Expression of a phosphorylated p130Cas substrate domain attenuates the phosphatidylinositol 3-kinase/Akt survival pathway in tamoxifen resistant breast cancer cells

Journal of Cellular Biochemistry

Volumn 107, Issue 2, 2009, Pages 364-375

  Soni, Shefali ^a   Lin, Bor Tyh ^a   August, Avery ^b   Nicholson, Robert I ^c   Kirsch, Kathrin H ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Apoptosis; Breast cancer; Decoy mechanism; P130Cas(BCAR1); Signal transduction; Tamoxifen resistance

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; CRK ASSOCIATED SUBSTRATE SRC HOMOLOGY DOMAIN FUSION PROTEIN; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN KINASE B; SMALL INTERFERING RNA; TAMOXIFEN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BCAR1 GENE; BREAST CANCER; CANCER RESISTANCE; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; DRUG SENSITIZATION; GENE EXPRESSION; HUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR GENE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CRK-ASSOCIATED SUBSTRATE PROTEIN; DRUG RESISTANCE, NEOPLASM; FEMALE; FLOW CYTOMETRY; HUMANS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION; TAMOXIFEN; TRANSFECTION;

EID: 66149098794     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22136     Document Type: Article

References (53)

1. Akagi T, Murata K, Shishido T, Hanafusa H. 2002. v-Crk activates the phosphoinositide 3-kinase/AKT pathway by utilizing focal adhesion kinase and H-Ras. Mol Cell Biol 22:7015-7023.
2. Alexandropoulos K, Baltimore D. 1996. Coordinate activation of c-Src by SH3- and SH2-binding sites on a novel p130Cas-related protein, Sin. Genes Dev 10:1341-1355. (Pubitemid 26260714)
3. Almeida EA, Ilic D, Han Q, Hauck CR, Jin F, Kawakatsu H, Schlaepfer DD, Damsky CH. 2000. Matrix survival signaling: From fibronectin via focal adhesion kinase to c-Jun NH(2) terminal kinase. J Cell Biol 149:741-754.
4. Barber MA, Welch HC. 2006. PI3K and RAC signalling in leukocyte and cancer cell migration. Bull Cancer 93:E44-E52.
5. Bhat-Nakshatri P, Campbell RA, Patel NM, Newton TR, King AJ, Marshall MS, Ali S, Nakshatri H. 2004. Tumour necrosis factor and PI3-kinase control oestrogen receptor alpha protein level and its transrepression function. Br J Cancer 90:853-859.
6. Bhat-Nakshatri P, Wang G, Appaiah H, Luktuke N, Carroll JS, Geistlinger TR, Brown M, Badve S, Liu Y, Nakshatri H. 2008. AKT alters genome-wide estrogen receptor alpha binding and impacts estrogen signaling in breast cancer. Mol Cell Biol 28:7487-7503.
7. Bouton AH, Riggins RB, Bruce-Staskal PJ. 2001. Functions of the adapter protein Cas: Signal convergence and the determination of cellular responses. Oncogene 20:6448-6458.
8. Brinkman A, van der Flier S, Kok EM, Dorssers LC. 2000. BCAR1, a human homologue of the adapter protein p130Cas, and antiestrogen resistance in breast cancer cells. J Natl Cancer Inst 92:112-120.
9. Burnham MR, Bruce-Staskal PJ, Harte MT, Weidow CL, Ma A, Weed SA, Bouton AH. 2000. Regulation of c-SRC activity and function by the adapter protein CAS. Mol Cell Biol 20:5865-5878.
10. Cabodi S, Moro L, Baj G, Smeriglio M, Di Stefano P, Gippone S, Surico N, Silengo L, Turco E, Tarone G, Defilippi P. 2004. p130Cas interacts with estrogen receptor alpha and modulates non-genomic estrogen signaling in breast cancer cells. J Cell Sci 117:1603-1611. (Pubitemid 38559834)
11. Cabodi S, Tinnirello A, Di Stefano P, Bisaro B, Ambrosino E, Castellano I, Sapino A, Arisio R, Cavallo F, Forni G, Glukhova M, Silengo L, Altruda F, Turco E, Tarone G, Defilippi P. 2006. p130Cas as a new regulator of mammary epithelial cell proliferation, survival, and HER2-neu oncogene-dependent breast tumorigenesis. Cancer Res 66:4672-4680.
12. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. 2001. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: A new model for anti-estrogen resistance. J Biol Chem 276:9817-9824.
13. Chan PC, Lai JF, Cheng CH, Tang MJ, Chiu CC, Chen HC. 1999. Suppression of ultraviolet irradiation-induced apoptosis by overexpression of focal adhesion kinase in Madin-Darby canine kidney cells. J Biol Chem 274:26901-26906.
