Impact of oncogenic driver mutations on feedback between the PI3K and MEK pathways in cancer cells

Bioscience Reports

Volumn 32, Issue 4, 2012, Pages 413-422

  Yuen, Hiu Fung ^a,b   Abramczykd, Olga ^c   Montgomery, Grant ^a   Chan, Ka Kui ^a   Huang, Yu Han ^b   Sasazuki, Takehiko ^d   Shirasawa, Senji ^d   Gopesh, Srivastava ^e   Chan, Kwok Wah ^e   Fennell, Dean ^f   Janne, Pasi ^g   El Tanani, Mohamed ^a   Murray, James T ^a,h  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d FUKUOKA UNIVERSITY   (Japan)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

^f UNIVERSITY OF LEICESTER   (United Kingdom)

^g HARVARD MEDICAL SCHOOL   (United States)

^h TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Akt; c Met; Cancer cell; K Ras; Mitogen activated protein kinase extracellular signal regulated kinase kinase (MEK); Phosphoinositide 3 kinase (PI3K)

Indexed keywords

2 (2 CHLORO 4 IODOANILINO) N CYCLOPROPYLMETHOXY 3,4 DIFLUOROBENZAMIDE; 2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; BIOLOGICAL MARKER; K RAS PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OKADAIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS PROTEIN; SCATTER FACTOR RECEPTOR;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CARCINOGENESIS; CELL SURVIVAL; COLORECTAL CANCER; CONTROLLED STUDY; DRUG RESPONSE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ESOPHAGUS CANCER; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MALE; MOLECULAR INTERACTION; MUTATIONAL ANALYSIS; NEGATIVE FEEDBACK; PROSTATE CANCER; PROTEIN EXPRESSION; UPREGULATION; WILD TYPE;

APOPTOSIS; BENZAMIDES; CELL LINE, TUMOR; CELL SURVIVAL; DRUG SYNERGISM; FEEDBACK, PHYSIOLOGICAL; FURANS; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASES; MUTATION; OKADAIC ACID; ONCOGENES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; PYRIDINES; PYRIMIDINES; RAS PROTEINS; SIROLIMUS; UP-REGULATION;

MAMMALIA;

EID: 84863644042     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20120050     Document Type: Article

References (40)

