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Review

Advances in the therapy of BRAFV600E metastatic colorectal cancer

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Pages 823-829 | Received 28 Apr 2019, Accepted 27 Aug 2019, Published online: 04 Sep 2019

References

  • Davies H, Bignell GR, Cox C, et al. Mutations of the BRAF gene in human cancer. Nature. 2002 Jun 27;417(6892):949–954. PubMed PMID: 12068308.
  • Loupakis F, Ruzzo A, Cremolini C, et al. KRAS codon 61, 146 and BRAF mutations predict resistance to cetuximab plus irinotecan in KRAS codon 12 and 13 wild-type metastatic colorectal cancer. Br J Cancer. 2009 Aug 18;101(4):715–721. PubMed PMID: 19603018; PubMed Central PMCID: PMCPMC2736831.
  • Marchetti A, Felicioni L, Malatesta S, et al. Clinical features and outcome of patients with non-small-cell lung cancer harboring BRAF mutations. J Clin Oncol. 2011 Sep 10;29(26):3574–3579. PubMed PMID: 21825258.
  • Xing M, Alzahrani AS, Carson KA, et al. Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA. 2013 Apr 10;309(14):1493–1501. PubMed PMID: 23571588; PubMed Central PMCID: PMCPMC3791140.
  • Goeppert B, Frauenschuh L, Renner M, et al. BRAF V600E-specific immunohistochemistry reveals low mutation rates in biliary tract cancer and restriction to intrahepatic cholangiocarcinoma. Mod Pathol. 2014 Jul;27(7):1028–1034. PubMed PMID: 24309328.
  • Grisham RN, Iyer G, Garg K, et al. BRAF mutation is associated with early stage disease and improved outcome in patients with low-grade serous ovarian cancer. Cancer. 2013 Feb 1;119(3):548–554. PubMed PMID: 22930283; PubMed Central PMCID: PMCPMC3961140.
  • Takahashi Y, Akahane T, Sawada T, et al. Adult classical glioblastoma with a BRAF V600E mutation. World J Surg Oncol. 2015 Mar 11;13:100. PubMed PMID: 25885250; PubMed Central PMCID: PMCPMC4358908.
  • Tie J, Gibbs P, Lipton L, et al. Optimizing targeted therapeutic development: analysis of a colorectal cancer patient population with the BRAF(V600E) mutation. Int J Cancer. 2011 May 1;128(9):2075–2084. PubMed PMID: 20635392.
  • Yoon HH, Shi Q, Alberts SR, et al. Racial differences in BRAF/KRAS mutation rates and survival in stage III colon cancer patients. J Natl Cancer Inst. 2015 Oct;107(10):djv186. PubMed PMID: 26160882; PubMed Central PMCID: PMCPMC5758035.
  • Loupakis F, Moretto R, Aprile G, et al. Clinico-pathological nomogram for predicting BRAF mutational status of metastatic colorectal cancer. Br J Cancer. 2016 Jan 12;114(1):30–36. PubMed PMID: 26575603; PubMed Central PMCID: PMCPMC4716533.
  • Tran B, Kopetz S, Tie J, et al. Impact of BRAF mutation and microsatellite instability on the pattern of metastatic spread and prognosis in metastatic colorectal cancer. Cancer. 2011 Oct 15;117(20):4623–4632. PubMed PMID: 21456008; PubMed Central PMCID: PMCPMC4257471.
  • Sinicrope FA, Shi Q, Smyrk TC, et al. Molecular markers identify subtypes of stage III colon cancer associated with patient outcomes. Gastroenterology. 2015 Jan;148(1):88–99. PubMed PMID: 25305506; PubMed Central PMCID: PMCPMC4274188.
  • Maughan TS, Adams RA, Smith CG, et al. Addition of cetuximab to oxaliplatin-based first-line combination chemotherapy for treatment of advanced colorectal cancer: results of the randomised phase 3 MRC COIN trial. Lancet. 2011 Jun 18;377(9783):2103–2114. PubMed PMID: 21641636; PubMed Central PMCID: PMCPMC3159415.
