Derepression of the Her-2 uORF is mediated by a novel post-transcriptional control mechanism in cancer cells

Genes and Development

Volumn 20, Issue 8, 2006, Pages 939-953

  Mehta, Anuradha ^a   Trotta, Christopher R ^a   Peltz, Stuart W ^a  

^a PTC THERAPEUTICS   (United States)

Author keywords

5 and 3 UTRs; Her 2; uORF

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; MESSENGER RNA;

ARTICLE; BREAST CARCINOMA; CANCER CELL; CANCER GROWTH; CONTROLLED STUDY; DOWNSTREAM PROCESSING; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; RNA STABILITY; RNA TRANSLATION;

BASE SEQUENCE; CELL LINE, TUMOR; DNA PRIMERS; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, FLUORESCENCE; MUTAGENESIS; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RECEPTOR, ERBB-2; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER;

EID: 33645859909     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1388706     Document Type: Article

References (63)

1. Bae, C.D., Juhnn, Y.S., and Park, J.B. 2001. Post-transcriptional control of c-erb B-2 overexpression in stomach cancer cells. Exp. Mol. Med. 33: 15-19.
2. Brunner, J.E., Nguyen, J.H., Roehl, H.H., Ho, T.V., Swiderek, K.M., and Semler, B.L. 2005. Functional interaction of heterogeneous nuclear ribonucleoprotein C with poliovirus RNA synthesis initiation complexes. J. Virol. 79: 3254-3266.
3. Burd, C.G. and Dreyfuss, G. 1994. RNA binding specificity of hnRNP A1: Significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J. 13: 1197-1204.
4. Child, S.J., Miller, M.K., and Geballe, A.P. 1999a. Cell type-dependent and -independent control of HER-2/neu translation. Int. J. Biochem. Cell Biol. 31: 201-213.
5. _. 1999b. Translational control by an upstream open reading frame in the HER-2/neu transcript. J. Biol. Chem. 274: 24335-24341.
6. Cho, P.F., Poulin, F., Cho-Park, Y.A., Cho-Park, I.B., Chicoine, J.D., Lasko, P., and Sonenberg, N. 2005. A new paradigm for translational control: Inhibition via 5′-3′ mRNA tethering by Bicoid and the eIF4E cognate 4EHP. Cell 121: 411-423.
7. Choi, Y.D., Grabowski, P.J., Sharp, P.A., and Dreyfuss, G. 1986. Heterogeneous nuclear ribonucleoproteins: Role in RNA splicing. Science 231: 1534-1539.
8. Copeland, P.R. 2003. Regulation of gene expression by stop codon recoding: Selenocysteine. Gene 312: 17-25.
9. Czaplinski, K., Ruiz-Echevarria, M.J., Paushkin, S.V., Han, X., Weng, Y., Perlick, H.A., Dietz, H.C., Ter Avanesyan, M.D., and Peltz, S.W. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes & Dev. 12: 1665-1677.
10. de Moor, C.H., Meijer, H., and Lissenden, S. 2005. Mechanisms of translational control by the 3′ UTR in development and differentiation. Semin. Cell Dev. Biol. 16: 49-58.
11. Denkert, C., Weichert, W., Winzer, K.J., Muller, B.M., Noske, A., Niesporek, S., Kristiansen, G., Guski, H., Dietel, M., and Hauptmann, S. 2004. Expression of the ELAV-like protein HuR is associated with higher tumor grade and increased cyclooxygenase-2 expression in human breast carcinoma. Clin. Cancer Res. 10: 5580-5586.
12. Dixon, D.A., Tolley, N.D., King, P.H., Nabors, L.B., McIntyre, T.M., Zimmerman, G.A., and Prescott, S.M. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108: 1657-1665.
13. Doherty, J.K., Bond, C.T., Hua, W., Adelman, J.P., and Clinton, G.M. 1999. An alternative HER-2/neu transcript of 8 kb has an extended 3′ UTR and displays increased stability in SKOV-3 ovarian carcinoma cells. Gynecol. Oncol. 74: 408-415.
14. Espel, E. 2005. The role of the AU-rich elements of mRNAs in controlling translation. Semin. Cell Dev. Biol. 16: 59-67.
15. Good, P.J. 1997. The role of elav-like genes, a conserved family encoding RNA-binding proteins, in growth and development. Semin. Cell Dev. Biol. 8: 577-584.
16. Gorlach, M., Burd, C.G., and Dreyfuss, G. 1994. The determinants of RNA-binding specificity of the heterogeneous nuclear ribonucleoprotein C proteins. J. Biol. Chem. 269: 23074-23078.
17. Grskovic, M., Hentze, M.W., and Gebauer, F. 2003. A co-repressor assembly nucleated by Sex-lethal in the 3′ UTR mediates translational control of Drosophila msl-2 mRNA. EMBO J. 22: 5571-5581.
