GSI-I (Z-LLNle-CHO) inhibits γ-secretase and the proteosome to trigger cell death in precursor-B acute lymphoblastic leukemia

Leukemia

Volumn 25, Issue 7, 2011, Pages 1135-1146

  Meng, X ^a,b,e   Matlawska Wasowska, K ^a,b   Girodon, F ^a,c   Mazel, T ^a   Willman, C L ^a,b   Atlas, S ^a,b   Chen, I M ^a,b   Harvey, R C ^a,b   Hunger, S P ^d,f   Ness, S A ^a,b   Winter, S S ^a,b,g   Wilson, B S ^a,b  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

^c DIJON UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF IOWA   (United States)

^f Ergen Family Department in Pediatric Cancer   (United States)

^g UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

gamma secretase inhibitor; Notch; precursor B acute lymphoblastic leukemia; proteosome

Indexed keywords

ANTINEOPLASTIC AGENT; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; GAMMA SECRETASE INHIBITOR I; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; PROTEASOME; PROTEIN P53; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; B LYMPHOBLAST; CANCER CELL CULTURE; CANCER INHIBITION; CHILD; CONTROLLED STUDY; DRUG MECHANISM; DRUG RESPONSE; ENZYME INHIBITION; FEMALE; GENE TARGETING; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN TARGETING; RECEPTOR BLOCKING; RNA ANALYSIS; TUMOR XENOGRAFT; UNFOLDED PROTEIN RESPONSE;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; B-LYMPHOCYTES; CELL LINE, TUMOR; CHILD; COHORT STUDIES; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM PROTEINS; OLIGOPEPTIDES; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEASE INHIBITORS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, NOTCH; RISK; RNA, MESSENGER; RNA, NEOPLASM; SPECIFIC PATHOGEN-FREE ORGANISMS; TRANSCRIPTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS; YOUNG ADULT;

EID: 79960222619     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2011.50     Document Type: Article

References (43)