  • Stintzing S, Miller-Phillips L, Modest DP, et al. Impact of BRAF and RAS mutations on first-line efficacy of FOLFIRI plus cetuximab versus FOLFIRI plus bevacizumab: analysis of the FIRE-3 (AIO KRK-0306) study. Eur J Cancer. 2017 Jul;79:50–60. PubMed PMID: 28463756.
  • Gryfe R, Kim H, Hsieh ET, et al. Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N Engl J Med. 2000 Jan 13;342(2):69–77. PubMed PMID: 10631274.
  • Sinicrope FA, Mahoney MR, Smyrk TC, et al. Prognostic impact of deficient DNA mismatch repair in patients with stage III colon cancer from a randomized trial of FOLFOX-based adjuvant chemotherapy. J Clin Oncol. 2013 Oct 10;31(29):3664–3672. PubMed PMID: 24019539; PubMed Central PMCID: PMCPMC3789216.
  • Overman MJ, Lonardi S, Wong KYM, et al. Durable clinical benefit with nivolumab plus ipilimumab in DNA mismatch repair-deficient/microsatellite instability-high metastatic colorectal cancer. J Clin Oncol. 2018 Mar 10;36(8):773. PubMed PMID: WOS:000427171900008; English.
  • Gonsalves WI, Mahoney MR, Sargent DJ, et al. Patient and tumor characteristics and BRAF and KRAS mutations in colon cancer, NCCTG/Alliance N0147. J Natl Cancer Inst. 2014 Jul;106(7). PubMed PMID: 24925349; PubMed Central PMCID: PMCPMC4110470. DOI:10.1093/jnci/dju106
  • Jin Z, Sanhueza CT, Johnson B, et al. Outcome of mismatch repair-deficient metastatic colorectal cancer: the Mayo clinic experience. Oncologist. 2018 Sep;23(9):1083–1091. PubMed PMID: 29674439; PubMed Central PMCID: PMCPMC6192616.
  • Venderbosch S, Nagtegaal ID, Maughan TS, et al. Mismatch repair status and BRAF mutation status in metastatic colorectal cancer patients: a pooled analysis of the CAIRO, CAIRO2, COIN, and FOCUS studies. Clin Cancer Res. 2014 Oct 15;20(20):5322–5330. PubMed PMID: 25139339; PubMed Central PMCID: PMCPMC4201568.
  • Overman MJ, McDermott R, Leach JL, et al. Nivolumab in patients with metastatic DNA mismatch repair-deficient or microsatellite instability-high colorectal cancer (CheckMate 142): an open-label, multicentre, phase 2 study. Lancet Oncol. 2017 Sep;18(9):1182–1191. PubMed PMID: 28734759; PubMed Central PMCID: PMCPMC6207072.
  • Le DT, Uram JN, Wang H, et al. PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015 Jun 25;372(26):2509–2520. PubMed PMID: 26028255; PubMed Central PMCID: PMCPMC4481136.
  • Masi G, Loupakis F, Salvatore L, et al. Bevacizumab with FOLFOXIRI (irinotecan, oxaliplatin, fluorouracil, and folinate) as first-line treatment for metastatic colorectal cancer: a phase 2 trial. Lancet Oncol. 2010 Sep;11(9):845–852. PubMed PMID: 20702138.
  • Loupakis F, Cremolini C, Salvatore L, et al. FOLFOXIRI plus bevacizumab as first-line treatment in BRAF mutant metastatic colorectal cancer. Eur J Cancer. 2014 Jan;50(1):57–63. PubMed PMID: 24138831.
  • Cremolini C, Loupakis F, Antoniotti C, et al. FOLFOXIRI plus bevacizumab versus FOLFIRI plus bevacizumab as first-line treatment of patients with metastatic colorectal cancer: updated overall survival and molecular subgroup analyses of the open-label, phase 3 TRIBE study. Lancet Oncol. 2015 Oct;16(13):1306–1315. PubMed PMID: 26338525.
