Exon 2-mediated c-myc mRNA decay in vivo is independent of its translation

Molecular and Cellular Biology

Volumn 16, Issue 9, 1996, Pages 5107-5116

  Pistoi, S ^a   Roland, J ^b   Babinet, C ^a   Morello, D ^a,c  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBOSOME RNA;

ARTICLE; EXON; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; ONCOGENE C MYC; PRIORITY JOURNAL; REGULATOR GENE; RNA TRANSLATION; SEQUENCE HOMOLOGY; STEADY STATE; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION;

EID: 0029785083     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.9.5107     Document Type: Article

References (58)

1. Aharon, T., and R. J. Schneider. 1993. Selective destabilization of short-lived mRNAs with the granulocyte-macrophage colony-stimulating factor AU-rich 3′ noncoding region is mediated by a cotranslational mechanism. Mol. Cell. Biol. 13:1971-1980.
2. Auffray, C., and F. Rougeon. 1980. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur. J. Biochem. 107:901-907.
3. Bernstein, P. L., D. J. Herrick, R. D. Prokipcak, and J. Ross. 1992. Control of c-myc mRNA half-life in vitro by a protein capable of binding to a coding region stability determinant. Genes Dev. 6:642-654.
4. Boeck, R., and D. Kolakofsky. 1994. Positions +5 and +6 can be major determinants of the efficiency of non-AUG initiation codons for protein synthesis. EMBO J. 13:3608-3617.
5. Bossone, S. A., C. Asselin, A. J. Patel, and K. B. Marcu. 1992. MAZ, a zinc finger protein, binds to c-MYC and C2 gene sequences regulating transcriptional initiation and termination. Proc. Natl. Acad. Sci. USA 89:7452-7456.
6. Brinster, R. L., H. Y. Chen, M. E. Trumbauer, M. K. Yagle, and R. D. Palmiter. 1985. Factors affecting the efficiency of introducing DNA into mice by microinjecting eggs. Proc. Natl. Acad. Sci. USA 82:4438-4442.
7. Chen, C.-Y. A., and A.-B. Shyu. 1996. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 11:465-470.
8. Chen, C.-Y. A., N. Xu, and A.-B. Shyu. 1995. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15:5777-5788.
9. Cleveland, D. W. 1988. Autoregulated instability of tubulin mRNAs: a novel eukaryotic regulatory mechanism. Trends Biochem. Sci. 13:339-343.
10. Curatola, A. M., M. S. Nadal, and R. J. Schneider. 1995. Rapid degradation of AU-rich element (ARE) mRNAs is activated by ribosome transit and blocked by secondary structure at any position 5′ to the ARE. Mol. Cell. Biol. 15:6331-6340.
11. Drezen, J. M., M. Cohen-Tannoudji, S. Pournin, C. Babinet, and D. Morello. 1995. Developmental expression of H-2K major histocompatibility complex class I transgenes requires the presence of proximal introns. Dev. Dyn. 204:98-105.
12. Eick, D., M. Piechaczyk, B. Henglein, J. M. Blanchard, B. Traub, E. Kofler, S. Wiest, G. M. Lenoir, and G. W. Bornkamm. 1985. Aberrant c-myc RNA of Burkitt's lymphoma cells have longer half-lives. Oncogene 4:3717-3725.
13. Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
14. Gazin, C., S. Dupont de Dinechin, A. Hampe, J. M. Masson, P. Martin, D. Stéhélin, and F. Galibert. 1984. Nucleotide sequence of the human c-myc locus: provocative open reading frame within the first exon. EMBO J. 3:383-387.
15. Geballe, A. P., and D. R. Morris. 1994. Initiation codons within 5′-leaders of mRNAs as regulators of translation. Trends Biochem. Sci. 19:159-164.
16. Hann, S. R. 1995. Methionine deprivation regulates the translation of functionally-distinct c-myc proteins. Adv. Exp. Med. Biol. 375:107-116.
17. Hann, S. R., M. W. King, D. L. Bentley, C. W. Anderson, and R. N. Eisenman. 1988. A non-AUG translational initiation in c-myc exon 1 generates an N-terminally distinct protein whose synthesis is disrupted in Burkitt's lymphomas. Cell 52:185-195.
