The adaptor proteins p66Shc and Grb2 regulate the activation of the GTPases ARF1 and ARF6 in invasive breast cancer cells

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5687-5703

  Haines, Eric ^a   Saucier, Caroline ^b   Claing, Audrey ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS; BASAL-LIKE BREAST CANCERS; BREAST CANCER CELLS; EPIDERMAL GROWTH FACTOR RECEPTORS; GROWTH FACTOR RECEPTORS; ISOFORMS; KEY REGULATORS; MDA-MB-231 CELLS;

CELL CULTURE; PROTEINS;

CELLS;

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PROTEIN P66 SHC; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME REGULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TUMOR INVASION;

ADAPTOR PROTEINS; ARF; BREAST CANCER; EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR); GTPASE;

ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; BREAST NEOPLASMS; CELL LINE, TUMOR; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; FEMALE; GRB2 ADAPTOR PROTEIN; HUMANS; NEOPLASM INVASIVENESS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 84896865710     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.516047     Document Type: Article

References (69)

1. Walker, R. A., and Dearing, S. J. (1999) Expression of epidermal growth factor receptor mRNA and protein in primary breast carcinomas. Breast Cancer Res. Treat. 53, 167-176 (Pubitemid 29161123)
2. Lo, H. W., Hsu, S. C., and Hung, M. C. (2006) EGFR signaling pathway in breast cancers. From traditional signal transduction to direct nuclear translocalization. Breast Cancer Res. Treat. 95, 211-218
3. Cohen, S., Fava, R. A., and Sawyer, S. T. (1982) Purification and characterization of epidermal growth factor receptor/protein kinase from normal mouse liver. Proc. Natl. Acad. Sci. U.S.A. 79, 6237-6241 (Pubitemid 13219841)
4. Cohen, S., and Taylor, J. M. (1974) Epidermal growth factor. Chemical and biological characterization. Recent Prog. Horm. Res. 30, 533-550
5. Haigler, H. T., McKanna, J. A., and Cohen, S. (1979) Direct visualization of the binding and internalization of a ferritin conjugate of epidermal growth factor in human carcinoma cells A-431. J. Cell Biol. 81, 382-395 (Pubitemid 9162943)
6. Schulze, W. X., Deng, L., and Mann, M. (2005) Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 1, 2005.0008
7. Kannan, S., De Santis, M., Lohmeyer, M., Riese, D. J., 2nd, Smith, G. H., Hynes, N., Seno, M., Brandt, R., Bianco, C., Persico, G., Kenney, N., Normanno, N., Martinez-Lacaci, I., Ciardiello, F., Stern, D. F., Gullick, W. J., and Salomon, D. S. (1997) Cripto enhances the tyrosine phosphorylation of Shc and activates mitogen-activated protein kinase (MAPK) in mammary epithelial cells. J. Biol. Chem. 272, 3330-3335
8. Rozakis-Adcock, M., Fernley, R., Wade, J., Pawson, T., and Bowtell, D. (1993) The SH2 and SH3 domains of mammalian Grb2 couple the EGF receptor to the Ras activator mSos1. Nature 363, 83-85 (Pubitemid 23144967)
9. Woodburn, J. R. (1999) The epidermal growth factor receptor and its inhibition in cancer therapy. Pharmacol. Ther. 82, 241-250
10. Sebolt-Leopold, J. S., and Herrera, R. (2004) Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat. Rev. Cancer 4, 937-947 (Pubitemid 39626217)
11. Ursini-Siegel, J., and Muller, W. J. (2008) The ShcA adaptor protein is a critical regulator of breast cancer progression. Cell Cycle 7, 1936-1943 (Pubitemid 352030337)
