Tumor suppressor p16INK4A inhibits cancer cell growth by downregulating eEF1A2 through a direct interaction

Journal of Cell Science

Volumn 126, Issue 8, 2013, Pages 1744-1752

  Lee, Mee Hyun ^a,b   Choi, Bu Young ^c   Cho, Yong Yeon ^a,d   Lee, Sung Young ^a,b   Huang, Zunnan ^a   Kundu, Joydeb Kumar ^b,f   Kim, Myoung Ok ^a,e   Kim, Dong Joon ^a,g   Bode, Ann M ^a   Surh, Young Joon ^b   Dong, Zigang ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Seoul National University   (South Korea)

^c C and C Research Laboratories   (South Korea)

^d The Catholic University of Korea   (South Korea)

^e Kyungpook National University   (South Korea)

^f GUANGDONG MEDICAL UNIVERSITY   (China)

^g Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Anti proliferative effects; eEF1A2; Ovarian cancer; p16INK4a; Translational activity

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; ELONGATION FACTOR; EUKARYOTIC ELONGATION FACTOR 1A2; UNCLASSIFIED DRUG;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RNA TRANSLATION; XENOPUS;

ANTI-PROLIFERATIVE EFFECTS; EEF1A2; OVARIAN CANCER; P16INK4A; TRANSLATIONAL ACTIVITY;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; CRICETULUS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; PEPTIDE ELONGATION FACTOR 1; PROTEIN BINDING; TWO-HYBRID SYSTEM TECHNIQUES; XENOPUS LAEVIS;

EID: 84877972047     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113613     Document Type: Article

References (48)

