Revisiting the Role of B-RAF Kinase as a Therapeutic Target in Melanoma


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Malignant melanoma is the rarest but most aggressive and deadly skin cancer. Melanoma is the result of a malignant transformation of melanocytes, which leads to their uncontrolled proliferation. Mutations in the mitogen-activated protein kinase (MAPK) pathway, which are crucial for the control of cellular processes, such as apoptosis, division, growth, differentiation, and migration, are one of its most common causes. BRAF kinase, as one of the known targets of this pathway, has been known for many years as a prominent molecular target in melanoma therapy, and the following mini-review outlines the state-of-the-art knowledge regarding its structure, mutations and mechanisms.

作者简介

Paweł Kozyra

Independent Radiopharmacy Unit, Faculty of Pharmacy,, Medical University of Lublin

编辑信件的主要联系方式.
Email: info@benthamscience.net

Monika Pitucha

Independent Radiopharmacy Unit, Faculty of Pharmacy,, Medical University of Lublin

Email: info@benthamscience.net

参考

  1. Ernst, M.; Giubellino, A. The current state of treatment and future directions in cutaneous malignant melanoma. Biomedicines, 2022, 10(4), 822. doi: 10.3390/biomedicines10040822 PMID: 35453572
  2. Dimitriou, F.; Krattinger, R.; Ramelyte, E.; Barysch, M.J.; Micaletto, S.; Dummer, R.; Goldinger, S.M. The world of melanoma: Epidemiologic, genetic, and anatomic differences of melanoma across the globe. Curr. Oncol. Rep., 2018, 20(11), 87. doi: 10.1007/s11912-018-0732-8 PMID: 30250984
  3. Millet, A.; Martin, A.R.; Ronco, C.; Rocchi, S.; Benhida, R. Metastatic melanoma: Insights into the evolution of the treatments and future challenges. Med. Res. Rev., 2017, 37(1), 98-148. doi: 10.1002/med.21404 PMID: 27569556
  4. Garbe, C.; Amaral, T.; Peris, K.; Hauschild, A.; Arenberger, P.; Bastholt, L.; Bataille, V.; del Marmol, V.; Dréno, B.; Fargnoli, M.C.; Grob, J.J.; Höller, C.; Kaufmann, R.; Lallas, A.; Lebbé, C.; Malvehy, J.; Middleton, M.; Moreno-Ramirez, D.; Pellacani, G.; Saiag, P.; Stratigos, A.J.; Vieira, R.; Zalaudek, I.; Eggermont, A.M.M. European consensus-based interdisciplinary guideline for melanoma. Part 1: Diagnostics – Update 2019. Eur. J. Cancer, 2020, 126, 141-158. doi: 10.1016/j.ejca.2019.11.014 PMID: 31928887
  5. Kozyra, P.; Krasowska, D.; Pitucha, M. New potential agents for malignant melanoma treatment-most recent studies 2020–2022. Int. J. Mol. Sci., 2022, 23(11), 6084. doi: 10.3390/ijms23116084 PMID: 35682764
  6. Kozyra, P.; Korga-Plewko, A.; Karczmarzyk, Z.; Hawrył, A.; Wysocki, W.; Człapski, M.; Iwan, M.; Ostrowska-Leśko, M.; Fornal, E.; Pitucha, M. Potential anticancer agents against melanoma cells based on an as-synthesized thiosemicarbazide derivative. Biomolecules, 2022, 12(2), 151. doi: 10.3390/biom12020151 PMID: 35204651
  7. Kozyra, P.; Pitucha, M. Terminal phenoxy group as a privileged moiety of the drug scaffold-A short review of most recent studies 2013–2022. Int. J. Mol. Sci., 2022, 23(16), 8874. doi: 10.3390/ijms23168874 PMID: 36012142
  8. Pitucha, M.; Korga-Plewko, A.; Kozyra, P.; Iwan, M.; Kaczor, A.A. 2,4-dichlorophenoxyacetic thiosemicarbazides as a new class of compounds against stomach cancer potentially intercalating with DNA. Biomolecules, 2020, 10(2), 296. doi: 10.3390/biom10020296 PMID: 32069994
  9. Matthews, N.H.; Li, W-Q.; Qureshi, A.A.; Weinstock, M.A.; Cho, E. Epidemiology of melanoma. In: Cutaneous Melanoma: Etiology and Therapy; Ward, W.H.; Farma, J.M., Eds.; Codon Publications: Brisbane (AU), 2017. doi: 10.15586/codon.cutaneousmelanoma.2017.ch1
  10. Rebecca, V.W.; Sondak, V.K.; Smalley, K.S.M. A brief history of melanoma. Melanoma Res., 2012, 22(2), 114-122. doi: 10.1097/CMR.0b013e328351fa4d PMID: 22395415
  11. Caksa, S.; Baqai, U.; Aplin, A.E. The future of targeted kinase inhibitors in melanoma. Pharmacol. Ther., 2022, 239, 108200. doi: 10.1016/j.pharmthera.2022.108200 PMID: 35513054
  12. Kłos, P.; Chlubek, D. Plant-derived terpenoids: A promising tool in the fight against melanoma. Cancers, 2022, 14(3), 502. doi: 10.3390/cancers14030502 PMID: 35158770
  13. Lopes, J.; Rodrigues, C.M.P.; Gaspar, M.M.; Reis, C.P. Melanoma management: From epidemiology to treatment and latest advances. Cancers, 2022, 14(19), 4652. doi: 10.3390/cancers14194652 PMID: 36230575
  14. Carr, S.; Smith, C.; Wernberg, J. Epidemiology and risk factors of melanoma. Surg. Clin. North Am., 2020, 100(1), 1-12. doi: 10.1016/j.suc.2019.09.005 PMID: 31753105
  15. Miller, A.J.; Mihm, M.C., Jr Melanoma. N. Engl. J. Med., 2006, 355(1), 51-65. doi: 10.1056/NEJMra052166 PMID: 16822996
  16. Azoury, S.C.; Lange, J.R. Epidemiology, risk factors, prevention, and early detection of melanoma. Surg. Clin. North Am., 2014, 94(5), 945-962. doi: 10.1016/j.suc.2014.07.013 PMID: 25245960
  17. Conforti, C.; Zalaudek, I. Epidemiology and risk factors of melanoma: A review. Dermatol. Pract. Concept., 2021, 11(Suppl. 1), 2021161S. doi: 10.5826/dpc.11S1a161S PMID: 34447610
  18. Melanoma Skin Cancer Statistics. Available from: https://www.cancer.org/cancer/melanoma-skin-cancer/ about/key-statistics.html(accessed on 9 January 2023)
  19. Dhillon, A.S.; Hagan, S.; Rath, O.; Kolch, W. MAP kinase signalling pathways in cancer. Oncogene, 2007, 26(22), 3279-3290. doi: 10.1038/sj.onc.1210421 PMID: 17496922
  20. Savoia, P.; Fava, P.; Casoni, F.; Cremona, O. Targeting the ERK signaling pathway in melanoma. Int. J. Mol. Sci., 2019, 20(6), 1483. doi: 10.3390/ijms20061483 PMID: 30934534
  21. Fang, J.Y.; Richardson, B.C. The MAPK signalling pathways and colorectal cancer. Lancet Oncol., 2005, 6(5), 322-327. doi: 10.1016/S1470-2045(05)70168-6 PMID: 15863380
  22. Sun, Y.; Liu, W.Z.; Liu, T.; Feng, X.; Yang, N.; Zhou, H.F. Signaling pathway of MAPK/ERK in cell proliferation, differentiation, migration, senescence and apoptosis. J. Recept. Signal Transduct. Res., 2015, 35(6), 600-604. doi: 10.3109/10799893.2015.1030412 PMID: 26096166
  23. Burotto, M.; Chiou, V.L.; Lee, J.M.; Kohn, E.C. The MAPK pathway across different malignancies: A new perspective. Cancer, 2014, 120(22), 3446-3456. doi: 10.1002/cncr.28864 PMID: 24948110
  24. Mandalà, M.; Voit, C. Targeting BRAF in melanoma: Biological and clinical challenges. Crit. Rev. Oncol. Hematol., 2013, 87(3), 239-255. doi: 10.1016/j.critrevonc.2013.01.003 PMID: 23415641
  25. Amaral, T.; Sinnberg, T.; Meier, F.; Krepler, C.; Levesque, M.; Niessner, H.; Garbe, C. The mitogen-activated protein kinase pathway in melanoma part I - Activation and primary resistance mechanisms to BRAF inhibition. Eur. J. Cancer, 2017, 73, 85-92. doi: 10.1016/j.ejca.2016.12.010 PMID: 28169047
  26. Garnett, M.J.; Rana, S.; Paterson, H.; Barford, D.; Marais, R. Wild-type and mutant B-RAF activate C-RAF through distinct mechanisms involving heterodimerization. Mol. Cell, 2005, 20(6), 963-969. doi: 10.1016/j.molcel.2005.10.022 PMID: 16364920
  27. Terai, K.; Matsuda, M. The amino-terminal B-Raf-specific region mediates calcium-dependent homo- and hetero-dimerization of Raf. EMBO J., 2006, 25(15), 3556-3564. doi: 10.1038/sj.emboj.7601241 PMID: 16858395
  28. Raman, M.; Chen, W.; Cobb, M.H. Differential regulation and properties of MAPKs. Oncogene, 2007, 26(22), 3100-3112. doi: 10.1038/sj.onc.1210392 PMID: 17496909
