Phosphoproteomic analysis of basal and therapy-induced adaptive signaling networks in BRAF and NRAS mutant melanoma

Proteomics

Volumn 15, Issue 2-3, 2015, Pages 327-339

  Fedorenko, Inna V ^a   Fang, Bin ^a   Munko, Ana Cecelia ^a   Gibney, Geoffrey T ^a   Koomen, John M ^a   Smalley, Keiran S M ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Biomedicine; BRAF; Melanoma; NRAS; Phosphoproteomics; Signaling

Indexed keywords

BETA CATENIN; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 3; CYTOSKELETON PROTEIN; DUAL SPECIFICITY TYROSINE PHOSPHORYLATION REGULATED KINASE 1A; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOGEN SYNTHASE KINASE 3ALPHA; INTERFERON REGULATORY FACTOR 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOLIPASE C1; PROTEIN KINASE C DELTA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE RECEPTOR A; RAS RASB INTERACTOR 1 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG; VEMURAFENIB; B RAF KINASE; BRAF PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; INDOLE DERIVATIVE; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NRAS PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; SULFONAMIDE;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE MUTATION; GENOTYPE; IMMUNOPRECIPITATION; MELANOMA; MELANOMA CELL LINE; NULL CELL; ONCOGENE; ONCOGENE N RAF; ONCOGENE N RAS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEOMICS; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; HUMAN; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE;

CELL LINE, TUMOR; GTP PHOSPHOHYDROLASES; HUMANS; INDOLES; MELANOMA; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MUTATION; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS B-RAF; SIGNAL TRANSDUCTION; SULFONAMIDES;

EID: 84921378248     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201400200     Document Type: Article

References (50)

