Comparative profiles of BRAF inhibitors: The paradox index as a predictor of clinical toxicity

Oncotarget

Volumn 7, Issue 21, 2016, Pages 30453-30460

  Adelmann, Charles H ^a   Ching, Grace ^a   Du, Lili ^a   Saporito, Rachael C ^a   Bansal, Varun ^a   Pence, Lindy J ^a   Liang, Roger ^a   Lee, Woojin ^a   Tsai, Kenneth Y ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

BRAF; Melanoma; Paradoxical ERK; Small molecule inhibitor; Squamous cell carcinoma

Indexed keywords

B RAF KINASE INHIBITOR; DABRAFENIB; ENCORAFENIB; PLX 8394; UNCLASSIFIED DRUG; VEMURAFENIB; B RAF KINASE; CARBAMIC ACID DERIVATIVE; FUSED HETEROCYCLIC RINGS; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; MAPK1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE 1; OXIME; PLX8394; PROTEIN KINASE INHIBITOR; SULFONAMIDE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; CANCER INHIBITION; CELL VIABILITY; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SKIN CARCINOMA; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMICALLY INDUCED; COMPARATIVE STUDY; DRUG EFFECTS; MAPK SIGNALING; METABOLISM; SKIN TUMOR; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

APOPTOSIS; CARBAMATES; CARCINOMA, SQUAMOUS CELL; CELL LINE; CELL LINE, TUMOR; ENZYME ACTIVATION; HETEROCYCLIC COMPOUNDS, 2-RING; HUMANS; IMIDAZOLES; INDOLES; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 1; OXIMES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SKIN NEOPLASMS; SULFONAMIDES;

EID: 84971506958     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8351     Document Type: Article

References (34)

1. Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, Jones CM, Marshall CJ, Springer CJ, Barford D and Marais R. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell. 2004; 116:855-867
2. Jang S and Atkins MB. Treatment of BRAF-mutant melanoma: the role of vemurafenib and other therapies. Clin Pharmacol Ther. 2014; 95:24-31
3. Dummer R, Robert C, Nyakas M, McArthur G, Kudchadkar R, Gomez Roca C, Sullivan R, Flaherty K, Murer C, Michel D, Tang Z, Moutouh-de Parseval L and Delord JP. Initial results from a phase I, open-label, dose escalation study of the oral BRAF inhibitor LGX818 in patients with BRAF V600 mutant advanced or metastatic melanoma. J Clin Oncol. 2013; 31
4. Sullivan R, Weber J, Patel S, Dummer R, Miller WH, Cosgrove D, Carlino M, Tan D, Lebbe C, Cipani T, Elez E, Maacke H, Nikolopoulos P, Aout M, Moutouh-de Parseval L and Ascierto P. A phase Ib/II study of BRAF inhibitor (BRAFi) encorafenib (ENCO) plus MEK inhibitor (MEKi) binimetinib (BINI) in cutaneous melanoma patients naive to BRAFi treatment. J Clin Oncol. 2013; 31
5. Zhang C, Spevak W, Zhang Y, Burton EA, Ma Y, Habets G, Zhang J, Lin J, Ewing T, Matusow B, Tsang G, Marimuthu A, Cho H, Wu G, Wang W, Fong D, et al. RAF inhibitors that evade paradoxical MAPK pathway activation. Nature. 2015; 526:583-586
6. Stuart DD, Li N, Poon DJ, Aardalen K, Kaufman S, Merritt H, Salangsang F, Lorenzana E, Li A, Ghoddusi M, Caponigro G, Sun F, Kulkarni S, Kakar S, Turner N, Zang R, et al. Abstract 3790: Preclinical profile of LGX818: A potent and selective RAF kinase inhibitor. Cancer Research. 2012; 72:3790
7. Menzies AM, Kefford RF and Long GV. Paradoxical oncogenesis: are all BRAF inhibitors equal? Pigment Cell Melanoma Res. 2013; 26:611-615
8. Vin H, Ojeda SS, Ching G, Leung ML, Chitsazzadeh V, Dwyer DW, Adelmann CH, Restrepo M, Richards KN, Stewart LR, Du L, Ferguson SB, Chakravarti D, Ehrenreiter K, Baccarini M, Ruggieri R, et al. BRAF inhibitors suppress apoptosis through off-target inhibition of JNK signaling. Elife. 2013; 2:e00969
9. Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber JS, McArthur GA, Hutson TE, Moschos SJ, Flaherty KT, Hersey P, Kefford R, Lawrence D, Puzanov I, Lewis KD, Amaravadi RK, et al. Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med. 2012; 366:707-714
10. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med. 2011; 364:2507-2516
11. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, Sosman JA, O'Dwyer PJ, Lee RJ, Grippo JF, Nolop K and Chapman PB. Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med. 2010; 363:809-819
12. Falchook GS, Long GV, Kurzrock R, Kim KB, Arkenau TH, Brown MP, Hamid O, Infante JR, Millward M, Pavlick AC, O'Day SJ, Blackman SC, Curtis CM, Lebowitz P, Ma B, Ouellet D, et al. Dabrafenib in patients with melanoma, untreated brain metastases, and other solid tumours: a phase 1 dose-escalation trial. Lancet. 2012; 379:1893-1901
13. Long GV, Trefzer U, Davies MA, Kefford RF, Ascierto PA, Chapman PB, Puzanov I, Hauschild A, Robert C, Algazi A, Mortier L, Tawbi H, Wilhelm T, Zimmer L, Switzky J, Swann S, et al. Dabrafenib in patients with Val600Glu or Val600Lys BRAF-mutant melanoma metastatic to the brain (BREAK-MB): a multicentre, open-label, phase 2 trial. Lancet Oncol. 2012; 13:1087-95. doi: 10.1016/S1470-2045:70431-X
14. Hauschild A, Grob JJ, Demidov LV, Jouary T, Gutzmer R, Millward M, Rutkowski P, Blank CU, Miller WH, Jr., Kaempgen E, Martin-Algarra S, Karaszewska B, Mauch C, Chiarion-Sileni V, Martin AM, Swann S, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised controlled trial. Lancet. 2012; 380:358-365
15. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R, Ludlam MJ, Stokoe D, Gloor SL, Vigers G, Morales T, Aliagas I, Liu B, Sideris S, Hoeflich KP, Jaiswal BS, et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature. 2010; 464:431-435
16. Poulikakos PI, Zhang C, Bollag G, Shokat KM and Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature. 2010; 464:427-430
17. Heidorn SJ, Milagre C, Whittaker S, Nourry A, Niculescu-Duvas I, Dhomen N, Hussain J, Reis-Filho JS, Springer CJ, Pritchard C and Marais R. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell. 2010; 140:209-221
