AXL mediates resistance to PI3Kα inhibition by activating the EGFR/PKC/mTOR Axis in Head and neck and esophageal squamous cell carcinomas

Cancer Cell

Volumn 27, Issue 4, 2015, Pages 533-546

  Elkabets, Moshe ^a   Pazarentzos, Evangelos ^b   Juric, Dejan ^c   Sheng, Qing ^d   Pelossof, Raphael A ^a   Brook, Samuel ^a   Benzaken, Ana Oaknin ^e   Rodon, Jordi ^e   Morse, Natasha ^a   Yan, Jenny Jiacheng ^b   Liu, Manway ^d   Das, Rita ^d   Chen, Yan ^d   Tam, Angela ^d   Wang, Huiqin ^d   Liang, Jinsheng ^d   Gurski, Joseph M ^c   Kerr, Darcy A ^c   Rosell, Rafael ^f,g   Teixidó, Cristina ^g   Huang, Alan ^d   Ghossein, Ronald A ^a   Rosen, Neal ^a   Bivona, Trever G ^b   Scaltriti, Maurizio ^a   Baselga, José ^a   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e VALL D HEBRON UNIVERSITY HOSPITAL   (Spain)

^f HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^g INSTITUT UNIVERSITARI DEXEUS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPELISIB; EPIDERMAL GROWTH FACTOR RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE ALPHA; PHOSPHOLIPASE C GAMMA; PROTEIN AXL; PROTEIN KINASE C; UNCLASSIFIED DRUG; AXL RECEPTOR TYROSINE KINASE; CETUXIMAB; MONOCLONAL ANTIBODY; MTOR PROTEIN, HUMAN; NVP-BYL719; ONCOPROTEIN; PIK3CA PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; PROTEIN TYROSINE KINASE; TARGET OF RAPAMYCIN KINASE; THIAZOLE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ENZYME ACTIVATION; ENZYME INHIBITION; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; FEMALE; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG RESISTANCE; DRUG SCREENING; ESOPHAGUS TUMOR; GENETICS; HEAD AND NECK TUMOR; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

MAMMALIA;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CETUXIMAB; DRUG RESISTANCE, NEOPLASM; ESOPHAGEAL NEOPLASMS; HEAD AND NECK NEOPLASMS; HUMANS; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; THIAZOLES; TOR SERINE-THREONINE KINASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84928015512     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.03.010     Document Type: Article

References (41)