1. Flaherty, K. T., Infante, J. R., Daud, A., Gonzalez, R. et al., Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. New Engl. J. Med. 2012, 367, 1694-1703.
2. Flaherty, K. T., Robert, C., Hersey, P., Nathan, P. et al., Improved survival with MEK inhibition in BRAF-mutated melanoma. New Engl. J. Med. 2012, 367, 107-114.
3. Van Allen, E. M., Wagle, N., Sucker, A., Treacy, D. J. et al., The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov. 2014, 4, 94-109.
4. Smalley, K. S., Nathanson, K. L., Flaherty, K. T., Genetic subgrouping of melanoma reveals new opportunities for targeted therapy. Cancer Res. 2009, 69, 3241-3244.
5. Davies, H., Bignell, G. R., Cox, C., Stephens, P. et al., Mutations of the BRAF gene in human cancer. Nature 2002, 417, 949-954.
6. Hodis, E., Watson, I. R., Kryukov, G. V., Arold, S. T. et al., A landscape of driver mutations in Melanoma. Cell 2012, 150, 251-263.
7. Fedorenko, I. V., Gibney, G. T., Smalley, K. S., NRAS mutant melanoma: biological behavior and future strategies for therapeutic management. Oncogene 2013, 32, 3009-3018.
8. Ascierto, P. A., Schadendorf, D., Berking, C., Agarwala, S. S. et al., MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAF mutations: a non-randomised, open-label phase 2 study. Lancet Oncol. 2013, 14, 249-256.
9. Rebecca, V. W., Massaro, R. R., Fedorenko, I. V., Sondak, V. K. et al., Inhibition of autophagy enhances the effects of the AKT inhibitor MK-2206 when combined with paclitaxel and carboplatin in BRAF wild-type melanoma. Pigment Cell Melanoma Res. 2014, 27, 465-478.
10. Berger, M. F., Hodis, E., Heffernan, T. P., Deribe, Y. L. et al., Melanoma genome sequencing reveals frequent PREX2 mutations. Nature 2012, 485, 502-506.
11. Wagle, N., Van Allen, E. M., Treacy, D. J., Frederick, D. T. et al., MAP kinase pathway alterations in BRAF-mutant melanoma patients with acquired resistance to combined RAF/MEK inhibition. Cancer Discov. 2014, 4, 61-68.
12. Chandarlapaty, S., Sawai, A., Scaltriti, M., Rodrik-Outmezguine, V. et al., AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 2011, 19, 58-71.
13. Lito, P., Pratilas, C. A., Joseph, E. W., Tadi, M. 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.
14. Paraiso, K. H., Fedorenko, I. V., Cantini, L. P., Munko, A. C. et al., Recovery of phospho-ERK activity allows melanoma cells to escape from BRAF inhibitor therapy. Brit. J. Cancer 2010, 102, 1724-1730.
15. Paraiso, K. H., Haarberg, H. E., Wood, E., Rebecca, V. W. et al., The HSP90 inhibitor XL888 overcomes BRAF inhibitor resistance mediated through diverse mechanisms. Clin. Cancer Res. 2012, 18, 2502-2514.
16. Acquaviva, J., Smith, D. L., Jimenez, J. P., Zhang, C. et al., Overcoming acquired BRAF inhibitor resistance in melanoma via targeted inhibition of Hsp90 with ganetespib. Mol. Cancer Ther. 2014, 13, 353-363.
17. Old, W. M., Shabb, J. B., Houel, S., Wang, H. et al., Functional proteomics identifies targets of phosphorylation by B-Raf signaling in melanoma. Mol. Cell 2009, 34, 115-131.
18. Kirkpatrick, D. S., Bustos, D. J., Dogan, T., Chan, J. et al., Phosphoproteomic characterization of DNA damage response in melanoma cells following MEK/PI3K dual inhibition. Proc. Natl. Acad. Sci. US A 2013, 110, 19426-19431.
19. Rush, J., Moritz, A., Lee, K. A., Guo, A. et al., Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23, 94-101.
20. Li, J., Rix, U., Fang, B., Bai, Y. et al., A chemical and phosphoproteomic characterization of dasatinib action in lung cancer. Nat. Chem. Biol. 2010, 6, 291-299.
21. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26, 1367-1372.
22. Cox, J., Matic, I., Hilger, M., Nagaraj, N. et al., A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 2009, 4, 698-705.
23. Paraiso, K. H., Xiang, Y., Rebecca, V. W., Abel, E. V. et al., PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res. 2011, 71, 2750-2760.
24. Paraiso, K. H., Xiang, Y., Rebecca, V. W., Abel, E. V. et al., PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res. 2011, 71, 2750-2760.
25. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., Ideker, T., Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27, 431-432.
