BRAF V600E is a determinant of sensitivity to proteasome inhibitors

Molecular Cancer Therapeutics

Volumn 12, Issue 12, 2013, Pages 2950-2961

  Zecchin, Davide ^a,c   Boscaro, Valentina ^b   Medico, Enzo ^a,c   Barault, Ludovic ^c   Martini, Miriam ^a,c   Arena, Sabrina ^c   Cancelliere, Carlotta ^c,d   Bartolini, Alice ^c   Crowley, Emily H ^c   Bardelli, Alberto ^a,c,d   Gallicchio, Margherita ^b   Di Nicolantonio, Federica ^a,c  

^a Departments of Orthopaedic Surgery and Oncology   (United States)

^b UNIVERSITY OF TURIN   (Italy)

^c CANDIOLO CANCER INSTITUTE   (Italy)

^d FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; CANERTINIB; CARFILZOMIB; ERLOTINIB; K RAS PROTEIN; LAPATINIB; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; VANDETANIB; VASCULOTROPIN RECEPTOR;

ALGORITHM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER GENETICS; CELL MUTANT; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; DRUG RESPONSE; DRUG SENSITIVITY; EPITHELIUM CELL; FEMALE; GENE MUTATION; GENE SILENCING; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; ONCOGENE; PHARMACOGENOMICS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

14-3-3 PROTEINS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CLUSTER ANALYSIS; DRUG RESISTANCE, NEOPLASM; DRUG SCREENING ASSAYS, ANTITUMOR; EXORIBONUCLEASES; FEMALE; GENOTYPE; HUMANS; INDOLES; MUTATION; PROTEASOME INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SIGNAL TRANSDUCTION; SULFONAMIDES; TELOMERASE; TUMOR MARKERS, BIOLOGICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84890444517     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-0243     Document Type: Article

References (49)

1. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004;350:2129-39
2. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500
3. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, et al. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci U S A 2004;101:13306-11
4. Sordella R, Bell DW, Haber DA, Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004;305:1163-7
5. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 2002;20:719-26
6. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507-16
7. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, et al. Dabrafenib in BRAF-mutated metastatic melanoma: A multicentre, open-label, phase 3 randomised controlled trial. Lancet 2012;380:358-65
8. Kwak EL, Bang YJ, Camidge DR, Shaw AT, Solomon B, Maki RG, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med 2010;363:1693-703
9. Shaw AT, Yeap BY, Solomon BJ, Riely GJ, Gainor J, Engelman JA, et al. Effect of crizotinib on overall survival in patients with advanced non-small-cell lung cancer harbouring ALK gene rearrangement: A retrospective analysis. Lancet Oncol 2011;12:1004-12
10. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007;318:1108-13
11. Mellinghoff IK, Wang MY, Vivanco I, Haas-Kogan DA, Zhu S, Dia EQ, et al. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N Engl J Med 2005;353:2012-24
12. Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, Zander T, et al. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res 2009;69:3256-61
13. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K, et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007;12:395-402
14. Esteva FJ, Guo H, Zhang S, Santa-Maria C, Stone S, Lanchbury JS, et al. PTEN, PIK3CA, p-AKT, and p-p70S6K status: Association with trastuzumab response and survival in patients with HER2-positive metastatic breast cancer. Am J Pathol 2010;177:1647-56
15. Zecchin D, Arena S, Martini M, Sassi F, Pisacane A, Di Nicolantonio F, et al. Modeling tumor progression by the sequential introduction of genetic alterations into the genome of human normal cells. Hum Mutat 2013;34:330-7
16. Richman SD, Seymour MT, Chambers P, Elliott F, Daly CL, MeadeAM, et al. KRAS and BRAF mutations in advanced colorectal cancer are associated with poor prognosis but do not preclude benefit from oxaliplatin or irinotecan: results from the MRC FOCUS trial. J Clin Oncol 2009;27:5931-7
17. Kopetz S, Desai J, Chan E, Hecht JR, O'Dwyer PJ, Lee RJ, et al. PLX4032 in metastatic colorectal cancer patients with mutant BRAF tumors. J Clin Oncol 28:15s, 2010 (suppl; abstr 3534)
18. Whitehead RH, Macrae FA, St John DJ, Ma J. A colon cancer cell line (LIM1215) derived from a patient with inherited nonpolyposis colorectal cancer. J Natl Cancer 1 1985;74:759-65
19. Zhang HH, Walker F, Kiflemariam S, Whitehead RH, Williams D, Phillips WA, et al. Selective inhibition of proliferation in colorectal carcinoma cell lines expressing mutant APC or activated B-Raf. Int J Cancer 2009;125:297-307
20. Di Nicolantonio F, Arena S, Gallicchio M, Zecchin D, Martini M, Flonta SE, et al. Replacement of normal with mutant alleles in the genome of normal human cells unveils mutation-specific drug responses. Proc Natl Acad Sci U S A 2008;105:20864-9
21. Zecchin D, Di Nicolantonio F. Transfection and DNA-mediated gene transfer. Methods Mol Biol 2011;731:435-50
22. Fu L, Medico E. FLAME, a novel fuzzy clustering method for the analysis of DNA microarray data. BMC Bioinformatics 2007;8:3
23. Poch G, Reiffenstein RJ, Kock P, Pancheva SN. Uniform characterization of potentiation in simple and complex situations when agents bind to different molecular sites. Can J Physiol Pharmacol 1995;73: 1574-81
24. Di Nicolantonio F, Martini M, Molinari F, Sartore-Bianchi A, Arena S, Saletti P, et al. Wild-type BRAF is required for response to panitumumab or cetuximab in metastatic colorectal cancer. J Clin Oncol 2008;26:5705-12
25. Gandhi J, Zhang J, Xie Y, Soh J, Shigematsu H, Zhang W, et al. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS ONE 2009;4:e4576
26. Jhawer M, Goel S, Wilson AJ, Montagna C, Ling YH, Byun DS, et al. PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res 2008;68:1953-61
27. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modeling of anticancer drug sensitivity. Nature 2012;483:603-7
28. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012;483:570-5
29. Prahallad A, Sun C, Huang S, Di Nicolantonio F, Salazar R, Zecchin D, et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012;483:100-3
30. -/- cells identifies CID1340132 as a novel compound that induces apoptosis in PTEN and PIK3CA mutant human cancer cells. J Biomol Screen 2011;16:383-93
31. Torrance CJ, Agrawal V, Vogelstein B, Kinzler KW. Use of isogenic human cancer cells for high-throughput screening and drug discovery. Nat Biotechnol 2001;19:940-5
32. Dolma S, Lessnick SL, Hahn WC, Stockwell BR. Identification of genotype-selective antitumor agents using synthetic lethal chemical screening in engineered human tumor cells. Cancer Cell 2003;3: 285-96
33. Shaw AT, Winslow MM, Magendantz M, Ouyang C, Dowdle J, Subramanian A, et al. Selective killing of K-ras mutant cancer cells by small molecule inducers of oxidative stress. Proc Natl Acad Sci U S A 2011;108:8773-8
34. Sur S, Pagliarini R, Bunz F, Rago C, Diaz LAJr., Kinzler KW, et al. A panel of isogenic human cancer cells suggests a therapeutic approach for cancers with inactivated p53. Proc Natl Acad Sci U S A 2009;106:3964-9
35. Weiss MB, Vitolo MI, Mohseni M, Rosen DM, Denmeade SR, Park BH, et al. Deletion of p53 in human mammary epithelial cells causes chromosomal instability and altered therapeutic response. Oncogene 2010;29:4715-24
36. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, Westbrook TF, et al. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009;137:835-48
37. Xing F, Persaud Y, Pratilas CA, Taylor BS, Janakiraman M, She QB, et al. Concurrent loss of the PTEN and RB1 tumor suppressors attenuates RAF dependence in melanomas harboring (V600E)BRAF. Oncogene 2012;31:446-57
38. Caponigro F, Lacombe D, Twelves C, Bauer J, Govaerts AS, Marreaud S, et al. An EORTC phase I study of Bortezomib in combination with oxaliplatin, leucovorin and 5-fluorouracil in patients with advanced colorectal cancer. Eur J Cancer 2009;45:48-55
39. Caravita T, de Fabritiis P, Palumbo A, Amadori S, Boccadoro M. Bortezomib: efficacy comparisons in solid tumors and hematologic malignancies. Nat Clin Pract Oncol 2006;3:374-87
40. Milano A, Perri F, Caponigro F. The ubiquitin-proteasome system as a molecular target in solid tumors: An update on bortezomib. Onco Targets Ther 2009;2:171-8
41. Kuhn DJ, Chen Q, Voorhees PM, Strader JS, Shenk KD, Sun CM, et al. Potent activity of carfilzomib, a novel, irreversible inhibitor of the ubiquitin-proteasome pathway, against preclinical models of multiple myeloma. Blood 2007;110:3281-90
42. Zang Y, Thomas SM, Chan ET, Kirk CJ, Freilino ML, DeLancey HM, et al. Carfilzomib and ONX 0912 inhibit cell survival and tumor growth of head and neck cancer and their activities are enhanced by suppression of Mcl-1 or autophagy. Clin Cancer Res 2012;18:5639-49
43. O'Connor OA, Stewart AK, Vallone M, Molineaux CJ, Kunkel LA, Gerecitano JF, et al. A phase 1 dose escalation study of the safety and pharmacokinetics of the novel proteasome inhibitor carfilzomib (PR-171) in patients with hematologic malignancies. Clin Cancer Res 2009;15:7085-91
44. Rajagopalan H, Bardelli A, Lengauer C, Kinzler KW, Vogelstein B, Velculescu VE. Tumorigenesis: RAF/RAS oncogenes and mismatchrepair status. Nature 2002;418:934
45. Dai C, Whitesell L, Rogers AB, Lindquist S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007;130: 1005-18
46. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature 2009;462:108-12
47. Bernards R. A missing link in genotype-directed cancer therapy. Cell 2012;151:465-8
48. Held MA, Langdon CG, Platt JT, Graham-Steed T, Liu Z, Chakraborty A, et al. Genotype-selective combination therapies for melanoma identified by high-throughput drug screening. Cancer Discov 2013; 3:52-67
49. Roller DG, Axelrod M, Capaldo BJ, Jensen K, Mackey A, Weber MJ, et al. Synthetic lethal screening with small-molecule inhibitors provides a pathway to rational combination therapies for melanoma.Mol Cancer Ther 2012;11:2505-15