The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma

Cancer Discovery

Volumn 4, Issue 1, 2014, Pages 94-109

  Van Allen, Eliezer M ^a,c   Wagle, Nikhil ^a,c   Sucker, Antje ^e,f   Treacy, Daniel J ^a   Johannessen, Cory M ^c   Goetz, Eva M ^a   Place, Chelsea S ^a,c   Taylor Weiner, Amaro ^c   Whittaker, Steven ^c   Kryukov, Gregory V ^c   Hodis, Eran ^a,c,d   Rosenberg, Mara ^c   Mckenna, Aaron ^a,c,e   Cibulskis, Kristian ^c   Farlow, Deborah ^c   Zimmer, Lisa ^e,f   Hillen, Uwe ^e,f   Gutzmer, Ralf ^h   Goldinger, Simone M ^p   Ugure, Selma ⁱ   Gogas, Helen J ^q   Egberts, Friederike ^j   Berking, Carola ^f,k   Trefzer, Uwe ^f,l   Loquai, Carmen ^f,m   Weide, Benjamin ^f,n   Hasse, Jessica C ^f,g   Gabrie, Stacey B ^c   Carter, Scott L ^c   Getz, Gad ^b,c   Garraway, Levi A ^a,c,o   Schadendorf, Dirk ^e,f   more..

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^h HANNOVER MEDICAL SCHOOL   (Germany)

ⁱ UNIVERSITY OF WÜRZBURG   (Germany)

^j UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^k UNIVERSITY OF MUNICH   (Germany)

^l CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^m JOHANNES GUTENBERG UNIVERSITY   (Germany)

ⁿ UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^o UNIVERSITY OF WASHINGTON   (United States)

^p UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^q UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

more..

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; DABRAFENIB; HOMEODOMAIN PROTEIN; HOMEODOMAIN PROTEIN HOXD8; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; N [3 (5 CHLORO 1H PYRROLO [2, 3 B] PYRIDINE 3 CARBONYL) 2, 4 DIFLUOROPHENYL] PROPANESULFONAMIDE; NEUROFIBROMIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PICTILISIB; RAC1 PROTEIN; SELUMETINIB; TRAMETINIB; UNCLASSIFIED DRUG; VEMURAFENIB; VRT11E;

ADULT; ARTICLE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENETIC RESISTANCE; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; METASTATIC MELANOMA; MIDDLE AGED; MUTATION; ONCOGENE N RAS; PHOSPHORYLATION; SEQUENCE ANALYSIS; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EXOME; FEMALE; HEK293 CELLS; HUMANS; IMIDAZOLES; INDOLES; MALE; MAP KINASE KINASE 1; MAP KINASE KINASE 2; MELANOMA; MIDDLE AGED; MUTATION; NEOPLASM METASTASIS; OXIMES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SEQUENCE ANALYSIS, DNA; SKIN NEOPLASMS; SULFONAMIDES;

EID: 84891894051     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.cd-13-0617     Document Type: Article

References (52)

