Genetic and pharmacologic inhibition of eIF4E reduces breast cancer cell migration, invasion, and metastasis

Cancer Research

Volumn 75, Issue 6, 2015, Pages 1102-1112

  Pettersson, Filippa ^a   Del Rincon, Sonia V ^a   Emond, Audrey ^a   Huor, Bonnie ^a   Ngan, Elaine ^b   Ng, Jonathan ^a   Dobocan, Monica C ^a   Siegel, Peter M ^b   Miller, Wilson H ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; INITIATION FACTOR 4E; MESSENGER RNA; RIBAVIRIN; STROMELYSIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER INHIBITION; CELL INVASION; CLONOGENIC ASSAY; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG POTENCY; DRUG SAFETY; DRUG TOLERABILITY; ENZYME INHIBITION; FEMALE; GENE SILENCING; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; METASTASIS POTENTIAL; MIGRATION INHIBITION; MOUSE; MURINE MODEL; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT DURATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CELL MOTION; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; LUNG TUMOR; PATHOLOGY; PHYSIOLOGY; SECONDARY; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; EUKARYOTIC INITIATION FACTOR-4E; FEMALE; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; NEOPLASM INVASIVENESS; RIBAVIRIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 84937511731     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-1996     Document Type: Article

References (45)

1. Holm N, Byrnes K, Johnson L, Abreo F, Sehon K, Alley J, et al. A prospective trial on initiation factor 4E (eIF4E) overexpression and cancer recurrence in node-negative breast cancer. Ann Surg Oncol 2008;15:3207-15.
2. Graff JR, Konicek BW, Carter JH, Marcusson EG. Targeting the eukaryotic translation initiation factor 4E for cancer therapy. Cancer Res 2008;68:631-4.
3. Pettersson F, Yau C, Dobocan MC, Culjkovic-Kraljacic B, Retrouvay H, Puckett R, et al. Ribavirin treatment effects on breast cancers overexpressing eif4e, a biomarker with prognostic specificity for luminal B-type breast cancer. Clin Cancer Res 2011;17:2874-84.
4. Larsson O, Li S, Issaenko OA, Avdulov S, Peterson M, Smith K, et al. Eukaryotic translation initiation factor 4E-Induced progression of primary human mammary epithelial cells along the cancer pathway is associated with targeted translational deregulation of oncogenic drivers and inhibitors. Cancer Res 2007;67:6814-6824.
5. Avdulov S, Li S, Michalek V, Burrichter D, Peterson M, Perlman D, 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 2004;5:553-63.
6. Graff J, Boghaert E, De Benedetti A, Tudor D, Zimmer C, Chan S, et al. Reduction of translation initiation factor 4E decreases the malignancy of ras-transformed cloned rat embryo fibroblasts. Int J Cancer 1995;60:255-63.
7. Sonenberg N. eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochem Cell Biol 2008;86:178-83.
8. Dong K, Wang R, Wang X, Lin F, Shen JJ, Gao P, et al. Tumor-specific RNAi targeting eIF4E suppresses tumor growth, induces apoptosis and enhances cisplatin cytotoxicity in human breast carcinoma cells. Breast Cancer Res Treat 2009;113:443-56.
9. Soni A, Akcakanat A, Singh G, Luyimbazi D, Zheng Y, Kim D, et al. eIF4E knockdown decreases breast cancer cell growth without activating Akt signaling. Mol Cancer Ther 2008;7:1782-8.
10. Graff JR, Konicek BW, Vincent TM, Lynch RL, Monteith D, Weir SN, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest 2007;117:2638-48.
11. Byrnes K, White S, Chu Q, Meschonat C, Yu H, Johnson LW, et al. High eIF4E, VEGF, and microvessel density in stage I to III breast cancer. Ann Surg 2006;243:684-90; discussion 691-2.
12. Coleman LJ, Peter MB, Teall TJ, Brannan RA, Hanby AM, Honarpisheh H, et al. Combined analysis of eIF4E and 4E-binding protein expression predicts breast cancer survival and estimates eIF4E activity. Br J Cancer 2009;100:1393-9.
13. Nasr Z, Robert F, Porco JA Jr., Muller WJ, Pelletier J. eIF4F suppression in breast cancer affects maintenance and progression. Oncogene 2013;32:861-71.
14. Robichaud N, Del Rincon SV, Huor B, Alain T, Petruccelli LA, Hearnden J, et al. Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3. Oncogene. 2014 Jun 9. [Epub ahead of print].
15. Tester AM, Ruangpanit N, Anderson RL, Thompson EW. MMP-9 secretion and MMP-2 activation distinguish invasive and metastatic sublines of a mouse mammary carcinoma system showing epithelial-mesenchymal transition traits. Clin Exp Metastasis 2000;18:553-60.
16. Lochter A, Galosy S, Muschler J, Freedman N, Werb Z, Bissell MJ. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol 1997;139:1861-72.
17. Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005;436:123-7.
18. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-1428.
