Application of sequencing, liquid biopsies, and patient-derived xenografts for personalized medicine in melanoma

Cancer Discovery

Volumn 6, Issue 3, 2016, Pages 286-299

  Girotti, Maria Romina ^a   Gremel, Gabriela ^a   Lee, Rebecca ^a   Galvani, Elena ^a   Rothwell, Dominic ^a   Viros, Amaya ^a   Mandal, Amit Kumar ^a   Lim, Kok Haw Jonathan ^a   Saturno, Grazia ^a   Furney, Simon J ^a   Baenke, Franziska ^a   Pedersen, Malin ^b   Rogan, Jane ^c   Swan, Jacqueline ^a   Smith, Matthew ^a   Fusi, Alberto ^c   Oudit, Deemesh ^c   Dhomen, Nathalie ^a   Brady, Ged ^a   Lorigan, Paul ^c   Dive, Caroline ^a   Marais, Richard ^a   more..

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; DABRAFENIB; N [3 (5 CHLORO 1H PYRROLO[2,3 B]PYRIDINE 3 CARBONYL) 2,4 DIFLUOROPHENYL]PROPANESULFONAMIDE; PACLITAXEL; TRAMETINIB; ANTINEOPLASTIC AGENT; TUMOR MARKER;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; CANCER STAGING; CANCER SURVIVAL; CIRCULATING TUMOR CELL; CLINICAL ASSESSMENT; CLINICAL DECISION MAKING; CLINICAL TRIAL; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DNA EXTRACTION; FEMALE; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MELANOMA; MOUSE; NONHUMAN; PERSONALIZED MEDICINE; REAL TIME POLYMERASE CHAIN REACTION; TREATMENT RESPONSE; TUMOR VOLUME; TUMOR XENOGRAFT; BIOPSY; BLOOD; CLUSTER ANALYSIS; DISEASE COURSE; DISEASE MANAGEMENT; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION PROFILING; GENETICS; HIGH THROUGHPUT SEQUENCING; MOLECULARLY TARGETED THERAPY; MUTATION; REPRODUCIBILITY; TREATMENT OUTCOME;

ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; BIOPSY; CLUSTER ANALYSIS; DISEASE MANAGEMENT; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION PROFILING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MELANOMA; MOLECULAR TARGETED THERAPY; MUTATION; NEOPLASM STAGING; PRECISION MEDICINE; REPRODUCIBILITY OF RESULTS; TREATMENT OUTCOME; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84960075353     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-15-1336     Document Type: Article

References (51)