26. Gopal, Y. N., Deng, W., Woodman, S. E., Komurov, K. et al., Basal and treatment-induced activation of AKT mediates resistance to cell death by AZD6244 (ARRY-142886) in Braf-mutant human cutaneous melanoma cells. Cancer Res. 2010, 70, 8736-8747.
27. Rebecca, V. W., Wood, E. R., Fedorenko, I. V., Paraiso, K. H. et al., Evaluating melanoma drug response and therapeutic escape with quantitative proteomics. Mol. Cell. Proteomics 2014, 13(7), 1844-1854.
28. Smalley, K. S. M., A pivotal role for ERK in the oncogenic behaviour of malignant melanoma? Int. J. Cancer 2003, 104, 527-532.
29. Fedorenko, I. V., Paraiso, K. H., Smalley, K. S., Acquired and intrinsic BRAF inhibitor resistance in BRAF V600E mutant melanoma. Biochem. Pharmacol. 2011, 82, 201-209.
30. Madhunapantula, S. V., Robertson, G. P., The PTEN-AKT3 signaling cascade as a therapeutic target in melanoma. Pigment Cell Melanoma Res. 2009, 22, 400-419.
31. Bhatt, K. V., Spofford, L. S., Aram, G., McMullen, M. et al., Adhesion control of cyclin D1 and p27Kip1 levels is deregulated in melanoma cells through BRAF-MEK-ERK signaling. Oncogene 2005, 24, 3459-3471.
32. Boisvert-Adamo, K., Aplin, A. E., Mutant B-RAF mediates resistance to anoikis via Bad and Bim. Oncogene 2008, 27, 3301-3312.
33. Klein, R. M., Aplin, A. E., Rnd3 regulation of the actin cytoskeleton promotes melanoma migration and invasive outgrowth in three dimensions. Cancer Res. 2009, 69, 2224-2233.
34. Arozarena, I., Sanchez-Laorden, B., Packer, L., Hidalgo-Carcedo, C. et al., Oncogenic BRAF induces melanoma cell invasion by downregulating the cGMP-specific phosphodiesterase PDE5A. Cancer Cell 2011, 19, 45-57.
35. Vredeveld, L. C., Possik, P. A., Smit, M. A., Meissl, K. et al., Abrogation of BRAFV600E-induced senescence by PI3K pathway activation contributes to melanomagenesis. Gene Dev. 2012, 26, 1055-1069.
36. Dankort, D., Curley, D. P., Cartlidge, R. A., Nelson, B. et al., Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 2009, 41, 544-552.
37. John, J. K., Paraiso, K. H., Rebecca, V. W., Cantini, L. P. et al., GSK3beta inhibition blocks melanoma cell/host interactions by downregulating N-cadherin expression and decreasing FAK phosphorylation. J. Invest. Dermatol. 2012, 132, 2818-2827.
38. Sensi, M., Catani, M., Castellano, G., Nicolini, G. et al., Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J. Invest. Dermatol. 2011, 131, 2448-2457.
39. Tworkoski, K., Singhal, G., Szpakowski, S., Zito, C. I. et al., Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol. Cancer Res. 2011, 9, 801-812.
40. Chattopadhyay, C., Ellerhorst, J. A., Ekmekcioglu, S., Greene, V. R. et al., Association of activated c-Met with NRAS-mutated human melanomas: a possible avenue for targeting. Int. J. Cancer 2012, 131, E56-E65.
41. Malumbres, M., Barbacid, M., RAS oncogenes: the first 30 years. Nat. Rev. Cancer 2003, 3, 459-465.
42. Ebi, H., Corcoran, R. B., Singh, A., Chen, Z. et al., Receptor tyrosine kinases exert dominant control over PI3K signaling in human KRAS mutant colorectal cancers. J. Clin. Invest. 2011, 121, 4311-4321.
43. Duncan, J. S., Whittle, M. C., Nakamura, K., Abell, A. N. et al., Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 2012, 149, 307-321.
44. Vultur, A., Villanueva, J., Krepler, C., Rajan, G. et al., MEK inhibition affects STAT3 signaling and invasion in human melanoma cell lines. Oncogene 2014, 33, 1850-1861.
45. 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, 598-609.
46. Liu, F., Cao, J., Wu, J., Sullivan, K. et al., Stat3-targeted therapies overcome the acquired resistance to vemurafenib in melanomas. J. Invest. Dermatol. 2013, 133, 2041-2049.
47. Prahallad, A., Sun, C., Huang, S., Di Nicolantonio, F. et al., Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 2012, 483, 100-103.
48. Girotti, M. R., Pedersen, M., Sanchez-Laorden, B., Viros, A. et al., Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov. 2013, 3, 158-167.
49. Nabha, S. M., Glaros, S., Hong, M., Lykkesfeldt, A. E. et al., Upregulation of PKC-delta contributes to antiestrogen resistance in mammary tumor cells. Oncogene 2005, 24, 3166-3176.
50. Diaz Bessone, M. I., Berardi, D. E., Campodonico, P. B., Todaro, L. B. et al., Involvement of PKC delta (PKCdelta) in the resistance against different doxorubicin analogs. Breast Cancer Res. Treat. 2011, 126, 577-587.