The ShcA SH2 domain engages a 14-3-3/PI3′K signaling complex and promotes breast cancer cell survival

Oncogene

Volumn 31, Issue 48, 2012, Pages 5038-5044

  Ursini Siegel, J ^a   Hardy, W R ^b   Zheng, Y ^c   Ling, C ^d   Zuo, D ^d   Zhang, C ^c   Podmore, L ^a   Pawson, T ^c   Muller, W J ^d  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c MOUNT SINAI HOSPITAL   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

AKT; breast cancer; polyoma virus middle T; SH2 domain; ShcA; signal transduction

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN 14 3 3; PROTEIN 14 3 3 ZETA; PROTEIN KINASE B; PROTEIN P85; PROTEIN TYROSINE PHOSPHATASE SHP; SHCA PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER CELL CULTURE; CANCER SURVIVAL; CELL SURVIVAL; CONTROLLED STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

14-3-3 PROTEINS; ANIMALS; BREAST NEOPLASMS; CELL SURVIVAL; MICE; MICE, TRANSGENIC; PHOSPHATIDYLINOSITOL 3-KINASES; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS;

MUS MUSCULUS; POLYOMAVIRUS;

EID: 84870522893     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.4     Document Type: Article

References (45)

1. Frackelton Jr AR, Lu L, Davol PA, Bagdasaryan R, Hafer LJ, Sgroi DC. p66 Shc and tyrosine-phosphorylated Shc in primary breast tumors identify patients likely to relapse despite tamoxifen therapy. Breast Cancer Res 2006; 8: R73.
2. Davol PA, Bagdasaryan R, Elfenbein GJ, Maizel AL, Frackelton Jr AR. Shc proteins are strong, independent prognostic markers for both node-negative and node-positive primary breast cancer. Cancer Res 2003; 63: 6772-6783. (Pubitemid 37322958)
3. Ursini-Siegel J, Cory S, Zuo D, Hardy WR, Rexhepaj E, Lam S et al. Receptor tyrosine kinase signaling favors a protumorigenic state in breast cancer cells by inhibiting the adaptive immune response. Cancer Res 2010; 70: 7776-7787.
4. Ursini-Siegel J, Hardy WR, Zuo D, Lam SH, Sanguin-Gendreau V, Cardiff RD et al. ShcA signalling is essential for tumour progression in mouse models of human breast cancer. EMBO J 2008; 27: 910-920. (Pubitemid 351417168)
5. Alimandi M, Romano A, Curia MC, Muraro R, Fedi P, Aaronson SA et al. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 1995; 10: 1813-1821.
6. Batzer AG, Blaikie P, Nelson K, Schlessinger J, Margolis B. The phosphotyrosine interaction domain of Shc binds an LXNPXY motif on the epidermal growth factor receptor. Mol Cell Biol 1995; 15: 4403-4409.
7. Dankort DL, Wang Z, Blackmore V, Moran MF, Muller WJ. Distinct tyrosine autophosphorylation sites negatively and positively modulate neu-mediated transformation. Mol Cell Biol 1997; 17: 5410-5425. (Pubitemid 27357639)
8. Gillgrass A, Cardiff RD, Sharan N, Kannan S, Muller WJ. Epidermal growth factor receptor-dependent activation of Gab1 is involved in ErbB-2-mediated mammary tumor progression. Oncogene 2003; 22: 9151-9155. (Pubitemid 38067990)
9. Ishiguro Y, Iwashita T, Murakami H, Asai N, Iida K, Goto H et al. The role of amino acids surrounding tyrosine 1062 in ret in specific binding of the shc phosphotyrosine-binding domain. Endocrinology 1999; 140: 3992-3998. (Pubitemid 30647093)
10. Jones RA, Campbell CI, Wood GA, Petrik JJ, Moorehead RA. Reversibility and recurrence of IGF-IR-induced mammary tumors. Oncogene 2009; 28: 2152-2162.
11. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 1988; 54: 105-115.
