Evaluating melanoma drug response and therapeutic escape with quantitative proteomics

Molecular and Cellular Proteomics

Volumn 13, Issue 7, 2014, Pages 1844-1854

  Rebecca, Vito W ^a   Wood, Elizabeth ^a   Fedorenko, Inna V ^a   Paraiso, Kim H T ^a   Haarberg, H Eirik ^a   Chen, Yi ^a   Xiang, Yun ^a   Sarnaik, Amod ^a   Gibney, Geoffrey T ^a   Sondak, Vernon K ^a   Koomen, John M ^a   Smalley, Keiran S M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CHECKPOINT KINASE 1; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90 INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; SCATTER FACTOR RECEPTOR; SELUMETINIB; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; VEMURAFENIB; XL 888; AZABICYCLO DERIVATIVE; B RAF KINASE; BENZIMIDAZOLE DERIVATIVE; BRAF PROTEIN, HUMAN; CRENOLANIB; GUANOSINE TRIPHOSPHATASE; HEAT SHOCK PROTEIN 90; INDOLE DERIVATIVE; MAP2K1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; NRAS PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PHTHALIC ACID DERIVATIVE; PIPERIDINE DERIVATIVE; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMALL INTERFERING RNA; SULFONAMIDE; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE; CELL MUTANT; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; DRUG RESPONSE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MELANOMA; MELANOMA CELL; MELANOMA CELL LINE; MOUSE; MTT ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TUMOR VOLUME; WESTERN BLOTTING; WNT SIGNALING PATHWAY; XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; RNA INTERFERENCE; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; AZABICYCLO COMPOUNDS; BENZIMIDAZOLES; BETA CATENIN; BIOMARKERS, TUMOR; CELL LINE, TUMOR; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DRUG RESISTANCE, NEOPLASM; GTP PHOSPHOHYDROLASES; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INDOLES; MAP KINASE KINASE 1; MAP KINASE SIGNALING SYSTEM; MASS SPECTROMETRY; MELANOMA; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, SCID; NEOPLASM TRANSPLANTATION; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PHTHALIC ACIDS; PIPERIDINES; PROTEOMICS; PROTO-ONCOGENE PROTEINS B-RAF; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFONAMIDES; TRANSPLANTATION, HETEROLOGOUS; WNT SIGNALING PATHWAY;

EID: 84904087853     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.037424     Document Type: Article

References (48)

1. 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., Dreno, B., Nolop, K., Li, J., Nelson, B., Hou, J., Lee, R. J., Flaherty, K. T., and McArthur, G. A. (2011) Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 364, 2507-2516
2. Trunzer, K., Pavlick, A. C., Schuchter, L., Gonzalez, R., McArthur, G. A., Hutson, T. E., Moschos, S. J., Flaherty, K. T., Kim, K. B., Weber, J. S., Hersey, P., Long, G. V., Lawrence, D., Ott, P. A., Amaravadi, R. K., Lewis, K. D., Puzanov, I., Lo, R. S., Koehler, A., Kockx, M., Spleiss, O., Schell-Steven, A., Gilbert, H. N., Cockey, L., Bollag, G., Lee, R. J., Joe, A. K., Sosman, J. A., and Ribas, A. (2013) Pharmacodynamic effects and mechanisms of resistance to vemurafenib in patients with metastatic melanoma. J. Clin. Oncol. 31, 1767-1774
