Regulation of EGFR trafficking and cell signaling by Sprouty2 and MIG6 in lung cancer cells

Journal of Cell Science

Volumn 126, Issue 19, 2013, Pages 4339-4348

  Walsh, Alice M ^a   Lazzara, Matthew J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Endocytosis; Extracellular signal regulated kinase (ERK); Feedback; Recycling

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN INDUCIBLE GENE 6; REGULATOR PROTEIN; SPROUTY PROTEIN; SPROUTY2; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL DEATH; CELL MIGRATION; CONTROLLED STUDY; ENDOCYTOSIS; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG CANCER; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WILD TYPE;

ENDOCYTOSIS; EXTRACELLULAR SIGNAL-REGULATED KINASE (ERK); FEEDBACK; RECYCLING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE, TUMOR; ENDOCYTOSIS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUNG NEOPLASMS; MALE; MEMBRANE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84885462640     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.123208     Document Type: Article

References (60)

1. Adjei, A. A., Cohen, R. B., Franklin, W., Morris, C., Wilson, D., Molina, J. R., Hanson, L. J., Gore, L., Chow, L., Leong, S. et al. (2008). Phase I pharmacokinetic and pharmacodynamic study of the oral, small-molecule mitogen-activated protein kinase kinase 1/2 inhibitor AZD6244 (ARRY-142886) in patients with advanced cancers. J. Clin. Oncol. 26, 2139-2146.
2. Anastasi, S., Sala, G., Huiping, C., Caprini, E., Russo, G., Iacovelli, S., Lucini, F., Ingvarsson, S. and Segatto, O. (2005). Loss of RALT/MIG-6 expression in ERBB2-amplified breast carcinomas enhances ErbB-2 oncogenic potency and favors resistance to Herceptin. Oncogene 24, 4540-4548.
3. Avraham, R., and Yarden, Y. (2011). Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117.
4. Brandman, O., Ferrell, J. E., Jr, Li, R., and Meyer, T. (2005). Interlinked fast and slow positive feedback loops drive reliable cell decisions. Science 310, 496-498.
5. 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.
6. Chung, B. M., Raja, S. M., Clubb, R. J., Tu, C., George, M., Band, V., and Band, H. (2009). Aberrant trafficking of NSCLC-associated EGFR mutants through the endocytic recycling pathway promotes interaction with Src. BMC Cell Biol. 10, 84.
7. Edwin, F., Singh, R., Endersby, R., Baker, S. J., and Patel, T. B. (2006). The tumor suppressor PTEN is necessary for human Sprouty 2-mediated inhibition of cell proliferation. J. Biol. Chem. 281, 4816-4822.
8. Egan, J. E., Hall, A. B., Yatsula, B. A., and Bar-Sagi, D. (2002). The bimodal regulation of epidermal growth factor signaling by human Sprouty proteins. Proc. Natl. Acad. Sci. USA 99, 6041-6046.
9. Feng, Y. H., Tsao, C. J., Wu, C. L., Chang, J. G., Lu, P. J., Yeh, K. T., Shieh, G. S., Shiau, A. L., and Lee, J. C. (2010). Sprouty2 protein enhances the response to gefitinib through epidermal growth factor receptor in colon cancer cells. Cancer Sci. 101, 2033-2038.
10. Fiorini, M., Ballarò, C., Sala, G., Falcone, G., Alemà, S., and Segatto, O. (2002). Expression of RALT, a feedback inhibitor of ErbB receptors, is subjected to an integrated transcriptional and post-translational control. Oncogene 21, 6530-6539.
11. French, A. R., Tadaki, D. K., Niyogi, S. K., and Lauffenburger, D. A. (1995). Intracellular trafficking of epidermal growth factor family ligands is directly influenced by the pH sensitivity of the receptor/ligand interaction. J. Biol. Chem. 270, 4334-4340.