1. Real PJ, Tosello V, Palomero T, Castillo M, Hernando E, de Stanchina E et al. Gamma-secretase inhibitors reverse glucocorticoid resistance in T cell acute lymphoblastic leukemia. Nat Med 2009; 15: 50-58.
2. Horton TM, Pati D, Plon SE, Thompson PA, Bomgaars LR, Adamson PC et al. A phase 1 study of the proteasome inhibitor bortezomib in pediatric patients with refractory leukemia: a Children's Oncology Group study. Clin Cancer Res 2007; 13: 1516-1522. (Pubitemid 46450443)
3. Han J, Ma I, Hendzel MJ, Allalunis-Turner J. The cytotoxicity of gamma-secretase inhibitor I to breast cancer cells is mediated by proteasome inhibition, not by gamma-secretase inhibition. Breast Cancer Res 2009; 11: R57.
4. Kogoshi H, Sato T, Koyama T, Nara N, Tohda S. Gamma-secretase inhibitors suppress the growth of leukemia and lymphoma cells. Oncol Rep 2007; 18: 77-80.
5. Nefedova Y, Sullivan DM, Bolick SC, Dalton WS, Gabrilovich DI. Inhibition of Notch signaling induces apoptosis of myeloma cells and enhances sensitivity to chemotherapy. Blood 2008; 111: 2220-2229. (Pubitemid 351451536)
6. Rosati E, Sabatini R, Rampino G, Tabilio A, Di Ianni M, Fettucciari K et al. Constitutively activated Notch signaling is involved in survival and apoptosis resistance of B-CLL cells. Blood 2009; 113: 856-865.
7. Masuda K, Germeraad WT, Satoh R, Itoi M, Ikawa T, Minato N et al. Notch activation in thymic epithelial cells induces development of thymic microenvironments. Mol Immunol 2009; 46: 1756-1767.
8. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 2006; 7: 678-689. (Pubitemid 44268213)
9. Miele L, Miao H, Nickoloff BJ. NOTCH signaling as a novel cancer therapeutic target. Curr Cancer Drug Targets 2006; 6: 313-323. (Pubitemid 43961866)
10. Ehebauer M, Hayward P, Arias AM. Notch, a universal arbiter of cell fate decisions. Science 2006; 314: 1414-1415. (Pubitemid 44871939)
11. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, Margolin A et al. NOTCH1 directly regulates c-MYC and activates a feedforward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci USA 2006; 103: 18261-18266. (Pubitemid 44871646)
12. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, Wai C et al. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev 2006; 20: 2096-2109. (Pubitemid 44157460)
13. Mungamuri SK, Yang X, Thor AD, Somasundaram K. Survival signaling by Notch1: mammalian target of rapamycin (mTOR)-dependent inhibition of p53. Cancer Res 2006; 66: 4715-4724.
14. Bheeshmachar G, Purushotaman D, Sade H, Gunasekharan V, Rangarajan A, Sarin A. Evidence for a role for notch signaling in the cytokine-dependent survival of activated T cells. J Immunol 2006; 177: 5041-5050. (Pubitemid 44527574)
15. Bianchi G, Oliva L, Cascio P, Pengo N, Fontana F, Cerruti F et al. The proteasome load versus capacity balance determines apoptotic sensitivity of multiple myeloma cells to proteasome inhibition. Blood 2009; 113: 3040-3049.
16. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article3.
17. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001; 98: 5116-5121. (Pubitemid 32397092)
18. Pui CH. T cell acute lymphoblastic leukemia: NOTCHing the way toward a better treatment outcome. Cancer Cell 2009; 15: 85-87.
19. Mungrue IN, Pagnon J, Kohannim O, Gargalovic PS, Lusis AJ. CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J Immunol 2009; 182: 466-476.
20. Pendino F, Nguyen E, Jonassen I, Dysvik B, Azouz A, Lanotte M et al. Functional involvement of RINF, retinoid-inducible nuclear factor (CXXC5), in normal and tumoral human myelopoiesis. Blood 2009; 113: 3172-3181.
21. Johnson NA, Boyle M, Bashashati A, Leach S, Brooks-Wilson A, Sehn LH et al. Diffuse large B-cell lymphoma: reduced CD20 expression is associated with an inferior survival. Blood 2009; 113: 3773-3780.
22. Birkenkamp KU, Coffer PJ. Regulation of cell survival and proliferation by the FOXO (Forkhead box, class O) subfamily of Forkhead transcription factors. Biochem Soc Trans 2003; 31 (Part 1): 292-297. (Pubitemid 36241447)
23. Essafi A, Fernandez de Mattos S, Hassen YA, Soeiro I, Mufti GJ, Thomas NS et al. Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene 2005; 24: 2317-2329. (Pubitemid 40546691)
24. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J Exp Med 2007; 204: 1813-1824. (Pubitemid 47236319)
25. Cario G, Stanulla M, Fine BM, Teuffel O, Neuhoff NV, Schrauder A et al. Distinct gene expression profiles determine molecular treatment response in childhood acute lymphoblastic leukemia. Blood 2005; 105: 821-826. (Pubitemid 40070770)
26. Gridley T. Kick it up a Notch: NOTCH1 activation in T-ALL. Cancer Cell 2004; 6: 431-432. (Pubitemid 39469977)
27. Zweidler-McKay PA, He Y, Xu L, Rodriguez CG, Karnell FG, Carpenter AC et al. Notch signaling is a potent inducer of growth arrest and apoptosis in a wide range of B-cell malignancies. Blood 2005; 106: 3898-3906. (Pubitemid 41739030)
28. He Y, Pear WS. Notch signalling in B cells. Semin Cell Dev Biol 2003; 14: 135-142. (Pubitemid 36315880)
29. Tohda S, Sato T, Kogoshi H, Fu L, Sakano S, Nara N. Establishment of a novel B-cell lymphoma cell line with suppressed growth by gamma-secretase inhibitors. Leuk Res 2006; 30: 1385-1390. (Pubitemid 44307330)
30. Houde C, Li Y, Song L, Barton K, Zhang Q, Godwin J et al. Overexpression of the NOTCH ligand JAG2 in malignant plasma cells from multiple myeloma patients and cell lines. Blood 2004; 104: 3697-3704. (Pubitemid 39564447)
31. Shin DM, Shaffer DJ, Wang H, Roopenian DC, Morse III HC. NOTCH is part of the transcriptional network regulating cell growth and survival in mouse plasmacytomas. Cancer Res 2008; 68: 9202-9211.
32. Weiser KC, Liu B, Hansen GM, Skapura D, Hentges KE, Yarlagadda S et al. Retroviral insertions in the VISION database identify molecular pathways in mouse lymphoid leukemia and lymphoma. Mamm Genome 2007; 18: 709-722. (Pubitemid 350112421)
33. Davidson MB, Thakkar S, Hix JK, Bhandarkar ND, Wong A, Schreiber MJ. Pathophysiology, clinical consequences, and treatment of tumor lysis syndrome. Am J Med 2004; 116: 546-554. (Pubitemid 38452647)
34. Dohda T, Maljukova A, Liu L, Heyman M, Grander D, Brodin D et al. Notch signaling induces SKP2 expression and promotes reduction of p27Kip1 in T-cell acute lymphoblastic leukemia cell lines. Exp Cell Res 2007; 313: 3141-3152. (Pubitemid 47161022)
35. Katayama T, Imaizumi K, Sato N, Miyoshi K, Kudo T, Hitomi J et al. Presenilin-1 mutations downregulate the signalling pathway of the unfolded-protein response. Nat Cell Biol 1999; 1: 479-485. (Pubitemid 129503667)
36. Curry CL, Reed LL, Nickoloff BJ, Miele L, Foreman KE. Notchindependent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab Invest 2006; 86: 842-852. (Pubitemid 44100482)
37. Osipo C, Golde TE, Osborne BA, Miele LA. Off the beaten pathway: the complex cross talk between Notch and NF-kappaB. Lab Invest 2008; 88: 11-17.
38. Aguilera C, Hoya-Arias R, Haegeman G, Espinosa L, Bigas A. Recruitment of IkappaBalpha to the hes1 promoter is associated with transcriptional repression. Proc Natl Acad Sci USA 2004; 101: 16537-16542. (Pubitemid 39557748)
39. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, Anderson GA et al. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 2010; 465: 86-90.
40. Miller CP, Rudra S, Keating MJ, Wierda WG, Palladino M, Chandra J. Caspase-8 dependent histone acetylation by a novel proteasome inhibitor, NPI-0052: a mechanism for synergy in leukemia cells. Blood 2009; 113: 4289-4299.
41. Schulz JB, Bremen D, Reed JC, Lommatzsch J, Takayama S, Wullner U et al. Cooperative interception of neuronal apoptosis by BCL-2 and BAG-1 expression: prevention of caspase activation and reduced production of reactive oxygen species. J Neurochem 1997; 69: 2075-2086. (Pubitemid 27452755)
42. Perumalsamy LR, Nagala M, Sarin A. Notch-activated signaling cascade interacts with mitochondrial remodeling proteins to regulate cell survival. Proc Natl Acad Sci USA 2010; 107: 6882-6887.
43. Cullion K, Draheim KM, Hermance N, Tammam J, Sharma VM, Ware C et al. Targeting the Notch1 and mTOR pathways in a mouse T-ALL model. Blood 2009; 113: 6172-6181.