3. Fedorenko, I. V., Paraiso, K. H., and Smalley, K. S. (2011) Acquired and intrinsic BRAF inhibitor resistance in BRAF V600E mutant melanoma. Biochem. Pharmacol. 82, 201-209
4. Poulikakos, P. I., Persaud, Y., Janakiraman, M., Kong, X., Ng, C., Moriceau, G., Shi, H., Atefi, M., Titz, B., Gabay, M. T., Salton, M., Dahlman, K. B., Tadi, M., Wargo, J. A., Flaherty, K. T., Kelley, M. C., Misteli, T., Chapman, P. B., Sosman, J. A., Graeber, T. G., Ribas, A., Lo, R. S., Rosen, N., and Solit, D. B. (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF(V600E). Nature 480, 387-390
5. 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., and Lo, R. S. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468, 973-977
6. Paraiso, K. H., Xiang, Y., Rebecca, V. W., Abel, E. V., Chen, Y. A., Munko, A. C., Wood, E., Fedorenko, I. V., Sondak, V. K., Anderson, A. R., Ribas, A., Palma, M. D., Nathanson, K. L., Koomen, J. M., Messina, J. L., and Smalley, K. S. (2011) PTEN loss confers BRAF inhibitor resistance to melanoma cells through the suppression of BIM expression. Cancer Res. 71, 2750-2760
7. Whittaker, S. R., Theurillat, J. P., Van Allen, E., Wagle, N., Hsiao, J., Cowley, G. S., Schadendorf, D., Root, D. E., and Garraway, L. A. (2013) A genome-scale RNA interference screen implicates NF1 loss in resistance to RAF inhibition. Cancer Discov., 3, 350-62
8. Paraiso, K. H., 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., and Smalley, K. S. (2012) The HSP90 inhibitor XL888 overcomes BRAF inhibitor resistance mediated through diverse mechanisms. Clin. Cancer Res. 18, 2502-2514
9. Wu, X., Marmarelis, M. E., and Hodi, F. S. (2013) Activity of the heat shock protein 90 inhibitor ganetespib in melanoma. PLoS ONE 8, e56134
10. Fedorenko, I. V., Gibney, G. T., and Smalley, K. S. (2013) NRAS mutant melanoma: biological behavior and future strategies for therapeutic management. Oncogene, 32, 3009-18
11. Ascierto, P. A., Schadendorf, D., Berking, C., Agarwala, S. S., van Herpen, C. M., Queirolo, P., Blank, C. U., Hauschild, A., Beck, J. T., St-Pierre, A., Niazi, F., Wandel, S., Peters, M., Zubel, A., and Dummer, R. (2013) MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAF mutations: a non-randomised, open-label phase 2 study. Lancet Oncol. 14, 249-256
12. 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., and Rosen, N. (2012) Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 22, 668-682
13. Chandarlapaty, S., Sawai, A., Scaltriti, M., Rodrik-Outmezguine, V., Grbovic-Huezo, O., Serra, V., Majumder, P. K., Baselga, J., and Rosen, N. (2011) AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 19, 58-71
14. Richardson, P. G., Chanan-Khan, A. A., Lonial, S., Krishnan, A. Y., Carroll, M. P., Alsina, M., Albitar, M., Berman, D., Messina, M., and Anderson, K. C. (2011) Tanespimycin and bortezomib combination treatment in patients with relapsed or relapsed and refractory multiple myeloma: results of a phase 1/2 study. Br. J. Haematol. 153, 729-740
