Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay

EMBO Journal

Volumn 16, Issue 8, 1997, Pages 2130-2139

  Myer, Vic E ^b   Fan, Xinhao C ^a   Steitz, Joan A ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

AU rich element; HuR; mRNA decay; UTR

Indexed keywords

CYTOKINE; DNA BINDING PROTEIN; LYMPHOKINE; MESSENGER RNA; NUCLEAR PROTEIN; TRANS ACTING FACTOR; URACIL;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PURIFICATION; PROTO ONCOGENE; RNA DEGRADATION;

3T3 CELLS; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, SURFACE; BASE COMPOSITION; CELL EXTRACTS; CROSS-LINKING REAGENTS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; RNA-BINDING PROTEINS; ULTRAVIOLET RAYS;

EID: 0030933006     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.8.2130     Document Type: Article

References (54)

1. Aharon, T. and Schneider, R.J. (1993) Selective degradation 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. Belasco, J. and Brawerman, G. (1993) Control of Messenger RNA Stability. Academic Press, Inc., San Diego, CA.
3. 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 mRNAs. Mol. Cell. Biol., 11, 3288-3295.
4. Bohjanen, P.R., Petryniak, B., June, C.H., Thompson, C.B. and Lindsten, T. (1992) AU RNA-binding factors differ in their binding specificities and affinities J. Biol. Chem., 267, 6302-6309.
5. Brewer, G. (1991) An A+U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro. Mol. Cell. Biol., 11, 2460-2466.
6. Campos, A.R., Grossman, D. and White, K. (1985) Mutant alleles at the locus elav in Drosophila melanogaster leads to nervous system detects. A developmental-genetic analysis. J. Neurogen., 2, 197-218.
7. 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 reaion of mRNA molecules specifying inflammatory mediators. Proc. Natl Acad. Sci. USA, 83, 1670-1674.
8. Chen, C.-Y.A. and Shyu, A.-B. (1994) Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements. Mol. Cell. Biol., 14, 8471-8482.
9. Chen, C.-Y.A. and Shyu, A.-B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci., 20, 465-470.
10. Chen, C.-Y.A., Chen, T.-M. and Shyu, A.-B. (1994) Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function. Mol. Cell. Biol., 14, 416-426.
11. Chen, C.-Y.A., Xu, N. and Shyu, A.-B. (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.
12. Cleveland, D.W., Fischer, S.G., Kirschner, M.W. and Laemmli, U.K. (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J. Biol. Chem., 252, 1102-1108.
13. Curatola, A.M., Nadal, M.S. and Schneider, R. (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.
14. Dalmau, J., Furneaux, H.M., Gralla, R.J., Kris, M.G. and Posner, J.B. (1990) Detection of the anti-Hu antibody in the serum of patients with small cell lung cancer: a quantitative western blot analysis. Ann. Neurol., 27, 544-552.
15. Dignam, J.D., Lebovitz, R.M. and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 1475-1498.
16. Ehrenman, K., Long, L., Wagner, B.J. and Brewer, G. (1994) Characterization of cDNAs encoding the murine A+U-rich RNA-binding protein AUF1. Gene, 149, 315-319.
17. Gao, F.-B., Carson, C.C. Levine, T.D. and Keene, J.D. (1994) Selection of a subset of mRNAs from combinatorial 3′ untranslated region libraries using neuronal RNA-binding protein Hel-N1. Proc. Natl Acad. Sci. USA, 91, 11207-11211.
18. Gillis, P. and Malter, J. (1991) The adenosine-uridine binding factor recognizes the AU-rich elements of cytokine, lymphokine, and oncogene mRNAs. J. Biol. Chem., 266, 3172-3177.
19. Good, P. (1995) A conserved family of elav-like genes in vertebrates. Proc. Natl Acad. Sci. USA, 92, 4557-4561.
20. Graus, F., Cordon-Cardo, C. and Posner, J.B. (1985) Neuronal antinuclear antibody in sensory neuronopathy from lung cancer. Neurology, 35, 538-543.
21. Greenberg, M., Harmanowski, A.L. and Ziff, E.B. (1986) Effect of protein synthesis inhibitors on growth factor activation of c-fos, c-myc, and actin gene transcription. Mol. Cell. Biol., 6, 1050-1057.
22. Hamilton, B.J., Nagy, E., Malter, J.S., Arrick, B.A. and Rigby, W.F. (1993) Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J. Biol. Chem., 268, 8881-8887.
23. 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.
24. Katz, D.A., Theodorakis, N.G., Cleveland, D.W., Lindsten, T. and Thompson, C.B. (1994) AU-A, an RNA-binding activity distinct from hnRNP A1, is selective for AUUUA repeats and shuttles between the nucleus and the cytoplasm. Nucleic Acids Res., 22, 238-246.
