Cap-translation inhibitor, 4EGI-1, restores sensitivity to ABT-737 apoptosis through cap-dependent and -independent mechanisms in chronic lymphocytic leukemia

Clinical Cancer Research

Volumn 19, Issue 12, 2013, Pages 3212-3223

  Willimott, Shaun ^a   Beck, Daniel ^a   Ahearne, Matthew J ^a,b   Adams, Victoria C ^a,b   Wagner, Simon D ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY HOSPITALS OF LEICESTER NHS TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 [4 (4' CHLORO 2 BIPHENYLYLMETHYL) 1 PIPERAZINYL] N [4 [3 DIMETHYLAMINO 1 (PHENYLTHIOMETHYL)PROPYLAMINO] 3 NITROBENZENESULFONYL]BENZAMIDE; 4EGI 1; ANTINEOPLASTIC AGENT; BCL2 RELATED PROTEIN A1; CAPPED RNA; CD40 LIGAND; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PHOSPHOTRANSFERASE; PIK 294; PROTEIN NOXA; RAPAMYCIN; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; DRUG SENSITIVITY; DRUG TARGETING; ENDOPLASMIC RETICULUM STRESS; FEMALE; HUMAN; HUMAN CELL; LEUKEMIA CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STROMA CELL; TUMOR MICROENVIRONMENT;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ELAFIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; NITRO COMPOUNDS; NITROPHENOLS; PIPERAZINES; PROTEIN BIOSYNTHESIS; SULFONAMIDES; THIAZOLES;

EID: 84879483218     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-2185     Document Type: Article

References (50)