14. Cho SY, Klemke RL. 2000. Extracellular-regulated kinase activation and CAS/Crk coupling regulate cell migration and suppress apoptosis during invasion of the extracellular matrix. J Cell Biol 149:223-236.
15. Couse JF, Korach KS. 1999. Reproductive phenotypes in the estrogen receptor-alpha knockout mouse. Ann Endocrinol (Paris) 60:143-148.
16. Cowell LN, Graham JD, Bouton AH, Clarke CL, O'Neill GM. 2006. Tamoxifen treatment promotes phosphorylation of the adhesion molecules, p130Cas/BCAR1, FAK and Src, via an adhesion-dependent pathway. Oncogene 25:7597-7607.
17. Gee JM, Robertson JF, Ellis IO, Nicholson RI. 2001. Phosphorylation of ERK1/2 mitogen-activated protein kinase is associated with poor response to anti-hormonal therapy and decreased patient survival in clinical breast cancer. Int J Cancer 95:247-254.
18. Group EBCCTsC. 1998. Tamoxifen for early breast cancer: An overview of the randomized trials. Lancet 351:1451-1468.
19. Guo S, Sonenshein GE. 2004. Forkhead box transcription factor FOXO3a regulates estrogen receptor alpha expression and is repressed by the Her-2/neu/phosphatidylinositol 3-kinase/Akt signaling pathway. Mol Cell Biol 24:8681-8690.
20. Guvakova MA, Surmacz E. 1999. The activated insulin-like growth factor I receptor induces depolarization in breast epithelial cells characterized by actin filament disassembly and tyrosine dephosphorylation of FAK, Cas, and paxillin. Exp Cell Res 251:244-255.
21. Henderson BE, Feigelson HS. 2000. Hormonal carcinogenesis. Carcinogenesis 21:427-433.
22. Henderson BE, Ross R, Bernstein L. 1988. Estrogens as a cause of human cancer: The Richard and Hinda Rosenthal Foundation award lecture. Cancer Res 48:246-253.
23. Hiscox S, Morgan L, Barrow D, Dutkowskil C, Wakeling A, Nicholson RI. 2004. Tamoxifen resistance in breast cancer cells is accompanied by an enhanced motile and invasive phenotype: Inhibition by gefitinib ('Iressa', ZD1839). Clin Exp Metastasis 21:201-212.
24. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R, Barrow D, Nicholson RI. 2006a. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. Int J Cancer 118:290-301.
25. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. 2006b. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat 97:263-274.
26. Huang J, Hamasaki H, Nakamoto T, Honda H, Hirai H, Saito M, Takato T, Sakai R. 2002. Differential regulation of cell migration, actin stress fiber organization, and cell transformation by functional domains of Crk-associated substrate. J Biol Chem 277:27265-27272.
27. Jordan NJ, Gee JM, Barrow D, Wakeling AE, Nicholson RI. 2004. Increased constitutive activity of PKB/Akt in tamoxifen resistant breast cancer MCF-7 cells. Breast Cancer Res Treat 87:167-180.
28. Kirsch KH, Georgescu MM, Hanafusa H. 1998. Direct binding of p130(Cas) to the guanine nucleotide exchange factor C3G. J Biol Chem 273:25673-25679.
29. Kirsch K, Kensinger M, Hanafusa H, August A. 2002. A p130Cas tyrosine phosphorylated substrate domain decoy disrupts v-crk signaling. BMC Cell Biol 3:18.
30. Klemke RL, Leng J, Molander R, Brooks PC, Vuori K, Cheresh DA. 1998. CAS/Crk coupling serves as a "molecular switch" for induction of cell migration. J Cell Biol 140:961-972.
31. Kmiecik TE, Shalloway D. 1987. Activation and suppression of pp60c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49:65-73.
32. Knowlden JM, Hutcheson IR, Jones HE, Madden T, Gee JM, Harper ME, Barrow D, Wakeling AE, Nicholson RI. 2003. Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144:1032-1044.
33. Lamorte L, Royal I, Naujokas M, Park M. 2002. Crk adapter proteins promote an epithelial-mesenchymal-like transition and are required for HGF-mediated cell spreading and breakdown of epithelial adherens junctions. Mol Biol Cell 13:1449-1461.
34. Lavinsky RM, Jepsen K, Heinzel T, Torchia J, Mullen TM, Schiff R, Del-Rio AL, Ricote M, Ngo S, Gemsch J, Hilsenbeck SG, Osborne CK, Glass CK, Rosenfeld MG, Rose DW. 1998. Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc Natl Acad Sci U S A 95:2920-2925.