1. Amiri, A., Noei, F., Jeganathan, S., Kulkarni, G., Pinke, D. E. and Lee, J. M. (2007). eEF1A2 activates Akt and stimulates Akt-dependent actin remodeling, invasion and migration. Oncogene 26, 3027-3040.
2. Anand, N., Murthy, S., Amann, G., Wernick, M., Porter, L. A., Cukier, I. H., Collins, C., Gray, J. W., Diebold, J., Demetrick, D. J. et al. (2002). Protein elongation factor EEF1A2 is a putative oncogene in ovarian cancer. Nat. Genet. 31, 301-305.
3. Bilanges, B. and Stokoe, D. (2007). Mechanisms of translational deregulation in human tumors and therapeutic intervention strategies. Oncogene 26, 5973-5990.
4. Browne, G. J. and Proud, C. G. (2002). Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269, 5360-5368.
5. Caldas, C., Hahn, S. A., da Costa, L. T., Redston, M. S., Schutte, M., Seymour, A. B., Weinstein, C. L., Hruban, R. H., Yeo, C. J. and Kern, S. E. (1994). Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat. Genet. 8, 27-32.
6. Chen, R. and Weng, Z. (2003). A novel shape complementarity scoring function for protein-protein docking. Proteins 51, 397-408.
7. Chen, R., Li, L. and Weng, Z. (2003). ZDOCK: an initial-stage protein-docking algorithm. Proteins 52, 80-87.
8. Choi, B. Y., Choi, H. S., Ko, K., Cho, Y. Y., Zhu, F., Kang, B. S., Ermakova, S. P., Ma, W. Y., Bode, A. M. and Dong, Z. (2005). The tumor suppressor p16(INK4a) prevents cell transformation through inhibition of c-Jun phosphorylation and AP-1 activity. Nat. Struct. Mol. Biol. 12, 699-707.
9. Collins, I. and Garrett, M. D. (2005). Targeting the cell division cycle in cancer: CDK and cell cycle checkpoint kinase inhibitors. Curr. Opin. Pharmacol. 5, 366-373.
10. Ejiri, S. (2002). Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-associated nuclear localization. Biosci. Biotechnol. Biochem. 66, 1-21.
11. Evangelou, K., Bramis, J., Peros, I., Zacharatos, P., Dasiou-Plakida, D., Kalogeropoulos, N., Asimacopoulos, P. J., Kittas, C., Marinos, E. and Gorgoulis, V. G. (2004). Electron microscopy evidence that cytoplasmic localization of the p16(INK4A) "nuclear" cyclin-dependent kinase inhibitor (CKI) in tumor cells is specific and not an artifact. A study in non-small cell lung carcinomas. Biotech. Histochem. 79, 5-10.
12. Gali-Muhtasib, H. and Bakkar, N. (2002). Modulating cell cycle: current applications and prospects for future drug development. Curr. Cancer Drug Targets 2, 309-336.
13. Hartwell, L. H. and Kastan, M. B. (1994). Cell cycle control and cancer. Science 266, 1821-1828.
14. Hartwell, L., Weinert, T., Kadyk, L. and Garvik, B. (1994). Cell cycle checkpoints, genomic integrity, and cancer. Cold Spring Harb. Symp. Quant. Biol. 59, 259-263.
15. Humphrey, W., Dalke, A. and Schulten, K. (1996). VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38.
16. Joseph, P., O'Kernick, C. M., Othumpangat, S., Lei, Y. X., Yuan, B. Z. and Ong, T. M. (2004). Expression profile of eukaryotic translation factors in human cancer tissues and cell lines. Mol. Carcinog. 40, 171-179.
17. Kahns, S., Lund, A., Kristensen, P., Knudsen, C. R., Clark, B. F., Cavallius, J. and Merrick, W. C. (1998). The elongation factor 1 A-2 isoform from rabbit: cloning of the cDNA and characterization of the protein. Nucleic Acids Res. 26, 1884-1890.
18. Khalyfa, A., Bourbeau, D., Chen, E., Petroulakis, E., Pan, J., Xu, S. and Wang, E. (2001). Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2/S1 protein expression in normal and wasted mice. J. Biol. Chem. 276, 22915-22922.
19. Knudsen, S. M., Frydenberg, J., Clark, B. F. and Leffers, H. (1993). Tissuedependent variation in the expression of elongation factor-1 alpha isoforms: isolation and characterisation of a cDNA encoding a novel variant of human elongation-factor 1 alpha. Eur. J. Biochem. 215, 549-554.
20. Krimpenfort, P., Quon, K. C., Mooi, W. J., Loonstra, A. and Berns, A. (2001). Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413, 83-86.
21. Kulkarni, G., Turbin, D. A., Amiri, A., Jeganathan, S., Andrade-Navarro, M. A., Wu, T. D., Huntsman, D. G. and Lee, J. M. (2007). Expression of protein elongation factor eEF1A2 predicts favorable outcome in breast cancer. Breast Cancer Res. Treat. 102, 31-41.
22. Lee, M. H. and Surh, Y. J. (2009). eEF1A2 as a putative oncogene. Ann. N. Y. Acad. Sci. 1171, 87-93.
23. Lee, S., Francoeur, A. M., Liu, S. and Wang, E. (1992). Tissue-specific expression in mammalian brain, heart, and muscle of S1, a member of the elongation factor-1 alpha gene family. J. Biol. Chem. 267, 24064-24068.
24. Lee, S., Wolfraim, L. A. and Wang, E. (1993). Differential expression of S1 and elongation factor-1 alpha during rat development. J. Biol. Chem. 268, 24453-24459.