12. Frosi, Y., Anastasi, S., Ballarò , C., Varsano, G., Castellani, L., Maspero, E., Polo, S., Alemà, S., and Segatto, O. (2010). A two-tiered mechanism of EGFR inhibition by RALT/MIG6 via kinase suppression and receptor degradation. J. Cell Biol. 189, 557-571.
13. Furcht, C. M., Muñoz Rojas, A. R., Nihalani, D., and Lazzara, M. J. (2013). Diminished functional role and altered localization of SHP2 in non-small cell lung cancer cells with EGFR-activating mutations. Oncogene 32, 2346-2355, e1-e10.
14. Grassian, A. R., Schafer, Z. T., and Brugge, J. S. (2011). ErbB2 stabilizes epidermal growth factor receptor (EGFR) expression via Erk and Sprouty2 in extracellular matrix-detached cells. J. Biol. Chem. 286, 79-90.
15. Guo, A., Villén, J., Kornhauser, J., Lee, K. A., Stokes, M. P., Rikova, K., Possemato, A., Nardone, J., Innocenti, G., Wetzel, R. et al. (2008). Signaling networks assembled by oncogenic EGFR and c-Met. Proc. Natl. Acad. Sci. USA 105, 692-697.
16. Hackel, P. O., Gishizky, M., and Ullrich, A. (2001). Mig-6 is a negative regulator of the epidermal growth factor receptor signal. Biol. Chem. 382, 1649-1662.
17. Haglund, K., Schmidt, M. H., Wong, E. S., Guy, G. R., and Dikic, I. (2005). Sprouty2 acts at the Cbl/CIN85 interface to inhibit epidermal growth factor receptor downregulation. EMBO Rep. 6, 635-641.
18. Haura, E. B., Ricart, A. D., Larson, T. G., Stella, P. J., Bazhenova, L., Miller, V. A., Cohen, R. B., Eisenberg, P. D., Selaru, P., Wilner, K. D. et al. (2010). A phase II study of PD-0325901, an oral MEK inhibitor, in previously treated patients with advanced non-small cell lung cancer. Clin. Cancer Res. 16, 2450-2457.
19. Hendriks, B. S., Griffiths, G. J., Benson, R., Kenyon, D., Lazzara, M., Swinton, J., Beck, S., Hickinson, M., Beusmans, J. M., Lauffenburger, D. et al. (2006). Decreased internalisation of erbB1 mutants in lung cancer is linked with a mechanism conferring sensitivity to gefitinib. Syst. Biol. (Stevenage) 153, 457-466.
20. Hirsch, F. R., Varella-Garcia, M., Bunn, P. A., Jr, Di Maria, M. V., Veve, R., Bremmes, R. M., Barón, A. E., Zeng, C., and Franklin, W. A. (2003). Epidermal growth factor receptor in non-small-cell lung carcinomas: correlation between gene copy number and protein expression and impact on prognosis. J. Clin. Oncol. 21, 3798-3807.
21. Itakura, Y., Sasano, H., Shiga, C., Furukawa, Y., Shiga, K., Mori, S., and Nagura, H. (1994). Epidermal growth factor receptor overexpression in esophageal carcinoma. An immunohistochemical study correlated with clinicopathologic findings and DNA amplification. Cancer 74, 795-804.
22. Kholodenko, B. N., Hancock, J. F., and Kolch, W. (2010). Signalling ballet in space and time. Nat. Rev. Mol. Cell Biol. 11, 414-426.
23. Kim, H. J., Taylor, L. J., and Bar-Sagi, D. (2007). Spatial regulation of EGFR signaling by Sprouty2. Curr. Biol. 17, 455-461.
24. Kirchhausen, T., Macia, E., and Pelish, H. E. (2008). Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods Enzymol. 438, 77-93.
25. Kobayashi, S., Boggon, T. J., Dayaram, T., Jänne, P. A., Kocher, O., Meyerson, M., Johnson, B. E., Eck, M. J., Tenen, D. G., and Halmos, B. (2005). EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 352, 786-792.
26. Kosaka, T., Yatabe, Y., Endoh, H., Yoshida, K., Hida, T., Tsuboi, M., Tada, H., Kuwano, H., and Mitsudomi, T. (2006). Analysis of epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer and acquired resistance to gefitinib. Clin. Cancer Res. 12, 5764-5769.