  29. Shain, A.H.; Yeh, I.; Kovalyshyn, I.; Sriharan, A.; Talevich, E.; Gagnon, A.; Dummer, R.; North, J.; Pincus, L.; Ruben, B.; Rickaby, W.; D’Arrigo, C.; Robson, A.; Bastian, B.C. The genetic evolution of melanoma from precursor lesions. N. Engl. J. Med., 2015, 373(20), 1926-1936. doi: 10.1056/NEJMoa1502583 PMID: 26559571
  30. Roskoski, R. Jr RAF protein-serine/threonine kinases: Structure and regulation. Biochem. Biophys. Res. Commun., 2010, 399(3), 313-317. doi: 10.1016/j.bbrc.2010.07.092 PMID: 20674547
  31. Palumbo, G.; Di Lorenzo, G.; Ottaviano, M.; Damiano, V. The future of melanoma therapy: Developing new drugs and improving the use of old ones. Future Oncol., 2016, 12(22), 2531-2534. doi: 10.2217/fon-2015-0045 PMID: 27715206
  32. Khan, P.S.; Rajesh, P.; Rajendra, P.; Chaskar, M.G.; Rohidas, A.; Jaiprakash, S. Recent advances in B-RAF inhibitors as anticancer agents. Bioorg. Chem., 2022, 120, 105597. doi: 10.1016/j.bioorg.2022.105597 PMID: 35033817
  33. Kudchadkar, R.; Paraiso, K.H.T.; Smalley, K.S.M. Targeting mutant BRAF in melanoma: Current status and future development of combination therapy strategies. Cancer J., 2012, 18(2), 124-131. doi: 10.1097/PPO.0b013e31824b436e PMID: 22453012
  34. Sabag, N.; Yakobson, A.; Retchkiman, M.; Silberstein, E. Novel biomarkers and therapeutic targets for melanoma. Int. J. Mol. Sci., 2022, 23(19), 11656. doi: 10.3390/ijms231911656 PMID: 36232957
  35. Ny, L.; Hernberg, M.; Nyakas, M.; Koivunen, J.; Oddershede, L.; Yoon, M.; Wang, X.; Guyot, P.; Geisler, J. BRAF mutational status as a prognostic marker for survival in malignant melanoma: A systematic review and meta-analysis. Acta Oncol., 2020, 59(7), 833-844. doi: 10.1080/0284186X.2020.1747636 PMID: 32285732
  36. Cancer Genome Atlas Network. Genomic classification of cutaneous melanoma. Cell, 2015, 161, 1681-1696. doi: 10.1016/j.cell.2015.05.044 PMID: 26091043
  37. Kimura, E.T.; Nikiforova, M.N.; Zhu, Z.; Knauf, J.A.; Nikiforov, Y.E.; Fagin, J.A. High prevalence of BRAF mutations in thyroid cancer: Genetic evidence for constitutive activation of the RET/PTC-RAS-BRAF signaling pathway in papillary thyroid carcinoma. Cancer Res., 2003, 63(7), 1454-1457. PMID: 12670889
  38. Collisson, E.A.; Campbell, J.D.; Brooks, A.N.; Berger, A.H.; Lee, W.; Chmielecki, J.; Beer, D.G.; Cope, L.; Creighton, C.J.; Danilova, L. Comprehensive molecular profiling of lung adenocarcinoma. Nature, 2014, 511(7511), 543-550. doi: 10.1038/nature13385 PMID: 25079552
  39. Subbiah, V.; Baik, C.; Kirkwood, J.M. Clinical development of BRAF plus MEK inhibitor combinations. Trends Cancer, 2020, 6(9), 797-810. doi: 10.1016/j.trecan.2020.05.009 PMID: 32540454
  40. Rajagopalan, H.; Bardelli, A.; Lengauer, C.; Kinzler, K.W.; Vogelstein, B.; Velculescu, V.E. RAF/RAS oncogenes and mismatch-repair status. Nature, 2002, 418(6901), 934-934. doi: 10.1038/418934a PMID: 12198537
  41. Tiacci, E.; Trifonov, V.; Schiavoni, G.; Holmes, A.; Kern, W.; Martelli, M.P.; Pucciarini, A.; Bigerna, B.; Pacini, R.; Wells, V.A.; Sportoletti, P.; Pettirossi, V.; Mannucci, R.; Elliott, O.; Liso, A.; Ambrosetti, A.; Pulsoni, A.; Forconi, F.; Trentin, L.; Semenzato, G.; Inghirami, G.; Capponi, M.; Di Raimondo, F.; Patti, C.; Arcaini, L.; Musto, P.; Pileri, S.; Haferlach, C.; Schnittger, S.; Pizzolo, G.; Foà, R.; Farinelli, L.; Haferlach, T.; Pasqualucci, L.; Rabadan, R.; Falini, B. BRAF mutations in hairy-cell leukemia. N. Engl. J. Med., 2011, 364(24), 2305-2315. doi: 10.1056/NEJMoa1014209 PMID: 21663470
  42. Badalian-Very, G.; Vergilio, J.A.; Degar, B.A.; MacConaill, L.E.; Brandner, B.; Calicchio, M.L.; Kuo, F.C.; Ligon, A.H.; Stevenson, K.E.; Kehoe, S.M.; Garraway, L.A.; Hahn, W.C.; Meyerson, M.; Fleming, M.D.; Rollins, B.J. Recurrent BRAF mutations in Langerhans cell histiocytosis. Blood, 2010, 116(11), 1919-1923. doi: 10.1182/blood-2010-04-279083 PMID: 20519626
  43. Bauer, J.; Büttner, P.; Murali, R.; Okamoto, I.; Kolaitis, N.A.; Landi, M.T.; Scolyer, R.A.; Bastian, B.C. BRAF mutations in cutaneous melanoma are independently associated with age, anatomic site of the primary tumor, and the degree of solar elastosis at the primary tumor site. Pigment Cell Melanoma Res., 2011, 24(2), 345-351. doi: 10.1111/j.1755-148X.2011.00837.x PMID: 21324100
  44. Yao, Z.; Yaeger, R.; Rodrik-Outmezguine, V.S.; Tao, A.; Torres, N.M.; Chang, M.T.; Drosten, M.; Zhao, H.; Cecchi, F.; Hembrough, T.; Michels, J.; Baumert, H.; Miles, L.; Campbell, N.M.; de Stanchina, E.; Solit, D.B.; Barbacid, M.; Taylor, B.S.; Rosen, N. Tumours with class 3 BRAF mutants are sensitive to the inhibition of activated RAS. Nature, 2017, 548(7666), 234-238. doi: 10.1038/nature23291 PMID: 28783719
  45. Lin, Q.; Zhang, H.; Ding, H.; Qian, J.; Lizaso, A.; Lin, J.; Han-Zhang, H.; Xiang, J.; Li, Y.; Zhu, H. The association between BRAF mutation class and clinical features in BRAF-mutant Chinese non-small cell lung cancer patients. J. Transl. Med., 2019, 17(1), 298. doi: 10.1186/s12967-019-2036-7 PMID: 31470866
  46. Śmiech, M.; Leszczyński, P.; Kono, H.; Wardell, C.; Taniguchi, H. Emerging BRAF mutations in cancer progression and their possible effects on transcriptional networks. Genes, 2020, 11(11), 1342. doi: 10.3390/genes11111342 PMID: 33198372
  47. Cantwell-Dorris, E.R.; O’Leary, J.J.; Sheils, O.M. BRAFV600E: Implications for carcinogenesis and molecular therapy. Mol. Cancer Ther., 2011, 10(3), 385-394. doi: 10.1158/1535-7163.MCT-10-0799 PMID: 21388974
  48. Wan, P.T.C.; Garnett, M.J.; Roe, S.M.; Lee, S.; Niculescu-Duvaz, D.; Good, V.M.; Project, C.G.; Jones, C.M.; Marshall, C.J.; Springer, C.J.; Barford, D.; Marais, R. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell, 2004, 116(6), 855-867. doi: 10.1016/S0092-8674(04)00215-6 PMID: 15035987
  49. Haling, J.R.; Sudhamsu, J.; Yen, I.; Sideris, S.; Sandoval, W.; Phung, W.; Bravo, B.J.; Giannetti, A.M.; Peck, A.; Masselot, A.; Morales, T.; Smith, D.; Brandhuber, B.J.; Hymowitz, S.G.; Malek, S. Structure of the BRAF-MEK complex reveals a kinase activity independent role for BRAF in MAPK signaling. Cancer Cell, 2014, 26(3), 402-413. doi: 10.1016/j.ccr.2014.07.007 PMID: 25155755
  50. Park, E.; Rawson, S.; Li, K.; Kim, B.W.; Ficarro, S.B.; Pino, G.G.D.; Sharif, H.; Marto, J.A.; Jeon, H.; Eck, M.J. Architecture of autoinhibited and active BRAF–MEK1–14-3-3 complexes. Nature, 2019, 575(7783), 545-550. doi: 10.1038/s41586-019-1660-y PMID: 31581174
  51. Wenglowsky, S.; Ren, L.; Ahrendt, K.A.; Laird, E.R.; Aliagas, I.; Alicke, B.; Buckmelter, A.J.; Choo, E.F.; Dinkel, V.; Feng, B.; Gloor, S.L.; Gould, S.E.; Gross, S.; Gunzner-Toste, J.; Hansen, J.D.; Hatzivassiliou, G.; Liu, B.; Malesky, K.; Mathieu, S.; Newhouse, B.; Raddatz, N.J.; Ran, Y.; Rana, S.; Randolph, N.; Risom, T.; Rudolph, J.; Savage, S.; Selby, L.T.; Shrag, M.; Song, K.; Sturgis, H.L.; Voegtli, W.C.; Wen, Z.; Willis, B.S.; Woessner, R.D.; Wu, W.I.; Young, W.B.; Grina, J. Pyrazolopyridine inhibitors of B-Raf V600E. Part 1: The development of selective, orally bioavailable, and efficacious inhibitors. ACS Med. Chem. Lett., 2011, 2(5), 342-347. doi: 10.1021/ml200025q PMID: 24900315
  52. Thevakumaran, N.; Lavoie, H.; Critton, D.A.; Tebben, A.; Marinier, A.; Sicheri, F.; Therrien, M. Crystal structure of a BRAF kinase domain monomer explains basis for allosteric regulation. Nat. Struct. Mol. Biol., 2015, 22, 37-43.