25. Lee, S., Ann, D. K. and Wang, E. (1994). Cloning of human and mouse brain cDNAs coding for S1, the second member of the mammalian elongation factor-1 alpha gene family: analysis of a possible evolutionary pathway. Biochem. Biophys. Res. Commun. 203, 1371-1377.
26. Lee, S., LeBlanc, A., Duttaroy, A. and Wang, E. (1995). Terminal differentiationdependent alteration in the expression of translation elongation factor-1 alpha and its sister gene, S1, in neurons. Exp. Cell Res. 219, 589-597.
27. Li, Z., Qi, C. F., Shin, D. M., Zingone, A., Newbery, H. J., Kovalchuk, A. L., Abbott, C. M. and Morse, H. C., 3rd (2010). Eef1a2 promotes cell growth, inhibits apoptosis and activates JAK/STAT and AKT signaling in mouse plasmacytomas. PLoS ONE 5, e10755.
28. Lund, A., Knudsen, S. M., Vissing, H., Clark, B. and Tommerup, N. (1996). Assignment of human elongation factor 1alpha genes: EEF1A maps to chromosome 6q14 and EEF1A2 to 20q13.3. Genomics 36, 359-361.
29. Marles, J. A., Dahesh, S., Haynes, J., Andrews, B. J. and Davidson, A. R. (2004). Protein-protein interaction affinity plays a crucial role in controlling the Sho1pmediated signal transduction pathway in yeast. Mol. Cell 14, 813-823.
30. Mintseris, J., Pierce, B., Wiehe, K., Anderson, R., Chen, R. and Weng, Z. (2007). Integrating statistical pair potentials into protein complex prediction. Proteins 69, 511-520.
31. Moldave, K. (1985). Eukaryotic protein synthesis. Annu. Rev. Biochem. 54, 1109-1149.
32. Panasyuk, G., Nemazanyy, I., Filonenko, V., Negrutskii, B. and El'skaya, A. V. (2008). A2 isoform of mammalian translation factor eEF1A displays increased tyrosine phosphorylation and ability to interact with different signalling molecules. Int. J. Biochem. Cell Biol. 40, 63-71.
33. Pardee, A. B. (1974). A restriction point for control of normal animal cell proliferation. Proc. Natl. Acad. Sci. USA 71, 1286-1290.
34. Pinke, D. E., Kalloger, S. E., Francetic, T., Huntsman, D. G. and Lee, J. M. (2008). The prognostic significance of elongation factor eEF1A2 in ovarian cancer. Gynecol. Oncol. 108, 561-568.
35. Richter, J. D., Wasserman, W. J. and Smith, L. D. (1982). The mechanism for increased protein synthesis during Xenopus oocyte maturation. Dev. Biol. 89, 159-167.
36. Ruas, M. and Peters, G. (1998). The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim. Biophys. Acta 1378, F115-F177.
37. Ruggero, D. and Pandolfi, P. P. (2003). Does the ribosome translate cancer? Nat. Rev. Cancer 3, 179-192.
38. Ruggero, D., Montanaro, L., Ma, L., Xu, W., Londei, P., Cordon-Cardo, C. and Pandolfi, P. P. (2004). The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat. Med. 10, 484-486.
39. Sanges, C., Scheuermann, C., Zahedi, R. P., Sickmann, A., Lamberti, A., Migliaccio, N., Baljuls, A., Marra, M., Zappavigna, S., Reinders, J. et al. (2012). Raf kinases mediate the phosphorylation of eukaryotic translation elongation factor 1A and regulate its stability in eukaryotic cells. Cell Death Dis. 3, e276.
40. Scaggiante, B., Dapas, B., Bonin, S., Grassi, M., Zennaro, C., Farra, R., Cristiano, L., Siracusano, S., Zanconati, F., Giansante, C. et al. (2012). Dissecting the expression of EEF1A1/2 genes in human prostate cancer cells: the potential of EEF1A2 as a hallmark for prostate transformation and progression. Br. J. Cancer 106, 166-173.
41. Serrano, M., Hannon, G. J. and Beach, D. (1993). A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 366, 704-707.
42. Sherr, C. J. (2001). Parsing Ink4a/Arf: ''pure'' p16-null mice. Cell 106, 531-534. Sherr, C. J. and Roberts, J. M. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
43. Sherr, C. J. and Roberts, J. M. (1999). CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
44. Soares, D. C., Barlow, P. N., Newbery, H. J., Porteous, D. J. and Abbott, C. M. (2009). Structural models of human eEF1A1 and eEF1A2 reveal two distinct surface clusters of sequence variation and potential differences in phosphorylation. PLoS ONE 4, e6315.
45. Sonenberg, N. and Hinnebusch, A. G. (2009). Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745.
46. Swanton, C. (2004). Cell-cycle targeted therapies. Lancet Oncol. 5, 27-36.
47. Tomlinson, V. A., Newbery, H. J., Wray, N. R., Jackson, J., Larionov, A., Miller, W. R., Dixon, J. M. and Abbott, C. M. (2005). Translation elongation factor eEF1A2 is a potential oncoprotein that is overexpressed in two-thirds of breast tumours. BMC Cancer 5, 113.
48. White-Gilbertson, S., Kurtz, D. T. and Voelkel-Johnson, C. (2009). The role of protein synthesis in cell cycling and cancer. Mol. Oncol. 3, 402-408.