A Hypoxia-Controlled Cap-Dependent to Cap-Independent Translation Switch in Breast Cancer

Molecular Cell

Volumn 28, Issue 3, 2007, Pages 501-512

  Braunstein, Steve ^a   Karpisheva, Ksenia ^a   Pola, Carolina ^a   Goldberg, Judith ^a   Hochman, Tsivia ^a   Yee, Herman ^a   Cangiarella, Joan ^a   Arju, Rezina ^a   Formenti, Silvia C ^a   Schneider, Robert J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CELLCYCLE; RNA

Indexed keywords

INITIATION FACTOR 4E BINDING PROTEIN 1; INITIATION FACTOR 4G;

ADULT; AGED; ANGIOGENESIS; ARTICLE; BREAST CANCER; CAPPING PHENOMENON; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; INTERNAL RIBOSOME ENTRY SITE; PROTEIN EXPRESSION; RNA TRANSLATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; ANIMALS; BREAST NEOPLASMS; CELL HYPOXIA; CELL LINE, TUMOR; EUKARYOTIC INITIATION FACTOR-4G; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHOPROTEINS; PROTEIN BIOSYNTHESIS; RNA CAPS; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

ANIMALIA;

EID: 35649001888     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.10.019     Document Type: Article

References (35)

1. Avdulov S., Li S., Michalek V., Burrichter D., Peterson M., Perlman D.M., Manivel J.C., Sonenberg N., Yee D., Bitterman P.B., et al. Activation of translation complex eIF4F is essential for the genesis and maintenance of the malignant phenotype in human mammary epithelial cells. Cancer Cell 5 (2004) 553-563
2. Barbet N.C., Schneider U., Helliwell S.B., Stansfield I., Tuite M.F., and Hall M.N. TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7 (1996) 25-42
3. Bergers G., and Benjamin L.E. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3 (2003) 401-410
4. Brooks P.C., Montgomery A.M., Rosenfeld M., Reisfeld R.A., Hu T., Klier G., and Cheresh D.A. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79 (1994) 1157-1164
5. Castellvi J., Garcia A., Rojo F., Ruiz-Marcellan C., Gil A., Baselga J., and Ramon y Cajal S. Phosphorylated 4E binding protein 1: a hallmark of cell signaling that correlates with survival in ovarian cancer. Cancer 107 (2006) 1801-1811
6. Chung J., Yoon S., Datta K., Bachelder R.E., and Mercurio A.M. Hypoxia-induced vascular endothelial growth factor transcription and protection from apoptosis are dependent on alpha6beta1 integrin in breast carcinoma cells. Cancer Res. 64 (2004) 4711-4716
7. Connolly E., Braunstein S., Formenti S., and Schneider R.J. Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol. Cell. Biol. 26 (2006) 3955-3965
8. Del Bufalo D., Ciuffreda L., Trisciuoglio D., Desideri M., Cognetti F., Zupi G., and Milella M. Antiangiogenic potential of the Mammalian target of rapamycin inhibitor temsirolimus. Cancer Res. 66 (2006) 5549-5554
9. Gingras A.-C., Raught B., and Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68 (1999) 913-963
10. Guba M., von Breitenbuch P., Steinbauer M., Koehl G., Flegel S., Hornung M., Bruns C.J., Zuelke C., Farkas S., Anthuber M., et al. Rapamycin inhibits primary and metastatic tumor growth by antiangiogenesis: involvement of vascular endothelial growth factor. Nat. Med. 8 (2002) 128-135
11. Hangai M., Kitaya N., Xu J., Chan C.K., Kim J.J., Werb Z., Ryan S.J., and Brooks P.C. Matrix metalloproteinase-9-dependent exposure of a cryptic migratory control site in collagen is required before retinal angiogenesis. Am. J. Pathol. 161 (2002) 1429-1437
12. Hellen C.U., and Sarnow P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15 (2001) 1593-1612
13. Holcik M., and Sonenberg N. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 6 (2005) 318-327
14. Kaper F., Dornhoefer N., and Giaccia A.J. Mutations in the PI3K/PTEN/TSC2 pathway contribute to mammalian target of rapamycin activity and increased translation under hypoxic conditions. Cancer Res. 66 (2006) 1561-1569
15. Kononen J., Bubendorf L., Kallioniemi A., Barlund M., Schraml P., Leighton S., Torhorst J., Mihatsch M.J., Sauter G., and Kallioniemi O.P. Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat. Med. 4 (1998) 844-847
16. Kremer C.L., Klein R.R., Mendelson J., Browne W., Samadzedeh L.K., Vanpatten K., Highstrom L., Pestano G.A., and Nagle R.B. Expression of mTOR signaling pathway markers in prostate cancer progression. Prostate 66 (2006) 1203-1212