  53. Karoulia, Z.; Wu, Y.; Ahmed, T.A.; Xin, Q.; Bollard, J.; Krepler, C.; Wu, X.; Zhang, C.; Bollag, G.; Herlyn, M.; Fagin, J.A.; Lujambio, A.; Gavathiotis, E.; Poulikakos, P.I. An integrated model of RAF inhibitor action predicts inhibitor activity against oncogenic BRAF signaling. Cancer Cell, 2016, 30(3), 485-498. doi: 10.1016/j.ccell.2016.06.024 PMID: 27523909
  54. Cotto-Rios, X.M.; Agianian, B.; Gitego, N.; Zacharioudakis, E.; Giricz, O.; Wu, Y.; Zou, Y.; Verma, A.; Poulikakos, P.I.; Gavathiotis, E. Inhibitors of BRAF dimers using an allosteric site. Nat. Commun., 2020, 11(1), 4370. doi: 10.1038/s41467-020-18123-2 PMID: 32873792
  55. Lavoie, H.; Therrien, M. Regulation of RAF protein kinases in ERK signalling. Nat. Rev. Mol. Cell Biol., 2015, 16(5), 281-298. doi: 10.1038/nrm3979 PMID: 25907612
  56. Wu, X.; Yan, J.; Dai, J.; Ma, M.; Tang, H.; Yu, J.; Xu, T.; Yu, H.; Si, L.; Chi, Z.; Sheng, X.; Cui, C.; Kong, Y.; Guo, J. Mutations in BRAF codons 594 and 596 predict good prognosis in melanoma. Oncol. Lett., 2017, 14(3), 3601-3605. doi: 10.3892/ol.2017.6608 PMID: 28927118
  57. Ottaviano, M.; Giunta, E.; Tortora, M.; Curvietto, M.; Attademo, L.; Bosso, D.; Cardalesi, C.; Rosanova, M.; De Placido, P.; Pietroluongo, E.; Riccio, V.; Mucci, B.; Parola, S.; Vitale, M.; Palmieri, G.; Daniele, B.; Simeone, E. BRAF gene and melanoma: Back to the future. Int. J. Mol. Sci., 2021, 22(7), 3474. doi: 10.3390/ijms22073474 PMID: 33801689
  58. Lu, H.; Villafane, N.; Dogruluk, T.; Grzeskowiak, C.L.; Kong, K.; Tsang, Y.H.; Zagorodna, O.; Pantazi, A.; Yang, L.; Neill, N.J.; Kim, Y.W.; Creighton, C.J.; Verhaak, R.G.; Mills, G.B.; Park, P.J.; Kucherlapati, R.; Scott, K.L. Engineering and functional characterization of fusion genes identifies novel oncogenic drivers of cancer. Cancer Res., 2017, 77(13), 3502-3512. doi: 10.1158/0008-5472.CAN-16-2745 PMID: 28512244
  59. Botton, T.; Talevich, E.; Mishra, V.K.; Zhang, T.; Shain, A.H.; Berquet, C.; Gagnon, A.; Judson, R.L.; Ballotti, R.; Ribas, A.; Herlyn, M.; Rocchi, S.; Brown, K.M.; Hayward, N.K.; Yeh, I.; Bastian, B.C. Genetic heterogeneity of BRAF fusion kinases in melanoma affects drug responses. Cell Rep., 2019, 29(3), 573-588.e7. doi: 10.1016/j.celrep.2019.09.009 PMID: 31618628
  60. Zebisch, A.; Troppmair, J. Back to the roots: The remarkable RAF oncogene story. Cell. Mol. Life Sci., 2006, 63(11), 1314-1330. doi: 10.1007/s00018-006-6005-y PMID: 16649144
  61. Hanks, S.K.; Hunter, T. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J., 1995, 9(8), 576-596. doi: 10.1096/fasebj.9.8.7768349 PMID: 7768349
  62. Tsai, J.; Lee, J.T.; Wang, W.; Zhang, J.; Cho, H.; Mamo, S.; Bremer, R.; Gillette, S.; Kong, J.; Haass, N.K.; Sproesser, K.; Li, L.; Smalley, K.S.M.; Fong, D.; Zhu, Y.L.; Marimuthu, A.; Nguyen, H.; Lam, B.; Liu, J.; Cheung, I.; Rice, J.; Suzuki, Y.; Luu, C.; Settachatgul, C.; Shellooe, R.; Cantwell, J.; Kim, S.H.; Schlessinger, J.; Zhang, K.Y.J.; West, B.L.; Powell, B.; Habets, G.; Zhang, C.; Ibrahim, P.N.; Hirth, P.; Artis, D.R.; Herlyn, M.; Bollag, G. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc. Natl. Acad. Sci., 2008, 105(8), 3041-3046. doi: 10.1073/pnas.0711741105 PMID: 18287029
  63. Weber, C.K.; Slupsky, J.R.; Kalmes, H.A.; Rapp, U.R. Active Ras induces heterodimerization of cRaf and BRaf. Cancer Res., 2001, 61(9), 3595-3598. PMID: 11325826
  64. Avruch, J.; Khokhlatchev, A.; Kyriakis, J.M.; Luo, Z.; Tzivion, G.; Vavvas, D.; Zhang, X.F. Ras activation of the Raf kinase: Tyrosine kinase recruitment of the map kinase cascade. Recent Prog. Horm. Res., 2001, 56(1), 127-156. doi: 10.1210/rp.56.1.127 PMID: 11237210
  65. Guo, Y-J.; Pan, W-W.; Liu, S-B.; Shen, Z-F.; Xu, Y.; Hu, L-L. ERK/MAPK signalling pathway and tumorigenesis. Exp. Ther. Med., 2020, 19(3), 1997-2007. PMID: 32104259
  66. Kim, A.; Cohen, M.S. The discovery of vemurafenib for the treatment of BRAF-mutated metastatic melanoma. Expert Opin. Drug Discov., 2016, 11(9), 907-916. doi: 10.1080/17460441.2016.1201057 PMID: 27327499
  67. Proietti, I.; Skroza, N.; Michelini, S.; Mambrin, A.; Balduzzi, V.; Bernardini, N.; Marchesiello, A.; Tolino, E.; Volpe, S.; Maddalena, P.; Di Fraia, M.; Mangino, G.; Romeo, G.; Potenza, C. BRAF inhibitors: Molecular targeting and immunomodulatory actions. Cancers, 2020, 12(7), 1823. doi: 10.3390/cancers12071823 PMID: 32645969
  68. Yang, H.; Higgins, B.; Kolinsky, K.; Packman, K.; Go, Z.; Iyer, R.; Kolis, S.; Zhao, S.; Lee, R.; Grippo, J.F.; Schostack, K.; Simcox, M.E.; Heimbrook, D.; Bollag, G.; Su, F. RG7204 (PLX4032), a selective BRAFV600E inhibitor, displays potent antitumor activity in preclinical melanoma models. Cancer Res., 2010, 70(13), 5518-5527. doi: 10.1158/0008-5472.CAN-10-0646 PMID: 20551065
  69. King, A.J.; Arnone, M.R.; Bleam, M.R.; Moss, K.G.; Yang, J.; Fedorowicz, K.E.; Smitheman, K.N.; Erhardt, J.A.; Hughes-Earle, A.; Kane-Carson, L.S.; Sinnamon, R.H.; Qi, H.; Rheault, T.R.; Uehling, D.E.; Laquerre, S.G. Dabrafenib; preclinical characterization, increased efficacy when combined with trametinib, while BRAF/MEK tool combination reduced skin lesions. PLoS One, 2013, 8(7), e67583. doi: 10.1371/journal.pone.0067583 PMID: 23844038
  70. Gentilcore, G.; Madonna, G.; Mozzillo, N.; Ribas, A.; Cossu, A.; Palmieri, G.; Ascierto, P.A. Effect of dabrafenib on melanoma cell lines harbouring the BRAF V600D/R mutations. BMC Cancer, 2013, 13(1), 17. doi: 10.1186/1471-2407-13-17 PMID: 23317446
  71. Rheault, T.R.; Stellwagen, J.C.; Adjabeng, G.M.; Hornberger, K.R.; Petrov, K.G.; Waterson, A.G.; Dickerson, S.H.; Mook, R.A., Jr; Laquerre, S.G.; King, A.J.; Rossanese, O.W.; Arnone, M.R.; Smitheman, K.N.; Kane-Carson, L.S.; Han, C.; Moorthy, G.S.; Moss, K.G.; Uehling, D.E. Discovery of dabrafenib: A selective inhibitor of raf kinases with antitumor activity against B-raf-driven tumors. ACS Med. Chem. Lett., 2013, 4(3), 358-362. doi: 10.1021/ml4000063 PMID: 24900673
  72. Koelblinger, P.; Thuerigen, O.; Dummer, R. Development of encorafenib for BRAF-mutated advanced melanoma. Curr. Opin. Oncol., 2018, 30(2), 125-133. doi: 10.1097/CCO.0000000000000426 PMID: 29356698
