Intra- and inter-tumor heterogeneity in a vemurafenib-resistant melanoma patient and derived xenografts

EMBO Molecular Medicine

Volumn 7, Issue 9, 2015, Pages 1104-1118

  Kemper, Kristel ^a   Krijgsman, Oscar ^a   Cornelissen Steijger, Paulien ^a   Shahrabi, Aida ^a   Weeber, Fleur ^a   Song, Ji Ying ^a   Kuilman, Thomas ^a   Vis, Daniel J ^a   Wessels, Lodewyk F ^a   Voest, Emile E ^a   Schumacher, Ton Nm ^a   Blank, Christian U ^a   Adams, David J ^b   Haanen, John B ^a   Peeper, Daniel S ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Drug resistance; Melanoma; Patient derived xenografts; Tumor heterogeneity

Indexed keywords

B RAF KINASE; IPILIMUMAB; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; VEMURAFENIB; ANTINEOPLASTIC AGENT; INDOLE DERIVATIVE; SULFONAMIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAF GENE; CASE REPORT; COMPUTER ASSISTED TOMOGRAPHY; DRUG RESPONSE; FEMALE; GENE AMPLIFICATION; GENE MUTATION; GENETIC HETEROGENEITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MEK1 GENE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR HETEROGENEITY; TUMOR INVASION; TUMOR XENOGRAFT; COMPLICATION; DNA SEQUENCE; DRUG RESISTANCE; GENETIC VARIATION; GENETICS; MUTATION; NEOPLASM METASTASIS; SKIN NEOPLASMS; XENOGRAFT;

ANTINEOPLASTIC AGENTS; DRUG RESISTANCE, NEOPLASM; GENETIC VARIATION; HETEROGRAFTS; HUMANS; INDOLES; MELANOMA; MUTATION; NEOPLASM METASTASIS; PROTO-ONCOGENE PROTEINS B-RAF; SEQUENCE ANALYSIS, DNA; SKIN NEOPLASMS; SULFONAMIDES;

EID: 84940790892     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201404914     Document Type: Article

References (42)