25. Koeller, D.M. Horowitz, J.A., Casey, J.L., Klausner, R.D. and Harford, J.B. (1991) Translation and the stability of mRNAs encoding the transferrin receptor and c-fos. Proc. Natl Acad. Sci. USA, 88, 7778-7782.
26. Lagnado, C.A., Brown, C.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.
27. Lee, S.I., Murthy, S.C., Trimble, J.J., Desrosiers, R.C. and Steitz, J.A. (1988) Four novel U RNAs are encoded by a herpesvirus. Cell, 54, 599-607.
28. Lee, W.M., Lin, C. and Curran, T. (1988) Activation of the transforming potential of the human fos proto-oncogene requires message stabilization and results in increased amounts of partially modified fos protein. Mol. Cell. Biol., 8, 5521-5527.
29. Levine, T.D., Gao, F. King, P.H., Andrews, L.G. and Keene, J.D. (1993) Hel-N1: an autoimmune RNA-binding protein with specificity for 3′ uridylate-rich untranslated regions of growth factor mRNAs. Mol. Cell. Biol., 13, 3494-3504.
30. Lindsten, T., June, C.H., Ledbetter, J.A., Stella, G. and Thompson, C.B. (1989) Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science, 244, 339-343.
31. Ma, W.-J., Cheng, S., Campbell, C., Wright, A. and Furneaux, H. (1996) Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem., 271, 8144-8151.
32. Malter, J. (1989) Identification of an AUUUA-specific messenger RNA binding protein. Science, 246, 664-666.
33. 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.
34. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. Marusich, M.F. and Weston, J.A. (1992) Identification of early neurogenic cells in the neural crest lineage. Dev. Biol., 149, 295-306.
36. Meijlink, F., Curran, T., Miller, A.D. and Verma, I.M. (1985) Removal of 67-base-pair sequence in the noncoding region of proto-oncogene fos converts it to a transforming gene. Proc. Natl Acad. Sci. USA, 82, 4987-4991.
37. Miller, A.D., Curran, T. and Verma, I.M. (1984) C-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene. Cell, 36, 51-60.
38. Myer, V.E. and Steitz, J.A. (1995) Isolation and characterization of a novel, low abundance hnRNP protein: A0. RNA, 1, 171-182.
39. Myer, V.E., Lee, S.I. and Steitz, J.A. (1992) Viral small nuclear ribonucleoproteins bind a protein implicated in messenger RNA destabilization. Proc. Natl Acad. Sci. USA, 89, 1296-1300.
40. Nakagawa, J., Waldner, H., Meyer-Monard, S., Hofsteenge, J., Jeno, P. and Moroni, C. (1995) AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity. Proc. Natl Acad. Sci. USA, 92, 2051-2055.
41. 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, 484-192.
42. Peng, S.S.-Y., Chen, C.-Y.A. and Shyu, A.-B. (1996) Functional characterization of a non-AUUUA AU-rich element from the c-jun proto-oncogene mRNA: evidence for a novel class of AU-rich elements. Mol. Cell. Biol., 16, 1490-1499.
43. Pinol-Roma, S. and Dreyfuss, G. (1991) Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins. Science, 253, 312-314.
44. Robinow, S., Campos, A.R., Yao, K.-M. and White, K. (1988) The elav gene product of Drosophila, required in neurons, has three RNP consensus motifs. Science, 242, 1570-1572.
45. Savant-Bhonsale, S. and Cleveland, D.W. (1992) Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a >20S degradation complex. Genes Dev., 6, 1927-1939.
46. Schuler, G.D. and Cole, M.D. (1988) GM-CSF and oncogene mRNA stabilities are independently regulated in trans in a mouse monocytic tumor. Cell, 55, 1115-1122.
47. Shaw, G. and Kamen, R. (1988) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell, 46, 659-667.
48. 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.
49. Shyu, A.-B., Belasco, J.G. and Greenberg, M.E. (1991) Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev., 5, 221-231.
50. Vakalopoulou, E., Schaack, J. and Shenk, T. (1991) A 32-kilodalton protein binds to AU-rich domains in the 3′ untranslated regions of rapidly degraded mRNAs. Mol. Cell. Biol., 11, 3355-3364.
51. Winstall, E., Gamache, M. and Raymond, V. (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.
52. You, Y., Chen, C.-Y.A. and Shyu, A.-B. (1992) U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3′ untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation. Mol. Cell. Biol., 12, 2931-2940.
53. Zhang, W., Wagner, B.J., Ehrenman, K., Schaefer, A.W., DeMaria, C.T., Crater, D., DeHaven, K., Long, L. and Brewer, G. (1993) Purification, characterization and cDNA cloning of an AU-rich element RNA binding protein. AUF1. Mol. Cell. Biol., 13, 7652-7665.
54. 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.