12. Pelicci, G., Dente, L., De Giuseppe, A., Verducci-Galletti, B., Giuli, S., Mele, S., Vetriani, C., Giorgio, M., Pandolfi, P. P., Cesareni, G., and Pelicci, P. G. (1996)Afamily of Shc related proteins with conserved PTB, CH1 and SH2 regions. Oncogene 13, 633-641 (Pubitemid 26283860)
13. Sakai, R., Henderson, J. T., O'Bryan, J. P., Elia, A. J., Saxton, T. M., and Pawson, T. (2000) The mammalian ShcB and ShcC phosphotyrosine docking proteins function in the maturation of sensory and sympathetic neurons. Neuron 28, 819-833 (Pubitemid 32038074)
14. Hawley, S. P., Wills, M. K., Rabalski, A. J., Bendall, A. J., and Jones, N. (2011) Expression patterns of ShcD and Shc family adaptor proteins during mouse embryonic development. Dev. Dyn. 240, 221-231
15. Jones, N., Hardy, W. R., Friese, M. B., Jorgensen, C., Smith, M. J., Woody, N. M., Burden, S. J., and Pawson, T. (2007) Analysis of a Shc family adaptor protein, ShcD/Shc4, that associates with muscle-specific kinase. Mol. Cell. Biol. 27, 4759-4773 (Pubitemid 47016129)
16. Migliaccio, E., Mele, S., Salcini, A. E., Pelicci, G., Lai, K. M., Superti-Furga, G., Pawson, T., Di Fiore, P. P., Lanfrancone, L., and Pelicci, P. G. (1997) Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J. 16, 706-716 (Pubitemid 27089518)
17. Pelicci, G., Lanfrancone, L., Grignani, F., McGlade, J., Cavallo, F., Forni, G., Nicoletti, I., Grignani, F., Pawson, T., and Pelicci, P. G. (1992) A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70, 93-104
18. Xi, G., Shen, X., and Clemmons, D. R. (2008) p66shc negatively regulates insulin-like growth factor I signal transduction via inhibition of p52shc binding to Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 leading to impaired growth factor receptor-bound protein-2 membrane recruitment. Mol. Endocrinol. 22, 2162-2175
19. Okada, S., Kao, A. W., Ceresa, B. P., Blaikie, P., Margolis, B., and Pessin, J. E. (1997) The 66-kDa Shc isoform is a negative regulator of the epidermal growth factor-stimulated mitogen-activated protein kinase pathway. J. Biol. Chem. 272, 28042-28049 (Pubitemid 27473612)
20. Dankort, D., Maslikowski, B., Warner, N., Kanno, N., Kim, H., Wang, Z., Moran, M. F., Oshima, R. G., Cardiff, R. D., and Muller, W. J. (2001) Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumorigenesis. Implications for human breast cancer. Mol. Cell. Biol. 21, 1540-1551 (Pubitemid 32156374)
21. Webster, M. A., Hutchinson, J. N., Rauh, M. J., Muthuswamy, S. K., Anton, M., Tortorice, C. G., Cardiff, R. D., Graham, F. L., Hassell, J. A., and Muller, W. J. (1998) Requirement for both Shc and phosphatidylinositol 3′ kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol. Cell. Biol. 18, 2344-2359 (Pubitemid 28152681)
22. Frackelton, A. R., Jr., Lu, L., Davol, P. A., Bagdasaryan, R., Hafer, L. J., and Sgroi, D. C. (2006) p66 Shc and tyrosine-phosphorylated Shc in primary breast tumors identify patients likely to relapse despite tamoxifen therapy. Breast Cancer Res. 8, R73
23. Davol, P. A., Bagdasaryan, R., Elfenbein, G. J., Maizel, A. L., and Frackelton, A. R., Jr. (2003) Shc proteins are strong, independent prognostic markers for both node-negative and node-positive primary breast cancer. Cancer Res. 63, 6772-6783 (Pubitemid 37322958)
24. Grossman, S. R., Lyle, S., Resnick, M. B., Sabo, E., Lis, R. T., Rosinha, E., Liu, Q., Hsieh, C. C., Bhat, G., Frackelton, A. R., Jr., and Hafer, L. J. (2007) p66 Shc tumor levels show a strong prognostic correlation with disease outcome in stage IIA colon cancer. Clin. Cancer Res. 13, 5798-5804 (Pubitemid 47583903)
