A conserved AU-rich element in the 3' untranslated region of bcl-2 mRNA is endowed with a destabilizing function that is involved in bcl-2 down- regulation during apoptosis

FASEB Journal

Volumn 14, Issue 1, 2000, Pages 174-184

  Schiavone, Nicola ^a   Rosini, Paolo ^a   Quattrone, Alessandro ^a,d   Donnini, Martino ^a   Lapucci, Andrea ^a   Citti, Lorenzo ^b   Bevilacqua, Anna ^c   Nicolin, Angelo ^c   Capaccioli, Sergio ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Bcl 2 regulation; Gene regulation; RNA decay; RNA half life

Indexed keywords

PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALIA; CAENORHABDITIS ELEGANS; CHORDATA;

EID: 0033957550     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.1.174     Document Type: Article

References (60)

1. Strasser, A., Huang, D. C., and Vaux, D. L. (1997) The role of the bcl-2/ced-9 gene family in cancer and general implications of defects in cell death control for tumourigenesis and resistance to chemotherapy. Biochim. Biophys. Acta 1333, F151-F178
2. Reed, J. C. (1997) Double identity for proteins of the Bcl-2 family. Nature (London) 387, 773-776
3. Ochiai, K., Kagami, M., Matsumura, R., and Tomioka, H. (1997) IL-5 but not interferon-gamma (IFN-gamma) inhibits eosinophil apoptosis by up-regulation of bcl-2 expression. Clin. Exp. Immunol. 107, 198-204
4. Teague, T. K., Marrack, P., Kappler, J. W., and Vella, A. T. (1997) IL-6 rescues resting mouse T cells from apoptosis. J. Immunol. 158, 5791-5796
5. Hernandez-Caselles, T., Martinez-Esparza, M., Sancho, D., Rubio, G., and Aparicio, P. (1995) Interleukin-7 rescues human activated T lymphocytes from apoptosis induced by glucocorticoesteroids and regulates bcl-2 and CD25 expression. Hum. Immunol. 43, 181-189
6. Jewell, A. P., Worman, C. P., Lydyard, P. M., Yong, K. L., Giles, F. J., and Goldstone, A. H. (1994) Interferon-alpha up-regulates bcl-2 expression and protects B-CLL cells from apoptosis in vitro and in vivo. Br. J. Haematol. 88, 268-274
7. Konig, A. (1997) Basic fibroblast growth factor (bFGF) upregulates the expression of bcl-2 in B cell chronic lymphocytic leukemia cell lines resulting in delaying apoptosis. Leukemia 11, 258-265
8. Genestier, L., Bonnefoy-Berard, N., Rouault, J. P., Flacher, M., and Revillard, J. P. (1995) Tumor necrosis factor-alpha up-regulates Bcl-2 expression and decreases calcium-dependent apoptosis in human B cell lines. Int. Immunol. 7, 533-540
9. Henderson, S., Rowe, M., Gregory, C., Croom-Carter, D., Wang, F., Longnecker, R., Kieff, E., and Rickinson, A. (1991) Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65, 1107-1115
10. Salomoni, P., Perrotti, D., Martinez, R., Franceschi, C., and Calabretta, B. (1997) Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc. Natl Acad. Sci. USA 94, 3296-3301
11. Fan, J., and Bertino, J. R. (1997) K-ras modulates the cell cycle via both positive and negative regulatory pathways. Oncogene 14, 2595-2607
12. Tangye, S. G., and Raison, R. L. (1997) Cytokines and cross-linking of sIgM augment PMA-induced activation of human leukaemic CD54+ B cells. Immunol. Cell Biol. 75, 127-135
13. Rinaudo, M. S., Su, K., Falk, L. A., Halder, S., and Mufson, R. A. (1995) Human interleukin-3 receptor modulates bcl-2 mRNA and protein levels through protein kinase C in TF-I cells. Blood 86, 80-88
14. Suzuki, A., Matsuzawa, A., and Iguchi, T. (1996) Down regulation of Bcl-2 is the first step on Fas-mediated apoptosis of male reproductive tract. Oncogene 13, 31-37
15. Miyashita, T., Krajewski, S., Krajewska, M., Wang, H.-G., Lin, H-K., Hoffman, B., Lieberman, D., and Reed, J.C. (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9, 1799-1805
16. Ziegler, A., Luedke, G. H., Fabbro, D., Altmann, K. H., Stahel, R. A., and Zangemeister-Wittke, U. J. (1997) Induction of apoptosis in small-cell lung cancer cells by an antisense oligodeoxynucleotide targeting the Bcl-2 coding sequence. J. Natl. Cancer Inst. 89, 1027-1036