15. Addona, T. A., Abbatiello, S. E., Schilling, B., Skates, S. J., Mani, D. R., Bunk, D. M., Spiegelman, C. H., Zimmerman, L. J., Ham, A. J., Keshishian, H., Hall, S. C., Allen, S., Blackman, R. K., Borchers, C. H., Buck, C., Cardasis, H. L., Cusack, M. P., Dodder, N. G., Gibson, B. W., Held, J. M., Hiltke, T., Jackson, A., Johansen, E. B., Kinsinger, C. R., Li, J., Mesri, M., Neubert, T. A., Niles, R. K., Pulsipher, T. C., Ransohoff, D., Rodriguez, H., Rudnick, P. A., Smith, D., Tabb, D. L., Tegeler, T. J., Variyath, A. M., Vega-Montoto, L. J., Wahlander, A., Waldemarson, S., Wang, M., Whiteaker, J. R., Zhao, L., Anderson, N. L., Fisher, S. J., Liebler, D. C., Paulovich, A. G., Regnier, F. E., Tempst, P., and Carr, S. A. (2009) Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma. Nat. Biotechnol. 27, 633-641
16. Kennedy, J. J., Abbatiello, S. E., Kim, K., Yan, P., Whiteaker, J. R., Lin, C., Kim, J. S., Zhang, Y., Wang, X., Ivey, R. G., Zhao, L., Min, H., Lee, Y., Yu, M. H., Yang, E. G., Lee, C., Wang, P., Rodriguez, H., Kim, Y., Carr, S. A., and Paulovich, A. G. (2014) Demonstrating the feasibility of large-scale development of standardized assays to quantify human proteins. Nat. Methods, 11, 149-55
17. Prakash, A., Rezai, T., Krastins, B., Sarracino, D., Athanas, M., Russo, P., Zhang, H., Tian, Y., Li, Y., Kulasingam, V., Drabovich, A., Smith, C. R., Batruch, I., Oran, P. E., Fredolini, C., Luchini, A., Liotta, L., Petricoin, E., Diamandis, E. P., Chan, D. W., Nelson, R., and Lopez, M. F. (2012) Interlaboratory reproducibility of selective reaction monitoring assays using multiple upfront analyte enrichment strategies. J. Proteome Res. 11, 3986-3995
18. Prakash, A., Rezai, T., Krastins, B., Sarracino, D., Athanas, M., Russo, P., Ross, M. M., Zhang, H., Tian, Y., Kulasingam, V., Drabovich, A. P., Smith, C., Batruch, I., Liotta, L., Petricoin, E., Diamandis, E. P., Chan, D. W., and Lopez, M. F. (2010) Platform for establishing interlaboratory reproducibility of selected reaction monitoring-based mass spectrometry peptide assays. J. Proteome Res. 9, 6678-6688
19. Wolf-Yadlin, A., Hautaniemi, S., Lauffenburger, D. A., and White, F. M. (2007) Multiple reaction monitoring for robust quantitative proteomic analysis of cellular signaling networks. Proc. Natl. Acad. Sci. U.S.A. 104, 5860-5865 (Pubitemid 47175624)
20. Chen, Y., Gruidl, M., Remily-Wood, E., Liu, R. Z., Eschrich, S., Lloyd, M., Nasir, A., Bui, M. M., Huang, E., Shibata, D., Yeatman, T., and Koomen, J. M. (2010) Quantification of β-catenin signaling components in colon cancer cell lines, tissue sections, and microdissected tumor cells using reaction monitoring mass spectrometry. J. Proteome Res. 9, 4215-4227
21. Xiang, Y., Remily-Wood, E. R., Oliveira, V., Yarde, D., He, L., Cheng, J. Q., Mathews, L., Boucher, K., Cubitt, C., Perez, L., Gauthier, T. J., Eschrich, S. A., Shain, K. H., Dalton, W. S., Hazlehurst, L., and Koomen, J. M. (2011) Monitoring a nuclear factor-κB signature of drug resistance in multiple myeloma. Mol. Cell. Proteomics,
22. Remily-Wood, E. R., Liu, R. Z., Xiang, Y., Chen, Y., Thomas, C. E., Rajyaguru, N., Kaufman, L. M., Ochoa, J. E., Hazlehurst, L., Pinilla-Ibarz, J., Lancet, J., Zhang, G., Haura, E., Shibata, D., Yeatman, T., Smalley, K. S., Dalton, W. S., Huang, E., Scott, E., Bloom, G. C., Eschrich, S. A., and Koomen, J. M. (2011) A database of reaction monitoring mass spectrometry assays for elucidating therapeutic response in cancer. Proteomics Clin. Appl. 5, 383-396