  73. Joseph, E.W.; Pratilas, C.A.; Poulikakos, P.I.; Tadi, M.; Wang, W.; Taylor, B.S.; Halilovic, E.; Persaud, Y.; Xing, F.; viale, A.; Tsai, J.; Chapman, P.B.; Bollag, G.; Solit, D.B.; Rosen, N. The RAF inhibitor PLX4032 inhibits ERK signaling and tumor cell proliferation in a V600E BRAF-selective manner. Proc. Natl. Acad. Sci., 2010, 107(33), 14903-14908. doi: 10.1073/pnas.1008990107 PMID: 20668238
  74. Savoia, P.; Zavattaro, E.; Cremona, O. Clinical implications of acquired BRAF inhibitors resistance in melanoma. Int. J. Mol. Sci., 2020, 21(24), 9730. doi: 10.3390/ijms21249730 PMID: 33419275
  75. Spagnolo, F.; Ghiorzo, P.; Queirolo, P. Overcoming resistance to BRAF inhibition in BRAF-mutated metastatic melanoma. Oncotarget, 2014, 5(21), 10206-10221. doi: 10.18632/oncotarget.2602 PMID: 25344914
  76. Shi, H.; Hugo, W.; Kong, X.; Hong, A.; Koya, R.C.; Moriceau, G.; Chodon, T.; Guo, R.; Johnson, D.B.; Dahlman, K.B.; Kelley, M.C.; Kefford, R.F.; Chmielowski, B.; Glaspy, J.A.; Sosman, J.A.; van Baren, N.; Long, G.V.; Ribas, A.; Lo, R.S. Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov., 2014, 4(1), 80-93. doi: 10.1158/2159-8290.CD-13-0642 PMID: 24265155
  77. Nazarian, R.; Shi, H.; Wang, Q.; Kong, X.; Koya, R.C.; Lee, H.; Chen, Z.; Lee, M.K.; Attar, N.; Sazegar, H.; Chodon, T.; Nelson, S.F.; McArthur, G.; Sosman, J.A.; Ribas, A.; Lo, R.S. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature, 2010, 468(7326), 973-977. doi: 10.1038/nature09626 PMID: 21107323
  78. Rizos, H.; Menzies, A.M.; Pupo, G.M.; Carlino, M.S.; Fung, C.; Hyman, J.; Haydu, L.E.; Mijatov, B.; Becker, T.M.; Boyd, S.C.; Howle, J.; Saw, R.; Thompson, J.F.; Kefford, R.F.; Scolyer, R.A.; Long, G.V. BRAF inhibitor resistance mechanisms in metastatic melanoma: Spectrum and clinical impact. Clin. Cancer Res., 2014, 20(7), 1965-1977. doi: 10.1158/1078-0432.CCR-13-3122 PMID: 24463458
  79. Johnson, D.B.; Menzies, A.M.; Zimmer, L.; Eroglu, Z.; Ye, F.; Zhao, S.; Rizos, H.; Sucker, A.; Scolyer, R.A.; Gutzmer, R.; Gogas, H.; Kefford, R.F.; Thompson, J.F.; Becker, J.C.; Berking, C.; Egberts, F.; Loquai, C.; Goldinger, S.M.; Pupo, G.M.; Hugo, W.; Kong, X.; Garraway, L.A.; Sosman, J.A.; Ribas, A.; Lo, R.S.; Long, G.V.; Schadendorf, D. Acquired BRAF inhibitor resistance: A multicenter meta-analysis of the spectrum and frequencies, clinical behaviour, and phenotypic associations of resistance mechanisms. Eur. J. Cancer, 2015, 51(18), 2792-2799. doi: 10.1016/j.ejca.2015.08.022 PMID: 26608120
  80. Montagut, C.; Sharma, S.V.; Shioda, T.; McDermott, U.; Ulman, M.; Ulkus, L.E.; Dias-Santagata, D.; Stubbs, H.; Lee, D.Y.; Singh, A.; Drew, L.; Haber, D.A.; Settleman, J. Elevated CRAF as a potential mechanism of acquired resistance to BRAF inhibition in melanoma. Cancer Res., 2008, 68(12), 4853-4861. doi: 10.1158/0008-5472.CAN-07-6787 PMID: 18559533
  81. Heidorn, S.J.; Milagre, C.; Whittaker, S.; Nourry, A.; Niculescu-Duvas, I.; Dhomen, N.; Hussain, J.; Reis-Filho, J.S.; Springer, C.J.; Pritchard, C.; Marais, R. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell, 2010, 140(2), 209-221. doi: 10.1016/j.cell.2009.12.040 PMID: 20141835
  82. Wang, J.; Yao, Z.; Jonsson, P.; Allen, A.N.; Qin, A.C.R.; Uddin, S.; Dunkel, I.J.; Petriccione, M.; Manova, K.; Haque, S.; Rosenblum, M.K.; Pisapia, D.J.; Rosen, N.; Taylor, B.S.; Pratilas, C.A. A secondary mutation in BRAF confers resistance to RAF inhibition in a BRAF V600E-mutant brain tumor. Cancer Discov., 2018, 8(9), 1130-1141. doi: 10.1158/2159-8290.CD-17-1263 PMID: 29880583
  83. Hoogstraat, M.; Gadellaa-van Hooijdonk, C.G.; Ubink, I.; Besselink, N.J.M.; Pieterse, M.; Veldhuis, W.; van Stralen, M.; Meijer, E.F.J.; Willems, S.M.; Hadders, M.A.; Kuilman, T.; Krijgsman, O.; Peeper, D.S.; Koudijs, M.J.; Cuppen, E.; Voest, E.E.; Lolkema, M.P. Detailed imaging and genetic analysis reveal a secondary BRAFL 505H resistance mutation and extensive intrapatient heterogeneity in metastatic BRAF mutant melanoma patients treated with vemurafenib. Pigment Cell Melanoma Res., 2015, 28(3), 318-323. doi: 10.1111/pcmr.12347 PMID: 25515853
  84. Amaral, T.; Sinnberg, T.; Meier, F.; Krepler, C.; Levesque, M.; Niessner, H.; Garbe, C. MAPK pathway in melanoma part II—secondary and adaptive resistance mechanisms to BRAF inhibition. Eur. J. Cancer, 2017, 73, 93-101. doi: 10.1016/j.ejca.2016.12.012 PMID: 28162869
  85. Gowrishankar, K.; Snoyman, S.; Pupo, G.M.; Becker, T.M.; Kefford, R.F.; Rizos, H. Acquired resistance to BRAF inhibition can confer cross-resistance to combined BRAF/MEK inhibition. J. Invest. Dermatol., 2012, 132(7), 1850-1859. doi: 10.1038/jid.2012.63 PMID: 22437314
  86. Chapman, P.B.; Hauschild, A.; Robert, C.; Haanen, J.B.; Ascierto, P.; Larkin, J.; Dummer, R.; Garbe, C.; Testori, A.; Maio, M.; Hogg, D.; Lorigan, P.; Lebbe, C.; Jouary, T.; Schadendorf, D.; Ribas, A.; O’Day, S.J.; Sosman, J.A.; Kirkwood, J.M.; Eggermont, A.M.M.; Dreno, B.; Nolop, K.; Li, J.; Nelson, B.; Hou, J.; Lee, R.J.; Flaherty, K.T.; McArthur, G.A. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med., 2011, 364(26), 2507-2516. doi: 10.1056/NEJMoa1103782 PMID: 21639808
  87. Hauschild, A.; Grob, J.J.; Demidov, L.V.; Jouary, T.; Gutzmer, R.; Millward, M.; Rutkowski, P.; Blank, C.U.; Miller, W.H., Jr; Kaempgen, E.; Martín-Algarra, S.; Karaszewska, B.; Mauch, C.; Chiarion-Sileni, V.; Martin, A.M.; Swann, S.; Haney, P.; Mirakhur, B.; Guckert, M.E.; Goodman, V.; Chapman, P.B. Dabrafenib in BRAF-mutated metastatic melanoma: A multicentre, open-label, phase 3 randomised controlled trial. Lancet, 2012, 380(9839), 358-365. doi: 10.1016/S0140-6736(12)60868-X PMID: 22735384
  88. Larkin, J.; Ascierto, P.A.; Dréno, B.; Atkinson, V.; Liszkay, G.; Maio, M.; Mandalà, M.; Demidov, L.; Stroyakovskiy, D.; Thomas, L.; de la Cruz-Merino, L.; Dutriaux, C.; Garbe, C.; Sovak, M.A.; Chang, I.; Choong, N.; Hack, S.P.; McArthur, G.A.; Ribas, A. Combined vemurafenib and cobimetinib in BRAF-mutated melanoma. N. Engl. J. Med., 2014, 371(20), 1867-1876. doi: 10.1056/NEJMoa1408868 PMID: 25265494
  89. Long, G.V.; Stroyakovskiy, D.; Gogas, H.; Levchenko, E.; de Braud, F.; Larkin, J.; Garbe, C.; Jouary, T.; Hauschild, A.; Grob, J.J.; Chiarion-Sileni, V.; Lebbe, C.; Mandalà, M.; Millward, M.; Arance, A.; Bondarenko, I.; Haanen, J.B.A.G.; Hansson, J.; Utikal, J.; Ferraresi, V.; Kovalenko, N.; Mohr, P.; Probachai, V.; Schadendorf, D.; Nathan, P.; Robert, C.; Ribas, A.; DeMarini, D.J.; Irani, J.G.; Swann, S.; Legos, J.J.; Jin, F.; Mookerjee, B.; Flaherty, K. Dabrafenib and trametinib versus dabrafenib and placebo for Val600 BRAF-mutant melanoma: A multicentre, double-blind, phase 3 randomised controlled trial. Lancet, 2015, 386(9992), 444-451. doi: 10.1016/S0140-6736(15)60898-4 PMID: 26037941