35. Law SF, Zhang YZ, Klein-Szanto AJ, Golemis EA. 1998. Cell cycle-regulated processing of HEF1 to multiple protein forms differentially targeted to multiple subcellular compartments. Mol Cell Biol 18:3540-3551.
36. Min C, Kirsch KH, Zhao Y, Jeay S, Palamakumbura AH, Trackman PC, Sonenshein GE. 2007. The tumor suppressor activity of the lysyl oxidase propeptide reverses the invasive phenotype of Her-2/neu-driven breast cancer. Cancer Res 67:1105-1112.
37. Nicholson RI, Hutcheson IR, Britton D, Knowlden JM, Jones HE, Harper ME, Hiscox SE, Barrow D, Gee JM. 2005. Growth factor signalling networks in breast cancer and resistance to endocrine agents: New therapeutic strategies. J Steroid Biochem Mol Biol 93:257-262.
38. Nollau P, Mayer BJ. 2001. Profiling the global tyrosine phosphorylation state by Src homology 2 domain binding. Proc Natl Acad Sci U S A 98:13531-13536.
39. O'Lone R, Frith MC, Karlsson EK, Hansen U. 2004. Genomic targets of nuclear estrogen receptors. Mol Endocrinol 18:1859-1875.
40. Piwnica-Worms H, Saunders KB, Roberts TM, Smith AE, Cheng SH. 1987. Tyrosine phosphorylation regulates the biochemical and biological properties of pp60c-src. Cell 49:75-82.
41. Riggins RB, DeBerry RM, Toosarvandani MD, Bouton AH. 2003. Src-dependent association of Cas and p85 phosphatidylinositol 3′-kinase in v-crk-transformed cells. Mol Cancer Res 1:428-437.
42. Riggins RB, Thomas KS, Ta HQ, Wen J, Davis RJ, Schuh NR, Donelan SS, Owen KA, Gibson MA, Shupnik MA, Silva CM, Parsons SJ, Clarke R, Bouton AH. 2006. Physical and functional interactions between Cas and c-Src induce tamoxifen resistance of breast cancer cells through pathways involving epidermal growth factor receptor and signal transducer and activator of transcription 5b. Cancer Res 66:7007-7015.
43. Riggins RB, Lan JP, Klimach U, Zwart A, Cavalli LR, Haddad BR, Chen L, Gong T, Xuan J, Ethier SP, Clarke R. 2008. ERRgamma mediates tamoxifen resistance in novel models of invasive lobular breast cancer. Cancer Res 68:8908-8917.
44. Rodrigues GA, Falasca M, Zhang Z, Ong SH, Schlessinger J. 2000. A novel positive feedback loop mediated by the docking protein Gab1 and phosphatidylinositol 3-kinase in epidermal growth factor receptor signaling. Mol Cell Biol 20:1448-1459.
45. Scibelli A, d'Angelo D, Pelagalli A, Tafuri S, Avallone L, Della Morte R, Staiano N. 2003. Expression levels of the focal adhesion-associated proteins paxillin and p130CAS in canine and feline mammary tumors. Vet Res 34:193-202.
46. Shou J, Massarweh S, Osborne CK, Wakeling AE, Ali S, Weiss H, Schiff R. 2004. Mechanisms of tamoxifen resistance: Increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 96:926-935.
47. Smith IE, Dowsett M. 2003. Aromatase inhibitors in breast cancer. N Engl J Med 348:2431-2442.
48. Soltoff SP, Carraway KL 3rd, Prigent SA, Gullick WG, Cantley LC. 1994. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol Cell Biol 14:3550-3558.
49. van Agthoven T, Veldscholte J, Smid M, van Agthoven TL, Vreede L, Broertjes M, de Vries I, de Jong D, Sarwari R, Dorssers LC. 2009. Functional identification of genes causing estrogen independence of human breast cancer cells. Breast Cancer Res Treat 114:23-30.
50. van der Flier S, Brinkman A, Look MP, Kok EM, Meijer-van Gelder ME, Klijn JG, Dorssers LC, Foekens JA. 2000. Bcar1/p130Cas protein and primary breast cancer: Prognosis and response to tamoxifen treatment. J Natl Cancer Inst 92:120-127.
51. Wakeling AE, Newboult E, Peters SW. 1989. Effects of antioestrogens on the proliferation of MCF-7 human breast cancer cells. J Mol Endocrinol 2:225-234.
52. Watanabe T, Tsuda M, Makino Y, Ichihara S, Sawa H, Minami A, Mochizuki N, Nagashima K, Tanaka S. 2006. Adaptor molecule Crk is required for sustained phosphorylation of Grb2-associated binder 1 and hepatocyte growth factor-induced cell motility of human synovial sarcoma cell lines. Mol Cancer Res 4:499-510.
53. Weng LP, Wang X, Yu Q. 1999. Transmembrane tyrosine phosphatase LAR induces apoptosis by dephosphorylating and destabilizing p130Cas. Genes Cells 4:185-196.