PTEN regulates IGF-1R-mediated therapy resistance in melanoma

Pigment Cell and Melanoma Research

Volumn 28, Issue 5, 2015, Pages 572-589

  Wang, Jun ^a   Sinnberg, Tobias ^a   Niessner, Heike ^a   Dölker, Rebecca ^a   Sauer, Birgit ^a   Kempf, Wolfgang E ^a   Meier, Friedegund ^a   Leslie, Nick ^b   Schittek, Birgit ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b HERIOT WATT UNIVERSITY   (United Kingdom)

Author keywords

IGF 1R; Melanoma; PTEN; Therapy resistance

Indexed keywords

B RAF KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR; BRAF PROTEIN, HUMAN; GREEN FLUORESCENT PROTEIN; INDOLE DERIVATIVE; PTEN PROTEIN, HUMAN; SULFONAMIDE; VEMURAFENIB;

ARTICLE; CELL CONTACT; ENZYME ACTIVITY; FIBROBLAST; HUMAN; MELANOMA; MELANOMA CELL LINE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STROMA CELL; THERAPY RESISTANCE; UPREGULATION; APOPTOSIS; CELL COMMUNICATION; CELL SURVIVAL; COCULTURE; DOWN REGULATION; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENE TRANSFER; METABOLISM; SKIN; SKIN NEOPLASMS; TUMOR CELL LINE;

APOPTOSIS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL SURVIVAL; COCULTURE TECHNIQUES; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE TRANSFER TECHNIQUES; GREEN FLUORESCENT PROTEINS; HUMANS; INDOLES; MELANOMA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS B-RAF; PTEN PHOSPHOHYDROLASE; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; SKIN; SKIN NEOPLASMS; SULFONAMIDES;

EID: 84939230746     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12390     Document Type: Article

References (48)

