Revisiting the Role of B-RAF Kinase as a Therapeutic Target in Melanoma
- Authors: Kozyra P.1, Pitucha M.1
-
Affiliations:
- Independent Radiopharmacy Unit, Faculty of Pharmacy,, Medical University of Lublin
- Issue: Vol 31, No 15 (2024)
- Pages: 2003-2020
- Section: Anti-Infectives and Infectious Diseases
- URL: https://j-morphology.com/0929-8673/article/view/644393
- DOI: https://doi.org/10.2174/0109298673258495231011065225
- ID: 644393
Cite item
Full Text
Abstract
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.
Keywords
About the authors
Paweł Kozyra
Independent Radiopharmacy Unit, Faculty of Pharmacy,, Medical University of Lublin
Author for correspondence.
Email: info@benthamscience.net
Monika Pitucha
Independent Radiopharmacy Unit, Faculty of Pharmacy,, Medical University of Lublin
Email: info@benthamscience.net
References
- 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
- 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
- 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
- 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
- Kozyra, P.; Krasowska, D.; Pitucha, M. New potential agents for malignant melanoma treatment-most recent studies 20202022. Int. J. Mol. Sci., 2022, 23(11), 6084. doi: 10.3390/ijms23116084 PMID: 35682764
- 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
- Kozyra, P.; Pitucha, M. Terminal phenoxy group as a privileged moiety of the drug scaffold-A short review of most recent studies 20132022. Int. J. Mol. Sci., 2022, 23(16), 8874. doi: 10.3390/ijms23168874 PMID: 36012142
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Miller, A.J.; Mihm, M.C., Jr Melanoma. N. Engl. J. Med., 2006, 355(1), 51-65. doi: 10.1056/NEJMra052166 PMID: 16822996
- 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
- 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
- Melanoma Skin Cancer Statistics. Available from: https://www.cancer.org/cancer/melanoma-skin-cancer/ about/key-statistics.html(accessed on 9 January 2023)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Shain, A.H.; Yeh, I.; Kovalyshyn, I.; Sriharan, A.; Talevich, E.; Gagnon, A.; Dummer, R.; North, J.; Pincus, L.; Ruben, B.; Rickaby, W.; DArrigo, 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
- 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
- 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
- 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
- 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
- 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
- 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
- Cancer Genome Atlas Network. Genomic classification of cutaneous melanoma. Cell, 2015, 161, 1681-1696. doi: 10.1016/j.cell.2015.05.044 PMID: 26091043
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Cantwell-Dorris, E.R.; OLeary, 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
- 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
- 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
- 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 BRAFMEK114-3-3 complexes. Nature, 2019, 575(7783), 545-550. doi: 10.1038/s41586-019-1660-y PMID: 31581174
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Amaral, T.; Sinnberg, T.; Meier, F.; Krepler, C.; Levesque, M.; Niessner, H.; Garbe, C. MAPK pathway in melanoma part IIsecondary and adaptive resistance mechanisms to BRAF inhibition. Eur. J. Cancer, 2017, 73, 93-101. doi: 10.1016/j.ejca.2016.12.012 PMID: 28162869
- 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
- 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.; ODay, 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
- 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
- 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
- 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
- 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
- Cybulska-Stopa, B.; Świtaj, T.; Koseła-Paterczyk, H. Combined or sequential treatment of advanced melanoma? Nowotwory. J. Oncol., 2019, 69, 125-132.
- 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
- 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
- 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
- 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
- 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
- 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 V600mutant metastatic melanoma receiving dabrafenib combined with trametinib. J. Clin. Oncol., 2016, 34(8), 871-878. doi: 10.1200/JCO.2015.62.9345 PMID: 26811525
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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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