1. Agrawal N., Frederick M.J., Pickering C.R., Bettegowda C., Chang K., Li R.J., Fakhry C., Xie T.X., Zhang J., Wang J., et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 2011, 333:1154-1157.
2. Akagi I., Miyashita M., Makino H., Nomura T., Hagiwara N., Takahashi K., Cho K., Mishima T., Ishibashi O., Ushijima T., et al. Overexpression of PIK3CA is associated with lymph node metastasis in esophageal squamous cell carcinoma. Int. J. Oncol. 2009, 34:767-775.
3. Baselga J., Trigo J.M., Bourhis J., Tortochaux J., Cortés-Funes H., Hitt R., Gascón P., Amellal N., Harstrick A., Eckardt A. Phase II multicenter study of the antiepidermal growth factor receptor monoclonal antibody cetuximab in combination with platinum-based chemotherapy in patients with platinum-refractory metastatic and/or recurrent squamous cell carcinoma of the head and neck. J.Clin. Oncol. 2005, 23:5568-5577.
4. Bonner J.A., Harari P.M., Giralt J., Azarnia N., Shin D.M., Cohen R.B., Jones C.U., Sur R., Raben D., Jassem J., et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N.Engl. J. Med. 2006, 354:567-578.
5. Brand T.M., Iida M., Stein A.P., Corrigan K.L., Braverman C.M., Luthar N., Toulany M., Gill P.S., Salgia R., Kimple R.J., Wheeler D.L. AXL mediates resistance to cetuximab therapy. Cancer Res. 2014, 74:5152-5164.
6. Byers L.A., Diao L., Wang J., Saintigny P., Girard L., Peyton M., Shen L., Fan Y., Giri U., Tumula P.K., et al. An epithelial-mesenchymal transition gene signature predicts resistance to EGFR and PI3K inhibitors and identifies Axl as a therapeutic target for overcoming EGFR inhibitor resistance. Clin. Cancer Res. 2013, 19:279-290.
7. Cerami E., Gao J., Dogrusoz U., Gross B.E., Sumer S.O., Aksoy B.A., Jacobsen A., Byrne C.J., Heuer M.L., Larsson E., et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012, 2:401-404.
8. Chattopadhyay A., Vecchi M., Ji Qs., Mernaugh R., Carpenter G. The role of individual SH2 domains in mediating association of phospholipase C-gamma1 with the activated EGF receptor. J.Biol. Chem. 1999, 274:26091-26097.
9. Cohen E.E., Lingen M.W., Zhu B., Zhu H., Straza M.W., Pierce C., Martin L.E., Rosner M.R. Protein kinase C zeta mediates epidermal growth factor-induced growth of head and neck tumor cells by regulating mitogen-activated protein kinase. Cancer Res. 2006, 66:6296-6303.
10. Disatnik M.H., Hernandez-Sotomayor S.M., Jones G., Carpenter G., Mochly-Rosen D. Phospholipase C-gamma 1 binding to intracellular receptors for activated protein kinase C. Proc. Natl. Acad. Sci. USA 1994, 91:559-563.
11. Elkabets M., Vora S., Juric D., Morse N., Mino-Kenudson M., Muranen T., Tao J., Campos A.B., Rodon J., Ibrahim Y.H., et al. mTORC1 inhibition is required for sensitivity to PI3K p110alpha inhibitors in PIK3CA-mutant breast cancer. Sci. Transl. Med. 2013, 5:196ra199.
12. Engelman J.A. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat. Rev. Cancer 2009, 9:550-562.
13. Fan Z., Masui H., Altas I., Mendelsohn J. Blockade of epidermal growth factor receptor function by bivalent and monovalent fragments of 225 anti-epidermal growth factor receptor monoclonal antibodies. Cancer Res. 1993, 53:4322-4328.
14. Fan Q.W., Cheng C., Knight Z.A., Haas-Kogan D., Stokoe D., James C.D., McCormick F., Shokat K.M., Weiss W.A. EGFR signals to mTOR through PKC and independently of Akt in glioma. Sci. Signal. 2009, 2:ra4.
15. Fritsch C., Huang A., Chatenay-Rivauday C., Schnell C., Reddy A., Liu M., Kauffmann A., Guthy D., Erdmann D., De Pover A., et al. Characterization of the novel and specific PI3Kα inhibitor NVP-BYL719 and development of the patient stratification strategy for clinical trials. Mol. Cancer Ther. 2014, 13:1117-1129.
16. Furet P., Guagnano V., Fairhurst R.A., Imbach-Weese P., Bruce I., Knapp M., Fritsch C., Blasco F., Blanz J., Aichholz R., et al. Discovery of NVP-BYL719 a potent and selective phosphatidylinositol-3 kinase alpha inhibitor selected for clinical evaluation. Bioorg. Med. Chem. Lett. 2013, 23:3741-3748.
17. Giles K.M., Kalinowski F.C., Candy P.A., Epis M.R., Zhang P.M., Redfern A.D., Stuart L.M., Goodall G.J., Leedman P.J. Axl mediates acquired resistance of head and neck cancer cells to the epidermal growth factor receptor inhibitor erlotinib. Mol. Cancer Ther. 2013, 12:2541-2558.
18. Graham D.K., DeRyckere D., Davies K.D., Earp H.S. The TAM family: phosphatidylserine sensing receptor tyrosine kinases gone awry in cancer. Nat. Rev. Cancer 2014, 14:769-785.