  90. Robert, C.; Karaszewska, B.; Schachter, J.; Rutkowski, P.; Mackiewicz, A.; Stroiakovski, D.; Lichinitser, M.; Dummer, R.; Grange, F.; Mortier, L.; Chiarion-Sileni, V.; Drucis, K.; Krajsova, I.; Hauschild, A.; Lorigan, P.; Wolter, P.; Long, G.V.; Flaherty, K.; Nathan, P.; Ribas, A.; Martin, A.M.; Sun, P.; Crist, W.; Legos, J.; Rubin, S.D.; Little, S.M.; Schadendorf, D. Improved overall survival in melanoma with combined dabrafenib and trametinib. N. Engl. J. Med., 2015, 372(1), 30-39. doi: 10.1056/NEJMoa1412690 PMID: 25399551
  91. Cybulska-Stopa, B.; Świtaj, T.; Koseła-Paterczyk, H. Combined or sequential treatment of advanced melanoma? Nowotwory. J. Oncol., 2019, 69, 125-132.
  92. Hamid, O.; Cowey, C.L.; Offner, M.; Faries, M.; Carvajal, R.D. Efficacy, safety, and tolerability of approved combination BRAF and MEK inhibitor regimens for BRAF-mutant melanoma. Cancers, 2019, 11(11), 1642. doi: 10.3390/cancers11111642 PMID: 31653096
  93. Arozarena, I.; Wellbrock, C. Overcoming resistance to BRAF inhibitors. Ann. Transl. Med., 2017, 5(19), 387. doi: 10.21037/atm.2017.06.09 PMID: 29114545
  94. Sanlorenzo, M.; Choudhry, A.; Vujic, I.; Posch, C.; Chong, K.; Johnston, K.; Meier, M.; Osella-Abate, S.; Quaglino, P.; Daud, A.; Algazi, A.; Rappersberger, K.; Ortiz-Urda, S. Comparative profile of cutaneous adverse events: BRAF/MEK inhibitor combination therapy versus BRAF monotherapy in melanoma. J. Am. Acad. Dermatol., 2014, 71(6), 1102-1109.e1. doi: 10.1016/j.jaad.2014.09.002 PMID: 25440439
  95. Grob, J.J.; Amonkar, M.M.; Karaszewska, B.; Schachter, J.; Dummer, R.; Mackiewicz, A.; Stroyakovskiy, D.; Drucis, K.; Grange, F.; Chiarion-Sileni, V.; Rutkowski, P.; Lichinitser, M.; Levchenko, E.; Wolter, P.; Hauschild, A.; Long, G.V.; Nathan, P.; Ribas, A.; Flaherty, K.; Sun, P.; Legos, J.J.; McDowell, D.O.; Mookerjee, B.; Schadendorf, D.; Robert, C. Comparison of dabrafenib and trametinib combination therapy with vemurafenib monotherapy on health-related quality of life in patients with unresectable or metastatic cutaneous BRAF Val600-mutation-positive melanoma (COMBI-v): Results of a phase 3, open-label, randomised trial. Lancet Oncol., 2015, 16(13), 1389-1398. doi: 10.1016/S1470-2045(15)00087-X PMID: 26433819
  96. Schadendorf, D.; Amonkar, M.M.; Stroyakovskiy, D.; Levchenko, E.; Gogas, H.; de Braud, F.; Grob, J.J.; Bondarenko, I.; Garbe, C.; Lebbe, C.; Larkin, J.; Chiarion-Sileni, V.; Millward, M.; Arance, A.; Mandalà, M.; Flaherty, K.T.; Nathan, P.; Ribas, A.; Robert, C.; Casey, M.; DeMarini, D.J.; Irani, J.G.; Aktan, G.; Long, G.V. Health-related quality of life impact in a randomised phase III study of the combination of dabrafenib and trametinib versus dabrafenib monotherapy in patients with BRAF V600 metastatic melanoma. Eur. J. Cancer, 2015, 51(7), 833-840. doi: 10.1016/j.ejca.2015.03.004 PMID: 25794603
  97. Long, G.V.; Weber, J.S.; Infante, J.R.; Kim, K.B.; Daud, A.; Gonzalez, R.; Sosman, J.A.; Hamid, O.; Schuchter, L.; Cebon, J.; Kefford, R.F.; Lawrence, D.; Kudchadkar, R.; Burris, H.A., III; Falchook, G.S.; Algazi, A.; Lewis, K.; Puzanov, I.; Ibrahim, N.; Sun, P.; Cunningham, E.; Kline, A.S.; Del Buono, H.; McDowell, D.O.; Patel, K.; Flaherty, K.T. Overall survival and durable responses in patients With BRAF V600–mutant metastatic melanoma receiving dabrafenib combined with trametinib. J. Clin. Oncol., 2016, 34(8), 871-878. doi: 10.1200/JCO.2015.62.9345 PMID: 26811525
  98. Puzanov, I.; Amaravadi, R.K.; McArthur, G.A.; Flaherty, K.T.; Chapman, P.B.; Sosman, J.A.; Ribas, A.; Shackleton, M.; Hwu, P.; Chmielowski, B.; Nolop, K.B.; Lin, P.S.; Kim, K.B. Long-term outcome in BRAFV600E melanoma patients treated with vemurafenib: Patterns of disease progression and clinical management of limited progression. Eur. J. Cancer, 2015, 51(11), 1435-1443. doi: 10.1016/j.ejca.2015.04.010 PMID: 25980594
  99. Smith, M.P.; Brunton, H.; Rowling, E.J.; Ferguson, J.; Arozarena, I.; Miskolczi, Z.; Lee, J.L.; Girotti, M.R.; Marais, R.; Levesque, M.P.; Dummer, R.; Frederick, D.T.; Flaherty, K.T.; Cooper, Z.A.; Wargo, J.A.; Wellbrock, C. Inhibiting drivers of non-mutational drug tolerance is a salvage strategy for targeted melanoma therapy. Cancer Cell, 2016, 29(3), 270-284. doi: 10.1016/j.ccell.2016.02.003 PMID: 26977879
  100. Villanueva, J.; Infante, J.R.; Krepler, C.; Reyes-Uribe, P.; Samanta, M.; Chen, H.Y.; Li, B.; Swoboda, R.K.; Wilson, M.; Vultur, A.; Fukunaba-Kalabis, M.; Wubbenhorst, B.; Chen, T.Y.; Liu, Q.; Sproesser, K.; DeMarini, D.J.; Gilmer, T.M.; Martin, A.M.; Marmorstein, R.; Schultz, D.C.; Speicher, D.W.; Karakousis, G.C.; Xu, W.; Amaravadi, R.K.; Xu, X.; Schuchter, L.M.; Herlyn, M.; Nathanson, K.L. Concurrent MEK2 mutation and BRAF amplification confer resistance to BRAF and MEK inhibitors in melanoma. Cell Rep., 2013, 4(6), 1090-1099. doi: 10.1016/j.celrep.2013.08.023 PMID: 24055054
  101. Wagle, N.; Van Allen, E.M.; Treacy, D.J.; Frederick, D.T.; Cooper, Z.A.; Taylor-Weiner, A.; Rosenberg, M.; Goetz, E.M.; Sullivan, R.J.; Farlow, D.N.; Friedrich, D.C.; Anderka, K.; Perrin, D.; Johannessen, C.M.; McKenna, A.; Cibulskis, K.; Kryukov, G.; Hodis, E.; Lawrence, D.P.; Fisher, S.; Getz, G.; Gabriel, S.B.; Carter, S.L.; Flaherty, K.T.; Wargo, J.A.; Garraway, L.A. MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov., 2014, 4(1), 61-68. doi: 10.1158/2159-8290.CD-13-0631 PMID: 24265154
  102. Lito, P.; Pratilas, C.A.; Joseph, E.W.; Tadi, M.; Halilovic, E.; Zubrowski, M.; Huang, A.; Wong, W.L.; Callahan, M.K.; Merghoub, T.; Wolchok, J.D.; de Stanchina, E.; Chandarlapaty, S.; Poulikakos, P.I.; Fagin, J.A.; Rosen, N. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell, 2012, 22(5), 668-682. doi: 10.1016/j.ccr.2012.10.009 PMID: 23153539
  103. Smith, M.P.; Wellbrock, C. Molecular pathways: Maintaining MAPK inhibitor sensitivity by targeting nonmutational tolerance. Clin. Cancer Res., 2016, 22(24), 5966-5970. doi: 10.1158/1078-0432.CCR-16-0954 PMID: 27797970