18. Hesketh, J. 2004. 3′-Untranslated regions are important in mRNA localization and translation: Lessons from selenium and metallothionein. Biochem. Soc. Trans. 32: 990-993.
19. Hinnebusch, A.G. (2000). Mechanism and regulation of initiator methionyl-tRNA binding to the ribosomes. In Translational control of gene expression (eds. N. Sonenberg et al.), pp. 185-243. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Holbro, T. and Hynes, N.E. 2004. ErbB receptors: Directing key signaling networks throughout life. Annu. Rev. Pharmacol. Toxicol. 44: 195-217.
21. Hollywood, D.P. and Hurst, H.C. 1993. A novel transcription factor, OB2-1, is required for overexpression of the protooncogene c-erbB-2 in mammary tumour lines. EMBO J. 12: 2369-2375.
22. Hornstein, E., Git, A., Braunstein, I., Avni, D., and Meyuhas, O. 1999. The expression of poly(A)-binding protein gene is translationally regulated in a growth-dependent fashion through a 5′-terminal oligopyrimidine tract motif. J. Biol. Chem. 274: 1708-1714.
23. Hoshino, S., Imai, M., Kobayashi, T., Uchida, N., and Katada, T. 1999. The eukaryotic polypeptide chain releasing factor (eRF3/GSPT) carrying the translation termination signal to the 3′-Poly(A) tail of mRNA. Direct association of erf3/ GSPT with polyadenylate-binding protein. J. Biol. Chem. 274: 16677-16680.
24. Hynes, N.E. and Lane, H.A. 2005. ERBB receptors and cancer: The complexity of targeted inhibitors. Nat. Rev. Cancer 5: 341-354.
25. Hynes, N.E. and Stern, D.F. 1994. The biology of erbB-2/neu/ HER-2 and its role in cancer. Biochim. Biophys. Acta 1198: 165-184.
26. Ishii, S., Imamoto, F., Yamanashi, Y., Toyoshima, K., and Yamamoto, T. 1987. Characterization of the promoter region of the human c-erbB-2 protooncogene. Proc. Natl. Acad. Sci. 84: 4374-4378.
27. Jordan, R.C., Macabeo-Ong, M., Shiboski, C.H., Dekker, N., Ginzinger, D.G., Wong, D.T., and Schmidt, B.L. 2004. Overexpression of matrix metalloproteinase-1 and -9 mRNA is associated with progression of oral dysplasia to cancer. Clin. Cancer Res. 10: 6460-6465.
28. Kahvejian, A., Roy, G., and Sonenberg, N. 2001. The mRNA closed-loop model: The function of PABP and PABP-interacting proteins in mRNA translation. Cold Spring Harb. Symp. Quant. Biol. 66: 293-300.
29. Kahvejian, A., Svitkin, Y.V., Sukarieh, R., M'Boutchou, M.N., and Sonenberg, N. 2005. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes & Dev. 19: 104-113.
30. Kozak, M. 1991a. Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266: 19867-19870.
31. _. 1991b. An analysis of vertebrate mRNA sequences: Intimations of translational control. J. Cell Biol. 115: 887-903.
32. Kraus, M.H., Popescu, N.C., Amsbaugh, S.C., and King, C.R. 1987. Overexpression of the EGF receptor-related proto-oncogene erbB-2 in human mammary tumor cell lines by different molecular mechanisms. EMBO J. 6: 605-610.
33. Kuersten, S. and Goodwin, E.B. 2003. The power of the 3′ UTR: Translational control and development. Nat. Rev. Genet. 4: 626-637.
34. Kuhn, U. and Wahle, E. 2004. Structure and function of poly(A) binding proteins. Biochim. Biophys. Acta 1678: 67-84.
35. Kuwada, S.K., Kuang, J., and Li, X. 2005. Integrin α5/β1 expression mediates HER-2 down-regulation in colon cancer cells. J. Biol. Chem. 280: 19027-19035.
36. Le, S.Y. and Maizel Jr., J.V. 1997. A common RNA structural motif involved in the internal initiation of translation of cellular mRNAs. Nucleic Acids Res. 25: 362-369.
37. Li, H., Park, S., Kilburn, B., Jelinek, M.A., Henschen-Edman, A., Aswad, D.W., Stallcup, M.R., and Laird-Offringa, I.A. 2002. Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J. Biol. Chem. 277: 44623-44630.
38. Lopez de Silanes, I., Zhan, M., Lal, A., Yang, X., and Gorospe, M. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. 101: 2987-2992.
39. Mangus, D.A., Evans, M.C., and Jacobson, A. 2003. Poly(A)-binding proteins: Multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol. 4: 223.
40. Mayrand, S.H., Dwen, P., and Pederson, T. 1993. Serine/threonine phosphorylation regulates binding of C hnRNP proteins to pre-mRNA. Proc. Natl. Acad. Sci. 90: 7764-7768.