17. Lang K.J., Kappel A., and Goodall G.J. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol. Biol. Cell 13 (2002) 1792-1801
18. Lasfargues E.Y., Coutinho W.G., and Redfield E.S. Isolation of two human tumor epithelial cell lines from solid breast carcinomas. J. Natl. Cancer Inst. 61 (1978) 967-978
19. Lin E.Y., Li J.F., Gnatovskiy L., Deng Y., Zhu L., Grzesik D.A., Qian H., Xue X.N., and Pollard J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res. 66 (2006) 11238-11246
20. Martin M.E., Perez M.I., Redondo C., Alvarez M.I., Salinas M., and Fando J.L. 4E binding protein 1 expression is inversely correlated to the progression of gastrointestinal cancers. Int. J. Biochem. Cell Biol. 32 (2000) 633-642
21. Miller W.J., Kayton M.L., Patton A., O'Connor S., He M., Vu H., Baibakov G., Lorang D., Knezevic V., Kohn E., et al. A novel technique for quantifying changes in vascular density, endothelial cell proliferation and protein expression in response to modulators of angiogenesis using the chick chorioallantoic membrane (CAM) assay. J. Transl. Med. 2 (2004) 1-12
22. Petricoin III E.F., Espina V., Araujo R.P., Midura B., Yeung C., Wan X., Eichler G.S., Johann Jr. D.J., Qualman S., Tsokos M., et al. Phosphoprotein pathway mapping: Akt/mammalian target of rapamycin activation is negatively associated with childhood rhabdomyosarcoma survival. Cancer Res. 67 (2007) 3431-3440
23. Ray M.E., Yang Z.Q., Albertson D., Kleer C.G., Washburn J.G., Macoska J.A., and Ethier S.P. Genomic and expression analysis of the 8p11-12 amplicon in human breast cancer cell lines. Cancer Res. 64 (2004) 40-47
24. Rojo F., Najera L., Lirola J., Jimenez J., Guzman M., Sabadell M.D., Baselga J., and Ramon y Cajal S. 4E-binding protein 1, a cell signaling hallmark in breast cancer that correlates with pathologic grade and prognosis. Clin. Cancer Res. 13 (2007) 81-89
25. Ruvinsky I., Sharon N., Lerer T., Cohen H., Stolovich-Rain M., Nir T., Dor Y., Zisman P., and Meyuhas O. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19 (2005) 2199-2211
26. Sarbassov D.D., Ali S.M., Sengupta S., Sheen J.H., Hsu P.P., Bagley A.F., Markhard A.L., and Sabatini D.M. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22 (2006) 159-168
27. Schneider R.J., and Sonenberg N. Translational Control in Cancer Development and Progression. In: Mathews M.B., Sonenberg N., and Hershey J.W.B. (Eds). Translational Control in Biology and Medicine (2007), Cold Spring Harbor Press, Cold Spring Harbor 401-432
28. Sherrill K.W., Byrd M.P., Van Eden M.E., and Lloyd R.E. BCL-2 translation is mediated via internal ribosome entry during cell stress. J. Biol. Chem. 279 (2004) 29066-29074
29. Svitkin Y.V., Herdy B., Costa-Mattioli M., Gingras A.C., Raught B., and Sonenberg N. Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry site-mediated translation. Mol. Cell. Biol. 25 (2005) 10556-10565
30. Teleman A.A., Chen Y.W., and Cohen S.M. 4E-BP functions as a metabolic brake used under stress conditions but not during normal growth. Genes Dev. 19 (2005) 1844-1848
31. Thomas G.V., Tran C., Mellinghoff I.K., Welsbie D.S., Chan E., Fueger B., Czernin J., and Sawyers C.L. Hypoxia-inducible factor determines sensitivity to inhibitors of mTOR in kidney cancer. Nat. Med. 12 (2006) 122-127
32. Vinals F., Chambard J.C., and Pouyssegur J. p70 S6 kinase-mediated protein synthesis is a critical step for vascular endothelial cell proliferation. J. Biol. Chem. 274 (1999) 26776-26782
33. Wendel H.G., De Stanchina E., Fridman J.S., Malina A., Ray S., Kogan S., Cordon-Cardo C., Pelletier J., and Lowe S.W. Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature 428 (2004) 332-337
34. Yu K., Toral-Barza L., Discafani C., Zhang W.G., Skotnicki J., Frost P., and Gibbons J.J. mTOR, a novel target in breast cancer: the effect of CCI-779, an mTOR inhibitor, in preclinical models of breast cancer. Endocr. Relat. Cancer 8 (2001) 249-258
35. Zhou X., Tan M., Stone Hawthorne V., Klos K.S., Lan K.H., Yang Y., Yang W., Smith T.L., Shi D., and Yu D. Activation of the Akt/mammalian target of rapamycin/4E-BP1 pathway by ErbB2 overexpression predicts tumor progression in breast cancers. Clin. Cancer Res. 10 (2004) 6779-6788