12. Vijapurkar U, Cheng K, Koland JG. Mutation of a Shc binding site tyrosine residue in ErbB3/HER3 blocks heregulin-dependent activation of mitogen-activated protein kinase. J Biol Chem 1998; 273: 20996-21002. (Pubitemid 28385383)
13. Zhang Z, Kumar R, Santen RJ, Song RX. The role of adapter protein Shc in estrogen non-genomic action. Steroids 2004; 69: 523-529. (Pubitemid 39013482)
14. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992; 12: 954-961.
15. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol 2003; 163: 2113-2126. (Pubitemid 37310040)
16. Webster MA, Hutchinson JN, Rauh MJ, Muthuswamy SK, Anton M, Tortorice CG et al. Requirement for both Shc and phosphatidylinositol 30 kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol Cell Biol 1998; 18: 2344-2359. (Pubitemid 28152681)
17. Rauh MJ, Blackmore V, Andrechek ER, Tortorice CG, Daly R, Lai VK et al. Accelerated mammary tumor development in mutant polyomavirus middle T transgenic mice expressing elevated levels of either the Shc or Grb2 adapter protein. Mol Cell Biol 1999; 19: 8169-8179. (Pubitemid 30414011)
18. Hardy WR, Li L, Wang Z, Sedy J, Fawcett J, Frank E et al. Combinatorial ShcA docking interactions support diversity in tissue morphogenesis. Science 2007; 317: 251-256. (Pubitemid 47076202)
19. Barry EF, Felquer FA, Powell JA, Biggs L, Stomski FC, Urbani A et al. 14-3-3:Shc scaffolds integrate phosphoserine and phosphotyrosine signaling to regulate phosphatidylinositol 3-kinase activation and cell survival. J Biol Chem 2009; 284: 12080-12090.
20. Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W et al. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 1992; 360: 689-692. (Pubitemid 23007687)
21. van der Geer P, Wiley S, Gish GD, Pawson T. The Shc adaptor protein is highly phosphorylated at conserved, twin tyrosine residues (Y239/240) that mediate protein-protein interactions. Curr Biol 1996; 6: 1435-1444. (Pubitemid 27012242)
22. Ling C, Zuo D, Xue B, Muthuswamy S, Muller WJ. A novel role for 14-3-3sigma in regulating epithelial cell polarity. Genes Dev 2010; 24: 947-956.
23. Orlando FA, Brown KD. Unraveling breast cancer heterogeneity through transcriptomic and epigenomic analysis. Ann Surg Oncol 2009; 16: 2270-2279.
24. Su CH, Zhao R, Zhang F, Qu C, Chen B, Feng YH et al. 14-3-3sigma exerts tumorsuppressor activity mediated by regulation of COP1 stability. Cancer Res 2011; 71: 884-894.
25. Hodgson JG, Malek T, Bornstein S, Hariono S, Ginzinger DG, Muller WJ et al. Copy number aberrations in mouse breast tumors reveal loci and genes important in tumorigenic receptor tyrosine kinase signaling. Cancer Res 2005; 65: 9695-9704. (Pubitemid 41541445)
26. Neal CL, Xu J, Li P, Mori S, Yang J, Neal NN et al. Overexpression of 14-3-3zeta in cancer cells activates PI3K via binding the p85 regulatory subunit. Oncogene 2011.
27. Gotoh N, Tojo A, Shibuya M. A novel pathway from phosphorylation of tyrosine residues 239/240 of Shc, contributing to suppress apoptosis by IL-3. EMBO J 1996; 15: 6197-6204. (Pubitemid 26397892)
28. Patrussi L, Savino MT, Pellegrini M, Paccani SR, Migliaccio E, Plyte S et al. Cooperation and selectivity of the two Grb2 binding sites of p52Shc in T-cell antigen receptor signaling to Ras family GTPases and Myc-dependent survival. Oncogene 2005; 24: 2218-2228. (Pubitemid 40516588)