1. http://www.Cancer.org. Accessed February 3, 2016.
2. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 2013;49:1374-403.
3. 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.
4. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford 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. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber JS, et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med 2012; 366: 707-14.
6. 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.
7. Larkin J, Ascierto PA, Dreno B, Atkinson V, Liszkay G, Maio M, et al. Combined vemurafenib and cobimetinib in BRAF-mutated melanoma . N Engl J Med 2014; 371: 1867-76.
8. Long GV, Stroyakovskiy D, Gogas H, Levchenko E, de Braud F, Larkin J, et al. Combined BRAF and MEK inhibition versus BRAF inhibition alone in melanoma. N Engl J Med 2014; 371: 1877-88.
9. Girotti MR, Saturno G, Lorigan P, Marais R. No longer an untreatable disease: How targeted and immunotherapies have changed the management of melanoma patients. Mol Oncol 2014; 8: 1140-58.
10. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015; 373: 23-34.
11. Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med 2015; 372: 2521-32.
12. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014; 371: 2189-99.
13. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014; 515: 568-71.
14. Ackerman A, Klein O, McDermott DF, Wang W, Ibrahim N, Lawrence DP, et al. Outcomes of patients with metastatic melanoma treated with immunotherapy prior to or after BRAF inhibitors. Cancer 2014; 120: 1695-701.
15. Chan M, Haydu L, Menzies AM, Azer MWF, Klein O, Guminski A, et al. Clinical characteristics and survival of BRAF-mutant (BRAF+) metastatic melanoma patients (pts) treated with BRAF inhibitor (BRAFi) dabrafenib or vemurafenib beyond disease progression (PD). J Clin Oncol 31, 2013 (suppl; abstr 9062).
16. Stratton MR. Exploring the genomes of cancer cells: progress and promise. Science 2011; 331: 1553-8.
17. 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.
18. Yang W, Soares J, Greninger P, Edelman EJ, Lightfoot H, Forbes S, et al. Genomics of Drug Sensitivity in Cancer (GDSC): a resource for therapeutic biomarker discovery in cancer cells. Nucleic Acids Res 2013; 41: D955-61.
19. Shi H, Hugo W, Kong X, Hong A, Koya RC, Moriceau G, et al. Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov 2014; 4: 80-93.
20. Chan KC, Jiang P, Zheng YW, Liao GJ, Sun H, Wong J, et al. Cancer genome scanning in plasma: detection of tumor-associated copy number aberrations, single-nucleotide variants, and tumoral heterogeneity by massively parallel sequencing. Clin Chem 2013; 59: 211-24.
21. Murtaza M, Dawson SJ, Tsui DW, Gale D, Forshew T, Piskorz A M, et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 2013; 497: 108-12.
22. Einarsdottir BO, Bagge RO, Bhadury J, Jespersen H, Mattsson J, N ilsson LM, et al. Melanoma patient-derived xenografts accurately model the disease and develop fast enough to guide treatment decisions. Oncotarget 2014; 5: 9609-18.
23. Hodgkinson CL, Morrow CJ, Li Y, Metcalf RL, Rothwell DG, Trapani F, et al. Tumorigenicity and genetic profiling of circulating tumor cells in small-cell lung cancer. Nat Med 2014; 20: 897-903.
24. http://www.ema.europa.eu.WC500021864-8.pdf. Accessed December 16, 2015.
25. Girotti MR, Lopes F, Preece N, Niculescu-Duvaz D, Zambon A, Davies L, et al. Paradox-breaking RAF inhibitors that also target SRC are effective in drug-resistant BRAF mutant melanoma. Cancer Cell 2015; 27: 85-96.
26. Su F, Viros A, Milagre C, Trunzer K, Bollag G, Spleiss O, et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med 2012; 366: 207-15.
27. Johnson DB, Flaherty KT, Weber JS, Infante JR, Kim KB, Kefford RF, et al. Combined BRAF (Dabrafenib) and MEK inhibition (Trametinib) in patients with BRAFV600-mutant melanoma experiencing progression with single-agent BRAF inhibitor. J Clin Oncol 2014; 32: 3697-704.
28. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 2010; 140: 209-21.
29. Sanchez-Laorden B, Viros A, Girotti MR, Pedersen M, Saturno G, Zambon A, et al. BRAF inhibitors induce metastasis in RAS mutant or inhibitor-resistant melanoma cells by reactivating MEK and ERK signaling. Sci Signal 2014; 7: ra30.
30. Cancer Genome Atlas Network. Genomic classification of cutaneous melanoma. Cell 2015; 161: 1681-96.
31. 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.
32. Van Allen EM, Wagle N, Sucker A, Treacy DJ, Johannessen CM, Goetz EM, et al. The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov 2014; 4: 94-109.
33. Busser B, Leccia MT, Gras-Combe G, Bricault I, Templier I, Claeys A, et al. Identification of a novel complex BRAF mutation associated with major clinical response to vemurafenib in a patient with metastatic melanoma. JAMA Dermatol 2013; 149: 1403-6.
34. Pedersen M, Viros A, Cook M, Marais R. (G12D) NRAS and kinasedead BRAF cooperate to drive naevogenesis and melanomagenesis. Pigment Cell Melanoma Res 2014; 27: 1162-6.
35. http://www.cancerrxgene.org. Accessed August 6, 2014.
36. Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014; 6: 224ra24.
37. Dawson SJ, Tsui DW, Murtaza M, Biggs H, Rueda OM, Chin SF, et al. Analysis of circulating tumor DNA to monitor metastatic breast cancer . N Engl J Med 2013; 368: 1199-209.
38. Garcia-Murillas I, Schiavon G, Weigelt B, Ng C, Hrebien S, Cutts RJ, et al. Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Sci Transl Med 2015; 7: 302ra133.
39. Chang-Hao Tsao S, Weiss J, Hudson C, Christophi C, Cebon J, Behren A, et al. Monitoring response to therapy in melanoma by quantifying circulating tumour DNA with droplet digital PCR for BRAF and NRAS mutations. Sci Rep 2015; 5: 11198.
40. Lipson EJ, Velculescu VE, Pritchard TS, Sausen M, Pardoll DM, T opalian SL, et al. Circulating tumor DNA analysis as a real-time method for monitoring tumor burden in melanoma patients undergoing treatment with immune checkpoint blockade. J Immunother Cancer 2014; 2: 42.
41. Oxnard GR, Paweletz CP, Kuang Y, Mach SL, O’Connell A, Messineo MM, et al. Noninvasive detection of response and resistance in EGFRmutant lung cancer using quantitative next-generation genotyping of cell-free plasma DNA. Clin Cancer Res 2014; 20: 1698-705.
42. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classifi- cation. J Clin Oncol 2009; 27: 6199-206.
43. Wroblewski F, Gregory KF. Lactic dehydrogenase isozymes and their distribution in normal tissues and plasma and in disease states. Ann N Y Acad Sci 1961; 94: 912-32.
44. Gray ES, Rizos H, Reid AL, Boyd SC, Pereira MR, Lo J, et al. Circulating tumor DNA to monitor treatment response and detect acquired resistance in patients with metastatic melanoma. Oncotarget 2015; 6: 42008-18.
45. Obenauf AC, Zou Y, Ji AL, Vanharanta S, Shu W, Shi H, et al. Therapyinduced tumour secretomes promote resistance and tumour progression . Nature 2015; 520: 368-72.
46. Guerreschi P, Scalbert C, Qassemyar A, Kluza J, Ravasi L, Huglo D, et al. Patient-derived tumor xenograft model to guide the use of BRAF inhibitors in metastatic melanoma. Melanoma Res 2013; 23: 373-80.
47. Whittle JR, Lewis MT, Lindeman GJ, Visvader JE. Patient-derived xenograft models of breast cancer and their predictive power. Breast Cancer Res 2015; 17: 17.
48. Cassidy JW, Caldas C, Bruna A. Maintaining tumor heterogeneity in patient-derived tumor xenografts. Cancer Res 2015; 75: 2963-8.
49. Tentler JJ, Tan AC, Weekes CD, Jimeno A, Leong S, Pitts TM, et al. Patient-derived tumour xenografts as models for oncology drug development. Nat Rev Clin Oncol 2012; 9: 338-50.
50. Coupe N, Corrie P, Hategan M, Larkin J, Gore M, Gupta A, et al. PACMEL: a phase 1 dose escalation trial of trametinib (GSK1120212) in combination with paclitaxel. Eur J Cancer 2015; 51: 359-66.
51. Turajlic S, Furney SJ, Stamp G, Rana S, Ricken G, Oduko Y, et al. Whole-genome sequencing reveals complex mechanisms of intrinsic resistance to BRAF inhibition. Ann Oncol 2014; 25: 959-67.