1. Roberts AW, Seymour JF, Brown JR, Wierda WG, Kipps TJ, Khaw SL, et al. Substantial susceptibility of chronic lymphocytic leukemia to BCL2 inhibition: results of a phase I study of navitoclax in patients with relapsed or refractory disease. J Clin Oncol 2012;30:488-96.
2. Wilson WH, O'Connor OA, Czuczman MS, LaCasce AS, Gerecitano JF, Leonard JP, et al. Navitoclax, a targeted high-affinity inhibitor of BCL-2, in lymphoid malignancies: a phase 1 dose-escalation study of safety, pharmacokinetics, pharmacodynamics, and antitumour activity. Lancet Oncol 2010;11:1149-59.
3. Merino D, Khaw SL, Glaser SP, Anderson DJ, Belmont LD, Wong C, et al. Bcl-2, Bcl-x(L), and Bcl-w are not equivalent targets of ABT-737 and navitoclax (ABT-263) in lymphoid and leukemic cells. Blood 2012;119:5807-16.
4. Vogler M, Butterworth M, Majid A, Walewska RJ, Sun XM, Dyer MJ, et al. Concurrent up-regulation of BCL-XL and BCL2A1 induces approximately 1000-fold resistance to ABT-737 in chronic lymphocytic leukemia. Blood 2009;113:4403-13.
5. Yecies D, Carlson NE, Deng J, Letai A. Acquired resistance to ABT-737 in lymphoma cells that up-regulate MCL-1 and BFL-1. Blood 2010;115:3304-13.
6. Lucas KM, Mohana-Kumaran N, Lau D, Zhang XD, Hersey P, Huang DC, et al. Modulation of NOXA and MCL-1 as a strategy for sensitizing melanoma cells to the BH3-mimetic ABT-737. Clin Cancer Res 2012;18:783-95.
7. Tromp JM, Geest CR, Breij EC, Elias JA, van Laar J, Luijks DM, et al. Tipping the Noxa/Mcl-1 balance overcomes ABT-737 resistance in chronic lymphocytic leukemia. Clin Cancer Res 2012;18: 487-98.
8. Hallaert DY, Jaspers A, van Noesel CJ, van Oers MH, Kater AP, Eldering E. c-Abl kinase inhibitors overcome CD40-mediated drug resistance in CLL: implications for therapeutic targeting of chemoresistant niches. Blood 2008;112:5141-9.
9. Willimott S, Baou M, Naresh K, Wagner SD. CD154 induces a switch in pro-survival Bcl-2 family members in chronic lymphocytic leukaemia. Br J Haematol 2007;138: 721-32.
10. Smit LA, Hallaert DY, Spijker R, de Goeij B, Jaspers A, Kater AP, et al. Differential Noxa/Mcl-1 balance in peripheral versus lymph node chronic lymphocytic leukemia cells correlates with survival capacity. Blood 2007;109:1660-8.
11. Burger JA, Ghia P, Rosenwald A, Caligaris-Cappio F. The microenvironment in mature B-cell malignancies: a target for new treatment strategies. Blood 2009;114:3367-75.
12. Kater AP, Evers LM, Remmerswaal EB, Jaspers A, Oosterwijk MF, van Lier RA, et al. CD40 stimulation of B-cell chronic lymphocytic leukaemia cells enhances the anti-apoptotic profile, but also Bid expression and cells remain susceptible to autologous cytotoxic T-lymphocyte attack. Br J Haematol 2004;127:404-15.
13. Petlickovski A, Laurenti L, Li X, Marietti S, Chiusolo P, Sica S, et al. Sustained signaling through the B-cell receptor induces Mcl-1 and promotes survival of chronic lymphocytic leukemia B cells. Blood 2005;105:4820-7.
14. Silvera D, Formenti SC, Schneider RJ. Translational control in cancer. Nat Rev Cancer 2010;10:254-66.
15. Lazaris-Karatzas A, Montine KS, Sonenberg N. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 50 cap. Nature 1990;345:544-7.
16. Lazaris-Karatzas A, Smith MR, Frederickson RM, Jaramillo ML, Liu YL, Kung HF, et al. Ras mediates translation initiation factor 4E-induced malignant transformation. Genes Dev 1992;6:1631-42.
17. Le Quesne JP, Spriggs KA, Bushell M, Willis AE. Dysregulation of protein synthesis and disease. J Pathol 2010;220:140-51.
18. Lazaris-Karatzas A, Sonenberg N. The mRNA 5′ cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts. Mol Cell Biol 1992;12:1234-8.
19. Ruggero D, Montanaro L, Ma L, Xu W, Londei P, Cordon-Cardo C, et al. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 2004;10:484-6.
20. Wendel HG, De Stanchina E, Fridman JS, Malina A, Ray S, Kogan S, et al. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 2004;428:332-7.
21. Wang S, Rosenwald IB, Hutzler MJ, Pihan GA, Savas L, Chen JJ, et al. Expression of the eukaryotic translation initiation factors 4E and 2alpha in non-Hodgkin's lymphomas. Am J Pathol 1999;155:247-55.
22. Graff JR, Konicek BW, Vincent TM, Lynch RL, Monteith D, Weir SN, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest 2007;117:2638-48.
23. Hagner PR, Schneider A, Gartenhaus RB. Targeting the translational machinery as a novel treatment strategy for hematologic malignancies. Blood 2010;115:2127-35.
24. Assouline S, Culjkovic B, Cocolakis E, Rousseau C, Beslu N, Amri A, et al. Molecular targeting of the oncogene eIF4E in acute myeloid leukemia (AML): a proof-of-principle clinical trial with ribavirin. Blood 2009;114:257-60.
25. Chen R, Guo L, Chen Y, Jiang Y, Wierda WG, Plunkett W. Homoharringtonine reduced Mcl-1 expression and induced apoptosis in chronic lymphocytic leukemia. Blood 2010;117:156-64.