29. Gu H, Maeda H, Moon JJ, Lord JD, Yoakim M, Nelson BH et al. New role for Shc in activation of the phosphatidylinositol 3-kinase/Akt pathway. Mol Cell Biol 2000; 20: 7109-7120.
30. Bone H, Welham MJ. Shc associates with the IL-3 receptor beta subunit, SHIP and Gab2 following IL-3 stimulation. Contribution of Shc PTB and SH2 domains. Cell Signal 2000; 12: 183-194.
31. Campbell KS, Ogris E, Burke B, Su W, Auger KR, Druker BJ et al. Polyoma middle tumor antigen interacts with SHC protein via the NPTY (Asn-Pro-Thr-Tyr) motif in middle tumor antigen. Proc Natl Acad Sci USA 1994; 91: 6344-6348.
32. Cook RS, Garrett JT, Sanchez V, Stanford JC, Young C, Chakrabarty A et al. ErbB3 ablation impairs PI3K/Akt-dependent mammary tumorigenesis. Cancer Res 2011; 71: 3941-3951.
33. Morrison DK. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 2009; 19: 16-23.
34. Backer JM, Myers Jr MG, Shoelson SE, Chin DJ, Sun XJ, Miralpeix M et al. Phosphatidylinositol 30-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J 1992; 11: 3469-3479.
35. Zhou MM, Harlan JE, Wade WS, Crosby S, Ravichandran KS, Burakoff SJ et al. Binding affinities of tyrosine-phosphorylated peptides to the COOH-terminal SH2 and NH2-terminal phosphotyrosine binding domains of Shc. J Biol Chem 1995; 270: 31119-31123.
36. Telles E, Hosing AS, Kundu ST, Venkatraman P, Dalal SN. A novel pocket in 14-3- 3epsilon is required to mediate specific complex formation with cdc25C and to inhibit cell cycle progression upon activation of checkpoint pathways. Exp Cell Res 2009; 315: 1448-1457.
37. Wang B, Liu K, Lin FT, Lin WC. A role for 14-3-3 tau in E2F1 stabilization and DNA damage-induced apoptosis. J Biol Chem 2004; 279: 54140-54152. (Pubitemid 40053150)
38. Komiya Y, Kurabe N, Katagiri K, Ogawa M, Sugiyama A, Kawasaki Y et al. A novel binding factor of 14-3-3beta functions as a transcriptional repressor and promotes anchorage-independent growth, tumorigenicity, and metastasis. J Biol Chem 2008; 283: 18753-18764.
39. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, Shi B et al. 14-3-3zeta Cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell 2009; 16: 195-207.
40. Neal CL, Yao J, Yang W, Zhou X, Nguyen NT, Lu J et al. 14-3-3zeta overexpression defines high risk for breast cancer recurrence and promotes cancer cell survival. Cancer Res 2009; 69: 3425-3432.
41. George R, Schuller AC, Harris R, Ladbury JE. A phosphorylation-dependent gating mechanism controls the SH2 domain interactions of the Shc adaptor protein. J Mol Biol 2008; 377: 740-747.
42. Dankort D, Maslikowski B, Warner N, Kanno N, Kim H, Wang Z et al. Grb2 and Shc adapter proteins play distinct roles in Neu (ErbB-2)-induced mammary tumorigenesis: implications for human breast cancer. Mol Cell Biol 2001; 21: 1540-1551. (Pubitemid 32156374)
43. Dilworth SM, Griffin BE. Monoclonal antibodies against polyoma virus tumor antigens. Proc Natl Acad Sci USA 1982; 79: 1059-1063. (Pubitemid 12114064)
44. Ranger JJ, Levy DE, Shahalizadeh S, Hallett M, Muller WJ. Identification of a Stat3- dependent transcription regulatory network involved in metastatic progression. Cancer Res 2009; 69: 6823-6830.
45. Ursini-Siegel J, Rajput AB, Lu H, Sanguin-Gendreau V, Zuo D, Papavasiliou V et al. Elevated expression of DecR1 impairs ErbB2/Neu-induced mammary tumor development. Mol Cell Biol 2007; 27: 6361-6371. (Pubitemid 47435743)