  • Cremolini C, Antoniotti C, Lonardi S, et al. Updated results of TRIBE2, a phase III, randomized strategy study by GONO in the first- and second-line treatment of unresectable mCRC. J Clin Oncol. 2019 May 20;37(15_suppl):3508.
  • Karapetis CS, Jonker D, Daneshmand M, et al. PIK3CA, BRAF, and PTEN status and benefit from cetuximab in the treatment of advanced colorectal cancer–results from NCIC CTG/AGITG CO.17. Clin Cancer Res. 2014 Feb 1;20(3):744–753. PubMed PMID: 24218517.
  • Peeters M, Oliner KS, Price TJ, et al. Analysis of KRAS/NRAS mutations in a phase III study of panitumumab with FOLFIRI compared with FOLFIRI alone as second-line treatment for metastatic colorectal cancer. Clin Cancer Res. 2015 Dec 15;21(24):5469–5479. PubMed PMID: 26341920.
  • Seymour MT, Brown SR, Middleton G, et al. Panitumumab and irinotecan versus irinotecan alone for patients with KRAS wild-type, fluorouracil-resistant advanced colorectal cancer (PICCOLO): a prospectively stratified randomised trial. Lancet Oncol. 2013 Jul;14(8):749–759. PubMed PMID: 23725851; PubMed Central PMCID: PMCPMC3699713.
  • Bokemeyer C, Van Cutsem E, Rougier P, et al. Addition of cetuximab to chemotherapy as first-line treatment for KRAS wild-type metastatic colorectal cancer: pooled analysis of the CRYSTAL and OPUS randomised clinical trials. Eur J Cancer. 2012 Jul;48(10):1466–1475. PubMed PMID: 22446022.
  • Geissler M, Riera-Knorrenschild J, Martens UM, et al. Final results and OS of the randomized phase II VOLFI trial (AIO- KRK0109): mFOLFOXIRI + panitumumab versus FOLFOXIRI as first-line treatment in patients with RAS wild- type metastatic colorectal cancer (mCRC). J Clin Oncol. 2019;37(15_suppl):3511.
  • Chapman PB, Hauschild A, Robert C, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011 Jun 30;364(26):2507–2516. PubMed PMID: 21639808; PubMed Central PMCID: PMCPMC3549296.
  • Yang H, Higgins B, Kolinsky K, et al. Antitumor activity of BRAF inhibitor vemurafenib in preclinical models of BRAF-mutant colorectal cancer. Cancer Res. 2012 Feb 1;72(3):779–789. PubMed PMID: 22180495.
  • Kopetz S, Desai J, Chan E, et al. Phase II pilot study of vemurafenib in patients with metastatic BRAF-mutated colorectal cancer. J Clin Oncol. 2015 Dec 1;33(34):4032–4038. PubMed PMID: 26460303; PubMed Central PMCID: PMCPMC4669589.
  • Prahallad A, Sun C, Huang S, et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature. 2012 Jan 26;483(7387):100–103. PubMed PMID: 22281684.
  • Corcoran RB, Ebi H, Turke AB, 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 Mar;2(3):227–235. PubMed PMID: 22448344; PubMed Central PMCID: PMCPMC3308191.
  • Yaeger R, Cercek A, O’Reilly EM, et al. Pilot trial of combined BRAF and EGFR inhibition in BRAF-mutant metastatic colorectal cancer patients. Clin Cancer Res. 2015 Mar 15;21(6):1313–1320. PubMed PMID: 25589621; PubMed Central PMCID: PMCPMC5546416.
  • Kopetz S, McDonough SL, Morris VK, et al. Randomized trial of irinotecan and cetuximab with or without vemurafenib in BRAF-mutant metastatic colorectal cancer (SWOG 1406). J Clin Oncol. 2017;35(4_suppl):520.