27. Lao, D. H., Chandramouli, S., Yusoff, P., Fong, C. W., Saw, T. Y., Tai, L. P., Yu, C. Y., Leong, H. F., and Guy, G. R. (2006). A Src homology 3-binding sequence on the C terminus of Sprouty2 is necessary for inhibition of the Ras/ERK pathway downstream of fibroblast growth factor receptor stimulation. J. Biol. Chem. 281, 29993-30000.
28. Lazzara, M. J., Lane, K., Chan, R., Jasper, P. J., Yaffe, M. B., Sorger, P. K., Jacks, T., Neel, B. G., and Lauffenburger, D. A. (2010). Impaired SHP2-mediated extracellular signal-regulated kinase activation contributes to gefitinib sensitivity of lung cancer cells with epidermal growth factor receptor-activating mutations. Cancer Res. 70, 3843-3850.
29. Li, Z., Dong, Q., Wang, Y., Qu, L., Qiu, X., and Wang, E. (2012). Downregulation of Mig-6 in nonsmall-cell lung cancer is associated with EGFR signaling. Mol. Carcinog. 51, 522-534.
30. Lund, K. A., Opresko, L. K., Starbuck, C., Walsh, B. J., and Wiley, H. S. (1990). Quantitative analysis of the endocytic system involved in hormone-induced receptor internalization. J. Biol. Chem. 265, 15713-15723.
31. Lynch, T. J., Bell, D. W., Sordella, R., Gurubhagavatula, S., Okimoto, R. A., Brannigan, B. W., Harris, P. L., Haserlat, S. M., Supko, J. G., Haluska, F. G. et al. (2004). Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350, 2129-2139.
32. Ma, W., Trusina, A., El-Samad, H., Lim, W. A., and Tang, C. (2009). Defining network topologies that can achieve biochemical adaptation. Cell 138, 760-773.
33. Mellinghoff, I. K., Wang, M. Y., Vivanco, I., Haas-Kogan, D. A., Zhu, S., Dia, E. Q., Lu, K. V., Yoshimoto, K., Huang, J. H., Chute, D. J. et al. (2005). Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N. Engl. J. Med. 353, 2012-2024.
34. 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.
35. Mitsudomi, T., and Yatabe, Y. (2007). Mutations of the epidermal growth factor receptor gene and related genes as determinants of epidermal growth factor receptor tyrosine kinase inhibitors sensitivity in lung cancer. Cancer Sci. 98, 1817-1824.
36. Nagashima, T., Ushikoshi-Nakayama, R., Suenaga, A., Ide, K., Yumoto, N., Naruo, Y., Takahashi, K., Saeki, Y., Taiji, M., Tanaka, H. et al. (2009). Mutation of epidermal growth factor receptor is associated with MIG6 expression. FEBS J. 276, 5239-5251.
37. Noro, R., Gemma, A., Kosaihira, S., Kokubo, Y., Chen, M., Seike, M., Kataoka, K., Matsuda, K., Okano, T., Minegishi, Y. et al. (2006). Gefitinib (IRESSA) sensitive lung cancer cell lines show phosphorylation of Akt without ligand stimulation. BMC Cancer 6, 277.
38. Ozaki, K., Kadomoto, R., Asato, K., Tanimura, S., Itoh, N., and Kohno, M. (2001). ERK pathway positively regulates the expression of Sprouty genes. Biochem. Biophys. Res. Commun. 285, 1084-1088.
39. Padrón, D., Sato, M., Shay, J. W., Gazdar, A. F., Minna, J. D., and Roth, M. G. (2007). Epidermal growth factor receptors with tyrosine kinase domain mutations exhibit reduced Cbl association, poor ubiquitylation, and down-regulation but are efficiently internalized. Cancer Res. 67, 7695-7702.
40. Paez, J. G., Jänne, P. A., Lee, J. C., Tracy, S., Greulich, H., Gabriel, S., Herman, P., Kaye, F. J., Lindeman, N., Boggon, T. J. et al. (2004). EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304, 1497-1500.
41. Parachoniak, C. A., Luo, Y., Abella, J. V., Keen, J. H., and Park, M. (2011). GGA3 functions as a switch to promote Met receptor recycling, essential for sustained ERK and cell migration. Dev. Cell 20, 751-763.
