Proteasome inhibitors exert cytotoxicity and increase chemosensitivity via transcriptional repression of Notch1 in T-cell acute lymphoblastic leukemia

Leukemia

Volumn 28, Issue 6, 2014, Pages 1216-1226

  Koyama, D ^a   Kikuchi, J ^a   Hiraoka, N ^a   Wada, T ^a   Kurosawa, H ^b   Chiba, S ^c   Furukawa, Y ^a  

^a JICHI MEDICAL UNIVERSITY   (Japan)

^b DOKKYO MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

chemosensitization; Notch1; proteasome inhibitor; Sp1; T cell acute lymphoblastic leukemia

Indexed keywords

BORTEZOMIB; CYCLOPHOSPHAMIDE; DEXAMETHASONE; DOXORUBICIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH1 RECEPTOR; PROTEASOME INHIBITOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR RUNX3; TRANSCRIPTION FACTOR SP1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CHEMOSENSITIVITY; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYELOMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL LEUKEMIA; TUMOR XENOGRAFT;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; BORONIC ACIDS; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CORE BINDING FACTOR ALPHA 3 SUBUNIT; DRUG RESISTANCE, NEOPLASM; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NF-KAPPA B; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEASOME INHIBITORS; PYRAZINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR CELLS, CULTURED;

EID: 84902103433     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.366     Document Type: Article

References (50)