  104. Malapelle, U.; Rossi, G.; Pisapia, P.; Barberis, M.; Buttitta, F.; Castiglione, F.; Cecere, F.L.; Grimaldi, A.M.; Iaccarino, A.; Marchetti, A.; Massi, D.; Medicina, D.; Mele, F.; Minari, R.; Orlando, E.; Pagni, F.; Palmieri, G.; Righi, L.; Russo, A.; Tommasi, S.; Vermi, W.; Troncone, G. BRAF as a positive predictive biomarker: Focus on lung cancer and melanoma patients. Crit. Rev. Oncol. Hematol., 2020, 156, 103118. doi: 10.1016/j.critrevonc.2020.103118 PMID: 33038627
  105. Cheng, L.; Lopez-Beltran, A.; Massari, F.; MacLennan, G.T.; Montironi, R. Molecular testing for BRAF mutations to inform melanoma treatment decisions: A move toward precision medicine. Mod. Pathol., 2018, 31(1), 24-38. doi: 10.1038/modpathol.2017.104 PMID: 29148538
  106. Chau, C.H.; Rixe, O.; McLeod, H.; Figg, W.D. Validation of analytic methods for biomarkers used in drug development. Clin. Cancer Res., 2008, 14(19), 5967-5976. doi: 10.1158/1078-0432.CCR-07-4535 PMID: 18829475
  107. de Gramont, A.; Watson, S.; Ellis, L.M.; Rodón, J.; Tabernero, J.; de Gramont, A.; Hamilton, S.R. Pragmatic issues in biomarker evaluation for targeted therapies in cancer. Nat. Rev. Clin. Oncol., 2015, 12(4), 197-212. doi: 10.1038/nrclinonc.2014.202 PMID: 25421275
  108. Armbruster, D.A.; Pry, T. Limit of blank, limit of detection and limit of quantitation. Clin. Biochem. Rev., 2008, 29(Suppl. 1), S49-S52. PMID: 18852857
  109. Sacco, A.; Forgione, L.; Carotenuto, M.; De Luca, A.; Ascierto, P.A.; Botti, G.; Normanno, N. Circulating tumor DNA testing opens new perspectives in melanoma management. Cancers, 2020, 12(10), 2914. doi: 10.3390/cancers12102914 PMID: 33050536
  110. Wan, J.C.M.; Massie, C.; Garcia-Corbacho, J.; Mouliere, F.; Brenton, J.D.; Caldas, C.; Pacey, S.; Baird, R.; Rosenfeld, N. Liquid biopsies come of age: Towards implementation of circulating tumour DNA. Nat. Rev. Cancer, 2017, 17(4), 223-238. doi: 10.1038/nrc.2017.7 PMID: 28233803
  111. Gracie, L.; Pan, Y.; Atenafu, E.G.; Ward, D.G.; Teng, M.; Pallan, L.; Stevens, N.M.; Khoja, L. Circulating tumour DNA (ctDNA) in metastatic melanoma, a systematic review and meta-analysis. Eur. J. Cancer, 2021, 158, 191-207. doi: 10.1016/j.ejca.2021.09.019 PMID: 34757258
  112. Woof, V.G.; Lee, R.J.; Lorigan, P.; French, D.P. Circulating tumour DNA monitoring and early treatment for relapse: Views from patients with early-stage melanoma. Br. J. Cancer, 2022, 126(10), 1450-1456. doi: 10.1038/s41416-022-01766-x PMID: 35301436
  113. Corcoran, R.B.; Chabner, B.A. Application of cell-free DNA analysis to cancer treatment. N. Engl. J. Med., 2018, 379(18), 1754-1765. doi: 10.1056/NEJMra1706174 PMID: 30380390
  114. Sun, K.; Jiang, P.; Chan, K.C.A.; Wong, J.; Cheng, Y.K.Y.; Liang, R.H.S.; Chan, W.; Ma, E.S.K.; Chan, S.L.; Cheng, S.H.; Chan, R.W.Y.; Tong, Y.K.; Ng, S.S.M.; Wong, R.S.M.; Hui, D.S.C.; Leung, T.N.; Leung, T.Y.; Lai, P.B.S.; Chiu, R.W.K.; Lo, Y.M.D. Plasma DNA tissue mapping by genome-wide methylation sequencing for noninvasive prenatal, cancer, and transplantation assessments. Proc. Natl. Acad. Sci., 2015, 112(40), E5503-E5512. doi: 10.1073/pnas.1508736112 PMID: 26392541
  115. Thierry, A.R.; El Messaoudi, S.; Gahan, P.B.; Anker, P.; Stroun, M. Origins, structures, and functions of circulating DNA in oncology. Cancer Metastasis Rev., 2016, 35(3), 347-376. doi: 10.1007/s10555-016-9629-x PMID: 27392603
  116. Normanno, N.; Cervantes, A.; Ciardiello, F.; De Luca, A.; Pinto, C. The liquid biopsy in the management of colorectal cancer patients: Current applications and future scenarios. Cancer Treat. Rev., 2018, 70, 1-8. doi: 10.1016/j.ctrv.2018.07.007 PMID: 30053724
  117. Couto, G.K.; Segatto, N.V.; Oliveira, T.L.; Seixas, F.K.; Schachtschneider, K.M.; Collares, T. The melding of drug screening platforms for melanoma. Front. Oncol., 2019, 9, 512. doi: 10.3389/fonc.2019.00512 PMID: 31293965
  118. Marconi, A.; Quadri, M.; Saltari, A.; Pincelli, C. Progress in melanoma modelling in vitro. Exp. Dermatol., 2018, 27(5), 578-586. doi: 10.1111/exd.13670 PMID: 29697862
  119. Huang, S.; Ingber, D.E. Cell tension, matrix mechanics, and cancer development. Cancer Cell, 2005, 8(3), 175-176. doi: 10.1016/j.ccr.2005.08.009 PMID: 16169461
  120. Van Allen, E.M.; Wagle, N.; Sucker, A.; Treacy, D.J.; Johannessen, C.M.; Goetz, E.M.; Place, C.S.; Taylor-Weiner, A.; Whittaker, S.; Kryukov, G.V.; Hodis, E.; Rosenberg, M.; McKenna, A.; Cibulskis, K.; Farlow, D.; Zimmer, L.; Hillen, U.; Gutzmer, R.; Goldinger, S.M.; Ugurel, S.; Gogas, H.J.; Egberts, F.; Berking, C.; Trefzer, U.; Loquai, C.; Weide, B.; Hassel, J.C.; Gabriel, S.B.; Carter, S.L.; Getz, G.; Garraway, L.A.; Schadendorf, D. The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov., 2014, 4(1), 94-109. doi: 10.1158/2159-8290.CD-13-0617 PMID: 24265153
  121. Wang, T.; Xiao, M.; Ge, Y.; Krepler, C.; Belser, E.; Lopez-Coral, A.; Xu, X.; Zhang, G.; Azuma, R.; Liu, Q.; Liu, R.; Li, L.; Amaravadi, R.K.; Xu, W.; Karakousis, G.; Gangadhar, T.C.; Schuchter, L.M.; Lieu, M.; Khare, S.; Halloran, M.B.; Herlyn, M.; Kaufman, R.E. BRAF inhibition stimulates melanoma-associated macrophages to drive tumor growth. Clin. Cancer Res., 2015, 21(7), 1652-1664. doi: 10.1158/1078-0432.CCR-14-1554 PMID: 25617424
  122. Atefi, M.; Titz, B.; Avramis, E.; Ng, C.; Wong, D.J.L.; Lassen, A.; Cerniglia, M.; Escuin-Ordinas, H.; Foulad, D.; Comin-Anduix, B.; Graeber, T.G.; Ribas, A. Combination of pan-RAF and MEK inhibitors in NRAS mutant melanoma. Mol. Cancer, 2015, 14(1), 27. doi: 10.1186/s12943-015-0293-5 PMID: 25645078
  123. Girotti, M.R.; Lopes, F.; Preece, N.; Niculescu-Duvaz, D.; Zambon, A.; Davies, L.; Whittaker, S.; Saturno, G.; Viros, A.; Pedersen, M.; Suijkerbuijk, B.M.J.M.; Menard, D.; McLeary, R.; Johnson, L.; Fish, L.; Ejiama, S.; Sanchez-Laorden, B.; Hohloch, J.; Carragher, N.; Macleod, K.; Ashton, G.; Marusiak, A.A.; Fusi, A.; Brognard, J.; Frame, M.; Lorigan, P.; Marais, R.; Springer, C. Paradox-breaking RAF inhibitors that also target SRC are effective in drug-resistant BRAF mutant melanoma. Cancer Cell, 2015, 27(1), 85-96. doi: 10.1016/j.ccell.2014.11.006 PMID: 25500121