1. Aguissa-Toure, A.H., and Li, G. (2012). Genetic alterations of PTEN in human melanoma. Cell. Mol. Life Sci. 69, 1475-1491.
2. Alimonti, A., Carracedo, A., Clohessy, J.G. et al. (2010). Subtle variations in Pten dose determine cancer susceptibility. Nat. Genet. 42, 454-458.
3. Capoluongo, E. (2011). Insulin-like growth factor system and sporadic malignant melanoma. Am. J. Pathol. 178, 26-31.
4. 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.
5. Chapman, P.B., Hauschild, A., Robert, C. et al. (2011). Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 364, 2507-2516.
6. Ciampolillo, A., De, T.C., and Giorgino, F. (2005). The IGF-I/IGF-I receptor pathway: implications in the Pathophysiology of Thyroid Cancer. Curr. Med. Chem. 12, 2881-2891.
7. Dankort, D., Curley, D.P., Cartlidge, R.A., Nelson, B., Karnezis, A.N., Damsky, W.E. Jr, You, M.J., DePinho, R.A., McMahon, M., and Bosenberg, M. (2009). Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 41, 544-552.
8. Davidson, L., Maccario, H., Perera, N.M. et al. (2010). Suppression of cellular proliferation and invasion by the concerted lipid and protein phosphatase activities of PTEN. Oncogene 29, 687-697.
9. Davies, H., Bignell, G.R., Cox, C. et al. (2002). Mutations of the BRAF gene in human cancer. Nature 417, 949-954.
10. Davies, M.A., Stemke-Hale, K., Lin, E. et al. (2009). Integrated Molecular and Clinical Analysis of AKT Activation in Metastatic Melanoma. Clin. Cancer Res. 15, 7538-7546.
11. Flaherty, K.T., Puzanov, I., Kim, K.B. et al. (2010). Inhibition of mutated, activated BRAF in metastatic melanoma. N. Engl. J. Med. 363, 809-819.
12. Garbe, C., Eigentler, T.K., Keilholz, U., Hauschild, A., and Kirkwood, J.M. (2011). Systematic review of medical treatment in melanoma: current status and future prospects. Oncologist 16, 5-24.
13. Hilmi, C., Larribere, L., Giuliano, S., Bille, K., Ortonne, J.P., Ballotti, R., and Bertolotto, C. (2008). IGF1 promotes resistance to apoptosis in melanoma cells through an increased expression of BCL2, BCL-X(L), and survivin. J. Invest. Dermatol. 128, 1499-1505.
14. Kanter-Lewensohn, L., Dricu, A., Wang, M., Wejde, J., Kiessling, R., and Larsson, O. (1998). Expression of the insulin-like growth factor-1 receptor and its anti-apoptotic effect in malignant melanoma: a potential therapeutic target. Melanoma Res. 8, 389-397.
15. Kanter-Lewensohn, L., Dricu, A., Girnita, L., Wejde, J., and Larsson, O. (2000). Expression of insulin-like growth factor-1 receptor (IGF-1R) and p27Kip1 in melanocytic tumors: a potential regulatory role of IGF-1 pathway in distribution of p27Kip1 between different cyclins. Growth Factors 17, 193-202.
16. Keniry, M., and Parsons, R. (2008). The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene 27, 5477-5485.
17. Lackey, J., Barnett, J., Davidson, L., Batty, I.H., Leslie, N.R., and Downes, C.P. (2007). Loss of PTEN selectively desensitizes upstream IGF1 and insulin signaling. Oncogene 26, 7132-7142.
18. Lasithiotakis, K.G., Sinnberg, T.W., Schittek, B., Flaherty, K.T., Kulms, D., Maczey, E., Garbe, C., and Meier, F.E. (2008). Combined inhibition of MAPK and mTOR signaling inhibits growth, induces cell death, and abrogates invasive growth of melanoma cells. J. Invest. Dermatol. 128, 2013-2023.
19. Macaulay, V.M., Middleton, M.R., Protheroe, A.S. et al. (2013). Phase I study of humanized monoclonal antibody AVE1642 directed against the type 1 insulin-like growth factor receptor (IGF-1R), administered in combination with anticancer therapies to patients with advanced solid tumors. Ann. Oncol. 24, 784-791.
20. Maloney, E.K., McLaughlin, J.L., Dagdigian, N.E., Garrett, L.M., Connors, K.M., Zhou, X.M., Blattler, W.A., Chittenden, T., and Singh, R. (2003). An anti-insulin-like growth factor I receptor antibody that is a potent inhibitor of cancer cell proliferation. Cancer Res. 63, 5073-5083.
21. Meier, F., Schittek, B., Busch, S., Garbe, C., Smalley, K., Satyamoorthy, K., Li, G., and Herlyn, M. (2005). The RAS/RAF/MEK/ERK and PI3K/AKT signaling pathways present molecular targets for the effective treatment of advanced melanoma. Front Biosci. 10, 2986-3001.
22. O'Connor, R. (2003). Regulation of IGF-I receptor signaling in tumor cells. Horm. Metab. Res. 35, 771-777.
23. Pollak, M. (2012). The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat. Rev. Cancer 12, 159-169.
24. Pollock, P.M., Harper, U.L., Hansen, K.S. et al. (2003). High frequency of BRAF mutations in nevi. Nat. Genet. 33, 19-20.