1. Pui CH, Evans WE. Treatment of acute lymphoblastic leukemia. N Engl J Med 2006; 354: 166-178. (Pubitemid 43076714)
2. Weng AP, Ferrando AA, Lee W, Morris JP, Silverman LB, Sanchez-Irizarry C et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004; 306: 269-271. (Pubitemid 39336870)
3. Callens C, Baleydier F, Lengline E, Abdelali RB, Petit A, Villarese P et al. Clinical impact of NOTCH1 and/or FBXW7 mutations, FLASH deletion, and TCR status in pediatric T-cell lymphoblastic lymphoma. J Clin Oncol 2012; 30: 1966-1973.
4. Jenkinson S, Koo K, Mansour MR, Goulden N, Vore A, Mitchell C et al. Impact of NOTCH1/FBXW7 mutations on outcome in pediatric T-cell acute lymphoblastic leukemia patients treated on the MRC UKALL 2003 trial. Leukemia 2013; 27: 41-47.
5. Pear WS, Aster JC, Scott ML, Hasserjian RP, Soffer B, Sklar J et al. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J Exp Med 1996; 183: 2283-2291. (Pubitemid 26158919)
6. Real PJ, Tosello V, Palomero T, Castillo M, Hernando E, de Stanchina E et al. g-Secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat Med 2009; 15: 50-58.
7. Wang Z, Li Y, Ahmad A, Azmi AS, Banerjee S, Kong D et al. Targeting Notch signaling pathway to overcome drug resistance for cancer therapy. Biochim Biophys Acta 2010; 1806: 258-267.
8. Annino L, Vegna ML, Camera A, Specchia G, Visani G, Floritoni G et al. Treatment of adult acute lymphoblastic leukemia (ALL): Long-Term follow-up of the GIMEMA ALL 0288 randomized study. Blood 2002; 99: 863-871. (Pubitemid 34525547)
9. Cialfi S, Palermo R, Manca S, Checquolo S, Bellavia D, Pelullo M et al. Glucocorticoid sensitivity of T-cell lymphoblastic leukemia/lymphoma is associated with glucocorticoid receptor-mediated inhibition of Notch1 expression. Leukemia 2013; 27: 485-488.
10. Koch U, Radtke F. Notch in T-ALL: New players in a complex disease. Trends Immunol 2011; 32: 434-442.
11. Lobry C, Oh P, Aifantis I. Oncogenic and tumor suppressor functions of Notch in cancer: It's NOTCH what you think. J Exp Med 2011; 208: 1931-1935.
12. Sanchez-Irizarry C, Carpenter AC, Weng AP, Pear WS, Aster JC, Blacklow SC. Notch subunit heterodimerization and prevention of ligand independent proteolytic activation depend, respectively, on a novel domain and the LNR repeats. Mol Cell Biol 2004; 24: 9265-9273. (Pubitemid 39391665)
13. Osipo C, Patel P, Rizzo P, Clementtz AG, Hao L, Golde TE et al. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a g-secretase inhibitor. Oncogene 2008; 27: 5019-5032.
14. Akiyoshi T, Nakamura M, Yanai K, Nagai S, Wada J, Koga K et al. g-Secretase inhibitors enhance taxane-induced mitotic arrest and apoptosis in colon cancer cells. Gastroenterology 2008; 134: 131-144. (Pubitemid 350309314)
15. Meng RD, Shelton CC, Li Y-M, Qin L-X, Notterman D, Paty PB et al. g-Secretase inhibitors abrogate oxaliplatin-induced activation of the Notch-1 signaling pathway in colon cancer cells resulting in enhanced chemosensitivity. Cancer Res 2009; 69: 573-582.
16. Masuda S, Kumano K, Suzuki T, Tomita T, Iwatsubo T, Natsugari H et al. Dual antitumor mechanisms of Notch signaling inhibitor in a T-cell acute lymphoblastic leukemia xenograft model. Cancer Sci 2009; 100: 2444-2450.
17. Krop I, Demuth T, Guthrie T, Wen PY, Mason WP, Chinnaiyan P et al. Phase I pharmacologic and pharmacodynamic study of the gamma secretase (Notch) inhibitor MK-0752 in adult patients with advanced solid tumors. J Clin Oncol 2012; 30: 2307-2313.
18. Tolcher AW, Messersmith WA, Mikulski SM, Papadopoulos KP, Kwak EL, Gibbon DG et al. Phase I study of RO4929097, a gamma secretase inhibitor of Notch signaling, in patients with refractory metastatic or locally advanced solid tumors. J Clin Oncol 2012; 30: 2348-2353.
19. Li K, Li Y, Wu W, Gordon WR, Chang DW, Lu M et al. Modulation of Notch signaling by antibodies specific for the extracellular negative regulatory region of NOTCH3. J Biol Chem 2008; 283: 8046-8054.
20. Wu Y, Cain-Hom C, Choy L, Hagenbeek TJ, de Leon GP, Chen Y et al. Therapeutic antibody targeting of individual Notch receptors. Nature 2010; 464: 1052-1057.
21. Aste-Ame'zaga M, Zhang N, Lineberger JE, Arnold BA, Toner TJ, Gu M et al. Characterization of Notch1 antibodies that inhibit signaling of both normal and mutated Notch1 receptors. PLoS One 2010; 5: E9094.
22. Moreau P, Richardson PG, Cavo M, Orlowski RZ, San Miguel JF, Palumbo A et al. Proteasome inhibitors in multiple myeloma: 10 years later. Blood 2012; 120: 947-959.
23. Hideshima T, Ikeda H, Chauhan D, Okawa Y, Raje N, Podar K et al. Bortezomib induces canonical nuclear factor-kB activation in multiple myeloma cells. Blood 2009; 114: 1046-1052.
24. Kikuchi J, Wada T, Shimizu R, Izumi T, Akutsu M, Mitsunaga K et al. Histone deacetylases are critical targets of bortezomib-induced cytotoxicity in multiple myeloma. Blood 2010; 116: 406-417.
25. Espinosa L, Cathelin S, D'Altri T, Trimarchi T, Statnikov A, Guiu J et al. The Notch/Hes1 pathway sustains NF-kB activation through CYLD repression in T cell leukemia. Cancer Cell 2010; 18: 268-281.
