Inhibition of vemurafenib-resistant melanoma by interference with pre-mRNA splicing

Nature Communications

Volumn 6, Issue , 2015, Pages

  Salton, Maayan ^a   Kasprzak, Wojciech K ^b   Voss, Ty ^a   Shapiro, Bruce A ^c   Poulikakos, Poulikos I ^d   Misteli, Tom ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; B RAF KINASE 3; B RAF KINASE 4; B RAF KINASE 5; B RAF KINASE 6; B RAF KINASE 7; B RAF KINASE 8; B RAF KINASE 9; ISOENZYME; UNCLASSIFIED DRUG; VEMURAFENIB; BRAF PROTEIN, HUMAN; BRAF PROTEIN, MOUSE; INDOLE DERIVATIVE; ISOPROTEIN; MESSENGER RNA; RNA PRECURSOR; SULFONAMIDE;

DRUG RESISTANCE; ENZYME ACTIVITY; GERM CELL; GROWTH RATE; MUTATION; NUMERICAL MODEL; RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CARCINOGENESIS; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; GENE FREQUENCY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRON; MALE; MELANOMA; MOUSE; NONHUMAN; POINT MUTATION; PROTEIN SECONDARY STRUCTURE; RNA INTERFERENCE; RNA SPLICING; SEQUENCE ANALYSIS; TUMOR GROWTH; TUMOR VOLUME; ALTERNATIVE RNA SPLICING; ANIMAL; CANCER TRANSPLANTATION; CHEMISTRY; DRUG RESISTANCE; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; SCID MOUSE; SKIN NEOPLASMS; TUMOR CELL LINE;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; GENES, REPORTER; HUMANS; INDOLES; INTRONS; MALE; MELANOMA; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; POINT MUTATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS B-RAF; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; SKIN NEOPLASMS; SULFONAMIDES;

EID: 84929603565     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8103     Document Type: Article

References (36)

1. Kudchadkar, R., Paraiso, K. H. & Smalley, K. S. Targeting mutant BRAF in melanoma: current status and future development of combination therapy strategies. Cancer J. 18, 124-131 (2012).
2. Pratilas, C. A. & Solit, D. B. Targeting the mitogen-activated protein kinase pathway: physiological feedback and drug response. Clin. Cancer Res. 16, 3329-3334 (2010).
3. Dhomen, N. & Marais, R. BRAF signaling and targeted therapies in melanoma. Hematol Oncol. Clin. N. Am. 23, 529-545 (2009).
4. Wan, P. T. et al. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116, 855-867 (2004).
5. Flaherty, K. T. et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363, 809-819 (2010).
6. Nazarian, R. et al. Melanomas acquire resistance to B-RAF (V600E) inhibition by RTK or N-RAS upregulation. Nature 468, 973-977 (2010).
7. Johannessen, C. M. et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 468, 968-972 (2010).
8. Wagle, N. et al. Dissecting therapeutic resistance to RAF inhibition in melanoma by tumor genomic profiling. J. Clin. Oncol. 29, 3085-3096 (2011).
9. Romano, E. et al. Identification of multiple mechanisms of resistance to vemurafenib in a patient with BRAFV600E-mutated cutaneous melanoma successfully rechallenged after progression. Clin. Cancer Res. 19, 5749-5757 (2013).
10. Sullivan, R. J. & Flaherty, K. T. Resistance to BRAF-targeted therapy in melanoma. Eur. J. Cancer 49, 1297-1304 (2013).
11. Montagut, C. et al. Elevated CRAF as a potential mechanism of acquired resistance to BRAF inhibition in melanoma. Cancer Res. 68, 4853-4861 (2008).
12. Shi, H. et al. Melanoma whole-exome sequencing identifies (V600E) B-RAF amplification-mediated acquired B-RAF inhibitor resistance. Nat. Commun. 3, 724 (2012).
13. Poulikakos, P. I. et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF (V600E). Nature 480, 387-390 (2011).
14. Villanueva, J. et al. Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 18, 683-695 (2010).
15. Sun, C. et al. Reversible and adaptive resistance to BRAF (V600E) inhibition in melanoma. Nature 508, 118-122 (2014).
16. Girotti, M. R. et al. Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov. 3, 158-167 (2013).
17. Wellbrock, C., Karasarides, M. & Marais, R. The RAF proteins take centre stage. Nature reviews. Mol. Cell Biol. 5, 875-885 (2004).
18. Freeman, A. K., Ritt, D. A. & Morrison, D. K. The importance of Raf dimerization in cell signaling. Small GTPases 4 (2013).
19. Shi, H. et al. Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov. 4, 80-93 (2014).
20. Cartegni, L., Wang, J., Zhu, Z., Zhang, M. Q. & Krainer, A. R. ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31, 3568-3571 (2003).
21. Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R. & Hofacker, I. L. The Vienna RNA websuite. Nucleic Acids Res. 36, W70-W74 (2008).
22. Nakajima, H. et al. New antitumor substances, FR901463, FR901464 and FR901465. II. Activities against experimental tumors in mice and mechanism of action. J. Antibiot. (Tokyo) 49, 1204-1211 (1996).
23. Bonnal, S., Vigevani, L. & Valcarcel, J. The spliceosome as a target of novel antitumour drugs. Nat. Rev. Drug Discov. 11, 847-859 (2012).
24. Albert, B. J., Sivaramakrishnan, A., Naka, T., Czaicki, N. L. & Koide, K. Total syntheses, fragmentation studies, and antitumor/antiproliferative activities of FR901464 and its low picomolar analogue. J. Am. Chem. Soc. 129, 2648-2659 (2007).
25. Aebersold, D. M. et al. Extracellular signal-regulated kinase 1c (ERK1c), a novel 42-kilodalton ERK, demonstrates unique modes of regulation, localization, and function. Mol. Cell. Biol. 24, 10000-10015 (2004).
26. Albert, B. J. et al. Meayamycin inhibits pre-messenger RNA splicing and exhibits picomolar activity against multidrug-resistant cells. Mol. Cancer Ther. 8, 2308-2318 (2009).
27. Lassen, A. et al. Effects of AKT inhibitor therapy in response and resistance to BRAF inhibition in melanoma. Mol. Cancer 13, 83 (2014).
28. O'Connell, M. P. et al. Hypoxia induces phenotypic plasticity and therapy resistance in melanoma via the tyrosine kinase receptors ROR1 and ROR2. Cancer Discov. 3, 1378-1393 (2013).
29. Kotake, Y. et al. Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat. Chem. Biol. 3, 570-575 (2007).
30. Eskens, F. A. et al. Phase I, pharmacokinetic and pharmacodynamic study of the first-in-class spliceosome inhibitor E7107 in patients with advanced solid tumors. Clin. Cancer Res. 19, 6296-6304 (2013).
31. Park, S. J. et al. The MEK1/2 inhibitor AS703026 circumvents resistance to the BRAF inhibitor PLX4032 in human malignant melanoma cells. Am. J. Med. Sci. 346, 494-498 (2013).
32. Flaherty, K. T. et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N. Engl. J. Med. 367, 1694-1703 (2012).
33. Johannessen, C. M. et al. A melanocyte lineage program confers resistance to MAP kinase pathway inhibition. Nature 504, 138-142 (2013).
34. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415 (2003).
35. Waugh, A. et al. RNAML: a standard syntax for exchanging RNA information. RNA 8, 707-717 (2002).
36. Mathews, D. H., Sabina, J., Zuker, M. & Turner, D. H. Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol. 288, 911-940 (1999).