  • Dummer R, Ascierto PA, Gogas HJ, et al. Encorafenib plus binimetinib versus vemurafenib or encorafenib in patients with BRAF-mutant melanoma (COLUMBUS): a multicentre, open-label, randomised phase 3 trial. Lancet Oncol. 2018 May;19(5):603–615. PubMed PMID: 29573941.
  • Planchard D, Besse B, Groen HJM, et al. Dabrafenib plus trametinib in patients with previously treated BRAF(V600E)-mutant metastatic non-small cell lung cancer: an open-label, multicentre phase 2 trial. Lancet Oncol. 2016 Jul;17(7):984–993. PubMed PMID: 27283860; PubMed Central PMCID: PMCPMC4993103.
  • Corcoran RB, Andre T, Atreya CE, et al. Combined BRAF, EGFR, and MEK inhibition in patients with BRAF(V600E)-mutant colorectal cancer. Cancer Discov. 2018 Apr;8(4):428–443. PubMed PMID: 29431699; PubMed Central PMCID: PMCPMC5882509.
  • Van Cutsem E, Huijberts S, Grothey A, et al. Binimetinib, encorafenib, and cetuximab triplet therapy for patients with BRAF V600E-mutant metastatic colorectal cancer: safety lead-in results from the phase III BEACON colorectal cancer study. J Clin Oncol. 2019 Mar 20;JCO1802459. PubMed PMID: 30892987. DOI:10.1200/JCO.18.02459
  • Kopetz S, Grothey A, Van Cutsem E, et al. LBA-006BEACON CRC: a randomized, 3-Arm, phase 3 study of encorafenib and cetuximab with or without binimetinib vs. choice of either irinotecan or FOLFIRI plus cetuximab in BRAF V600E–mutant metastatic colorectal cancer. Ann Oncol. 2019;30(Supplement_4). DOI:10.1093/annonc/mdz183.004
  • Mao M, Tian F, Mariadason JM, et al. Resistance to BRAF inhibition in BRAF-mutant colon cancer can be overcome with PI3K inhibition or demethylating agents. Clin Cancer Res. 2013 Feb 1;19(3):657–667. PubMed PMID: 23251002; PubMed Central PMCID: PMCPMC3563727.
  • van Geel R, Tabernero J, Elez E, 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 Jun;7(6):610–619. PubMed PMID: 28363909; PubMed Central PMCID: PMCPMC5546207.
  • Sinicrope FA. Lynch Syndrome-Associated Colorectal Cancer. N Engl J Med. 2018 Aug 23;379(8):764–773. PubMed PMID: 30134129.
  • Le DT, Durham JN, Smith KN, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 2017 Jul 28;357(6349):409–413. PubMed PMID: 28596308; PubMed Central PMCID: PMCPMC5576142.
  • Gavin PG, Colangelo LH, Fumagalli D, et al. Mutation profiling and microsatellite instability in stage II and III colon cancer: an assessment of their prognostic and oxaliplatin predictive value. Clin Cancer Res. 2012 Dec 1;18(23):6531–6541. PubMed PMID: 23045248; PubMed Central PMCID: PMCPMC4273673.
  • Roth AD, Tejpar S, Delorenzi M, et al. Prognostic role of KRAS and BRAF in stage II and III resected colon cancer: results of the translational study on the PETACC-3, EORTC 40993, SAKK 60-00 trial. J Clin Oncol. 2010 Jan 20;28(3):466–474. PubMed PMID: 20008640.
  • Taieb J, Le Malicot K, Shi Q, et al. Prognostic value of BRAF and KRAS mutations in MSI and MSS stage III colon cancer. J Natl Cancer Inst. 2017 May;109(5). PubMed PMID: 28040692; PubMed Central PMCID: PMCPMC6075212. DOI:10.1093/jnci/djw272
  • Sinicrope FA, Shi Q, Allegra CJ, et al. Association of DNA mismatch repair and mutations in BRAF and KRAS with survival after recurrence in stage III colon cancers: a secondary analysis of 2 randomized clinical trials. JAMA Oncol. 2017 Apr 1;3(4):472–480. PubMed PMID: 28006055; PubMed Central PMCID: PMCPMC5498991.
