Research brief convergent therapeutic strategies to overcome the heterogeneity of acquired resistance in BRAFv600e colorectal cancer

Cancer Discovery

Volumn 8, Issue 4, 2018, Pages 417-427

  Hazar Rethinam, Mehlika ^a,b   Kleyman, Marianna ^a,b   Han, G Celine ^c,d   Liu, David ^c,d   Ahronian, Leanne G ^a,b   Shahzade, Heather A ^a,b   Chen, Lifeng ^a,b   Parikh, Aparna R ^a,b   Allen, Jill N ^a,b   Clark, Jeffrey W ^a,b   Kwak, Eunice L ^a,b   Faris, Jason E ^a,b   Murphy, Janet E ^a,b   Hong, Theodore S ^a,e   van Seventer, Emily E ^a,b   Nadres, Brandon ^a,b   Hong, Catriona B ^a,b   Gurski, Joseph M ^a,b   Jessop, Nicholas A ^a,e   Dias Santagata, Dora ^a,e   Iafrate, A John ^a,e   van Allen, Eliezer M ^c,d   Corcoran, Ryan B ^a,b   more..

^a MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

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

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPELISIB; B RAF KINASE; CETUXIMAB; DABRAFENIB; ENCORAFENIB; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PANITUMUMAB; TRAMETINIB; ULIXERTINIB; ANTINEOPLASTIC AGENT; BRAF PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HETEROGENEITY; COLORECTAL CANCER; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DROPLET DIGITAL POLYMERASE CHAIN REACTION; FEMALE; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAPK SIGNALING; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR VOLUME; WHOLE EXOME SEQUENCING; ANIMAL; ANTAGONISTS AND INHIBITORS; COLORECTAL TUMOR; DRUG RESISTANCE; DRUG SCREENING; ENZYMOLOGY; GENETICS; METABOLISM; MISSENSE MUTATION; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, NUDE; MUTATION, MISSENSE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; WHOLE EXOME SEQUENCING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 85047872487     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-17-1227     Document Type: Article

References (36)

1. Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012;487: 330-7.
2. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, et al. Mutations of the BRAF gene in human cancer. Nature 2002;417: 949-54.
3. Richman SD, Seymour MT, Chambers P, Elliott F, Daly CL, Meade AM, 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.
4. Kopetz S, Desai J, Chan E, Hecht JR, O’Dwyer PJ, Maru D, et al. Phase II pilot study of vemurafenib in patients with metastatic BRAFmutated colorectal cancer. J Clin Oncol 2015;33:4032-8.
5. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, et al. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 2010;363:809-19.
6. 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.
7. Corcoran RB, Dias-Santagata D, Bergethon K, Iafrate AJ, Settleman J, Engelman JA. BRAF gene amplification can promote acquired resistance to MEK inhibitors in cancer cells harboring the BRAF V600E mutation. Sci Signal 2010;3:ra84.
8. Corcoran RB, Ebi H, Turke AB, Coffee EM, Nishino M, Cogdill AP, et al. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov 2012;2:227-35.
9. 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.
10. Montero-Conde C, Ruiz-Llorente S, Dominguez JM, Knauf JA, Viale A, Sherman EJ, et al. Relief of feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAF-mutant thyroid carcinomas. Cancer Discov 2013;3:520-33.
11. van Geel R, Tabernero J, Elez E, Bendell JC, Spreafico A, Schuler M, et al. A Phase Ib dose-escalation study of encorafenib and cetuximab with or without alpelisib in metastatic BRAF-mutant colorectal cancer. Cancer Discov 2017;7:610-9.
12. Hong DS, Morris VK, El Osta B, Sorokin AV, Janku F, Fu S, et al. Phase IB study of vemurafenib in combination with irinotecan and cetuximab in patients with metastatic colorectal cancer with BRAFV600E mutation. Cancer Discov 2016;6:1352-65.
13. Corcoran RB, Atreya CE, Falchook GS, Kwak EL, Ryan DP, Bendell JC, et al. Combined BRAF and MEK inhibition with dabrafenib and trametinib in BRAF V600-mutant colorectal cancer. J Clin Oncol 2015;33:4023-31.
14. Hyman DM, Puzanov I, Subbiah V, Faris JE, Chau I, Blay JY, et al. Vemurafenib in multiple nonmelanoma cancers with BRAF V600 mutations. N Engl J Med 2015;373:726-36.
15. Yaeger R, Cercek A, O’Reilly EM, Reidy DL, Kemeny N, Wolinsky T, et al. Pilot trial of combined BRAF and EGFR inhibition in BRAFmutant metastatic colorectal cancer patients. Clin Cancer Res 2015;21: 1313-20.
16. Corcoran RB, André T, Atreya CE, Schellens JHM, Yoshino T, Bendell JC, et al. Combined BRAF, EGFR, and MEK inhibition in patients with BRAFV600E-mutant colorectal cancer. Cancer Discov 2018;8:428-43.
17. Ahronian LG, Sennott EM, Van Allen EM, Wagle N, Kwak EL, Faris JE, et al. Clinical acquired resistance to RAF inhibitor combinations in BRAF-mutant colorectal cancer through MAPK pathway alterations. Cancer Discov 2015;5:358-67.
18. Oddo D, Sennott EM, Barault L, Valtorta E, Arena S, Cassingena A, et al. Molecular landscape of acquired resistance to targeted therapy combinations in BRAF-mutant colorectal cancer. Cancer Res 2016;76:4504-15.
19. Pietrantonio F, Oddo D, Gloghini A, Valtorta E, Berenato R, Barault L, et al. MET-driven resistance to dual EGFR and BRAF blockade may be overcome by switching from EGFR to MET inhibition in BRAFmutated colorectal cancer. Cancer Discov 2016;6:963-71.
20. Russo M, Bardelli A. Lesion-directed therapies and monitoring tumor evolution using liquid biopsies. Cold Spring Harb Perspect Med 2017;7:a029587.
21. 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.
22. Misale S, Yaeger R, Hobor S, Scala E, Janakiraman M, Liska D, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012;486:532-6.
23. Russo M, Siravegna G, Blaszkowsky LS, Corti G, Crisafulli G, Ahronian LG, et al. Tumor heterogeneity and lesion-specific response to targeted therapy in colorectal cancer. Cancer Discov 2016;6:147-53.
24. Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J, Endesfelder D, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 2012;366:883-92.
25. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS, et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012;481:506-10.
26. Turke AB, Zejnullahu K, Wu YL, Song Y, Dias-Santagata D, Lifshits E, et al. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010;17:77-88.
27. Yaeger R, Yao Z, Hyman DM, Hechtman JF, Vakiani E, Zhao H, et al. Mechanisms of acquired resistance to BRAF V600E inhibition in colon cancers converge on RAF dimerization and are sensitive to its inhibition. Cancer Res 2017;77:6513-23.
28. Misale S, Di Nicolantonio F, Sartore-Bianchi A, Siena S, Bardelli A. Resistance to anti-EGFR therapy in colorectal cancer: from heterogeneity to convergent evolution. Cancer Discov 2014;4:1269-80.
29. Tricker EM, Xu C, Uddin S, Capelletti M, Ercan D, Ogino A, et al. Combined EGFR/MEK inhibition prevents the emergence of resistance in EGFR-mutant lung cancer. Cancer Discov 2015;5:960-71.
30. Hrustanovic G, Olivas V, Pazarentzos E, Tulpule A, Asthana S, Blakely CM, et al. RAS-MAPK dependence underlies a rational polytherapy strategy in EML4-ALK-positive lung cancer. Nat Med 2015;21:1038-47.
31. Little AS, Balmanno K, Sale MJ, Newman S, Dry JR, Hampson M, et al. Amplification of the driving oncogene, KRAS or BRAF, underpins acquired resistance to MEK1/2 inhibitors in colorectal cancer cells. Sci Signal 2011;4:ra17.
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. Van Allen EM, Wagle N, Stojanov P, Perrin DL, Cibulskis K, Marlow S, et al. Whole-exome sequencing and clinical interpretation of formalin-fixed, paraffin-embedded tumor samples to guide precision cancer medicine. Nat Med 2014;20:682-8.
34. 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.
35. Lanman RB, Mortimer SA, Zill OA, Sebisanovic D, Lopez R, Blau S, et al. Analytical and clinical validation of a digital sequencing panel for quantitative, highly accurate evaluation of cell-free circulating tumor DNA. PLoS One 2015;10:e0140712.
36. Siravegna G, Mussolin B, Buscarino M, Corti G, Cassingena A, Crisafulli G, et al. Clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nat Med 2015;21:795-801.