23. Barnidge, D. R., Goodmanson, M. K., Klee, G. G., and Muddiman, D. C. (2004) Absolute quantification of the model biomarker prostate-specific antigen in serum by LC-Ms/MS using protein cleavage and isotope dilution mass spectrometry. J. Proteome Res. 3, 644-652 (Pubitemid 39207371)
24. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W., and Gygi, S. P. (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. U.S.A. 100, 6940-6945 (Pubitemid 36706372)
25. Havlis, J., and Shevchenko, A. (2004) Absolute quantification of proteins in solutions and in polyacrylamide gels by mass spectrometry. Anal. Chem. 76, 3029-3036 (Pubitemid 38715692)
26. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
27. Taipale, M., Krykbaeva, I., Koeva, M., Kayatekin, C., Westover, K. D., Karras, G. I., and Lindquist, S. (2012) Quantitative analysis of hsp90-client interactions reveals principles of substrate recognition. Cell 150, 987-1001
28. Sawyers, C. (2004) Targeted cancer therapy. Nature 432, 294-297
29. Kwak, E. L., Bang, Y. J., Camidge, D. R., Shaw, A. T., Solomon, B., Maki, R. G., Ou, S. H., Dezube, B. J., Jänne, P. A., Costa, D. B., Varella-Garcia, M., Kim, W. H., Lynch, T. J., Fidias, P., Stubbs, H., Engelman, J. A., Sequist, L. V., Tan, W., Gandhi, L., Mino-Kenudson, M., Wei, G. C., Shreeve, S. M., Ratain, M. J., Settleman, J., Christensen, J. G., Haber, D. A., Wilner, K., Salgia, R., Shapiro, G. I., Clark, J. W., and Iafrate, A. J. (2010) Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N. Engl. J. Med. 363, 1693-1703
30. 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., and Lo, R. S. (2014) Acquired Resistance and Clonal Evolution in Melanoma during BRAF Inhibitor Therapy. Cancer Discov., 4, 80-93
31. Wagle, N., Emery, C., Berger, M. F., Davis, M. J., Sawyer, A., Pochanard, P., Kehoe, S. M., Johannessen, C. M., Macconaill, L. E., Hahn, W. C., Meyerson, M., and Garraway, L. A. (2011) Dissecting therapeutic resistance to RAF inhibition in melanoma by tumor genomic profiling. J. Clin. Oncol., 29, 3085-96
32. Trepel, J., Mollapour, M., Giaccone, G., and Neckers, L. (2010) Targeting the dynamic HSP90 complex in cancer. Nat. Rev. Cancer 10, 537-549
33. Taipale, M., Jarosz, D. F., and Lindquist, S. (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11, 515-528
34. Xu, W., and Neckers, L. (2007) Targeting the molecular chaperone heat shock protein 90 provides a multifaceted effect on diverse cell signaling pathways of cancer cells. Clin. Cancer Res. 13, 1625-1629 (Pubitemid 46952925)
35. Modi, S., Stopeck, A., Linden, H., Solit, D., Chandarlapaty, S., Rosen, N., D'Andrea, G., Dickler, M., Moynahan, M. E., Sugarman, S., Ma, W., Patil, S., Norton, L., Hannah, A. L., and Hudis, C. (2011) HSP90 Inhibition is effective in breast cancer: a phase II trial of tanespimycin (17-AAG) plus trastuzumab in patients with HER2-positive metastatic breast cancer progressing on trastuzumab. Clin. Cancer Res. 17, 5132-5139
36. Solit, D. B., Osman, I., Polsky, D., Panageas, K. S., Daud, A., Goydos, J. S., Teitcher, J., Wolchok, J. D., Germino, F. J., Krown, S. E., Coit, D., Rosen, N., and Chapman, P. B. (2008) Phase II trial of 17-allylamino-17- demethoxygeldanamycin in patients with metastatic melanoma. Clin. Cancer Res. 14, 8302-8307