42. Petrelli, A., Gilestro, G. F., Lanzardo, S., Comoglio, P. M., Migone, N., and Giordano, S. (2002). The endophilin-CIN85-Cbl complex mediates ligand-dependent downregulation of c-Met. Nature 416, 187-190.
43. Pratilas, C. A., Taylor, B. S., Ye, Q., Viale, A., Sander, C., Solit, D. B., and Rosen, N. (2009). (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proc. Natl. Acad. Sci. USA 106, 4519-4524.
44. 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.
45. Robertson, S. E., Setty, S. R., Sitaram, A., Marks, M. S., Lewis, R. E., and Chou, M. M. (2006). Extracellular signal-regulated kinase regulates clathrin-independent endosomal trafficking. Mol. Biol. Cell 17, 645-657.
46. Rubin, C., Litvak, V., Medvedovsky, H., Zwang, Y., Lev, S., and Yarden, Y. (2003). Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr. Biol. 13, 297-307.
47. Sheng, Q., and Liu, J. (2011). The therapeutic potential of targeting the EGFR family in epithelial ovarian cancer. Br. J. Cancer 104, 1241-1245.
48. Sigismund, S., Woelk, T., Puri, C., Maspero, E., Tacchetti, C., Transidico, P., Di Fiore, P. P., and Polo, S. (2005). Clathrin-independent endocytosis of ubiquitinated cargos. Proc. Natl. Acad. Sci. USA 102, 2760-2765.
49. Sigismund, S., Argenzio, E., Tosoni, D., Cavallaro, E., Polo, S., and Di Fiore, P. P. (2008). Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev. Cell 15, 209-219.
50. Swaminathan, G., and Tsygankov, A. Y. (2006). The Cbl family proteins: ring leaders in regulation of cell signaling. J. Cell. Physiol. 209, 21-43.
51. Tracy, S., Mukohara, T., Hansen, M., Meyerson, M., Johnson, B. E., and Jänne, P. A. (2004). Gefitinib induces apoptosis in the EGFRL858R non-small-cell lung cancer cell line H3255. Cancer Res. 64, 7241-7244.
52. Ventura, A., Meissner, A., Dillon, C. P., McManus, M., Sharp, P. A., Van Parijs, L., Jaenisch, R., and Jacks, T. (2004). Cre-lox-regulated conditional RNA interference from transgenes. Proc. Natl. Acad. Sci. USA 101, 10380-10385.
53. Vieira, A. V., Lamaze, C., and Schmid, S. L. (1996). Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 274, 2086-2089.
54. Wiley, H. S., and Cunningham, D. D. (1982). The endocytotic rate constant. A cellular parameter for quantitating receptor-mediated endocytosis. J. Biol. Chem. 257, 4222-4229.
55. Wong, E. S., Fong, C. W., Lim, J., Yusoff, P., Low, B. C., Langdon, W. Y., and Guy, G. R. (2002). Sprouty2 attenuates epidermal growth factor receptor ubiquitylation and endocytosis, and consequently enhances Ras/ERK signalling. EMBO J. 21, 4796-4808.
56. Ying, H., Zheng, H., Scott, K., Wiedemeyer, R., Yan, H., Lim, C., Huang, J., Dhakal, S., Ivanova, E., Xiao, Y. et al. (2010). Mig-6 controls EGFR trafficking and suppresses gliomagenesis. Proc. Natl. Acad. Sci. USA 107, 6912-6917.
57. Yusoff, P., Lao, D. H., Ong, S. H., Wong, E. S., Lim, J., Lo, T. L., Leong, H. F., Fong, C. W., and Guy, G. R. (2002). Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J. Biol. Chem. 277, 3195-3201.
58. Zhang, X., Gureasko, J., Shen, K., Cole, P. A., and Kuriyan, J. (2006). An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell 125, 1137-1149.
59. Zhang, X., Pickin, K. A., Bose, R., Jura, N., Cole, P. A., and Kuriyan, J. (2007). Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface. Nature 450, 741-744.
60. Zhang, Y. W., Staal, B., Su, Y., Swiatek, P., Zhao, P., Cao, B., Resau, J., Sigler, R., Bronson, R., and Vande Woude, G. F. (2007). Evidence that MIG-6 is a tumorsuppressor gene. Oncogene 26, 269-276.