1. Grant, S. (2008) Cotargeting survival signaling pathways in cancer. J. Clin. Invest. 118, 3003-3006
2. Sebolt-Leopold, J. S. (2000) Development of anticancer drugs targeting the MAP kinase pathway. Oncogene 19, 6594-6599
3. Sebolt-Leopold, J. S., Dudley, D. T., Herrera, R., Van Becelaere, K., Wiland, A., Gowan, R. C., Tecle, H., Barrett, S. D., Bridges, A., Przybranowski, S. et al. (1999) Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat. Med. 5, 810-816 (Pubitemid 29318616)
4. Allen, L. F., Sebolt-Leopold, J. and Meyer, M. B. (2003) CI-1040 (PD184352), a targeted signal transduction inhibitor of MEK (MAPKK). Semin. Oncol. 30, 105-116 (Pubitemid 37433401)
5. Rinehart, J., Adjei, A. A., Lorusso, P. M., Waterhouse, D., Hecht, J. R., Natale, R. B., Hamid, O., Varterasian, M., Asbury, P., Kaldjian, E. P. et al. (2004) Multicenter phase II study of the oral MEK inhibitor, CI-1040, in patients with advanced non-small-cell lung, breast, colon, and pancreatic cancer. J. Clin. Oncol. 22, 4456-4462 (Pubitemid 41185111)
6. Lorusso, P. M., Adjei, A. A., Varterasian, M., Gadgeel, S., Reid, J., Mitchell, D. Y., Hanson, L., DeLuca, P., Bruzek, L., Piens, J. et al. (2005) Phase I and pharmacodynamic study of the oral MEK inhibitor CI-1040 in patients with advanced malignancies. J. Clin. Oncol. 23, 5281-5293 (Pubitemid 46206982)
7. Wang, Y., Van Becelaere, K., Jiang, P., Przybranowski, S., Omer, C. and Sebolt-Leopold, J. (2005) A role for K-ras in conferring resistance to the MEK inhibitor, CI-1040. Neoplasia 7, 336-347 (Pubitemid 40664223)
8. Liu, D., Liu, Z., Jiang, D., Dackiw, A. P. and Xing, M. (2007) Inhibitory effects of the mitogen-activated protein kinase kinase inhibitor CI-1040 on the proliferation and tumor growth of thyroid cancer cells with BRAF or RAS mutations. J. Clin. Endocrinol. Metab. 92, 4686-4695 (Pubitemid 350223445)
9. Mirzoeva, O. K., Das, D., Heiser, L. M., Bhattacharya, S., Siwak, D., Gendelman, R., Bayani, N., Wang, N. J., Neve, R. M., Guan, Y. et al. (2009) Basal subtype and MAPK/ERK kinase (MEK)- phosphoinositide 3-kinase feedback signaling determine susceptibility of breast cancer cells to MEK inhibition. Cancer Res. 69, 565-572
10. McDaid, H. M., Lopez-Barcons, L., Grossman, A., Lia, M., Keller, S., Perez-Soler, R. and Horwitz, S. B. (2005) Enhancement of the therapeutic efficacy of taxol by the mitogen-activated protein kinase kinase inhibitor CI-1040 in nude mice bearing human heterotransplants. Cancer Res. 65, 2854-2860 (Pubitemid 40490089)
11. Ou, D. L., Shen, Y. C., Liang, J. D., Liou, J. Y., Yu, S. L., Fan, H. H., Wang, D. S., Lu, Y. S., Hsu, C. and Cheng, A. L. (2009) Induction of Bim expression contributes to the antitumor synergy between sorafenib and mitogen-activated protein kinase/extracellular signal-regulated kinase kinase inhibitor CI-1040 in hepatocellular carcinoma. Clin. Cancer Res. 15, 5820-5828
12. Pellicano, F., Simara, P., Sinclair, A., Helgason, G. V., Copland, M., Grant, S. and Holyoake, T. L. (2011) The MEK inhibitor PD184352 enhances BMS-214662-induced apoptosis in CD34+ CML stem/progenitor cells. Leukemia 25, 1159-1167
13. Workman, P., Clarke, P. A., Raynaud, F. I. and van Montfort, R. L. (2010) Drugging the PI3 kinome: from chemical tools to drugs in the clinic. Cancer Res. 70, 2146-2157