  • Sinicrope FA, Ou F-S, Shi Q, et al. Randomized trial of FOLFOX alone or combined with atezolizumab as adjuvant therapy for patients with stage III colon cancer and deficient DNA mismatch repair or microsatellite instability (ATOMIC, Alliance A021502). J Clin Oncol. 2017;35(15_suppl):TPS3630–TPS3630.
  • Poulikakos PI, Zhang C, Bollag G, et al. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature. 2010 Mar 18;464(7287):427–430. PubMed PMID: 20179705; PubMed Central PMCID: PMCPMC3178447.
  • Pratilas CA, Taylor BS, Ye Q, et al. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4519–4524. PubMed PMID: 19251651; PubMed Central PMCID: PMCPMC2649208.
  • Van Allen EM, Wagle N, Sucker A, et al. The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov. 2014 Jan;4(1):94–109. PubMed PMID: 24265153; PubMed Central PMCID: PMCPMC3947264.
  • Lito P, Pratilas CA, Joseph EW, et al. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell. 2012 Nov 13;22(5):668–682. PubMed PMID: 23153539; PubMed Central PMCID: PMCPMC3713778.
  • Yao Z, Torres NM, Tao A, et al. BRAF mutants evade ERK-dependent feedback by different mechanisms that determine their sensitivity to pharmacologic inhibition. Cancer Cell. 2015 Sep 14;28(3):370–383. PubMed PMID: 26343582; PubMed Central PMCID: PMCPMC4894664.
  • Yao Z, Gao Y, Su W, et al. RAF inhibitor PLX8394 selectively disrupts BRAF dimers and RAS-independent BRAF-mutant-driven signaling. Nat Med. 2019 Feb;25(2):284–291. PubMed PMID: 30559419; PubMed Central PMCID: PMCPMC6404779.
  • Hazar-Rethinam M, Kleyman M, Han GC, et al. Convergent therapeutic strategies to overcome the heterogeneity of acquired resistance in BRAF(V600E) colorectal cancer. Cancer Discov. 2018 Apr;8(4):417–427. PubMed PMID: 29431697; PubMed Central PMCID: PMCPMC5882515.
  • Xue G, Kohler R, Tang F, et al. mTORC1/autophagy-regulated MerTK in mutant BRAFV600 melanoma with acquired resistance to BRAF inhibition. Oncotarget. 2017 Sep 19;8(41):69204–69218. PubMed PMID: 29050198; PubMed Central PMCID: PMCPMC5642473.
  • Bettegowda C, Sausen M, Leary RJ, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 2014 Feb 19;6(224):224ra24. PubMed PMID: 24553385; PubMed Central PMCID: PMCPMC4017867.
  • Thierry AR, Mouliere F, El Messaoudi S, et al. Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA. Nat Med. 2014 Apr;20(4):430–435. PubMed PMID: 24658074.
  • Siravegna G, Mussolin B, Buscarino M, et al. Clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nat Med. 2015 Jul;21(7):795–801. PubMed PMID: 26030179; PubMed Central PMCID: PMCPMC4868598.
  • Toledo RA, Cubillo A, Vega E, et al. Clinical validation of prospective liquid biopsy monitoring in patients with wild-type RAS metastatic colorectal cancer treated with FOLFIRI-cetuximab. Oncotarget. 2017 May 23;8(21):35289–35300. PubMed PMID: 27852040; PubMed Central PMCID: PMCPMC5471055.
  • Thierry AR, Pastor B, Jiang ZQ, et al. Circulating DNA demonstrates convergent evolution and common resistance mechanisms during treatment of colorectal cancer. Clin Cancer Res. 2017 Aug 15;23(16):4578–4591. PubMed PMID: 28400427; PubMed Central PMCID: PMCPMC5562356.

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