Identification of a novel AU-rich element in the 3′ untranslated region of epidermal growth factor receptor mRNA that is the target for regulated RNA-binding proteins

Molecular and Cellular Biology

Volumn 21, Issue 6, 2001, Pages 2070-2084

  Balmer, L A ^a,b   Beveridge, D J ^a,b   Jazayeri, J A ^b   Thomson, A M ^a,b   Walker, C E ^b   Leedman, P J ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE; CIS ACTING ELEMENT; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR; MESSENGER RNA; PHORBOL ESTER; RNA BINDING PROTEIN; URIDINE;

ARTICLE; BINDING AFFINITY; BREAST CANCER; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MOLECULAR STABILITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA STABILITY; SECOND MESSENGER;

3' UNTRANSLATED REGIONS; BASE SEQUENCE; BREAST NEOPLASMS; CYTOPLASM; DNA MUTATIONAL ANALYSIS; EPIDERMAL GROWTH FACTOR; HUMANS; MOLECULAR SEQUENCE DATA; RECEPTOR, EPIDERMAL GROWTH FACTOR; REGULATORY SEQUENCES, NUCLEIC ACID; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; TETRADECANOYLPHORBOL ACETATE; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0035023179     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.21.6.2070-2084.2001     Document Type: Article

References (68)

