Activation of phosphatidylinositol 3-kinase by membrane localization of p110α predisposes mammary glands to neoplastic transformation

Cancer Research

Volumn 68, Issue 23, 2008, Pages 9643-9653

  Renner, Oliver ^a   Blanco Aparicio, Carmen ^a   Grassow, Maja ^a   Cañamero, Marta ^a   Leal, Juan F M ^a   Carnero, Amancio ^a  

^a Centro Nacional de Investigations Oncológicas   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 4; ESTROGEN RECEPTOR ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P110; PROTEIN P110ALPHA; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER MODEL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE MUTATION; INVOLUTION; KNOCKOUT MOUSE; MALIGNANT TRANSFORMATION; MORPHOLOGY; MOUSE; MYRISTYLATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL LINE, TUMOR; CELL MEMBRANE; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN-DEPENDENT KINASE 4; ENZYME ACTIVATION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; MICE, TRANSGENIC; PHENOTYPE; PROMOTER REGIONS, GENETIC; RETINOBLASTOMA PROTEIN; TRANSGENES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 57149098047     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1539     Document Type: Article

References (49)

1. Vivanco I, Sawyers CL. The phosphatidylinositol 3-kinase AKT pathway in human cancer. Nat Rev Cancer 2002;2:489-501.
2. Parsons DW, Wang TL, Samuels Y, et al. Colorectal cancer: mutations in a signalling pathway. Nature 2005;436:792.
3. Blanco-Aparicio C, Renner O, Leal JF, Carnero A. PTEN, more than the AKT pathway. Carcinogenesis 2007;28:1379-86.
4. Samuels Y, Wang Z, Bardelli A, et al. High frequency of mutations of the PIK3CA gene in human cancers. Science 2004;304:554.
5. Freeman D, Lesche R, Kertesz N, et al. Genetic background controls tumor development in PTEN-deficient mice. Cancer Res 2006;66:6492-6.
6. Li Y, Podsypanina K, Liu X, et al. Deficiency of Pten accelerates mammary oncogenesis in MMTV-Wnt-1 transgenic mice. BMC Mol Biol 2001;2:2.
7. Li G, Robinson GW, Lesche R, et al. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development 2002;129:4159-70.
8. Ackler S, Ahmad S, Tobias C, Johnson MD, Glazer RI. Delayed mammary gland involution in MMTV-AKT1 transgenic mice. Oncogene 2002;21:198-206.
9. Hutchinson J, Jin J, Cardiff RD, Woodgett JR, Muller WJ. Activation of Akt (protein kinase B) in mammary epithelium provides a critical cell survival signal required for tumor progression. Mol Cell Biol 2001;21:2203-12.
10. Schwertfeger KL, Richert MM, Anderson SM. Mammary gland involution is delayed by activated Akt in transgenic mice. Mol Endocrinol 2001;15:867-81.
11. Blanco-Aparicio C, Perez-Gallego L, Pequeno B, Leal JF, Renner O, Carnero A. Mice expressing myrAKT1 in the mammary gland develop carcinogen-induced ER-positive mammary tumors that mimic human breast cancer. Carcinogenesis 2007;28:584-94.
12. Cross FR, Garber EA, Pellman D, Hanafusa H. A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Mol Cell Biol 1984;4:1834-42.
13. Klippel A, Reinhard C, Kavanaugh WM, Apell G, Escobedo MA, Williams LT. Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol Cell Biol 1996;16:4117-27.
14. Kang S, Bader AG, Vogt PK. Phosphatidylinositol 3-kinase mutations identified in human cancer are oncogenic. Proc Natl Acad Sci U S A 2005;102:802-7.
15. Zhang H, Liu G, Dziubinski M, Yang Z, Ethier SP, Wu G. Comprehensive analysis of oncogenic effects of PIK3CA mutations in human mammary epithelial cells. Breast Cancer Res Treat 2007;112:217-27.
16. Liu Z, Roberts TM. Human tumor mutants in the p110a subunit of PI3K. Cell Cycle 2006;5:675-7.
17. Zhao JJ, Liu Z, Wang L, Shin E, Loda MF, Roberts TM. The oncogenic properties of mutant p110α and p110β phosphatidylinositol 3-kinases in human mammary epithelial cells. Proc Natl Acad Sci U S A 2005;102:18443-8.
18. Bader AG, Kang S, Vogt PK. Cancer-specific mutations in PIK3CA are oncogenic in vivo. Proc Natl Acad Sci U S A 2006;103:1475-9.
19. Cardiff RD, Anver MR, Gusterson BA, et al. The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 2000;19:968-88.
