BRAF Mutants Evade ERK-Dependent Feedback by Different Mechanisms that Determine Their Sensitivity to Pharmacologic Inhibition

Cancer Cell

Volumn 28, Issue 3, 2015, Pages 370-383

  Yao, Zhan ^a   Torres, Neilawattie M ^a   Tao, Anthony ^c   Gao, Yijun ^a   Luo, Lusong ^d   Li, Qi ^a   de Stanchina, Elisa ^a   Abdel Wahab, Omar ^a   Solit, David B ^a   Poulikakos, Poulikos I ^b   Rosen, Neal ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d Zhong Guan Cun Life Science Park   (China)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; BGB 659; DABRAFENIB; DIMER; DOXYCYCLINE; ENCORAFENIB; ENZYME INHIBITOR; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE; MONOMER; TRAMETINIB; UNCLASSIFIED DRUG; VEMURAFENIB; BRAF PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; RAS PROTEIN;

3T3 CELL LINE; ALLOSTERISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER INHIBITION; CANCER RESISTANCE; CHEMOSENSITIVITY; CONTROLLED STUDY; DIMERIZATION; DRUG EFFECT; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME INHIBITION; FEEDBACK SYSTEM; GENE MUTATION; HUMAN; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; MUTATION; TUMOR CELL LINE;

CELL LINE, TUMOR; DIMERIZATION; DRUG RESISTANCE, NEOPLASM; HUMANS; MAP KINASE SIGNALING SYSTEM; MUTATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; RAS PROTEINS;

EID: 84942319957     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.08.001     Document Type: Article

References (28)