25. Lee, M. S., Igawa, T., and Lin, M. F. (2004) Tyrosine-317 of p52(Shc) mediates androgen-stimulated proliferation signals in human prostate cancer cells. Oncogene 23, 3048-3058 (Pubitemid 38648195)
26. Jackson, J. G., Yoneda, T., Clark, G. M., and Yee, D. (2000) Elevated levels of p66 Shc are found in breast cancer cell lines and primary tumors with high metastatic potential. Clin. Cancer Res. 6, 1135-1139 (Pubitemid 30159377)
27. Veeramani, S., Igawa, T., Yuan, T. C., Lin, F. F., Lee, M. S., Lin, J. S., Johansson, S. L., and Lin, M. F. (2005) Expression of p66(Shc) protein correlates with proliferation of human prostate cancer cells. Oncogene 24, 7203-7212 (Pubitemid 41679282)
28. Hashimoto, S., Onodera, Y., Hashimoto, A., Tanaka, M., Hamaguchi, M., Yamada, A., and Sabe, H. (2004) Requirement for Arf6 in breast cancer invasive activities. Proc. Natl. Acad. Sci. U.S.A. 101, 6647-6652 (Pubitemid 38586028)
29. Boulay, P. L., Cotton, M., Melançon, P., and Claing, A. (2008) ADP-ribosylation factor 1 controls the activation of the phosphatidylinositol 3-kinase pathway to regulate epidermal growth factor-dependent growth and migration of breast cancer cells. J. Biol. Chem. 283, 36425-36434
30. D'Souza-Schorey, C., and Chavrier, P. (2006) ARF proteins. Roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358
31. Sabe, H., Hashimoto, S., Morishige, M., Hashimoto, A., and Ogawa, E. (2008) The EGFR-GEP100-Arf6 pathway in breast cancer. Full invasiveness is not from the inside. Cell Adh. Migr. 2, 71-73
32. Morishige, M., Hashimoto, S., Ogawa, E., Toda, Y., Kotani, H., Hirose, M., Wei, S., Hashimoto, A., Yamada, A., Yano, H., Mazaki, Y., Kodama, H., Nio, Y., Manabe, T., Wada, H., Kobayashi, H., and Sabe, H. (2008) GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 10, 85-92
33. Kisielow, M., Kleiner, S., Nagasawa, M., Faisal, A., and Nagamine, Y. (2002) Isoform-specific knockdown and expression of adaptor protein ShcA using small interfering RNA. Biochem. J. 363, 1-5 (Pubitemid 34280605)
34. Cotton, M., Boulay, P. L., Houndolo, T., Vitale, N., Pitcher, J. A., and Claing, A. (2007) Endogenous ARF6 interacts with Rac1 upon angiotensin II stimulation to regulate membrane ruffling and cell migration. Mol. Biol. Cell 18, 501-511 (Pubitemid 46213219)
35. q forms molecular complexes with ARNO and ARF6. Cell. Signal. 18, 1988-1994
36. Margolis, B., and Skolnik, E. Y. (1994) Activation of Ras by receptor tyrosine kinases. J. Am. Soc. Nephrol. 5, 1288-1299 (Pubitemid 24977112)
37. Ma, Z., Liu, Z., Wu, R. F., and Terada, L. S. (2010) p66(Shc) restrains Ras hyperactivation and suppresses metastatic behavior. Oncogene 29, 5559-5567
38. Debnath, J. (2010) p66(Shc) and Ras. Controlling anoikis from the insideout. Oncogene 29, 5556-5558
39. Kirmani, D., Bhat, H. F., Bashir, M., Zargar, M. A., and Khanday, F. A. (2013) P66Shc-rac1 pathway-mediated ROS production and cell migration is down-regulated by ascorbic acid. J. Recept. Signal Transduct. Res. 33, 107-113
40. Rajendran, M., Thomes, P., Zhang, L., Veeramani, S., and Lin, M. F. (2010) p66Shc-a longevity redox protein in human prostate cancer progression and metastasis. p66Shc in cancer progression and metastasis. Cancer Metastasis Rev. 29, 207-222
41. Elias, A. D. (2010) Triple-negative breast cancer. A short review. Am. J. Clin. Oncol. 33, 637-645
