kinase contributes to the survival of Hodgkin's lymphoma cells through a mechanism involving Akt kinase and mTOR. The Journal of pathology. 2005; 205:498-506.
31. Wlodarski P, Kasprzycka M, Liu X, Marzec M, Robertson ES, Slupianek A, Wasik MA. Activation of mammalian target of rapamycin in transformed B lymphocytes is nutrient dependent but independent of Akt, mitogen-activated protein kinase/extracellular signal-regulated kinase kinase, insulin growth factor-I, and serum. Cancer research. 2005; 65:7800-7808.
32. Wall M, Poortinga G, Hannan KM, Pearson RB, Hannan RD, McArthur GA. Translational control of c-MYC by rapamycin promotes terminal myeloid differentiation. Blood. 2008; 112:2305-2317.
33. Mills JR, Hippo Y, Robert F, Chen SM, Malina A, Lin CJ, Trojahn U, Wendel HG, Charest A, Bronson RT, Kogan SC, Nadon R, Housman DE, Lowe SW, Pelletier J. mTORC1 promotes survival through translational control of Mcl-1. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105:10853-10858.
34. Mortensen DS, Sapienza J, Lee BG, Perrin-Ninkovic SM, Harris R, Shevlin G, Parnes JS, Whitefield B, Hickman M, Khambatta G, Bisonette RR, Peng S, Gamez JC, Leisten J, Narla RK, Fultz KE, et al. Use of core modification in the discovery of CC214-2, an orally available, selective inhibitor of mTOR kinase. Bioorg Med Chem Lett. 2013; 23:1588-1591.
35. Hu G, Witzig TE, Gupta M. A novel missense (M206K) STAT3 mutation in diffuse large B cell lymphoma deregulates STAT3 signaling. PLoS One. 2013; 8:e67851.
36. Bert AG, Grepin R, Vadas MA, Goodall GJ. Assessing IRES activity in the HIF-1alpha and other cellular 5′ UTRs. Rna. 2006; 12:1074-1083.
37. Gupta M, Dillon SR, Ziesmer SC, Feldman AL, Witzig TE, Ansell SM, Cerhan JR, Novak AJ. A proliferation-inducing ligand mediates follicular lymphoma B-cell proliferation and cyclin D1 expression through phosphatidylinositol 3-kinase-regulated mammalian target of rapamycin activation. Blood. 2009; 113:5206-5216.
38. Gumireddy K, Li A, Yan J, Setoyama T, Johannes GJ, Orom UA, Tchou J, Liu Q, Zhang L, Speicher DW, Calin GA, Huang Q. Identification of a long non-coding RNA-associated RNP complex regulating metastasis at the translational step. Embo J. 2013; 32:2672-2684.
39. Johannes G, Sarnow P. Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIFG conferred by internal ribosome entry sites. RNA. 1998; 4:1500-1513.
40. Hans CP, Weisenburger DD, Greiner TC, Gascoyne RD, Delabie J, Ott G, Muller-Hermelink HK, Campo E, Braziel RM, Jaffe ES, Pan Z, Farinha P, Smith LM, Falini B, Banham AH, Rosenwald A, et al. Confirmation of the molecular classification of diffuse large B-cell lymphoma by immunohistochemistry using a tissue microarray. Blood. 2004; 103:275-282.
41. Gupta M, Maurer MJ, Wellik LE, Law ME, Han JJ, Ozsan N, Micallef IN, Dogan A, Witzig TE. Expression of Myc, but not pSTAT3, is an adverse prognostic factor for diffuse large B-cell lymphoma treated with epratuzumab/R-CHOP. Blood. 2012; 120:4400-4406.