14. Hayakawa, M., Kaizawa, H., Moritomo, H., Koizumi, T., Ohishi, T., Yamano, M., Okada, M., Ohta, M., Tsukamoto, S., Raynaud, F. I. et al. (2007) Synthesis and biological evaluation of pyrido[3′,2′:4,5]furo[3,2-d]pyrimidine derivatives as novel PI3 kinase p110á inhibitors. Bioorg. Med. Chem. Lett. 17, 2438-2442 (Pubitemid 46507793)
15. Raynaud, F. I., Eccles, S., Clarke, P. A., Hayes, A., Nutley, B., Alix, S., Henley, A., Di-Stefano, F., Ahmad, Z., Guillard, S. et al. (2007) Pharmacologic characterization of a potent inhibitor of class I phosphatidylinositide 3-kinases. Cancer Res. 67, 5840-5850 (Pubitemid 46985018)
16. Guillard, S., Clarke, P. A., Te Poele, R., Mohri, Z., Bjerke, L., Valenti, M., Raynaud, F., Eccles, S. A. and Workman, P. (2009) Molecular pharmacology of phosphatidylinositol 3-kinase inhibition in human glioma. Cell Cycle 8, 443-453
17. Prevo, R., Deutsch, E., Sampson, O., Diplexcito, J., Cengel, K., Harper, J., O'Neill, P., McKenna, W. G., Patel, S. and Bernhard, E. J. (2008) Class I PI3 kinase inhibition by the pyridinylfuranopyrimidine inhibitor PI-103 enhances tumor radiosensitivity. Cancer Res. 68, 5915-5923
18. Westhoff, M. A., Kandenwein, J. A., Karl, S., Vellanki, S. H., Braun, V., Eramo, A., Antoniadis, G., Debatin, K. M. and Fulda, S. (2009) The pyridinylfuranopyrimidine inhibitor, PI-103, chemosensitizes glioblastoma cells for apoptosis by inhibiting DNA repair. Oncogene 28, 3586-3596
19. Lopez-Fauqued, M., Gil, R., Grueso, J., Hernandez-Losa, J., Pujol, A., Moline, T. and Recio, J. A. (2010) The dual PI3K/mTOR inhibitor PI-103 promotes immunosuppression, in vivo tumor growth and increases survival of sorafenib-treated melanoma cells. Int. J. Cancer 126, 1549-1561
20. Gedaly, R., Angulo, P., Hundley, J., Daily, M. F., Chen, C., Koch, A. and Evers, B. M. (2010) PI-103 and sorafenib inhibit hepatocellular carcinoma cell proliferation by blocking Ras/Raf/MAPK and PI3K/AKT/mTOR pathways. Anticancer Res. 30, 4951-4958
21. Serra, V., Scaltriti, M., Prudkin, L., Eichhorn, P. J., Ibrahim, Y. H., Chandarlapaty, S., Markman, B., Rodriguez, O., Guzman, M., Rodriguez, S. et al. (2011) PI3K inhibition results in enhanced HER signaling and acquired ERK dependency in HER2-overexpressing breast cancer. Oncogene 30, 2547-2557
22. Yuen, H. F., McCrudden, C. M., Grills, C., Zhang, S. D., Huang, Y. H., Chan, K. K., Chan, Y. P., Wong, M. L., Law, S., Srivastava, G. et al. (2012) Combinatorial use of bone morphogenetic protein 6, noggin and SOST significantly predicts cancer progression. Cancer Sci. 103, 1145-1154
23. Engelman, J. A., Zejnullahu, K., Mitsudomi, T., Song, Y., Hyland, C., Park, J. O., Lindeman, N., Gale, C. M., Zhao, X., Christensen, J. et al. (2007) MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043 (Pubitemid 46799492)
24. Shirasawa, S., Furuse, M., Yokoyama, N. and Sasazuki, T. (1993) Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260, 85-88 (Pubitemid 23122749)
25. Yuen, H. F., Chan, K. K., Grills, C., Murray, J. T., Platt-Higgins, A., Eldin, O. S., O'Byrne, K., Janne, P., Fennell, D. A., Johnston, P. G. et al. (2012) Ran is a potential therapeutic target for cancer cells with molecular changes associated with activation of the PI3K/Akt/mTORC1 and Ras/MEK/ERK pathways. Clin. Cancer Res. 18, 380-391
26. Yuen, H. F., McCrudden, C. M., Chan, K. K., Chan, Y. P., Wong, M. L., Chan, K. Y., Khoo, U. S., Law, S., Srivastava, G., Lappin, T. R. et al. (2011) The role of Pea3 group transcription factors in esophageal squamous cell carcinoma. Am. J. Pathol. 179, 992-1003