17. Chen, M., Quintans, J., Fuks, Z., Thompson, C., Kufe, D. W., and Weichselbaum, R. R. (1995) Suppression of Bcl-2 messenger RNA production may mediate apoptosis after ionizing radiation, tumor necrosis factor alpha, and ceramide. Cancer Res. 55, 991-994
18. Young, R. L., and Korsmeyer, S. (1993) A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol. 13, 3686-3697
19. Miyashita, T., Harigai, M., Hanada, M., and Reed, J. (1994) Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res. 54, 3131-3135
20. Harigai, M., Miyashita, T., Hanada, M., and Reed, J. (1996) A cis-acting element in the BCL-2 gene controls expression through translational mechanisms. Oncogene 12, 1369-1374
21. Blagosklonny, M. V., Giannakakou, P., el-Deiry, W. S., Kingston, D. G., Higgs, P. I., Neckers, L., and Fojo, T. (1997) Raf-1/bcl-2 phosphorylation: a step from microtubule damage to cell death. Cancer Res. 57, 130-135
22. Haldar, S., Chintapalli, J., and Croce, C. M. (1996). Taxol induces bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res. 56, 1253-1255
23. Capaccioli, S., Quattrone, A., Schiavone, N., Calastretti, A., Copreni, E., Bevilacqua, A., Canti, G., Gong, L., Morelli, S., and Nicolin, A. (1996) A bcl-2/IgH antisense transcript deregulates bcl-2 gene expression in human follicular lymphoma t(14;18) cell lines. Oncogene 13, 105-115
24. Morelli, S., Delia, D., Capaccioli, S., Quattrone, A., Schiavone, N., Bevilacqua, A., Tomasini, S., and Nicolin, A. (1997) The antisense bcl-2-IgH transcript is an optimal target for synthetic oligonucleotides. Proc. Natl. Acad. Sci. USA 94, 8150-8155
25. Belasco, J., and Brawerman, G., eds (1993) Control of Messenger RNA Stability, Academic Press, San Diego, California
26. Chen C. Y. A., and Shyu, A. B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470
27. Shyu, A. B., Belasco, J. G., and Greenberg, M. E. (1991) Two distinct destabilizing elements in the c-fos message trigger the deadenylation as a first step in rapid mRNA decay. Genes Dev. 5, 221-231
28. Xu, N., Chen, C. Y. A., and Shyu, A. B. (1997) Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17, 4611-4621
29. Ross, J. (1995) mRNA stability in mammalian cells. Microbiol. Rev. 59, 423-450
30. Biamonti, G., and Riva, S. (1994) New insights into the auxiliary domains of eukaryotic RNA binding proteins. FEBS Lett. 340, 1-8
31. Nakamaki, T., Imamura, J., Brewer, G., Tsuruoka, N., and Koeffler, H. P. (1995) Characterization of adenosine-uridine-rich RNA binding factors. J. Cell. Physiol. 165, 484-492
32. Antic, D., and Keene, J. D. (1997) Insights from model systems - embryonic lethal abnormal visual RNA binding proteins involved in growth, differentiation and posttranscriptional gene expression. Am. J. Hum. Genet. 61, 273-278
33. Fan, X. C., and Steits, J. A. (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17, 3448-3460
34. Pemg, S. S.-Y., C.-Y. A., Chen, Xu, N., and Shyu A.-B. (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17, 3461-3470
35. Carballo, E., Lai, W. S., and Blackshear, P. J. (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281, 1001-1005
36. Meijlink, F., Curran, T., Miller, A. D., and Verma, I. M. (1985) Removal of a 67-base-pair sequence in the noncoding region of protooncogene fos converts it to a transforming gene. Proc. Natl. Acad. Sci. USA 82, 4987-4991
37. Aghib, D. F., Bishop, J. M., Ottolenghi, S., Guerrasio, A., Serra, A., and Saglio, G. (1990) A 3′ truncation of MYC caused by chromosomal translocation in a human T-cell leukemia increases mRNA stability. Oncagene 5, 707-711
38. Shyu, A. B., Greenberg, M. E., and Belasco, J. G. (1989) The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev. 3, 60-72
39. Seto, M., Ulrich, J., Hockett, R. D., Graninger, W., Bennett, S., Goldman, P., and Korsmeyer, S. J. (1988) Alternative promoters and exons, somatic mutation and deregulation of the Bcl-2-Ig fusion gene in lymphoma. EMBO J. 7, 123-131
40. Lagnado, C. A., Brown, G. Y., and Goodall, G. J. (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