18. Herrick, D. J., and J. Ross. 1994. The half-life of c-myc mRNA in growing and serum-stimulated cells: influence of the coding and 3′ untranslated regions and role of ribosome translocation. Mol. Cell. Biol. 14:2119-2128.
19. Herschman, H. R. 1991. Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem. 60:281-319.
20. Hershey, J. W. 1991. Translational control in mammalian cells. Annu. Rev. Biochem. 60:717-755.
21. Hesketh, J., G. Campbell, M. Piechaczyk, and J.-M. Blanchard. 1994. Targeting of c-myc and β-globin coding sequences to cytoskeletal-bound polysomes by c-myc 3′ untranslated region. Biochem. J. 298:143-148.
22. Ishida, S., K. Shudo, S. Takada, and K. Koike. 1994. Transcription from the P2 promoter of human protooncogene myc is suppressed by retinoic acid through an interaction between the E2F element and its binding proteins. Cell Growth Differ. 5:287-294.
23. Jacobson, A., and S. Peltz. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem., in press.
24. Koeller, D. M., J. A. Horowitz, J. L. Casey, R. D. Klausner, and J. B. Harford. 1991. Translation and the stability of mRNAs encoding the transferrin receptor and c-fos. Proc. Natl. Acad. Sci. USA 88:7778-7782.
25. Kozak, M. 1981. An analysis of vertebrate mRNA sequences: intimations of translational control. J. Cell Biol. 115:887-903.
26. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
27. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
28. Lagnado, C. A., C. Y. Brown, and G. J. Goodall. 1994. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A). Mol. Cell. Biol. 14:7984-7995.
29. Laird-Offringa, I. A. 1992. What determines the instability of c-myc proto-oncogene mRNA? BioEssays 14:119-124.
30. Laird-Offringa, I. A., P. Elfferich, and A. J. van der Eb. 1991. Rapid c-myc mRNA degradation does not require (A + U)-rich sequences or complete translation of the mRNA. Nucleic Acids Res. 19:2387-2394.
31. Lavenu, A., S. Pistoi, S. Pournin, C. Babinet, and D. Morello. 1995. Both coding exons of the c-myc gene contribute to its posttranscriptional regulation in the quiescent and regenerating liver and after protein synthesis inhibition. Mol. Cell. Biol. 15:4410-4419.
32. Lavenu, A., S. Pournin, C. Babinet, and D. Morello. 1994. The cis-acting elements known to regulate c-myc expression ex vivo are not sufficient for correct transcription in vivo. Oncogene 9:527-536.
33. Lavenu, A., J. Roland, C. Poirier, P.-A. Cazenave, C. Babinet, and D. Morello. 1996. Genomic structure and precise mapping of a thymic regulatory region on mouse chromosome 17 revealed by a c-myc transgene insertion. Genomics 34:381-388.
34. Lindsten, T., C. H. June, and C. B. Thompson. 1988. Multiple mechanisms regulate c-myc gene expression during normal T cell activation. EMBO J. 7:2787-2794.
35. Linial, M., N. Gunderson, and M. Groudine. 1985. Enhanced transcription of c-myc in bursal lymphoma cells requires continuous protein synthesis. Science 230:1126-1132.
36. Makino, R., K. Hayashi, and T. Sugimura. 1984. c-myc transcript is induced in rat liver at a very early stage of regeneration or by cycloheximide treatment. Nature (London) 310:697-698.
37. Maquat, L. E. 1995. When cells stop making sense: effects of nonsense codons on mRNA metabolism in vertebrate cells. RNA 1:453-465.
38. Marcu, K. B., S. A. Bossone, and A. J. Patel. 1992. myc function and regulation. Annu. Rev. Biochem. 61:809-860.
39. Mitchell, R. L., L. Zokas, R. D. Schreiber, and I. M. Verma. 1985. Rapid induction of the expression of protooncogene fos during human monocytic differentiation. Cell 40:209-217.