37. Arteaga, C. L. (2011) Why is this effective HSP90 inhibitor not being developed in HER2+ breast cancer? Clin. Cancer Res. 17, 4919-4921
38. Scaltriti, M., Dawood, S., and Cortes, J. (2012) Molecular pathways: targeting hsp90-who benefits and who does not. Clin. Cancer Res. 18, 4508-4513
39. Leu, J. I., Pimkina, J., Frank, A., Murphy, M. E., and George, D. L. (2009) A small molecule inhibitor of inducible heat shock protein 70. Mol. Cell 36, 15-27
40. Murphy, M. E. (2013) The HSP70 family and cancer. Carcinogenesis 34, 1181-1188
41. Balaburski, G. M., Leu, J. I., Beeharry, N., Hayik, S., Andrake, M. D., Zhang, G., Herlyn, M., Villanueva, J., Dunbrack, R. L., Jr., Yen, T., George, D. L., and Murphy, M. E. (2013) A modified HSP70 inhibitor shows broad activity as an anticancer agent. Mol. Cancer Res. 11, 219-229
42. Shi, H., Hong, A., Kong, X., Koya, R. C., Song, C., Moriceau, G., Hugo, W., Yu, C. C., Ng, C., Chodon, T., Scolyer, R. A., Kefford, R. F., Ribas, A., Long, G. V., and Lo, R. S. (2014) A novel AKT1 mutant amplifies an adaptive melanoma response to BRAF inhibition. Cancer Discov., 4, 69-79
43. Duncan, J. S., Whittle, M. C., Nakamura, K., Abell, A. N., Midland, A. A., Zawistowski, J. S., Johnson, N. L., Granger, D. A., Jordan, N. V., Darr, D. B., Usary, J., Kuan, P. F., Smalley, D. M., Major, B., He, X., Hoadley, K. A., Zhou, B., Sharpless, N. E., Perou, C. M., Kim, W. Y., Gomez, S. M., Chen, X., Jin, J., Frye, S. V., Earp, H. S., Graves, L. M., and Johnson, G. L. (2012) Dynamic reprogramming of the kinome in response to targeted MEK inhibition in triple-negative breast cancer. Cell 149, 307-321
44. Abel, E. V., Basile, K. J., Kugel, C. H., 3rd, Witkiewicz, A. K., Le, K., Amaravadi, R. K., Karakousis, G. C., Xu, X., Xu, W., Schuchter, L. M., Lee, J. B., Ertel, A., Fortina, P., and Aplin, A. E. (2013) Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3. J. Clin. Invest. 123, 2155-2168
45. Tworkoski, K., Singhal, G., Szpakowski, S., Zito, C. I., Bacchiocchi, A., Muthusamy, V., Bosenberg, M., Krauthammer, M., Halaban, R., and Stern, D. F. (2011) Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol. Cancer Res. 9, 801-812
46. Sensi, M., Catani, M., Castellano, G., Nicolini, G., Alciato, F., Tragni, G., De Santis, G., Bersani, I., Avanzi, G., Tomassetti, A., Canevari, S., and Anichini, A. (2011) Human cutaneous melanomas lacking MITF and melanocyte differentiation antigens express a functional Axl receptor kinase. J. Invest. Dermatol. 131, 2448-2457
47. Conrad, W. H., Swift, R. D., Biechele, T. L., Kulikauskas, R. M., Moon, R. T., and Chien, A. J. (2012) Regulating the response to targeted MEK inhibition in melanoma: enhancing apoptosis in NRAS- and BRAF-mutant melanoma cells with Wnt/β-catenin activation. Cell Cycle 11, 3724-3730
48. Biechele, T. L., Kulikauskas, R. M., Toroni, R. A., Lucero, O. M., Swift, R. D., James, R. G., Robin, N. C., Dawson, D. W., Moon, R. T., and Chien, A. J. (2012) Wnt/β-catenin signaling and AXIN1 regulate apoptosis triggered by inhibition of the mutant kinase BRAFV600E in human melanoma. Sci. Signal. 5, ra3