19. Harbinski F., Craig V.J., Sanghavi S., Jeffery D., Liu L., Sheppard K.A., Wagner S., Stamm C., Buness A., Chatenay-Rivauday C., et al. Rescue screens with secreted proteins reveal compensatory potential of receptor tyrosine kinases in driving cancer growth. Cancer Discov. 2012, 2:948-959.
20. Hennessy B.T., Smith D.L., Ram P.T., Lu Y., Mills G.B. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat. Rev. Drug Discov. 2005, 4:988-1004.
21. Holland S.J., Powell M.J., Franci C., Chan E.W., Friera A.M., Atchison R.E., McLaughlin J., Swift S.E., Pali E.S., Yam G., et al. Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res. 2005, 65:9294-9303.
22. Holland S.J., Pan A., Franci C., Hu Y., Chang B., Li W., Duan M., Torneros A., Yu J., Heckrodt T.J., et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res. 2010, 70:1544-1554.
23. Janssen J.W., Schulz A.S., Steenvoorden A.C., Schmidberger M., Strehl S., Ambros P.F., Bartram C.R. A novel putative tyrosine kinase receptor with oncogenic potential. Oncogene 1991, 6:2113-2120.
24. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J. Clin. 2011, 61:69-90.
25. Kamangar F., Dores G.M., Anderson W.F. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J.Clin. Oncol. 2006, 24:2137-2150.
26. Lin D.C., Hao J.J., Nagata Y., Xu L., Shang L., Meng X., Sato Y., Okuno Y., Varela A.M., Ding L.W., et al. Genomic and molecular characterization of esophageal squamous cell carcinoma. Nat. Genet. 2014, 46:467-473.
27. Liu L., Greger J., Shi H., Liu Y., Greshock J., Annan R., Halsey W., Sathe G.M., Martin A.M., Gilmer T.M. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res. 2009, 69:6871-6878.
28. Lui V.W., Hedberg M.L., Li H., Vangara B.S., Pendleton K., Zeng Y., Lu Y., Zhang Q., Du Y., Gilbert B.R., et al. Frequent mutation of the PI3K pathway in head and neck cancer defines predictive biomarkers. Cancer Discov. 2013, 3:761-769.
29. Meyer A.S., Miller M.A., Gertler F.B., Lauffenburger D.A. The receptor AXL diversifies EGFR signaling and limits the response to EGFR-targeted inhibitors in triple-negative breast cancer cells. Sci. Signal. 2013, 6:ra66.
30. Mochly-Rosen D., Das K., Grimes K.V. Protein kinase C, an elusive therapeutic target?. Nat. Rev. Drug Discov. 2012, 11:937-957.
31. Paccez J.D., Vogelsang M., Parker M.I., Zerbini L.F. The receptor tyrosine kinase Axl in cancer: biological functions and therapeutic implications. Int. J. Cancer 2014, 134:1024-1033.
32. Rosse C., Linch M., Kermorgant S., Cameron A.J., Boeckeler K., Parker P.J. PKC and the control of localized signal dynamics. Nat. Rev. Mol. Cell Biol. 2010, 11:103-112.
33. Söderberg O., Leuchowius K.J., Gullberg M., Jarvius M., Weibrecht I., Larsson L.G., Landegren U. Characterizing proteins and their interactions in cells and tissues using the insitu proximity ligation assay. Methods 2008, 45:227-232.
34. Song Y., Li L., Ou Y., Gao Z., Li E., Li X., Zhang W., Wang J., Xu L., Zhou Y., et al. Identification of genomic alterations in oesophageal squamous cell cancer. Nature 2014, 509:91-95.
35. Stransky N., Egloff A.M., Tward A.D., Kostic A.D., Cibulskis K., Sivachenko A., Kryukov G.V., Lawrence M.S., Sougnez C., McKenna A., et al. The mutational landscape of head and neck squamous cell carcinoma. Science 2011, 333:1157-1160.
36. Straussman R., Morikawa T., Shee K., Barzily-Rokni M., Qian Z.R., Du J., Davis A., Mongare M.M., Gould J., Frederick D.T., et al. Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 2012, 487:500-504.
37. Suda T., Hama T., Kondo S., Yuza Y., Yoshikawa M., Urashima M., Kato T., Moriyama H. Copy number amplification of the PIK3CA gene is associated with poor prognosis in non-lymph node metastatic head and neck squamous cell carcinoma. BMC Cancer 2012, 12:416.
38. Vermorken J.B., Mesia R., Rivera F., Remenar E., Kawecki A., Rottey S., Erfan J., Zabolotnyy D., Kienzer H.R., Cupissol D., et al. Platinum-based chemotherapy plus cetuximab in head and neck cancer. N.Engl. J. Med. 2008, 359:1116-1127.
39. Vivanco I., Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2002, 2:489-501.
40. Wilson T.R., Fridlyand J., Yan Y., Penuel E., Burton L., Chan E., Peng J., Lin E., Wang Y., Sosman J., et al. Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 2012, 487:505-509.
41. Zhang Z., Lee J.C., Lin L., Olivas V., Au V., LaFramboise T., Abdel-Rahman M., Wang X., Levine A.D., Rho J.K., et al. Activation of the AXL kinase causes resistance to EGFR-targeted therapy in lung cancer. Nat. Genet. 2012, 44:852-860.