1. Avraham R., Yarden Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 2011, 12:104-117.
2. Berghoff A.S., Preusser M. BRAF alterations in brain tumours: molecular pathology and therapeutic opportunities. Curr. Opin. Neurol. 2014, 27:689-696.
3. Corcoran R.B., Ebi H., Turke A.B., Coffee E.M., Nishino M., Cogdill A.P., Brown R.D., Della Pelle P., Dias-Santagata D., Hung K.E., et al. EGFR-mediated re-activation of MAPK signaling contributes to insensitivity of BRAF mutant colorectal cancers to RAF inhibition with vemurafenib. Cancer Discov. 2012, 2:227-235.
4. Cutler R.E., Stephens R.M., Saracino M.R., Morrison D.K. Autoregulation of the Raf-1 serine/threonine kinase. Proc. Natl. Acad. Sci. U S A 1998, 95:9214-9219.
5. Davies H., Bignell G.R., Cox C., Stephens P., Edkins S., Clegg S., Teague J., Woffendin H., Garnett M.J., Bottomley W., et al. Mutations of the BRAF gene in human cancer. Nature 2002, 417:949-954.
6. Dong C., Waters S.B., Holt K.H., Pessin J.E. SOS phosphorylation and disassociation of the Grb2-SOS complex by the ERK and JNK signaling pathways. J. Biol. Chem. 1996, 271:6328-6332.
7. Dougherty M.K., Müller J., Ritt D.A., Zhou M., Zhou X.Z., Copeland T.D., Conrads T.P., Veenstra T.D., Lu K.P., Morrison D.K. Regulation of Raf-1 by direct feedback phosphorylation. Mol. Cell 2005, 17:215-224.
8. Drosten M., Sum E.Y., Lechuga C.G., Simón-Carrasco L., Jacob H.K., García-Medina R., Huang S., Beijersbergen R.L., Bernards R., Barbacid M. Loss of p53 induces cell proliferation via Ras-independent activation of the Raf/Mek/Erk signaling pathway. Proc. Natl. Acad. Sci. U S A 2014, 111:15155-15160.
9. Fabian J.R., Vojtek A.B., Cooper J.A., Morrison D.K. A single amino acid change in Raf-1 inhibits Ras binding and alters Raf-1 function. Proc. Natl. Acad. Sci. U S A 1994, 91:5982-5986.
10. Freeman A.K., Ritt D.A., Morrison D.K. Effects of Raf dimerization and its inhibition on normal and disease-associated Raf signaling. Mol. Cell 2013, 49:751-758.
11. Gould A.E., Adams R., Adhikari S., Aertgeerts K., Afroze R., Blackburn C., Calderwood E.F., Chau R., Chouitar J., Duffey M.O., et al. Design and optimization of potent and orally bioavailable tetrahydronaphthalene Raf inhibitors. J. Med. Chem. 2011, 54:1836-1846.
12. Hatzivassiliou G., Song K., Yen I., Brandhuber B.J., Anderson D.J., Alvarado R., Ludlam M.J., Stokoe D., Gloor S.L., Vigers G., et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010, 464:431-435.
13. 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, 140:209-221.
14. Lang R., Hammer M., Mages J. DUSP meet immunology: dual specificity MAPK phosphatases in control of the inflammatory response. J. Immunol. 2006, 177:7497-7504.
15. Lavoie H., Thevakumaran N., Gavory G., Li J.J., Padeganeh A., Guiral S., Duchaine J., Mao D.Y., Bouvier M., Sicheri F., Therrien M. Inhibitors that stabilize a closed RAF kinase domain conformation induce dimerization. Nat. Chem. Biol. 2013, 9:428-436.
16. Lito P., Pratilas C.A., Joseph E.W., Tadi M., Halilovic E., Zubrowski M., Huang A., Wong W.L., Callahan M.K., Merghoub T., et al. Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 2012, 22:668-682.
17. Luo Z., Tzivion G., Belshaw P.J., Vavvas D., Marshall M., Avruch J. Oligomerization activates c-Raf-1 through a Ras-dependent mechanism. Nature 1996, 383:181-185.
18. Mason C.S., Springer C.J., Cooper R.G., Superti-Furga G., Marshall C.J., Marais R. Serine and tyrosine phosphorylations cooperate in Raf-1, but not B-Raf activation. EMBO J. 1999, 18:2137-2148.
19. Montero-Conde C., Ruiz-Llorente S., Dominguez J.M., Knauf J.A., Viale A., Sherman E.J., Ryder M., Ghossein R.A., Rosen N., Fagin J.A. Relief of feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAF-mutant thyroid carcinomas. Cancer Discov. 2013, 3:520-533.
20. Nazarian R., Shi H., Wang Q., Kong X., Koya R.C., Lee H., Chen Z., Lee M.K., Attar N., Sazegar H., et al. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010, 468:973-977.
21. Paik P.K., Arcila M.E., Fara M., Sima C.S., Miller V.A., Kris M.G., Ladanyi M., Riely G.J. Clinical characteristics of patients with lung adenocarcinomas harboring BRAF mutations. J. Clin. Oncol. 2011, 29:2046-2051.
22. Palanisamy N., Ateeq B., Kalyana-Sundaram S., Pflueger D., Ramnarayanan K., Shankar S., Han B., Cao Q., Cao X., Suleman K., et al. Rearrangements of the RAF kinase pathway in prostate cancer, gastric cancer and melanoma. Nat. Med. 2010, 16:793-798.
23. Poulikakos P.I., Zhang C., Bollag G., Shokat K.M., Rosen N. RAF inhibitors transactivate RAF dimers and ERK signalling in cells with wild-type BRAF. Nature 2010, 464:427-430.
24. Poulikakos P.I., Persaud Y., Janakiraman M., Kong X., Ng C., Moriceau G., Shi H., Atefi M., Titz B., Gabay M.T., et al. RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 2011, 480:387-390.
25. Pratilas C.A., Taylor B.S., Ye Q., Viale A., Sander C., Solit D.B., Rosen N. (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc. Natl. Acad. Sci. U S A 2009, 106:4519-4524.
26. Rajakulendran T., Sahmi M., Lefrançois M., Sicheri F., Therrien M. A dimerization-dependent mechanism drives RAF catalytic activation. Nature 2009, 461:542-545.
27. Shi H., Moriceau G., Kong X., Lee M.K., Lee H., Koya R.C., Ng C., Chodon T., Scolyer R.A., Dahlman K.B., et al. Melanoma whole-exome sequencing identifies (V600E)B-RAF amplification-mediated acquired B-RAF inhibitor resistance. Nat. Commun. 2012, 3:724.
28. Wan P.T., Garnett M.J., Roe S.M., Lee S., Niculescu-Duvaz D., Good V.M., 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, 116:855-867. Cancer Genome Project.