1. Bertolotto C, Lesueur F, Giuliano S, Strub T, deLichy M, Bille K, Dessen P, d'Hayer B, Mohamdi H, Remenieras A et al (2011) A SUMOylation-defective MITF germline mutation predisposes to melanoma and renal carcinoma. Nature 480: 94-98
2. Botton T, Yeh I, Nelson T, Vemula SS, Sparatta A, Garrido MC, Allegra M, Rocchi S, Bahadoran P, McCalmont TH et al (2013) Recurrent BRAF kinase fusions in melanocytic tumors offer an opportunity for targeted therapy. Pigment Cell Melanoma Res 26: 845-851
3. Carlino MS, Fung C, Shahheydari H, Todd JR, Boyd SC, Irvine M, Nagrial AM, Scolyer RA, Kefford RF, Long GV et al (2015) Preexisting MEK1P124 mutations diminish response to BRAF inhibitors in metastatic melanoma patients. Clin Cancer Res 21: 98-105
4. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M et al (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 364: 2507-2516
5. Ciampi R, Knauf JA, Kerler R, Gandhi M, Zhu Z, Nikiforova MN, Rabes HM, Fagin JA, Nikiforov YE (2005) Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. J Clin Invest 115: 94-101
6. Cin H, Meyer C, Herr R, Janzarik WG, Lambert S, Jones DTW, Jacob K, Benner A, Witt H, Remke M et al (2011) Oncogenic FAM131B-BRAF fusion resulting from 7q34 deletion comprises an alternative mechanism of MAPK pathway activation in pilocytic astrocytoma. Acta Neuropathol 121: 763-774
7. Das Thakur M, Salangsang F, Landman AS, Sellers WR, Pryer NK, Levesque MP, Dummer R, McMahon M, Stuart DD (2013) Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature 494: 251-255
8. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, del Angel G, Rivas MA, Hanna M et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498
9. Diaz LA, Williams RT, Wu J, Kinde I, Hecht JR, Berlin J, Allen B, Bozic I, Reiter JG, Nowak MA et al (2012) The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486: 537-540
10. Fischmann TO, Smith CK, Mayhood TW, Myers JE, Reichert P, Mannarino A, Carr D, Zhu H, Wong J, Yang R-S et al (2009) Crystal structures of MEK1 binary and ternary complexes with nucleotides and inhibitors. Biochemistry 48: 2661-2674
11. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, Hamid O, Schuchter L, Cebon J, Ibrahim N et al (2012) Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 367: 1694-1703
12. Gerlinger M, Swanton C (2010) How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br J Cancer 103: 1139-1143
13. Gilmartin AG, Bleam MR, Groy A, Moss KG, Minthorn EA, Kulkarni SG, Rominger CM, Erskine S, Fisher KE, Yang J et al (2011) GSK1120212 (JTP-74057) is an inhibitor of MEK activity and activation with favorable pharmacokinetic properties for sustained in vivo pathway inhibition. Clin Cancer Res 17: 989-1000
14. Inukai M, Toyooka S, Ito S, Asano H, Ichihara S, Soh J, Suehisa H, Ouchida M, Aoe K, Aoe M et al (2006) Presence of epidermal growth factor receptor gene T790M mutation as a minor clone in non-small cell lung cancer. Cancer Res 66: 7854-7858
15. Kuilman T, Velds A, Kemper K, Ranzani M, Bombardelli L, Hoogstraat M, Nevedomskaya E, Xu G, de Ruiter J, Lolkema MP et al (2015) CopywriteR: DNA copy number detection from off-target sequence data. Genome Biol 16: R163
16. Larkin J, Ascierto PA, Dreno B, Atkinson V, Liszkay G, Maio M, Mandalà M, Demidov L, Stroyakovskiy D, Thomas L et al (2014) Combined vemurafenib and cobimetinib in BRAF-mutated melanoma. N Engl J Med 371: 1867-1876
17. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589-595
18. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079
19. Long GV, Stroyakovskiy D, Gogas H, Levchenko E, de Braud F, Larkin J, Garbe C, Jouary T, Hauschild A, Grob JJ et al (2014) Combined BRAF and MEK inhibition versus BRAF inhibition alone in melanoma. N Engl J Med 371: 1877-1888
20. Maheswaran S, Sequist LV, Nagrath S, Ulkus L, Brannigan B, Collura CV, Inserra E, Diederichs S, Iafrate AJ, Bell DW et al (2008) Detection of mutations in EGFR in circulating lung-cancer cells. N Engl J Med 359: 366-377
21. Moriceau G, Hugo W, Hong A, Shi H, Kong X, Yu CC, Koya RC, Samatar AA, Khanlou N, Braun J et al (2015) Tunable-combinatorial mechanisms of acquired resistance limit the efficacy of BRAF/MEK cotargeting but result in melanoma drug addiction. Cancer Cell 27: 240-256
22. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, Lee H, Chen Z, Lee M-K, Attar N, Sazegar H et al (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-977
23. Nikolaev SI, Rimoldi D, Iseli C, Valsesia A, Robyr D, Gehrig C, Harshman K, Guipponi M, Bukach O, Zoete V et al (2012) Exome sequencing identifies recurrent somatic MAP2K1 and MAP2K2 mutations in melanoma. Nat Genet 44: 133-139
24. Olshen AB, Venkatraman ES, Lucito R, Wigler M (2004) Circular binary segmentation for the analysis of array-based DNA copy number data. Biostatistics 5: 557-572
25. Possik PA, Müller J, Gerlach C, Kenski JCN, Huang X, Shahrabi A, Krijgsman O, Song J-Y, Smit MA, Gerritsen B et al (2014) Parallel in vivo and in vitro melanoma RNAi dropout screens reveal synthetic lethality between hypoxia and DNA damage response inhibition. Cell Rep 9: 1375-1386
26. Poulikakos PI, Persaud Y, Janakiraman M, Kong X, Ng C, Moriceau G, Shi H, Atefi M, Titz B, Gabay MT et al (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 480: 387-390
27. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, Kuriyan J, Sawyers CL (2002) Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2: 117-125
28. Shi H, Hong A, Kong X, Koya RC, Song C, Moriceau G, Hugo W, Yu CC, Ng C, Chodon T et al (2014a) A novel AKT1 mutant amplifies an adaptive melanoma response to BRAF inhibition. Cancer Discov 4: 69-79
29. Shi H, Hugo W, Kong X, Hong A, Koya RC, Moriceau G, Chodon T, Guo R, Johnson DB, Dahlman KB et al (2014b) Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov 4: 80-93
30. Shi H, Moriceau G, Kong X, Lee M-K, Lee H, Koya RC, Ng C, Chodon T, Scolyer RA, Dahlman KB et al (2012) Melanoma whole-exome sequencing identifies (V600E)B-RAF amplification-mediated acquired B-RAF inhibitor resistance. Nat Commun 3: 724
31. Su F, Bradley WD, Wang Q, Yang H, Xu L, Higgins B, Kolinsky K, Packman K, Kim MJ, Trunzer K et al (2012a) Resistance to selective BRAF inhibition can be mediated by modest upstream pathway activation. Cancer Res 72: 969-978
32. Su K-Y, Chen H-Y, Li K-C, Kuo M-L, Yang JC-H, Chan W-K, Ho B-C, Chang G-C, Shih J-Y, Yu S-L et al (2012b) Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J Clin Oncol 30: 433-440
33. Sun C, Wang L, Huang S, Heynen GJJE, Prahallad A, Robert C, Haanen J, Blank C, Wesseling J, Willems SM et al (2014) Reversible and adaptive resistance to BRAF(V600E) inhibition in melanoma. Nature 508: 118-122
34. Trunzer K, Pavlick AC, Schuchter L, Gonzalez R, McArthur GA, Hutson TE, Moschos SJ, Flaherty KT, Kim KB, Weber JS et al (2013) Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J Clin Oncol 31: 1767-1774
35. Van Allen EM, Wagle N, Sucker A, Treacy DJ, Johannessen CM, Goetz EM, Place CS, Taylor-Weiner A, Whittaker S, Kryukov GV et al (2014) The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov 4: 94-109
36. Villanueva J, Infante JR, Krepler C, Reyes-Uribe P, Samanta M, Chen H-Y, Li B, Swoboda RK, Wilson M, Vultur A et al (2013) Concurrent MEK2 mutation and BRAF amplification confer resistance to BRAF and MEK inhibitors in melanoma. Cell Rep 4: 1090-1099
37. Villanueva J, Vultur A, Lee JT, Somasundaram R, Fukunaga-Kalabis M, Cipolla AK, Wubbenhorst B, Xu X, Gimotty PA, Kee D et al (2010) 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
38. Vredeveld LCW, Possik PA, Smit MA, Meissl K, Michaloglou C, Horlings HM, Ajouaou A, Kortman PC, Dankort D, McMahon M et al (2012) Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Genes Dev 26: 1055-1069
39. Wagle N, Emery C, Berger MF, Davis MJ, Sawyer A, Pochanard P, Kehoe SM, Johannessen CM, Macconaill LE, Hahn WC et al (2011) Dissecting therapeutic resistance to RAF inhibition in melanoma by tumor genomic profiling. J Clin Oncol 29: 3085-3096
40. Wagle N, Van Allen EM, Treacy DJ, Frederick DT, Cooper ZA, Taylor-Weiner A, Rosenberg M, Goetz EM, Sullivan RJ, Farlow DN et al (2014) MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov 4: 61-68
41. Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38: e164
42. Yokoyama S, Woods SL, Boyle GM, Aoude LG, MacGregor S, Zismann V, Gartside M, Cust AE, Haq R, Harland M et al (2011) A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 480: 99-103