27. Sunayama, J., Matsuda, K., Sato, A., Tachibana, K., Suzuki, K., Narita, Y., Shibui, S., Sakurada, K., Kayama, T., Tomiyama, A. and Kitanaka, C. (2010) Crosstalk between the PI3K/mTOR and MEK/ERK pathways involved in the maintenance of self-renewal and tumorigenicity of glioblastoma stem-like cells. Stem Cells 28, 1930-1939
28. Boucher, M. J., Morisset, J., Vachon, P. H., Reed, J. C., Laine, J. and Rivard, N. (2000) MEK/ERK signaling pathway regulates the expression of Bcl-2, Bcl-XL, and Mcl-1 and promotes survival of human pancreatic cancer cells. J. Cell Biochem. 79, 355-369
29. Jost, M., Huggett, T. M., Kari, C., Boise, L. H. and Rodeck, U. (2001) Epidermal growth factor receptor-dependent control of keratinocyte survival and Bcl-XL expression through a MEK-dependent pathway. J. Biol. Chem. 276, 6320-6326
30. Sun, S. Y., Rosenberg, L. M., Wang, X., Zhou, Z., Yue, P., Fu, H. and Khuri, F. R. (2005) Activation of Akt and eIF4E survival pathways by rapamycin-mediated mammalian target of rapamycin inhibition. Cancer Res. 65, 7052-7058 (Pubitemid 41161231)
31. Kinkade, C. W., Castillo-Martin, M., Puzio-Kuter, A., Yan, J., Foster, T. H., Gao, H., Sun, Y., Ouyang, X., Gerald, W. L., Cordon-Cardo, C. and Abate-Shen, C. (2008) Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. J. Clin. Invest. 118, 3051-3064
32. Sarbassov, D. D., Ali, S. M., Sengupta, S., Sheen, J. H., Hsu, P. P., Bagley, A. F., Markhard, A. L. and Sabatini, D. M. (2006) Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168
33. Engelman, J. A., Chen, L., Tan, X., Crosby, K., Guimaraes, A. R., Upadhyay, R., Maira, M., McNamara, K., Perera, S. A., Song, Y. et al. (2008) Effective use of PI3K and MEK inhibitors to treat mutant Kras G12D and PIK3CA H1047R murine lung cancers. Nat. Med. 14, 1351-1356
34. Xiao, G. H., Jeffers, M., Bellacosa, A., Mitsuuchi, Y., Vande Woude, G. F. and Testa, J. R. (2001) Anti-apoptotic signaling by hepatocyte growth factor/Met via the phosphatidylinositol 3-kinase/Akt and mitogen-activated protein kinase pathways. Proc. Natl. Acad. Sci. U.S.A. 98, 247-252 (Pubitemid 32095895)
35. Donev, I. S., Wang, W., Yamada, T., Li, Q., Takeuchi, S., Matsumoto, K., Yamori, T., Nishioka, Y., Sone, S. and Yano, S. (2011) Transient PI3K inhibition induces apoptosis and overcomes HGF-mediated resistance to EGFR-TKIs in EGFR mutant lung cancer. Clin. Cancer Res. 17, 2260-2269
36. Kang, T. H. and Kim, K. T. (2006) Negative regulation of ERK activity by VRK3-mediated activation of VHR phosphatase. Nat. Cell Biol. 8, 863-869
37. von Kriegsheim, A, Pitt, A., Grindlay, G. J., Kolch, W. and Dhillon, A. S. (2006) Regulation of the Raf-MEK-ERK pathway by protein phosphatase 5. Nat. Cell Biol. 8, 1011-1016 (Pubitemid 44314733)
38. Jurek, A., Amagasaki, K., Gembarska, A., Heldin, C. H. and Lennartsson, J. (2009) Negative and positive regulation of MAPK phosphatase 3 controls platelet-derived growth factor-induced Erk activation. J. Biol. Chem. 284, 4626-4634
39. Domercq, M., Alberdi, E., Sanchez-Gomez, M. V., Ariz, U., Perez-Samartin, A. and Matute, C. (2011) Dual-specific phosphatase-6 (Dusp6) and ERK mediate AMPA receptor-induced oligodendrocyte death. J. Biol. Chem. 286, 11825-11836
40. Bermudez, O., Marchetti, S., Pages, G. and Gimond, C. (2008) Post-translational regulation of the ERK phosphatase DUSP6/MKP3 by the mTOR pathway. Oncogene 27, 3685-3691 (Pubitemid 351912973)