The novel gamma secretase inhibitor RO4929097 reduces the tumor initiating potential of melanoma

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Huynh, Chanh ^a   Poliseno, Laura ^a   Segura, Miguel F ^a   Medicherla, Ratna ^a   Haimovic, Adele ^a   Menendez, Silvia ^a   Shang, Shulian ^a   Pavlick, Anna ^a   Shao, Yongzhao ^a   Darvishian, Farbod ^a   Boylan, John F ^b,c   Osman, Iman ^a   Hernando, Eva ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOFFMANN LA ROCHE INC   (United States)

^c CELGENE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; GAMMA SECRETASE INHIBITOR; NOTCH RECEPTOR; RO 4929097; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG; 2,2 DIMETHYL N (6 OXO 6,7 DIHYDRO 5H DIBENZO(B,D)AZEPIN 7 YL) N' (2,2,3,3,3 PENTAFLUOROPROPYL)MALONAMIDE; 2,2-DIMETHYL-N-(6-OXO-6,7-DIHYDRO-5H-DIBENZO(B,D)AZEPIN-7-YL)-N'-(2,2,3,3,3-PENTAFLUOROPROPYL)MALONAMIDE; BENZAZEPINE DERIVATIVE; SECRETASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER INVASION; CANCER RECURRENCE; CANCER SIZE; CANCER SURVIVAL; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MELANOMA CELL; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STEM CELL; SURVIVAL TIME; TUMOR XENOGRAFT; XENOTRANSPLANTATION; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; DRUG SCREENING; IMMUNOHISTOCHEMISTRY; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

MUS;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BENZAZEPINES; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; IMMUNOHISTOCHEMISTRY; MELANOMA; MICE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80053331448     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025264     Document Type: Article

References (53)