20. Renner O, Fominaya J, Alonso S, Blanco-Aparicio C, Leal JF, Carnero A. Mst1, RanBP2, and eIF4G are new markers for in vivo PI3K activation in murine and human prostate. Carcinogenesis 2007;28:1418-25.
21. Allred DC, Brown P, Medina D. The origins of estrogen receptor α-positive and estrogen receptor α-negative human breast cancer. Breast Cancer Res 2004;6:240-5.
22. Sharpless NE, DePinho RA. Cancer: crime and punishment. Nature 2005;436:636-7.
23. Chen Z, Trotman LC, Shaffer D, et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 2005;436:725-30.
24. Kim JS, Lee C, Bonifant CL, Ressom H, Waldman T. Activation of p53-dependent growth suppression in human cells by mutations in PTEN or PIK3CA. Mol Cell Biol 2007;27:662-77.
25. Hallstrom TC, Mori S, Nevins JR. An E2F1-dependent gene expression program that determines the balance between proliferation and cell death. Cancer Cell 2008;13:11-22.
26. Sotillo R, Dubus P, Martin J, et al. Wide spectrum of tumors in knock-in mice carrying a Cdk4 protein insensitive to INK4 inhibitors. EMBO J 2001;20:6637-47.
27. Quereda V, Martinalbo J, Dubus P, Carnero A, Malumbres M. Genetic cooperation between p21Cip1 and INK4 inhibitors in cellular senescence and tumor suppression. Oncogene 2007;26:7665-74.
28. Weng L, Brown J, Eng C. PTEN induces apoptosis and cell cycle arrest through phosphoinositol-3-kinase/Akt-dependent and -independent pathways. Hum Mol Genet 2001;10:237-42.
29. Chang CJ, Freeman DJ, Wu H. PTEN regulates Mdm2 expression through the P1 promoter. J Biol Chem 2004;279:29841-8.
30. Freeman DJ, Li AG, Wei G, et al. PTEN tumor suppressor regulates p53 protein levels and activity through phosphatase-dependent and -independent mechanisms. Cancer Cell 2003;3:117-30.
31. Li AG, Piluso LG, Cai X, Wei G, Sellers WR, Liu X. Mechanistic insights into maintenance of high p53 acetylation by PTEN. Mol Cell 2006;23:575-87.
32. Gu J, Tamura M, Yamada KM. Tumor suppressor PTEN inhibits integrin- and growth factor-mediated mitogen-activated protein (MAP) kinase signaling pathways. J Cell Biol 1998;143:1375-83.
33. Tamura M, Gu J, Takino T, Yamada KM. Tumor suppressor PTEN inhibition of cell invasion, migration, and growth: differential involvement of focal adhesion kinase and p130Cas. Cancer Res 1999;59:442-9.
34. Lian Z, Di Cristofano A. Class reunion: PTEN joins the nuclear crew. Oncogene 2005;24:7394-400.
35. Gil A, Andres-Pons A, Pulido R. Nuclear PTEN: a tale of many tails. Cell Death Differ 2007;14:395-9.
36. Baker SJ. PTEN enters the nuclear age. Cell 2007;128:25-8.
37. Cardone MH, Roy N, Stennicke HR, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282:1318-21.
38. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997;91:231-41.
39. Toikkanen S. Primary squamous cell carcinoma of the breast. Cancer 1981;48:1629-32.
40. Colozza M, Azambuja E, Cardoso F, Sotiriou C, Larsimont D, Piccart MJ. Proliferative markers as prognostic and predictive tools in early breast cancer: where are we now? Ann Oncol 2005;16:1723-39.
41. Roy PG, Thompson AM. Cyclin D1 and breast cancer. Breast 2006;15:718-27.
42. Harari D, Yarden Y. Molecular mechanisms underlying ErbB2/HER2 action in breast cancer. Oncogene 2000;19:6102-14.
43. Liu W, Bagaitkar J, Watabe K. Roles of AKT signal in breast cancer. Front Biosci 2007;12:4011-9.
44. Dillon RL, White DE, Muller WJ. The phosphatidyl inositol 3-kinase signaling network: implications for human breast cancer. Oncogene 2007;26:1338-45.
45. Greenwald P. Clinical trials in cancer prevention: current results and perspectives for the future. J Nutr 2004;134:3507-12S.
46. Osborne CK. Steroid hormone receptors in breast cancer management. Breast Cancer Res Treat 1998;51:227-38.
47. Campbell IG, Russell SE, Choong DY, et al. Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res 2004;64:7678-81.
48. Stoica GE, Franke TF, Moroni M, et al. Effect of estradiol on estrogen receptor-α gene expression and activity can be modulated by the ErbB2/PI 3-K/Akt pathway. Oncogene 2003;22:7998-8011.
49. Perez-Tenorio G, Alkhori L, Olsson B, et al. PIK3CA mutations and PTEN loss correlate with similar prognostic factors and are not mutually exclusive in breast cancer. Clin Cancer Res 2007;13:3577-84.