40. Morello, D., C. Asselin, A. Lavenu, K. B. Marcu, and C. Babinet. 1989. Tissue-specific post-transcriptional regulation of c-myc expression in normal and H-2K/human c-myc transgenic mice. Oncogene 4:955-961.
41. Morello, D., M. J. Fitzgerald, C. Babinet, and N. Fausto. 1990. c-myc, c-fos, c-jun regulation in the regenerating livers of normal and H-2K/c-myc transgenic mice. Mol. Cell. Biol. 10:3185-3193.
42. Morello, D., A. Lavenu, and C. Babinet. 1990. Differential regulation and expression of jun, c-fos and c-myc proto-oncogenes during mouse liver regeneration and after inhibition of protein synthesis. Oncogene 5:1511-1519.
43. Morello, D., A. Lavenu, S. Pournin, and C. Babinet. 1993. The 5′ and 3′ non coding sequences of the c-myc gene, required in vitro for its post-transcriptional regulation, are dispensable in vivo. Oncogene 8:1921-1929.
44. Negishi, Y., Y. Nishita, Y. Saegusa, I. Kakizaki, I. Galli, F. Kihara, K. Tamai, N. Miyajima, A. S. Iguchi, and H. Ariga. 1994. Identification and cDNA cloning of single-stranded DNA binding proteins that interact with the region upstream of the human c-myc gene. Oncogene 9:1133-1143.
45. Pandey, N. B., A. S. Williams, J.-H. Sun, V. D. Brown, U. Bond, and W. F. Marzluff. 1994. Point mutations in the stem-loop at the 3′ end of mouse histone mRNA reduce expression by reducing the efficiency of 3′ and formation. Mol. Cell. Biol. 14:1709-1720.
46. Parkin, N., A. Darveau, R. Nicholson, and N. Sonenberg. 1988. cis-acting translational effects of the 5′ noncoding region of c-myc mRNA. Mol. Cell. Biol. 8:2875-2883.
47. Parkin, N. T., and N. Sonenberg. 1989. Identification of a protein that binds specifically to RNA from the first exon of c-myc. Oncogene 4:815-822.
48. Pellegrini, S., J. John, M. Shearer, I. M. Kerr, and G. R. Stark. 1989. Use of a selectable marker regulated by alpha interferon to obtain mutations in the signaling pathway. Mol. Cell. Biol. 9:4505-4612.
49. Ray, R., and D. M. Miller. 1991. Cloning and characterization of a human c-myc promoter-binding protein. Mol. Cell. Biol. 11:2154-2161.
50. Savant-Bhonsale, S., and D. W. Cleveland. 1992. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a >20S degradation complex. Genes Dev. 6:1927-1939.
51. Schiavi, S. C., J. G. Belasco, and M. E. Greenberg. 1992. Regulation of proto-oncogene mRNA stability. Biochim. Biophys. Acta 1114:95-106.
52. Schiavi, S. C., C. L. Wellington, A. B. Shyu, C. Y. Chen, M. E. Greenberg, and J. G. Belaseo. 1994. Multiple elements in the c-fos protein-coding region facilitate mRNA deadenylation and decay by a mechanism coupled to translation. J. Biol. Chem. 269:3441-3448.
53. Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659-667.
54. Sobczak, J., N. Mechtir, M.-F. Tournier, J. M. Blanchard, and M. Duguet. 1989. c-myc and c-fos gene regulation during mouse liver regeneration. Oncogene 4:1503-1508.
55. Tarun, S. Z., and A. B. Sachs. 1995. A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev. 9:2997-3007.
56. Winstall, E., M. Gamache, and V. Raymond. 1995. Rapid mRNA degradation mediated by the c-fos 3′ AU-rich element and that mediated by the granulocyte-macrophage colony-stimulating factor 3′ AU-rich element occur through similar polysome-associated mechanisms. Mol. Cell. Biol. 15:3796-3804.
57. Wisdom, R., and W. Lee. 1991. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev. 5:232-243.
58. Zajac-Kaye, M., and D. Levens. 1990. Phosphorylation-dependent binding of a 138-kDa myc intron factor to a regulatory element in the first intron of the c-myc gene. J. Biol. Chem. 265:4547-4551.