1. 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.
2. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber J S, et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med 2012;366:707-14.
3. 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.
4. Flaherty K T, Infante JR, Daud A, Gonzalez R, Kef ford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
5. Trunzer K, Pavlick AC, Schuchter L, Gonzalez R, McArthur GA, Hutson TE, et al. Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J Clin Oncol 2013;31:1767-74.
6. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010;468:973-7.
7. Wagle N, Emery C, Berger MF, Davis MJ, Sawyer A, Pochanard P, et al. Dissecting therapeutic resistance to RAF inhibition in melanoma by tumor genomic profiling. J Clin Oncol 2011;29:3085-96.
8. Shi H, Moriceau G, Kong X, Lee MK, Lee H, Koya RC, et al. Melanoma whole-exome sequencing identifi es (V600E)B-RAF amplifi cation-mediated acquired B-RAF inhibitor resistance. Nat Commun 2012; 3:724.
9. Whittaker SR, Theurillat JP, Van Allen E, Wagle N, Hsiao J, Cowley GS, et al. A genome-scale RNA interference screen implicates NF1 loss in resistance to RAF inhibition. Cancer Discov 2013;3:350-62.
10. Johannessen CM, Boehm JS, Kim SY, Thomas SR, Wardwell L, Johnson LA, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature 2010;468:968-72.
11. Girotti MR, Pedersen M, Sanchez-Laorden B, Viros A, Turajlic S, Niculescu-Duvaz D, et al. Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov 2013;3:158-67.
12. Paraiso KH, Xiang Y, Rebecca VW, Abel EV, Chen YA, Munko A C, et al. PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res 2011;71:2750-60.
13. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, Moriceau G, et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 2011;480:387-90.
14. Lito P, Pratilas CA, Joseph EW, Tadi M, Halilovic E, Zubrowski M, et al. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 2012;22:668-82.
15. Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, 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 2010;18:683-95.
16. Straussman R, Morikawa T, Shee K, Barzily-Rokni M, Qian ZR, Du J, et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012;487:500-4.
17. Wilson TR, Fridlyand J, Yan Y, Penuel E, Burton L, Chan E, et al. Widespread potential for growth-factor-driven resistance to antican-cer kinase inhibitors. Nature 2012;487:505-9.
18. Catalanotti F, Reyes G, Jesenberger V, Galabova-Kovacs G, de Matos Simoes R, Carugo O, et al. A Mek1-Mek2 heterodimer determines the strength and duration of the Erk signal. Nat Struct Mol Biol 2009;16:294-303.
19. Shi H, Moriceau G, Kong X, Koya RC, Nazarian R, Pupo GM, et al. Preexisting MEK1 exon 3 mutations in V600E/KBRAF melanomas do not confer resistance to BRAF inhibitors. Cancer Discov 2012; 2: 414-24.
20. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, Ram-aswamy S, et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplifi ed in malignant melanoma. Nature 2005;436:117-22.
21. Johannessen CM, Johnson LA, Piccioni F, Townes A, Frederick DT, Donahue MK, et al. A melanocyte lineage program confers resistance to MAP kinase pathway inhibition. Nature. 2013 Nov 3. doi: 10.1038/ nature12688. [Epub ahead of print]. PMID: 24185007]
22. Schubbert S, Zenker M, Rowe SL, Boll S, Klein C, Bollag G, et al. Germline KRAS mutations cause Noonan syndrome. Nat Genet 2006;38:331-6.
23. Romano E, Pradervand S, Paillusson A, Weber J, Harshman K, Muehlethaler K, 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. 2013 Aug 15. [Epub ahead of print].
24. Deng W, Gopal YN, Scott A, Chen G, Woodman SE, Davies MA. Role and therapeutic potential of PI3K-mTOR signaling in de novo resistance to BRAF inhibition. Pigment Cell Melanoma Res 2012;25: 248-58.
25. Greger JG, Eastman SD, Zhang V, Bleam MR, Hughes AM, Smitheman KN, et al. Combinations of BRAF, MEK, and PI3K/mTOR inhibitors overcome acquired resistance to the BRAF inhibitor GSK2118436 dabrafenib, mediated by NRAS or MEK mutations. Mol Cancer Ther 2012;11:909-20.
26. Xing F, Persaud Y, Pratilas CA, Taylor BS, Janakiraman M, She Q B, et al. Concurrent loss of the PTEN and RB1 tumor suppressors attenuates RAF dependence in melanomas harboring (V600E)BRAF. Oncogene 2012;31:446-57.
27. Nathanson KL, Martin AM, Wubbenhorst B, Greshock J, Letrero R, D'Andrea K, et al. Tumor genetic analyses of patients with metastatic melanoma treated with the BRAF inhibitor dabrafenib (GSK2118436). Clin Cancer Res 2013;19:4868-78.