1. Garbe C, Leiter U, (2009) Melanoma epidemiology and trends. Clin Dermatol 27: 3-9.
2. Molife R, Hancock BW, (2002) Adjuvant therapy of malignant melanoma. Crit Rev Oncol Hematol 44: 81-102.
3. Kirkwood JM, Manola J, Ibrahim J, Sondak V, Ernstoff MS, et al. (2004) A pooled analysis of eastern cooperative oncology group and intergroup trials of adjuvant high-dose interferon for melanoma. Clin Cancer Res 10: 1670-1677.
4. Ko JM, Fisher DE, (2011) A new era: melanoma genetics and therapeutics. J Pathol 223: 241-250.
5. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, et al. (2011) COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 468: 968-972.
6. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, et al. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-977.
7. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, et al. (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516.
8. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, et al. (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363: 711-723.
9. Poulikakos PI, Rosen N, (2011) Mutant BRAF melanomas-dependence and resistance. Cancer Cell 19: 11-15.
10. Robert C, Thomas L, Bondarenko I, O'Day S, M DJ, et al. (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364: 2517-2526.
11. Miele L, Golde T, Osborne B, (2006) Notch signaling in cancer. Curr Mol Med 6: 905-918.
12. Balint K, Xiao M, Pinnix CC, Soma A, Veres I, et al. (2005) Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J Clin Invest 115: 3166-3176.
13. Pinnix CC, Lee JT, Liu ZJ, McDaid R, Balint K, et al. (2009) Active Notch1 confers a transformed phenotype to primary human melanocytes. Cancer Res 69: 5312-5320.
14. Liu ZJ, Xiao M, Balint K, Smalley KS, Brafford P, et al. (2006) Notch1 signaling promotes primary melanoma progression by activating mitogen-activated protein kinase/phosphatidylinositol 3-kinase-Akt pathways and up-regulating N-cadherin expression. Cancer Res 66: 4182-4190.
15. Bedogni B, Warneke JA, Nickoloff BJ, Giaccia AJ, Powell MB, (2008) Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest 118: 3660-3670.
16. Hardy KM, Kirschmann DA, Seftor EA, Margaryan NV, Postovit LM, et al. (2010) Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 70: 10340-10350.
17. Thurber AE, Douglas G, Sturm EC, Zabierowski SE, Smit DJ, et al. (2011) Inverse expression states of the BRN2 and MITF transcription factors in melanoma spheres and tumour xenografts regulate the NOTCH pathway. Oncogene 30: 3036-3048.
18. Pannuti A, Foreman K, Rizzo P, Osipo C, Golde T, et al. (2010) Targeting notch to target cancer stem cells. Clin Cancer Res 16: 3141-3152.
19. Boiko AD, Razorenova OV, van de Rijn M, Swetter SM, Johnson DL, et al. (2010) Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 466: 133-137.
20. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, et al. (2008) Identification of cells initiating human melanomas. Nature 451: 345-349.
21. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, et al. (2010) A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141: 583-594.
22. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, et al. (2010) Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18: 510-523.
23. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, et al. (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593-598.
24. Shackleton M, Quintana E, (2010) Progress in understanding melanoma propagation. Mol Oncol 4: 451-457.
25. Qin JZ, Stennett L, Bacon P, Bodner B, Hendrix MJ, et al. (2004) p53-independent NOXA induction overcomes apoptotic resistance of malignant melanomas. Mol Cancer Ther 3: 895-902.
26. Shih Ie M, Wang TL, (2007) Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res 67: 1879-1882.
27. Luistro L, He W, Smith M, Packman K, Vilenchik M, et al. (2009) Preclinical profile of a potent gamma-secretase inhibitor targeting notch signaling with in vivo efficacy and pharmacodynamic properties. Cancer Res 69: 7672-7680.
28. Fang D, Nguyen TK, Leishear K, Finko R, Kulp AN, et al. (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65: 9328-9337.
29. Cheli Y, Giuliano S, Botton T, Rocchi S, Hofman V, et al. (2011) Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny. Oncogene 30: 2307-2318.
30. Klein WM, Wu BP, Zhao S, Wu H, Klein-Szanto AJ, et al. (2007) Increased expression of stem cell markers in malignant melanoma. Mod Pathol 20: 102-107.
31. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344.
32. Talantov D, Mazumder A, Yu JX, Briggs T, Jiang Y, et al. (2005) Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 11: 7234-7242.
33. Riker AI, Enkemann SA, Fodstad O, Liu S, Ren S, et al. (2008) The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med Genomics 1: 13.
34. Rose AE, Poliseno L, Wang J, Clark M, Pearlman A, et al. (2010) Integrative genomics identifies molecular alterations that challenge the linear model of melanoma progression. Cancer Res 71: 2561-2571.
35. Massi D, Tarantini F, Franchi A, Paglierani M, Di Serio C, et al. (2006) Evidence for differential expression of Notch receptors and their ligands in melanocytic nevi and cutaneous malignant melanoma. Mod Pathol 19: 246-254.
36. Hoek K, Rimm DL, Williams KR, Zhao H, Ariyan S, et al. (2004) Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res 64: 5270-5282.
37. Bogunovic D, O'Neill DW, Belitskaya-Levy I, Vacic V, Yu YL, et al. (2009) Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival. Proc Natl Acad Sci U S A 106: 20429-20434.
38. La Porta CA, (2009) Mechanism of drug sensitivity and resistance in melanoma. Curr Cancer Drug Targets 9: 391-397.
39. Postovit LM, Margaryan NV, Seftor EA, Hendrix MJ, (2008) Role of nodal signaling and the microenvironment underlying melanoma plasticity. Pigment Cell Melanoma Res 21: 348-357.
40. Schatton T, Frank MH, (2008) Cancer stem cells and human malignant melanoma. Pigment Cell Melanoma Res 21: 39-55.
41. Gray-Schopfer V, Wellbrock C, Marais R, (2007) Melanoma biology and new targeted therapy. Nature 445: 851-857.
42. Kwong L, Chin L, Wagner SN, (2007) Growth factors and oncogenes as targets in melanoma: lost in translation? Adv Dermatol 23: 99-129.
43. Gilbert CA, Daou MC, Moser RP, Ross AH, (2010) Gamma-secretase inhibitors enhance temozolomide treatment of human gliomas by inhibiting neurosphere repopulation and xenograft recurrence. Cancer Res 70: 6870-6879.
44. Grudzien P, Lo S, Albain KS, Robinson P, Rajan P, et al. (2010) Inhibition of Notch signaling reduces the stem-like population of breast cancer cells and prevents mammosphere formation. Anticancer Res 30: 3853-3867.
45. Hovinga KE, Shimizu F, Wang R, Panagiotakos G, Van Der Heijden M, et al. (2010) Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 28: 1019-1029.
46. Sethi N, Dai X, Winter CG, Kang Y, (2011) Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 19: 192-205.
47. Reedijk M, Odorcic S, Chang L, Zhang H, Miller N, et al. (2005) High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res 65: 8530-8537.
48. Yao K, Rizzo P, Rajan P, Albain K, Rychlik K, et al. (2011) Notch-1 and Notch-4 Receptors as Prognostic Markers in Breast Cancer. Int J Surg Pathol.
49. Chang HH, Lee H, Hu MK, Tsao PN, Juan HF, et al. (2010) Notch1 expression predicts an unfavorable prognosis and serves as a therapeutic target of patients with neuroblastoma. Clin Cancer Res 16: 4411-4420.
50. Handolias D, Hamilton AL, Salemi R, Tan A, Moodie K, et al. (2010) Clinical responses observed with imatinib or sorafenib in melanoma patients expressing mutations in KIT. Br J Cancer 102: 1219-1223.
51. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, et al. (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819.
52. Drabkin HA, Parsy C, Ferguson K, Guilhot F, Lacotte L, et al. (2002) Quantitative HOX expression in chromosomally defined subsets of acute myelogenous leukemia. Leukemia 16: 186-195.
53. Klein JP, (2002) Survival analysis methods in cancer studies. Cancer Treat Res 113: 37-57.