  124. Nakamura, A.; Arita, T.; Tsuchiya, S.; Donelan, J.; Chouitar, J.; Carideo, E.; Galvin, K.; Okaniwa, M.; Ishikawa, T.; Yoshida, S. Antitumor activity of the selective pan-RAF inhibitor TAK-632 in BRAF inhibitor-resistant melanoma. Cancer Res., 2013, 73(23), 7043-7055. doi: 10.1158/0008-5472.CAN-13-1825 PMID: 24121489
  125. Peng, S.B.; Henry, J.R.; Kaufman, M.D.; Lu, W.P.; Smith, B.D.; Vogeti, S.; Rutkoski, T.J.; Wise, S.; Chun, L.; Zhang, Y.; Van Horn, R.D.; Yin, T.; Zhang, X.; Yadav, V.; Chen, S.H.; Gong, X.; Ma, X.; Webster, Y.; Buchanan, S.; Mochalkin, I.; Huber, L.; Kays, L.; Donoho, G.P.; Walgren, J.; McCann, D.; Patel, P.; Conti, I.; Plowman, G.D.; Starling, J.J.; Flynn, D.L. Inhibition of RAF isoforms and active dimers by LY3009120 leads to anti-tumor activities in RAS or BRAF mutant cancers. Cancer Cell, 2015, 28(3), 384-398. doi: 10.1016/j.ccell.2015.08.002 PMID: 26343583
  126. Yao, Z.; Torres, N.M.; Tao, A.; Gao, Y.; Luo, L.; Li, Q.; de Stanchina, E.; Abdel-Wahab, O.; Solit, D.B.; Poulikakos, P.I.; Rosen, N. BRAF mutants evade ERK-dependent feedback by different mechanisms that determine their sensitivity to pharmacologic inhibition. Cancer Cell, 2015, 28(3), 370-383. doi: 10.1016/j.ccell.2015.08.001 PMID: 26343582
  127. Zhang, C.; Spevak, W.; Zhang, Y.; Burton, E.A.; Ma, Y.; Habets, G.; Zhang, J.; Lin, J.; Ewing, T.; Matusow, B.; Tsang, G.; Marimuthu, A.; Cho, H.; Wu, G.; Wang, W.; Fong, D.; Nguyen, H.; Shi, S.; Womack, P.; Nespi, M.; Shellooe, R.; Carias, H.; Powell, B.; Light, E.; Sanftner, L.; Walters, J.; Tsai, J.; West, B.L.; Visor, G.; Rezaei, H.; Lin, P.S.; Nolop, K.; Ibrahim, P.N.; Hirth, P.; Bollag, G. RAF inhibitors that evade paradoxical MAPK pathway activation. Nature, 2015, 526(7574), 583-586. doi: 10.1038/nature14982 PMID: 26466569
  128. Acquaviva, J.; Smith, D.L.; Jimenez, J.P.; Zhang, C.; Sequeira, M.; He, S.; Sang, J.; Bates, R.C.; Proia, D.A. Overcoming acquired BRAF inhibitor resistance in melanoma via targeted inhibition of Hsp90 with ganetespib. Mol. Cancer Ther., 2014, 13(2), 353-363. doi: 10.1158/1535-7163.MCT-13-0481 PMID: 24398428
  129. Paraiso, K.H.T.; Haarberg, H.E.; Wood, E.; Rebecca, V.W.; Chen, Y.A.; Xiang, Y.; Ribas, A.; Lo, R.S.; Weber, J.S.; Sondak, V.K.; John, J.K.; Sarnaik, A.A.; Koomen, J.M.; Smalley, K.S.M. The HSP90 inhibitor XL888 overcomes BRAF inhibitor resistance mediated through diverse mechanisms. Clin. Cancer Res., 2012, 18(9), 2502-2514. doi: 10.1158/1078-0432.CCR-11-2612 PMID: 22351686
  130. da Rocha Dias, S.; Friedlos, F.; Light, Y.; Springer, C.; Workman, P.; Marais, R. Activated B-RAF is an Hsp90 client protein that is targeted by the anticancer drug 17-allylamino-17-demethoxygeldanamycin. Cancer Res., 2005, 65(23), 10686-10691. doi: 10.1158/0008-5472.CAN-05-2632 PMID: 16322212
  131. Grbovic, O.M.; Basso, A.D.; Sawai, A.; Ye, Q.; Friedlander, P.; Solit, D.; Rosen, N. V600E B-Raf requires the Hsp90 chaperone for stability and is degraded in response to Hsp90 inhibitors. Proc. Natl. Acad. Sci., 2006, 103(1), 57-62. doi: 10.1073/pnas.0609973103 PMID: 16371460
  132. Zhong, J.; Yan, W.; Wang, C.; Liu, W.; Lin, X.; Zou, Z.; Sun, W.; Chen, Y. BRAF inhibitor resistance in melanoma: Mechanisms and alternative therapeutic strategies. Curr. Treat. Options Oncol., 2022, 23(11), 1503-1521. doi: 10.1007/s11864-022-01006-7 PMID: 36181568
  133. Wei, H.; Guan, Y.D.; Zhang, L.X.; Liu, S.; Lu, A.P.; Cheng, Y.; Cao, D.S. A combinatorial target screening strategy for deorphaning macromolecular targets of natural product. Eur. J. Med. Chem., 2020, 204, 112644. doi: 10.1016/j.ejmech.2020.112644 PMID: 32738412
  134. Deuker, M.M.; Marsh Durban, V.; Phillips, W.A.; McMahon, M. PI3′-kinase inhibition forestalls the onset of MEK1/2 inhibitor resistance in BRAF-mutated melanoma. Cancer Discov., 2015, 5(2), 143-153. doi: 10.1158/2159-8290.CD-14-0856 PMID: 25472943
  135. Atefi, M.; von Euw, E.; Attar, N.; Ng, C.; Chu, C.; Guo, D.; Nazarian, R.; Chmielowski, B.; Glaspy, J.A.; Comin-Anduix, B.; Mischel, P.S.; Lo, R.S.; Ribas, A. Reversing melanoma cross-resistance to BRAF and MEK inhibitors by co-targeting the AKT/mTOR pathway. PLoS One, 2011, 6(12), e28973. doi: 10.1371/journal.pone.0028973 PMID: 22194965
  136. Bedard, P.L.; Tabernero, J.; Janku, F.; Wainberg, Z.A.; Paz-Ares, L.; Vansteenkiste, J.; Van Cutsem, E.; Pérez-García, J.; Stathis, A.; Britten, C.D.; Le, N.; Carter, K.; Demanse, D.; Csonka, D.; Peters, M.; Zubel, A.; Nauwelaerts, H.; Sessa, C. A phase Ib dose-escalation study of the oral pan-PI3K inhibitor buparlisib (BKM120) in combination with the oral MEK1/2 inhibitor trametinib (GSK1120212) in patients with selected advanced solid tumors. Clin. Cancer Res., 2015, 21(4), 730-738. doi: 10.1158/1078-0432.CCR-14-1814 PMID: 25500057
  137. Greger, J.G.; Eastman, S.D.; Zhang, V.; Bleam, M.R.; Hughes, A.M.; Smitheman, K.N.; Dickerson, S.H.; Laquerre, S.G.; Liu, L.; Gilmer, T.M. 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(4), 909-920. doi: 10.1158/1535-7163.MCT-11-0989 PMID: 22389471
  138. Sweetlove, M.; Wrightson, E.; Kolekar, S.; Rewcastle, G.W.; Baguley, B.C.; Shepherd, P.R.; Jamieson, S.M.F. Inhibitors of pan-PI3K signaling synergize with BRAF or MEK inhibitors to prevent BRAF-mutant melanoma cell growth. Front. Oncol., 2015, 5, 135. doi: 10.3389/fonc.2015.00135 PMID: 26137449
  139. Tolcher, A.W.; Patnaik, A.; Papadopoulos, K.P.; Rasco, D.W.; Becerra, C.R.; Allred, A.J.; Orford, K.; Aktan, G.; Ferron-Brady, G.; Ibrahim, N.; Gauvin, J.; Motwani, M.; Cornfeld, M. Phase I study of the MEK inhibitor trametinib in combination with the AKT inhibitor afuresertib in patients with solid tumors and multiple myeloma. Cancer Chemother. Pharmacol., 2015, 75(1), 183-189. doi: 10.1007/s00280-014-2615-5 PMID: 25417902
  140. Smith, M.P.; Ferguson, J.; Arozarena, I.; Hayward, R.; Marais, R.; Chapman, A.; Hurlstone, A.; Wellbrock, C. Effect of SMURF2 targeting on susceptibility to MEK inhibitors in melanoma. J. Natl. Cancer Inst., 2013, 105(1), 33-46. doi: 10.1093/jnci/djs471 PMID: 23250956
  141. Smith, M.P.; Brunton, H.; Rowling, E.J.; Ferguson, J.; Arozarena, I.; Miskolczi, Z.; Lee, J.L.; Girotti, M.R.; Marais, R.; Levesque, M.P.; Dummer, R.; Frederick, D.T.; Flaherty, K.T.; Cooper, Z.A.; Wargo, J.A.; Wellbrock, C. Inhibiting drivers of non-mutational drug tolerance is a salvage strategy for targeted melanoma therapy. Cancer Cell, 2016, 29, 270-284.