18. Halaban R, Zhang W, Bacchiocchi A, Cheng E, Parisi F, Ariyan S, Krauthammer M, McCusker JP, Kluger Y and Sznol M. PLX4032, a selective BRAF(V600E) kinase inhibitor, activates the ERK pathway and enhances cell migration and proliferation of BRAF melanoma cells. Pigment Cell Melanoma Res. 2010; 23:190-200
19. Karreth FA, DeNicola GM, Winter SP and Tuveson DA. C-Raf inhibits MAPK activation and transformation by B-Raf(V600E). Mol Cell. 2009; 36:477-486
20. Oberholzer PA, Kee D, Dziunycz P, Sucker A, Kamsukom N, Jones R, Roden C, Chalk CJ, Ardlie K, Palescandolo E, Piris A, Macconaill LE, Robert C, Hofbauer GF, McArthur GA, Schadendorf D, et al. RAS Mutations Are Associated With the Development of Cutaneous Squamous Cell Tumors in Patients Treated With RAF Inhibitors. J Clin Oncol. 2012; 30:316-21. doi: 10.1200/JCO.2011.36.7680
21. Su F, Viros A, Milagre C, Trunzer K, Bollag G, Spleiss O, Reis-Filho JS, Kong X, Koya RC, Flaherty KT, Chapman PB, Kim MJ, Hayward R, Martin M, Yang H, Wang Q, et al. RAS mutations in cutaneous squamous-cell carcinomas in patients treated with BRAF inhibitors. N Engl J Med. 2012; 366:207-215
22. Callahan MK, Rampal R, Harding JJ, Klimek VM, Chung YR, Merghoub T, Wolchok JD, Solit DB, Rosen N, Abdel-Wahab O, Levine RL and Chapman PB. Progression of RAS-mutant leukemia during RAF inhibitor treatment. N Engl J Med. 2012; 367:2316-2321
23. Zimmer L, Hillen U, Livingstone E, Lacouture ME, Busam K, Carvajal RD, Egberts F, Hauschild A, Kashani-Sabet M, Goldinger SM, Dummer R, Long GV, McArthur G, Scherag A, Sucker A and Schadendorf D. Atypical melanocytic proliferations and new primary melanomas in patients with advanced melanoma undergoing selective BRAF inhibition. J Clin Oncol. 2012; 30:2375-2383
24. Jang S and Atkins MB. Which drug, and when, for patients with BRAF-mutant melanoma? Lancet Oncol. 2013; 14:e60-69
25. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, Hamid O, Schuchter L, Cebon J, Ibrahim N, Kudchadkar R, Burris HA, 3rd, Falchook G, Algazi A, Lewis K, Long GV, et al. Combined BRAF and MEK Inhibition in Melanoma with BRAF V600 Mutations. N Engl J Med. 2012
26. Vin H, Ching G, Ojeda SS, Adelmann CH, Chitsazzadeh V, Dwyer DW, Ma H, Ehrenreiter K, Baccarini M, Ruggieri R, Curry JL, Ciurea AM, Duvic M, Busaidy NL, Tannir NM and Tsai KY. Sorafenib Suppresses JNK-Dependent Apoptosis through Inhibition of ZAK. Mol Cancer Ther. 2014; 13:221-229
27. Boukamp P, Stanbridge EJ, Foo DY, Cerutti PA and Fusenig NE. c-Ha-ras oncogene expression in immortalized human keratinocytes (HaCaT) alters growth potential in vivo but lacks correlation with malignancy. Cancer Res. 1990; 50:2840-2847
28. Lito P, Pratilas CA, Joseph EW, Tadi M, Halilovic E, Zubrowski M, Huang A, Wong WL, Callahan MK, Merghoub T, Wolchok JD, de Stanchina E, Chandarlapaty S, Poulikakos PI, Fagin JA and Rosen N. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell. 2012; 22:668-682
29. Das Thakur M, Salangsang F, Landman AS, Sellers WR, Pryer NK, Levesque MP, Dummer R, McMahon M and Stuart DD. Modelling vemurafenib resistance in melanoma reveals a strategy to forestall drug resistance. Nature. 2013; 494:251-255
30. Dimauro T and David G. Ras-induced senescence and its physiological relevance in cancer. Curr Cancer Drug Targets. 2010; 10:869-876
31. Han EK, Leverson JD, McGonigal T, Shah OJ, Woods KW, Hunter T, Giranda VL and Luo Y. Akt inhibitor A-443654 induces rapid Akt Ser-473 phosphorylation independent of mTORC1 inhibition. Oncogene. 2007; 26:5655-5661
32. Chan TO, Zhang J, Rodeck U, Pascal JM, Armen RS, Spring M, Dumitru CD, Myers V, Li X, Cheung JY and Feldman AM. Resistance of Akt kinases to dephosphorylation through ATP-dependent conformational plasticity. Proc Natl Acad Sci U S A. 2011; 108:E1120-1127
33. Laquerre S, Arnone M, Moss K, Yang J, Fisher K, Kane-Carson LS, Smitheman K, Ward J, Heidrich B, Rheault T, Adjabeng G, Hornberger K, Stellwagen J, Waterson A, Han C, Mook RA, et al. Abstract B88: A selective Raf kinase inhibitor induces cell death and tumor regression of human cancer cell lines encoding B-RafV600E mutation. Molecular Cancer Therapeutics. 2009; 8:B88
34. Bollag G, Hirth P, Tsai J, Zhang J, Ibrahim PN, Cho H, Spevak W, Zhang C, Zhang Y, Habets G, Burton EA, Wong B, Tsang G, West BL, Powell B, Shellooe R, et al. Clinical efficacy of a RAF inhibitor needs broad target blockade in BRAF-mutant melanoma. Nature. 2010; 467:596-599