25. Poulikakos, P.I., and Rosen, N. (2011). Mutant BRAF melanomas-dependence and resistance. Cancer Cell 19, 11-15.
26. Qin, Y., Li, L., Pan, W., and Wu, D. (2009). Regulation of phosphatidylinositol kinases and metabolism by Wnt3a and Dvl. J. Biol. Chem. 284, 22544-22548.
27. Qin, L., Wang, Y., Tao, L., and Wang, Z. (2011). AKT down-regulates insulin-like growth factor-1 receptor as a negative feedback. J. Biochem. 150, 151-156.
28. Reuveni, H., Flashner-Abramson, E., Steiner, L., Makedonski, K., Song, R., Shir, A., Herlyn, M., Bar-Eli, M., and Levitzki, A. (2013). Therapeutic destruction of insulin receptor substrates for cancer treatment. Cancer Res. 73, 4383-4394.
29. Rodeck, U., Melber, K., Kath, R., Menssen, H.D., Varello, M., Atkinson, B., and Herlyn, M. (1991). Constitutive expression of multiple growth factor genes by melanoma cells but not normal melanocytes. J. Invest. Dermatol. 97, 20-26.
30. Salmena, L., Carracedo, A., and Pandolfi, P.P. (2008). Tenets of PTEN tumor suppression. Cell 133, 403-414.
31. Samani, A.A., Yakar, S., LeRoith, D., and Brodt, P. (2007). The role of the IGF system in cancer growth and metastasis: overview and recent insights. Endocr. Rev. 28, 20-47.
32. Satyamoorthy, K., Li, G., Vaidya, B., Patel, D., and Herlyn, M. (2001). Insulin-like growth factor-1 induces survival and growth of biologically early melanoma cells through both the mitogen-activated protein kinase and beta-catenin pathways. Cancer Res. 61, 7318-7324.
33. Sinnberg, T., Lasithiotakis, K., Niessner, H. et al. (2009). Inhibition of PI3K-AKT-mTOR signaling sensitizes melanoma cells to cisplatin and temozolomide. J. Invest. Dermatol. 129, 1500-1515.
34. Sinnberg, T., Menzel, M., Kaesler, S., Biedermann, T., Sauer, B., Nahnsen, S., Schwarz, M., Garbe, C., and Schittek, B. (2010). Suppression of casein kinase 1alpha in melanoma cells induces a switch in beta-catenin signaling to promote metastasis. Cancer Res. 70, 6999-7009.
35. Stahl, J.M., Sharma, A., Cheung, M., Zimmerman, M., Cheng, J.Q., Bosenberg, M.W., Kester, M., Sandirasegarane, L., and Robertson, G.P. (2004). Deregulated Akt3 activity promotes development of malignant melanoma. Cancer Res. 64, 7002-7010.
36. Straussman, R., Morikawa, T., Shee, K. et al. (2012). Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504.
37. Teng, D.H., Hu, R., Lin, H. et al. (1997). MMAC1/PTEN mutations in primary tumor specimens and tumor cell lines. Cancer Res. 57, 5221-5225.
38. Tsao, H., Zhang, X., Benoit, E., and Haluska, F.G. (1998). Identification of PTEN/MMAC1 alterations in uncultured melanomas and melanoma cell lines. Oncogene 16, 3397-3402.
39. Tsao, H., Zhang, X., Fowlkes, K., and Haluska, F.G. (2000). Relative reciprocity of NRAS and PTEN/MMAC1 alterations in cutaneous melanoma cell lines. Cancer Res. 60, 1800-1804.
40. Tsao, H., Goel, V., Wu, H., Yang, G., and Haluska, F.G. (2004). Genetic interaction between NRAS and BRAF mutations and PTEN/MMAC1 inactivation in melanoma. J. Invest. Dermatol. 122, 337-341.
41. Ucar, D.A., Kurenova, E., Garrett, T.J. et al. (2012). Disruption of the protein interaction between FAK and IGF-1R inhibits melanoma tumor growth. Cell Cycle 11, 3250-3259.
42. Villanueva, J., Vultur, A., Lee, J.T. et al. (2010). Acquired resistance to BRAF inhibitors mediated by a RAF kinase switch in melanoma can be overcome by cotargeting MEK and IGF-1R/PI3K. Cancer Cell 18, 683-695.
43. Villanueva, J., Vultur, A., and Herlyn, M. (2011). Resistance to BRAF inhibitors: unraveling mechanisms and future treatment options. Cancer Res. 71, 7137-7140.
44. Werner, H. (2012). Tumor suppressors govern insulin-like growth factor signaling pathways: implications in metabolism and cancer. Oncogene 31, 2703-2714.
45. Wilson, T.R., Fridlyand, J., Yan, Y. et al. (2012). Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509.
46. Yazdi, A.S., Palmedo, G., Flaig, M.J. et al. (2003). Mutations of the BRAF gene in benign and malignant melanocytic lesions. J. Invest. Dermatol. 121, 1160-1162.
47. Yeh, A.H., Bohula, E.A., and Macaulay, V.M. (2006). Human melanoma cells expressing V600E B-RAF are susceptible to IGF1R targeting by small interfering RNAs. Oncogene 25, 6574-6581.
48. Zhao, H., Dupont, J., Yakar, S., Karas, M., and LeRoith, D. (2004). PTEN inhibits cell proliferation and induces apoptosis by downregulating cell surface IGF-IR expression in prostate cancer cells. Oncogene 23, 786-794.