42. Cooke, T., Reeves, J., Lannigan, A., and Stanton, P. (2001) The value of the human epidermal growth factor receptor-2 (HER2) as a prognostic marker. Eur. J. Cancer 37, S3-10
43. Xie, Y., and Hung, M. C. (1996) p66Shc isoform down-regulated and not required for HER-2/neu signaling pathway in human breast cancer cell lines with HER-2/neu overexpression. Biochem. Biophys. Res. Commun. 221, 140-145
44. Beltrami, E., Valtorta, S., Moresco, R., Marcu, R., Belloli, S., Fassina, A., Fazio, F., Pelicci, P., and Giorgio, M. (2013) The p53-p66Shc apoptotic pathway is dispensable for tumor suppression whereas the p66Shc-generated oxidative stress initiates tumorigenesis. Curr. Pharm. Des. 19, 2708-2714
45. Veeramani, S., Chou, Y. W., Lin, F. C., Muniyan, S., Lin, F. F., Kumar, S., Xie, Y., Lele, S. M., Tu, Y., and Lin, M. F. (2012) Reactive oxygen species induced by p66Shc longevity protein mediate nongenomic androgen action via tyrosine phosphorylation signaling to enhance tumorigenicity of prostate cancer cells. Free Radic. Biol. Med. 53, 95-108
46. Giorgio, M., Migliaccio, E., Orsini, F., Paolucci, D., Moroni, M., Contursi, C., Pelliccia, G., Luzi, L., Minucci, S., Marcaccio, M., Pinton, P., Rizzuto, R., Bernardi, P., Paolucci, F., and Pelicci, P. G. (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122, 221-233 (Pubitemid 41032986)
47. Pacini, S., Pellegrini, M., Migliaccio, E., Patrussi, L., Ulivieri, C., Ventura, A., Carraro, F., Naldini, A., Lanfrancone, L., Pelicci, P., and Baldari, C. T. (2004) p66SHC promotes apoptosis and antagonizes mitogenic signaling in T cells. Mol. Cell. Biol. 24, 1747-1757 (Pubitemid 38167095)
48. Sakao, K., and Singh, S. V. (2012) D,L-Sulforaphane-induced apoptosis in human breast cancer cells is regulated by the adapter protein p66Shc. J. Cell. Biochem. 113, 599-610
49. Xiao, D., and Singh, S. V. (2010) p66Shc is indispensable for phenethyl isothiocyanate-induced apoptosis in human prostate cancer cells. Cancer Res. 70, 3150-3158
50. Lewis-Saravalli, S., Campbell, S., and Claing, A. (2013) ARF1 controls Rac1 signaling to regulate migration of MDA-MB-231 invasive breast cancer cells. Cell. Signal. 25, 1813-1819
51. Lowenstein, E. J., Daly, R. J., Batzer, A. G., Li, W., Margolis, B., Lammers, R., Ullrich, A., Skolnik, E. Y., Bar-Sagi, D., and Schlessinger, J. (1992) The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 70, 431-442
52. van der Geer, P., and Pawson, T. (1995) The PTB domain. A new protein module implicated in signal transduction. Trends Biochem. Sci. 20, 277-280
53. Borrello, M. G., Pelicci, G., Arighi, E., De Filippis, L., Greco, A., Bongarzone, I., Rizzetti, M., Pelicci, P. G., and Pierotti, M. A. (1994) The oncogenic versions of the Ret and Trk tyrosine kinases bind Shc and Grb2 adaptor proteins. Oncogene 9, 1661-1668 (Pubitemid 24163393)
54. Arany, I., Faisal, A., Nagamine, Y., and Safirstein, R. L. (2008) p66shc inhibits pro-survival epidermal growth factor receptor/ERK signaling during severe oxidative stress in mouse renal proximal tubule cells. J. Biol. Chem. 283, 6110-6117
55. Borkowska, A., Sielicka-Dudzin, A., Herman-Antosiewicz, A., Wozniak, M., Fedeli, D., Falcioni, G., and Antosiewicz, J. (2012) Diallyl trisulfide-induced prostate cancer cell death is associated with Akt/PKB dephosphorylation mediated by P-p66shc. Eur. J. Nutr. 51, 817-825