26. D'Altri T, Gonzalez J, Aifantis I, Espinosa L, Bigas A. Hes1 expression and CYLD repression are essential events downstream of Notch1 in T-cell leukemia. Cell Cycle 2011; 10: 1031-1036.
27. Moreno DA, Scridel CA, Cortez MAA, de Paula Queiroz R, Valera ET, da Silva Silveira V et al. Differential expression of HDAC3, HDAC7 and HDAC9 is associated with prognosis and survival in childhood acute lymphoblastic leukaemia. Br J Haematol 2010; 150: 665-673.
28. Aldana-Masangkay GI, Rodriguez-Gonzalez A, Lin T, Ikeda AK, Hsieh Y-T, Kim Y-M et al. Tubacin suppresses proliferation and induces apoptosis of acute lymphoblastic leukemia cells. Leuk Lymphoma 2011; 52: 1544-1555.
29. Huang C, Hu X, Wang L, LüS, Cheng H, Song X et al. Bortezomib suppresses the growth of leukemia cells with Notch1 overexpression in vivo and in vitro. Cancer Chemother Pharmacol 2012; 70: 801-809.
30. Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 2010; 70: 440-446.
31. Wada T, Kikuchi J, Furukawa Y. Histone deacetylase 1 enhances microRNA processing via deacetylation of DGCR8. EMBO Rep 2012; 13: 142-149.
32. Renard P, Ernest I, Houbion A, Art M, Le Calvez H, Raes M et al. Development of a sensitive multi-well colorimetric assay for active NFkB. Nucleic Acid Res 2001; 29: E21.
33. Kikuchi J, Shibayama N, Yamada S, Wada T, Nobuyoshi M, Izumi T et al. Homopiperazine derivatives as a novel class of proteasome inhibitors with a unique mode of proteasome binding. PLoS One 2013; 8: E61649.
34. Kikuchi J, Yamada S, Koyama D, Wada T, Nobuyoshi M, Izumi T et al. The novel orally active proteasome inhibitor K-7174 exerts anti-myeloma activity in vitro and in vivo by down-regulating the expression of class I histone deacetylases. J Biol Chem 2013; 288: 25593-25602.
35. Nakahara F, Sakata-Yanagimoto M, Komeno Y, Kato N, Uchida T, Haraguchi K et al. Hes1 immortalizes committed progenitors and plays a role in blast crisis transition in chronic myelogenous leukemia. Blood 2010; 115: 2872-2881.
36. van Hamburg JP, de Bruijn MJW, Dingjan GM, Beverloo HB, Diepstraten H, Ling K-W et al. Cooperation of Gata3 c-Myc and Notch in malignant transformation of double positive thymocytes. Mol. Immunol 2008; 45: 3085-3095.
37. Giambra V, Jenkins CR, Wang H, Lam SH, Shevchuk OO, Nemirovsky O et al. NOTCH1 promotes T cell leukemia-initiating activity by RUNX-mediated regulation of PKC-y and reactive oxygen species. Nat Med 2012; 18: 1693-1698.
38. Chang P-Y, Draheim K, Kelliher MA, Miyamoto S. NFKB1 is a direct target of the TAL1 oncoprotein in human T leukemia cells. Cancer Res 2006; 66: 6009-6013.
39. Vilimas T, Mascarenhas J, Palomero T, Mandal M, Buonamici S, Meng F et al. Targeting the NF-kB signaling pathway in Notch1-induced T-cell leukemia. Nat Med 2007; 13: 70-77. (Pubitemid 46067388)
40. Lambertini C, Pantano S, Dotto GP. Differential control of Notch1 gene transcription by Klf4 and Sp3 transcription factors in normal versus cancerderived keratinocytes. PLoS One 2010; 5: E10369.
41. Blume SW, Snyder RC, Ray R, Thomas S, Koller CA, Miller DM. Mithramycin inhibits SP1 binding and selectively inhibits transcriptional activity of the dihydrofolate reductase gene in vitro and in vivo. J Clin Invest 1991; 88: 1613-1621.
42. Deacon K, Onion D, Kumari R, Watson SA, Knox AJ. Elevated SP-1 transcription factor expression and activity drives basal and hypoxia-induced vascular endothelial growth factor (VEGF) expression in non-small cell lung cancer. J Biol Chem 2012; 287: 39967-39981.
43. Gu L, Findley HW, Zhou M. MDM2 induces NF-kB/p65 expression transcriptionally through Sp1-binding sites: A novel, p53-independent role of MDM2 in doxorubicin resistance in acute lymphoblastic leukemia. Blood 2002; 99: 3367-3375. (Pubitemid 34525318)
44. Cohen LY, Bourbonniere M, Sabbagh L, Bouchard A, Chew T, Jeannequin P et al. Notch1 antiapoptotic activity is abrogated by caspase cleavage in dying T lymphocytes. Cell Death Differ 2005; 12: 243-254. (Pubitemid 40360948)
45. Zheng L, Saunders CA, Sorensen EB, Waxmonsky NC, Conner SD. Notch signaling from the endosome requires a conserved dileucine motif. Mol Biol Cell 2013; 24: 297-307.
46. Wang YT, Yang WB, Chang WC, Hung JJ. Interplay of posttranslational modifications in Sp1 mediates Sp1 stability during cell cycle progression. J Mol Biol 2011; 414: 1-14.
47. Shin HM, Minter LM, Cho OH, Gottipati S, Fauq AH, Golde TE et al. Notch1 augments NF-kB activity by facilitating its nuclear retention. EMBO J 2006; 25: 129-138. (Pubitemid 43077302)
48. Hideshima T, Chauhan D, Kiziltepe T, Ikeda H, Okawa Y, Podar K et al. Biologic sequelae of IkB kinase (IKK) inhibition in multiple myeloma: Therapeutic implications. Blood 2009; 113: 5228-5236.
49. Love'n J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013; 153: 320-334.
50. Fulciniti M, Amin S, Nanjappa P, Rodig S, Prabhala R, Li C et al. Significant biological role of Sp1 transactivation in multiple myeloma. Clin Cancer Res 2011; 17: 6500-6509.