41. Quattrone, A., Papucci, L., Santini, V., Schiavone, N., Noferini, D., Calastretti, A., Copreni, E., Morelli, S., Rossi Ferrini, P. L., Nicolin, A., and Capaccioli, S. (1995) Quantitation of bcl-2 oncogene in cultured lymphoma/leukemia cell lines and in primary leukemia B-cells by a highly sensitive RT-PCR method. Haematologica 80, 495-504
42. Zubiaga, A. M., Belasco, J. G., and Greenberg, M. E. (1995) The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15, 2219-2230
43. Hengartner, M. O., and Horvitz, H. R. (1994) C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 6, 665-676
44. Asson-Batres, M. A., Spurgeon, S. L., Diaz, J., DeLoughery, T. G., and Bagby, G. C., Jr. (1994) Evolutionary conservation of the AU-rich 3′ untranslated region of messenger RNA. Proc. Natl. Acad. Sci. USA 91, 1318-1322
45. Caput, D., Beutler, B., Hartog, K., Thayer, R., Brown-Shimer, S., and Cerami, A. (1986) Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA 83, 1670-1674
46. Zaidi, S. H., and Malter, J. S. (1994) Amyloid precursor protein mRNA stability is controlled by a 29-base element in the 3′-untranslated region. J. Biol. Chem. 269, 24007-24013
47. Iwai, Y., Bickel, M., Pluznik, D. H., and Cohen, R. B. (1991) Identification of sequences within the murine granulocyte-macrophage colony-stimulating factor mRNA 3′-untranslated region that mediate mRNA stabilization induced by mitogen treatment of EL-4 thymoma cells. J. Biol. Chem. 266, 17959-17965
48. Marer, F., and Medcalf, R. L. (1996) Plasminogen activator inhibitor type 2 gene induction by tumor necrosis factor and phorbol ester involves transcriptional and post-transcriptional events. Identification of a functional nonameric AU-rich motif in the 3′-untranslated region. J. Biol. Chem. 271, 26074-26080
49. Bohjanen, P. R., Petryniak, B., June, C. H., Thompson, C. B., and Lindsten, T. (1991) An inducible cytoplasmic factor (AU-B) binds selectively to AUUUA multimers in the 3′ untranslated region of lymphokine mRNA. Mol. Cell. Biol. 11, 3288-3295
50. Malter, J. S., and Hong, Y. (1991) A redox switch and phosphorylation are involved in the post-translational up-regulation of the adenosine-uridine binding factor by phorbol ester and ionophore. J. Biol. Chem. 266, 3167-3171
51. Suzuki, A., Goto, Y., and Iguchi, T. (1997) Progression of PDMT is accompanied by lack of Fas and intense expression of Bcl-2 and PKC-epsilon. Carcinogenesis 18, 883-887
52. Whitman, S. P., Civoli, F., and Daniel, L. W. (1997) Protein kinase CbetaII activation by 1-beta-D-arabinofuranosylcytosine is antagonistic to stimulation of apoptosis and Bcl-2alpha down-regulation. J. Biol. Chem. 272, 23481-23484
53. Hannun, Y. A. (1996) Functions of ceramide in coordinating cellular responses to stress. Science 274, 1855-9
54. Mathias, S., Pena, L. A., and Kolesnick, R. N. (1998) Signal transduction of stress via ceramide. Biochem. J. 335, 465-480
55. Verheij, M., Bose, R., Lin, X. H., Yao, B., Jarvis, W. D., Grant, S., Birrer, M. J., Szabo, E., Zon, L. I., Kyriakis, J. M., Haimovitz-Friedman, A., Fuks, Z., and Kolesnick, R. N. (1996) Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature (London) 380, 75-79
56. Cleary, M. L., Smith, S. D., and Sklar, J. (1986) Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/ immunoglobulin transcript resulting from the t(14;18) translocation. Cell 47, 19-28
57. Tsujimoto, Y., and Croce, C. M. (1986) Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc. Natl. Acad. Sci. USA 83, 5214-5218
58. Reed, J. C. (1997) Bcl-2 family proteins: regulators of apoptosis and chemoresistance in hematologic malignancies. Semin. Hematol. 34, 9-19
59. Lu, Q. L., Abel, P., Foster, C. S., and Lalani, E. N. (1996) bcl-2: role in epithelial differentiation and oncogenesis. Hum. Pathol. 27, 102-110
60. Monni, O., Joensuu, H., Franssila, K., Klefstrom, J., Alitalo, K., and Knuutila, S. (1997) BCL-2 overexpression associated with chromosomal amplification in diffuse large B-cell lymphoma. Blood 90, 1168-1174