56. Xi, G., Shen, X., Radhakrishnan, Y., Maile, L., and Clemmons, D. (2010) Hyperglycemia-induced p66shc inhibits insulin-like growth factor I-dependent cell survival via impairment of Src kinase-mediated phosphoinositide-3 kinase/AKT activation in vascular smooth muscle cells. Endocrinology 151, 3611-3623
57. Verbeek, B. S., Adriaansen-Slot, S. S., Rijksen, G., and Vroom, T. M. (1997) Grb2 overexpression in nuclei and cytoplasm of human breast cells. A histochemical and biochemical study of normal and neoplastic mammary tissue specimens. J. Pathol. 183, 195-203 (Pubitemid 27436024)
58. Daly, R. J., Binder, M. D., and Sutherland, R. L. (1994) Overexpression of the Grb2 gene in human breast cancer cell lines. Oncogene 9, 2723-2727 (Pubitemid 24254050)
59. Suen, K. L., Bustelo, X. R., Pawson, T., and Barbacid, M. (1993) Molecular cloning of the mouse grb2 gene. Differential interaction of the Grb2 adaptor protein with epidermal growth factor and nerve growth factor receptors. Mol. Cell. Biol. 13, 5500-5512 (Pubitemid 23260653)
60. Gale, N. W., Kaplan, S., Lowenstein, E. J., Schlessinger, J., and Bar-Sagi, D. (1993) Grb2 mediates the EGF-dependent activation of guanine nucleotide exchange on Ras. Nature 363, 88-92 (Pubitemid 23144969)
61. Skolnik, E. Y., Batzer, A., Li, N., Lee, C. H., Lowenstein, E., Mohammadi, M., Margolis, B., and Schlessinger, J. (1993) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science 260, 1953-1955 (Pubitemid 23258278)
62. Cheng, A. M., Saxton, T. M., Sakai, R., Kulkarni, S., Mbamalu, G., Vogel, W., Tortorice, C. G., Cardiff, R. D., Cross, J. C., Muller, W. J., and Pawson, T. (1998) Mammalian Grb2 regulates multiple steps in embryonic development and malignant transformation. Cell 95, 793-803 (Pubitemid 29014459)
63. Menju, T., Hashimoto, S., Hashimoto, A., Otsuka, Y., Handa, H., Ogawa, E., Toda, Y., Wada, H., Date, H., and Sabe, H. (2011) Engagement of over-expressed Her2 with GEP100 induces autonomous invasive activities and provides a biomarker for metastases of lung adenocarcinoma. PLoS One 6, e25301
64. Batzer, A. G., Rotin, D., Ureña, J. M., Skolnik, E. Y., and Schlessinger, J. (1994) Hierarchy of binding sites for Grb2 and Shc on the epidermal growth factor receptor. Mol. Cell. Biol. 14, 5192-5201
65. Ono, M., and Kuwano, M. (2006) Molecular mechanisms of epidermal growth factor receptor (EGFR) activation and response to gefitinib and other EGFR-targeting drugs. Clin. Cancer Res. 12, 7242-7251 (Pubitemid 46095395)
66. Chardin, P., Camonis, J. H., Gale, N. W., van Aelst, L., Schlessinger, J., Wigler, M. H., and Bar-Sagi, D. (1993) Human Sos1. A guanine nucleotide exchange factor for Ras that binds to GRB2. Science 260, 1338-1343 (Pubitemid 23231980)
67. Li, N., Batzer, A., Daly, R., Yajnik, V., Skolnik, E., Chardin, P., Bar-Sagi, D., Margolis, B., and Schlessinger, J. (1993) Guanine-nucleotide- releasing factor hSos1 binds to Grb2 and links receptor tyrosine kinases to Ras signalling. Nature 363, 85-88 (Pubitemid 23144968)
68. Chen, R. H., Corbalan-Garcia, S., and Bar-Sagi, D. (1997) The role of the PH domain in the signal-dependent membrane targeting of Sos. EMBO J. 16, 1351-1359 (Pubitemid 27136100)
69. Bourguignon, L. Y., Zhu, H., Zhou, B., Diedrich, F., Singleton, P. A., and Hung, M. C. (2001) Hyaluronan promotes CD44v3-Vav2 interaction with Grb2-p185(HER2) and induces Rac1 and Ras signaling during ovarian tumor cell migration and growth. J. Biol. Chem. 276, 48679-48692