  142. Koya, R.C.; Mok, S.; Otte, N.; Blacketor, K.J.; Comin-Anduix, B.; Tumeh, P.C.; Minasyan, A.; Graham, N.A.; Graeber, T.G.; Chodon, T.; Ribas, A. BRAF inhibitor vemurafenib improves the antitumor activity of adoptive cell immunotherapy. Cancer Res., 2012, 72(16), 3928-3937. doi: 10.1158/0008-5472.CAN-11-2837 PMID: 22693252
  143. Liu, L.; Mayes, P.A.; Eastman, S.; Shi, H.; Yadavilli, S.; Zhang, T.; Yang, J.; Seestaller-Wehr, L.; Zhang, S.Y.; Hopson, C.; Tsvetkov, L.; Jing, J.; Zhang, S.; Smothers, J.; Hoos, A. The BRAF and MEK inhibitors dabrafenib and trametinib: Effects on immune function and in combination with immunomodulatory antibodies targeting PD-1, PD-L1, and CTLA-4. Clin. Cancer Res., 2015, 21(7), 1639-1651. doi: 10.1158/1078-0432.CCR-14-2339 PMID: 25589619
  144. Jiang, X.; Zhou, J.; Giobbie-Hurder, A.; Wargo, J.; Hodi, F.S. The activation of MAPK in melanoma cells resistant to BRAF inhibition promotes PD-L1 expression that is reversible by MEK and PI3K inhibition. Clin. Cancer Res., 2013, 19(3), 598-609. doi: 10.1158/1078-0432.CCR-12-2731 PMID: 23095323
  145. Lim, S.Y.; Menzies, A.M.; Rizos, H. Mechanisms and strategies to overcome resistance to molecularly targeted therapy for melanoma. Cancer, 2017, 123(S11), 2118-2129. doi: 10.1002/cncr.30435 PMID: 28543695
  146. Atefi, M.; Avramis, E.; Lassen, A.; Wong, D.J.L.; Robert, L.; Foulad, D.; Cerniglia, M.; Titz, B.; Chodon, T.; Graeber, T.G.; Comin-Anduix, B.; Ribas, A. Effects of MAPK and PI3K pathways on PD-L1 expression in melanoma. Clin. Cancer Res., 2014, 20(13), 3446-3457. doi: 10.1158/1078-0432.CCR-13-2797 PMID: 24812408
  147. Boni, A.; Cogdill, A.P.; Dang, P.; Udayakumar, D.; Njauw, C.N.J.; Sloss, C.M.; Ferrone, C.R.; Flaherty, K.T.; Lawrence, D.P.; Fisher, D.E.; Tsao, H.; Wargo, J.A. Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. Cancer Res., 2010, 70(13), 5213-5219. doi: 10.1158/0008-5472.CAN-10-0118 PMID: 20551059
  148. Szczepaniak Sloane, R.A.; Gopalakrishnan, V.; Reddy, S.M.; Zhang, X.; Reuben, A.; Wargo, J.A. Interaction of molecular alterations with immune response in melanoma. Cancer, 2017, 123(S11), 2130-2142. doi: 10.1002/cncr.30681 PMID: 28543700
  149. Frederick, D.T.; Piris, A.; Cogdill, A.P.; Cooper, Z.A.; Lezcano, C.; Ferrone, C.R.; Mitra, D.; Boni, A.; Newton, L.P.; Liu, C.; Peng, W.; Sullivan, R.J.; Lawrence, D.P.; Hodi, F.S.; Overwijk, W.W.; Lizée, G.; Murphy, G.F.; Hwu, P.; Flaherty, K.T.; Fisher, D.E.; Wargo, J.A. BRAF inhibition is associated with enhanced melanoma antigen expression and a more favorable tumor microenvironment in patients with metastatic melanoma. Clin. Cancer Res., 2013, 19(5), 1225-1231. doi: 10.1158/1078-0432.CCR-12-1630 PMID: 23307859
  150. Wilmott, J.S.; Long, G.V.; Howle, J.R.; Haydu, L.E.; Sharma, R.N.; Thompson, J.F.; Kefford, R.F.; Hersey, P.; Scolyer, R.A. Selective BRAF inhibitors induce marked T-cell infiltration into human metastatic melanoma. Clin. Cancer Res., 2012, 18(5), 1386-1394. doi: 10.1158/1078-0432.CCR-11-2479 PMID: 22156613
  151. Bai, X.; Flaherty, K.T. Targeted and immunotherapies in BRAF mutant melanoma: Where we stand and what to expect. Br. J. Dermatol., 2021, 185(2), 253-262. doi: 10.1111/bjd.19394 PMID: 32652567
  152. Huynh, S.; Mortier, L.; Dutriaux, C.; Maubec, E.; Boileau, M.; Dereure, O.; Leccia, M.T.; Arnault, J.P.; Brunet-Possenti, F.; Aubin, F.; Dreno, B.; Beylot-Barry, M.; Lebbe, C.; Lefevre, W.; Delyon, J. Combined therapy with Anti-PD1 and BRAF and/or MEK inhibitor for advanced melanoma: A multicenter cohort study. Cancers, 2020, 12(6), 1666. doi: 10.3390/cancers12061666 PMID: 32585901
  153. Welti, M.; Dimitriou, F.; Gutzmer, R.; Dummer, R. Triple combination of immune checkpoint inhibitors and BRAF/MEK inhibitors in BRAFV600 melanoma: Current status and future perspectives. Cancers, 2022, 14(22), 5489. doi: 10.3390/cancers14225489 PMID: 36428582
  154. Moriceau, G.; Hugo, W.; Hong, A.; Shi, H.; Kong, X.; Yu, C.C.; Koya, R.C.; Samatar, A.A.; Khanlou, N.; Braun, J.; Ruchalski, K.; Seifert, H.; Larkin, J.; Dahlman, K.B.; Johnson, D.B.; Algazi, A.; Sosman, J.A.; Ribas, A.; Lo, R.S. Tunable-combinatorial mechanisms of acquired resistance limit the efficacy of BRAF/MEK cotargeting but result in melanoma drug addiction. Cancer Cell, 2015, 27(2), 240-256. doi: 10.1016/j.ccell.2014.11.018 PMID: 25600339
  155. Algazi, A.P.; Othus, M.; Daud, A.I.; Lo, R.S.; Mehnert, J.M.; Truong, T.G.; Conry, R.; Kendra, K.; Doolittle, G.C.; Clark, J.I.; Messino, M.J.; Moore, D.F., Jr; Lao, C.; Faller, B.A.; Govindarajan, R.; Harker-Murray, A.; Dreisbach, L.; Moon, J.; Grossmann, K.F.; Ribas, A. Continuous versus intermittent BRAF and MEK inhibition in patients with BRAF-mutated melanoma: A randomized phase 2 trial. Nat. Med., 2020, 26(10), 1564-1568. doi: 10.1038/s41591-020-1060-8 PMID: 33020646
  156. Cook, F.A.; Cook, S.J. Inhibition of RAF dimers: It takes two to tango. Biochem. Soc. Trans., 2021, 49(1), 237-251. doi: 10.1042/BST20200485 PMID: 33367512
  157. Noeparast, A.; Giron, P.; De Brakeleer, S.; Eggermont, C.; De Ridder, U.; Teugels, E.; De Grève, J. Type II RAF inhibitor causes superior ERK pathway suppression compared to type I RAF inhibitor in cells expressing different BRAF mutant types recurrently found in lung cancer. Oncotarget, 2018, 9(22), 16110-16123. doi: 10.18632/oncotarget.24576 PMID: 29662630
  158. Basile, K.J.; Le, K.; Hartsough, E.J.; Aplin, A.E. Inhibition of mutant BRAF splice variant signaling by next-generation, selective RAF inhibitors. Pigment Cell Melanoma Res., 2014, 27(3), 479-484. doi: 10.1111/pcmr.12218 PMID: 24422853
  159. Jin, T.; Lavoie, H.; Sahmi, M.; David, M.; Hilt, C.; Hammell, A.; Therrien, M. RAF inhibitors promote RAS-RAF interaction by allosterically disrupting RAF autoinhibition. Nat. Commun., 2017, 8(1), 1211. doi: 10.1038/s41467-017-01274-0 PMID: 29084939

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