26. Lucas DM, Edwards RB, Lozanski G, West DA, Shin JD, Vargo MA, et al. The novel plant-derived agent silvestrol has B-cell selective activity in chronic lymphocytic leukemia and acute lymphoblastic leukemia in vitro and in vivo. Blood 2009;113:4656-66.
27. Fluckiger AC, Rossi JF, Bussel A, Bryon P, Banchereau J, Defrance T. Responsiveness of chronic lymphocytic leukemia B cells activated via surface Igs or CD40 to B-cell tropic factors. Blood 1992; 80:3173-81.
28. Moerke NJ, Aktas H, Chen H, Cantel S, Reibarkh MY, Fahmy A, et al. Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 2007;128:257-67.
29. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, et al. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 2005;307:935-9.
30. Chou TC, Talaly P. A simple generalized equation for the analysis of multiple inhibitions of Michaelis-Menten kinetic systems. J Biol Chem 1977;252:6438-42.
31. Shehata M, Schnabl S, Demirtas D, Hilgarth M, Hubmann R, Ponath E, et al. Reconstitution of PTEN activity byCK2inhibitors and interference with the PI3K/AKT cascade counteract the antiapoptotic effect of human stromal cells in chronic lymphocytic leukemia. Blood 2010;116:2513-21.
32. She QB, Halilovic E, Ye Q, Zhen W, Shirasawa S, Sasazuki T, et al. 4EBP1 is a key effector of the oncogenic activation of the AKT and ERK signaling pathways that integrates their function in tumors. Cancer Cell 2010;18:39-51.
33. Rousseau D, Kaspar R, Rosenwald I, Gehrke L, Sonenberg N. Translation initiation of ornithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc Natl Acad Sci U S A 1996;93:1065-70.
34. Descamps G, Gomez-Bougie P, Tamburini J, Green A, Bouscary D, Maiga S, et al. The cap-translation inhibitor 4EGI-1 induces apoptosis inmultiple myeloma through Noxa induction. Br J Cancer 2012;106:1660-7.
35. Wang Q, Mora-Jensen H, Weniger MA, Perez-Galan P, Wolford C, Hai T, et al. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci U S A 2009;106:2200-5.
36. Paterson A, Mockridge CI, Adams JE, Krysov S, Potter KN, Duncombe AS, et al. Mechanisms and clinical significance of BIM phosphorylation in chronic lymphocytic leukemia. Blood 2012;119:1726-36.
37. Pepper C, Lin TT, Pratt G, Hewamana S, Brennan P, Hiller L, et al. Mcl-1 expression has in vitro and in vivo significance in chronic lymphocytic leukemia and is associated with other poor prognostic markers. Blood 2008;112:3807-17.
38. Herishanu Y, Perez-Galan P, Liu D, Biancotto A, Pittaluga S, Vire B, et al. The lymph node microenvironment promotes B-cell receptor signaling, NF-kappaB activation, and tumor proliferation in chronic lymphocytic leukemia. Blood 2011;117:563-74.
39. Scielzo C, Apollonio B, Scarfo L, Janus A, Muzio M, Ten Hacken E, et al. The functional in vitro response to CD40 ligation reflects a different clinical outcome in patients with chronic lymphocytic leukemia. Leukemia 2011;25:1760-7.
40. Burger JA, Tsukada N, Burger M, Zvaifler NJ, Dell'Aquila M, Kipps TJ. Blood-derived nurse-like cells protect chronic lymphocytic leukemia B cells from spontaneous apoptosis through stromal cell-derived factor-1. Blood 2000;96:2655-63.
41. 1 arrest in cyclingB-CLL cells is associated with reduced expression of cyclin D3, cyclin E, cyclin A, and survivin. Blood 2003;101:278-85.
42. Kurtova AV, Balakrishnan K, Chen R, Ding W, Schnabl S, Quiroga MP, et al. Diverse marrow stromal cells protect CLL cells from spontaneous and drug-induced apoptosis: development of a reliable and reproducible system to assess stromal cell adhesion-mediated drug resistance. Blood 2009;114:4441-50.
43. Willimott S, Baou M, Huf S, Wagner SD. Separate cell culture conditions to promote proliferation or quiescent cell survival in chronic lymphocytic leukemia. Leuk Lymphoma 2007;48:1647-50.
44. Yoon A, Peng G, Brandenburger Y, Zollo O, Xu W, Rego E, et al. Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 2006;312:902-6.
45. Morales AA, Kurtoglu M, Matulis SM, Liu J, Siefker D, GutmanDM, et al. Distribution of Bim determines Mcl-1 dependence or codependence with Bcl-xL/Bcl-2 in Mcl-1-expressing myeloma cells. Blood 2012;118:1329-39.
46. Del Gaizo Moore V, Brown JR, Certo M, Love TM, Novina CD, Letai A. Chronic lymphocytic leukemia requires BCL2 to sequester prodeath BIM, explaining sensitivity to BCL2 antagonist ABT-737. J Clin Invest 2007;117:112-21.
47. van Delft MF, Wei AH, Mason KD, Vandenberg CJ, Chen L, Czabotar PE, 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.
48. Albershardt TC, Salerni BL, Soderquist RS, Bates DJP, Pletnev AA, Kisselev AF, et al. Multiple BH3 mimetics antagonize antiapoptotic MCL 1 protein by inducing the endoplasmic reticulum stress response and upregulating BH3-only protein NOXA. J Biol Chem 2011;286:24882-95.
49. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-29.
50. Rosati E, Sabatini R, Rampino G, De Falco F, Di Ianni M, Falzetti F, et al. Novel targets for endoplasmic reticulum stress-induced apoptosis in B-CLL. Blood 2010;116:2713-23.