41. Michael, W.M., Choi, M., and Dreyfuss, G. 1995. A nuclear export signal in hnRNP A1: A signal-mediated, temperaturedependent nuclear protein export pathway. Cell 83: 415-422.
42. Millard, S.S., Vidal, A., Markus, M., and Koff, A. 2000. A U-rich element in the 5′ untranslated region is necessary for the translation of p27 mRNA. Mol. Cell. Biol. 20: 5947-5959.
43. Morris, D.R. and Geballe, A.P. 2000. Upstream open reading frames as regulators of mRNA translation. Mol. Cell. Biol. 20: 8635-8642.
44. Muhlrad, D., Decker, C.J., and Parker, R. 1995. Turnover mechanisms of the stable yeast PGK1 mRNA. Mol. Cell. Biol. 15: 2145-2156.
45. Niranjanakumari, S., Lasda, E., Brazas, R., and Garcia-Blanco, M.A. 2002. Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26: 182-190.
46. Olayioye, M.A., Neve, R.M., Lane, H.A., and Hynes, N.E. 2000. The ErbB signaling network: Receptor heterodimerization in development and cancer. EMBO J. 19: 3159-3167.
47. Ostareck, D.H., Ostareck-Lederer, A., Wilm, M., Thiele, B.J., Mann, M., and Hentze, M.W. 1997. mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell 89: 597-606.
48. Pinol-Roma, S. and Dreyfuss, G. 1993. Cell cycle-regulated phosphorylation of the pre-mRNA-binding (heterogeneous nuclear ribonucleoprotein) C proteins. Mol. Cell. Biol. 13: 5762-5770.
49. Sachs, A.B. and Davis, R.W. 1989. The poly(A) binding protein is required for poly(A) shortening and 60S ribosomal subunitdependent translation initiation. Cell 58: 857-867.
50. Sella, O., Gerlitz, G., Le, S.Y., and Elroy-Stein, O. 1999. Differentiation-induced internal translation of c-sis mRNA: Analysis of the cis elements and their differentiation-linked binding to the hnRNP C protein. Mol. Cell. Biol. 19: 5429-5440.
51. Stansfield, I., Jones, K.M., Kushnirov, V.V., Dagkesamanskaya, A.R., Poznyakovski, A.I., Paushkin, S.V., Nierras, C.R., Cox, B.S., Ter Avanesyan, M.D., and Tuite, M.F. 1995a. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14: 4365-4373.
52. Stansfield, I., Jones, K.M., and Tuite, M.F. 1995b. The end in sight: Terminating translation in eukaryotes. Trends Biochem. Sci. 20: 489-491.
53. Swanson, M.S., Nakagawa, T.Y., LeVan, K., and Dreyfuss, G. 1987. Primary structure of human nuclear ribonucleoprotein particle C proteins: Conservation of sequence and domain structures in heterogeneous nuclear RNA, mRNA, and prerRNA-binding proteins. Mol. Cell. Biol. 7: 1731-1739.
54. Tal, M., King, C.R., Kraus, M.H., Ullrich, A., Schlessinger, J., and Givol, D. 1987. Human HER2 (neu) promoter: Evidence for multiple mechanisms for transcriptional initiation. Mol. Cell. Biol. 7: 2597-2601.
55. Tarun Jr., S.Z. and Sachs, A.B. 1996. Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J. 15: 7168-7177.
56. Tarun Jr., S.Z., Wells, S.E., Deardorff, J.A., and Sachs, A.B. 1997. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl. Acad. Sci. 94: 9046-9051.
57. Vernimmen, D., Gueders, M., Pisvin, S., Delvenne, P., and Winkler, R. 2003. Different mechanisms are implicated in ERBB2 gene overexpression in breast and in other cancers. Br. J. Cancer 89: 899-906.
58. Welch, E.M., Wong, W., and Peltz, S.W. (2000). Translation termination: It's not the end of the story. In Translational control of gene expression (eds. N. Sonenberg et al.), pp. 467-485. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
59. Wells, S.E., Hillner, P.E., Vale, R.D., and Sachs, A.B. 1998. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell 2: 135-140.
60. Wilkie, G.S., Dickson, K.S., and Gray, N.K. 2003. Regulation of mRNA translation by 5′- and 3′-UTR-binding factors. Trends Biochem. Sci. 28: 182-188.
61. Yaman, I., Fernandez, J., Sarkar, B., Schneider, R.J., Snider, M.D., Nagy, L.E., and Hatzoglou, M. 2002. Nutritional control of mRNA stability is mediated by a conserved AU-rich element that binds the cytoplasmic shuttling protein HuR. J. Biol. Chem. 277: 41539-41546.
62. Yarden, Y. and Sliwkowski, M.X. 2001. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2: 127-137.
63. Yohn, C.B., Cohen, A., Danon, A., and Mayfield, S.P. 1998. A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc. Natl. Acad. Sci. 95: 2238-2243.