19. Katsuno Y, Lamouille S, Derynck R. TGF-beta signaling and epithelial-mesenchymal transition in cancer progression. Curr Opin Oncol 2013;25:76-84.
20. Wendt M, Tian M, Schiemann W. Deconstructing the mechanisms and consequences of TGF-β-induced EMT during cancer progression. Cell Tissue Res 2012;347:85-101.
21. Jian X, Samy L, RikD. TGF-β-induced epithelial to mesenchymal transition. Cell Res 2009;19:156-172.
22. Assouline S, Culjkovic B, Cocolakis E, Rousseau C, Beslu N, Amri A, et al. Molecular targeting of the oncogene eIF4E in AML: a proof-of-principle clinical trial with ribavirin. Blood 2009;114:257-60.
23. Kentsis A, Topisirovic I, Culjkovic B, Shao L, Borden KL. Ribavirin suppresses eIF4E-mediated oncogenic transformation by physical mimicry of the 7-methyl guanosine mRNA cap. Proc Natl Acad Sci U S A 2004;101:18105-10.
24. Volpon L, Osborne MJ, Zahreddine H, Romeo AA, Borden KL. Conformational changes induced in the eukaryotic translation initiation factor eIF4E by a clinically relevant inhibitor, ribavirin triphosphate. Biochem Biophys Res Commun 2013;434:614-9.
25. Tan K, Culjkovic B, Amri A, Borden KL. Ribavirin targets eIF4E dependent Akt survival signaling. Biochem Biophys Res Commun 2008;375:341-5.
26. Guy C, Cardiff R, Muller W. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
27. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992;52:1399-405.
28. Ngan E, Northey JJ, Brown CM, Ursini-Siegel J, Siegel PM. A complex containing LPP and alpha-actinin mediates TGFbeta-induced migration and invasion of ErbB2-expressing breast cancer cells. J Cell Sci 2013;126:1981-91.
29. Northey JJ, Chmielecki J, Ngan E, Russo C, Annis MG, Muller WJ, et al. Signaling through ShcA is required for transforming growth factor beta- and Neu/ErbB-2-induced breast cancer cell motility and invasion. Mol Cell Biol 2008;28:3162-76.
30. Konicek BW, Dumstorf CA, Graff JR. Targeting the eIF4F translation initiation complex for cancer therapy. Cell Cycle 2008;7:2466-71.
31. Miettinen PJ, Ebner R, Lopez AR, Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994;127:2021-36.
32. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001;12:27-36.
33. Muraoka RS, Dumont N, Ritter CA, Dugger TC, Brantley DM, Chen J, et al. Blockade of TGF-beta inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 2002;109:1551-9.
34. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, et al. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 2005;8:197-209.
35. Tester A, Ruangpanit N, Anderson R, Thompson E. MMP-9 secretion and MMP-2 activation distinguish invasive and metastatic sublines of a mouse mammary carcinoma system showing epithelial-mesenchymal transition traits. Clin Exp Metastasis 2000;18:553-560.
36. Borden KL, Culjkovic-Kraljacic B. Ribavirin as an anti-cancer therapy: acute myeloid leukemia and beyond? Leuk Lymphoma 2010;51:1805-15.
37. Sternlicht MD, Lochter A, Sympson CJ, Huey B, Rougier J-P, Gray JW, et al. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 1999;98:137-146.
38. Lochter A, Srebrow A, Sympson CJ, Terracio N, Werb Z, Bissell MJ. Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J Biol Chem 1997;272:5007-15.
39. Wiercinska E, Naber HP, Pardali E, van der Pluijm G, van Dam H, ten Dijke P, et al. The TGF-beta/Smad pathway induces breast cancer cell invasion through the up-regulation of matrix metalloproteinase 2 and 9 in a spheroid invasion model system. Breast Cancer Res Treat 2011;128:657-66.
40. Martin MD, Carter KJ, Jean-Philippe SR, Chang M, Mobashery S, Thiolloy S, et al. Effect of ablation or inhibition of stromal matrix metalloproteinase-9 on lung metastasis in a breast cancer model is dependent on genetic background. Cancer Res 2008;68:6251-9.
41. Nakasone Elizabeth S, Askautrud Hanne A, Kees T, Park J-H, Plaks V, Ewald Andrew J, et al. Imaging tumor-stroma interactions during chemotherapy reveals contributions of the microenvironment to resistance. Cancer Cell 2012;21:488-503.
42. Furic L, Rong L, Larsson O, Koumakpayi I, Yoshida K, Brueschke A, et al. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci U S A 2010;107:14134-9.
43. Ueda T, Sasaki M, Elia AJ, Chio II, Hamada K, Fukunaga R, et al. Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. Proc Natl Acad Sci U S A 2010;107:13984-90.
44. Konicek BW, Stephens JR, McNulty AM, Robichaud N, Peery RB, Dumstorf CA, et al. Therapeutic inhibition of MAP kinase interacting kinase blocks eukaryotic initiation factor 4E phosphorylation and suppresses outgrowth of experimental lung metastases. Cancer Res 2011;71:1849-57.
45. Grzmil M, Morin P Jr, Lino MM, Merlo A, Frank S, Wang Y, et al. MAP kinase-interacting kinase 1 regulates SMAD2-dependent TGF-beta signaling pathway in human glioblastoma. Cancer Res 2011;71:2392-402.