28. Janku F, Wheler JJ, Naing A, Falchook GS, Hong DS, Stepanek V M, et al. PIK3CA mutation H1047R is associated with response to PI3K/ AKT/mTOR signaling pathway inhibitors in early-phase clinical trials. Cancer Res 2013;73:276-84.
29. Rodriguez-Escudero I, Oliver MD, Andres-Pons A, Molina M, Cid VJ, Pulido R. A comprehensive functional analysis of PTEN mutations: implications in tumor- and autism-related syndromes. Hum Mol Genet 2011;20:4132-42.
30. Han SY, Kato H, Kato S, Suzuki T, Shibata H, Ishii S, et al. Functional evaluation of PTEN missense mutations using in vitro phosphoi-nositide phosphatase assay. Cancer Res 2000;60:3147-51.
31. Gopal YN, Deng W, Woodman SE, Komurov K, Ram P, Smith PD, et al. Basal and treatment-induced activation of AKT mediates resistance to cell death by AZD6244 (ARRY-142886) in Braf-mutant human cutaneous melanoma cells. Cancer Res 2010;70:8736-47.
32. Hoeflich KP, Herter S, Tien J, Wong L, Berry L, Chan J, et al. Antitu-mor effi cacy of the novel RAF inhibitor GDC-0879 is predicted by BRAFV600E mutational status and sustained extracellular signal-regulated kinase/mitogen-activated protein kinase pathway suppression. Cancer Res 2009;69:3042-51.
33. Hoeflich KP, Merchant M, Orr C, Chan J, Den Otter D, Berry L, et al. Intermittent administration of MEK inhibitor GDC-0973 plus PI3K inhibitor GDC-0941 triggers robust apoptosis and tumor growth inhibition. Cancer Res 2012;72:210-9.
34. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell 2012; 150: 251-63.
35. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, et al. Exome sequencing identifi es recurrent somatic RAC1 mutations in melanoma. Nat Genet 2012;44:1006-14.
36. Spitz F, Gonzalez F, Peichel C, Vogt TF, Duboule D, Zakany J. Large scale transgenic and cluster deletion analysis of the HoxD complex separate an ancestral regulatory module from evolutionary innovations. Genes Dev 2001;15:2209-14.
37. Shinawi T, Hill VK, Krex D, Schackert G, Gentle D, Morris MR, et al. DNA methylation profi les of long- and short-term glioblastoma survivors. Epigenetics 2013;8:149-56.
38. Leshchenko VV, Kuo PY, Shaknovich R, Yang DT, Gellen T, Petrich A, et al. Genomewide DNA methylation analysis reveals novel targets for drug development in mantle cell lymphoma. Blood 2010; 116: 1025-34.
39. Garraway LA, Lander ES. Lessons from the cancer genome. Cell 2013;153:17-37.
40. Wagle N, Van Allen EM, Treacy DJ, Frederick DT, Cooper ZA, Taylor-Weiner A, et al. MAP kinase pathway alterations in BRAF -mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov 2014;4:61-8.
41. Kefford R, Miller WH Jr, Tan D, Sullivan RJ, Long GV, Dienstmann R, et al. Preliminary results from a phase Ib/II, open-label, dose-escalation study of the oral BRAF inhibitor LGV818 in combination with the oral MEK1/2 inhibitor MEK162 in BRAF V600-dependent advanced solid tumors. J Clin Oncol 31, 2013(suppl; abstr 9029).
42. Morris EJ, Jha S, Restaino CR, Dayananth P, Zhu H, Cooper A, et al. Discovery of a novel ERK inhibitor with activity in models of acquired resistance to BRAF and MEK inhibitors. Cancer Discov 2013; 3: 742-50.
43. Vogelstein B, Papadopoulos N, Velculescu VE, Zhou S, Diaz LA Jr, Kinzler KW. Cancer genome landscapes. Science 2013;339:1546-58.
44. Das Thakur M, Salangsang F, Landman AS, Sellers WR, Pryer NK, Levesque MP, et al. Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 2013;494:251-5.
45. Fisher S, Barry A, Abreu J, Minie B, Nolan J, Delorey TM, et al. A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol 2011;12:R1.
46. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePat-tern 2.0. Nat Genet 2006;38:500-1.
47. Cibulskis K, McKenna A, Fennell T, Banks E, DePristo M, Getz G. ContEst: estimating cross-contamination of human samples in next-generation sequencing data. Bioinformatics 2011;27:2601-2.
48. Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 2013; 31: 213-9.
49. Costello M, Pugh TJ, Fennell TJ, Stewart C, Lichtenstein L, Meldrim JC, et al. Discovery and characterization of artifactual mutations in deep coverage targeted capture sequencing data due to oxidative DNA damage during sample preparation. Nucleic Acids Res 2013;41:e67.
50. Olshen AB, Venkatraman ES, Lucito R, Wigler M. Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 2004;5:557-72.
51. Berger MF, Hodis E, Heffernan TP, Deribe YL, Lawrence MS, Pro-topopov A, et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 2012;485:502-6.
52. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984;22:27-55.