1. Anant, S., and N. O. Davidson. 2000. An AU-rich sequence element (UUU N[A/U]U) downstream of the edited C in apolipoprotein B mRNA is a high-altinity binding site for apobec-1: binding of apobec-1 to this motif in the 3′ untranslated region of c-myc increases mRNA stability. Mol. Cell. Biol. 20:1982-1992.
2. Belasco, J. 1993. mRNA degradation in prokaryotic cells: an overview, p. 3-12. In J. Belasco and G. Brawerman (ed.), Control of messenger RNA stability. Academic Press, San Diego, Calif.
3. Hjorge, J. D., A. J. Paterson, and J. E. Kudlow. 1989. Phorbol ester or epidermal growth factor (EGF) stimulates the concurrent accumulation of mRNA for the EGF receptor and its ligand transforming growth factor-alpha in a breast cancer cell line. J. Biol. Chem. 264:4021-4027.
4. Bohjanen, P. R., B. Petryniak, C. H. June, C. B. Thompson, and T. Lindsten. 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.
5. Bohjanen, P. K., B. Petryniak, C. H. June, C. B. Thompson, and T. Lindsten. 1992. AU RNA-binding factors differ in their binding specificities and affinities. J. Biol. Chem. 267:6302-6309.
6. Brewer, G. 1991. An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro. Mol. Cell. Biol. 11:2460-2466.
7. Chen, F. Y., F. M. Amara, and J. A. Wright. 1994. Defining a novel ribonucleotide reductase R1 mRNA cis element that binds to a unique cytoplasmic trans-acting protein. Nucleic Acids Res. 22:4796-4797.
8. Chen, C. Y., T. M. Chen, and A. B. Shyu. 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.
9. Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20:465-470.
10. Chen, C. Y., F. De Gatto-Konczak, Z. Wu, and M. Karin. 1998. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280:1945-1949.
11. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
12. Clark, A. J. L., S. Ishii, N. Richert, G. T. Merlino, and I. Pastan. 1985. Epidermal growth factor regulates the expression of its own receptor. Proc. Natl. Acad. Sci. USA 82:8374-8378.
13. Cleveland, D. W., and T. J. Yen. 1989. Multiple determinates of eukaryotic mRNA stability. New Biol. 1:121-126.
14. Davis, R. J., and M. P. Czech. 1985. Tumor-promoting phorbol diesters cause the phosphorylation of epidermal growth factor receptors in normal human fibroblasts at threonine-654. Proc. Natl. Acad. Sci. USA 82:1974-1978.
15. DeMaria, C. T., and G. Brewer. 1996. AUFI binding affinity to A + U-rich elements correlates with rapid mRNA degradation. J. Biol. Chem. 271: 12179-12184.
16. DeMaria, C. T., Y. Sun, L. Long, B. J. Wagner, and G. Brewer. 1997. Structural determinants in AUF1 required for high affinity binding to A + U-rich elements. J. Biol. Chem. 272:27635-27643.
17. Downward, J., Y. Yarden, E. Mayes, G. Scarce, N. Totty, P. Stockwell, A. Ullrich, J. Schlessinger, and M. D. Waterfield. 1984. Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences. Nature 307:521-527.
18. Fan, X. C., and J. A. Steitz. 1998. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95:15293-15298.
19. Fernandez-Pol, J. A., P. D. Hamilton, and D. J. Klos. 1989. Transcriptional regulation of proto-oncogene expression by epidermal growth factor, transforming growth factor beta I, and triiodothyronine in MDA-MB-468 cells. J. Biol. Chem. 264:4151-4166.
20. Fernandez-Pol, J. A. 1991. Modulation of EGF receptor protooncogene expression by growth factors and hormones in human breast carcinoma cells. Crit. Rev. Oncog. 2:173-185.
21. Filmus, J., M. N. Pollak, R. Cailleau, and R. N. Buick. 1985. MDA-MB-468, a human breast cancer cell line with a high numher of epidermal growth factor (EGF) receptors, has an amplified EGF receptor gene and is growth inhibited by EGF. Biochem. Biophys. Res. Commun. 128:898-905.
22. Ford, L. P., J. Watson, J. D. Keene, and J. Wilusz. 1999. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev. 13:188-201.
23. Gillis, P., and J. S. Malter. 1991. The adenosine-uridine binding factor recognizes the AU-rich elements of cytokine, lymphokine, and oncogene mRNAs. J. Biol. Chem. 266:3172-3177.
24. Gorospe, M., and C. Baglioni. 1994. Degradation of unstable interleukin-I alpha mRNA in a rabbit reticulocyte cell-free system. Localization of an instability determinant to a cluster of AUUUA motifs. J. Biol. Chem. 269: 11845-11851.
25. Iwai, Y., M. Bickel, D. H. Pluznik, and R. B. Cohen. 1991. Identification of sequences within the murine granulocyte-macrophage colony-stimulating factor mRNA 3′-untranslated region that mediate stabilization induced by mitogen treatment of EL-4 thymoma cells. J. Biol. Chem. 266:17959-17965.
26. Jain, R. G., L. G. Andrews, K. M. McGowan, P. H. Pekala, and J. D. Keene. 1997. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-1,1 adipocytes. Mol. Cell. Biol. 17:954-962.
27. Joseph, B., M. Orlian, and H. Furneaux. 1998. P21(waf1) mRNA contains a conserved element in its 3′-untranslated region that is bound by the Elav-like mRNA-stabilizalion proteins. J. Biol. Chem. 273:20511-20516.
28. Kesavan, P., S. Mukhopadhayay, S. Murphy, M. Rengaraju, M. A. Lazer, and M. Das. 1991. Thyroid hormone decreases the expression of epidermal growth factor receptor. J. Biol. Chem. 266:10282-10286.
29. King, C. R., M. H. Kraus, L. T. Williams, G. T. Merlino, I. H. Pastan, and S. A. Aaronson. 1985. Human tumor cell lines with EGF receptor gene amplification in the absence of aberrant sized mRNAs. Nucleic Acids Res. 13:8477-8486.
30. Klijn, J. G., P. M. Berns, P. I. Schmitz, and J. A. Foekens. 1992. The clinical significance of epidermal growth factor receptor (EGF-R) in human breast cancer: a review on 5232 patients. Endocrine Rev. 13:3-17.
31. Kontoyiannis, D., M. Pasparakis, T. T. Pizarro, F. Cominelli, and G. Kollias. 1999. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10:387-398.
32. Kudlow, J. E., C. Y. Cheung, and J. D. Bjorge. 1986. Epidermal growth factor stimulates the synthesis of its own receptor in a human breast cancer cell line. J. Biol. Chem. 26:4134-4138.
33. Lafon, I., F. Carballes, G. Brewer, M. Poiret, and D. Morello. 1998. Developmental expression of AUFI and HUR, two c-myc mRNA binding proteins. Oncogene 16:3413-3421.
34. 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.
35. Leedman, P. J., A. H. Stein, and W. W. Chin. 1995. Regulated specific protein binding to a conserved region of the 3′-untranslated region of thyrotropin beta-subunit mRNA. Mol. Endocrinol. 9:375-387.
36. Leedman, P. J., A. R. Stein, W. W. Chen, and J. T. Rogers. 1996. Thyroid hormone modulates the interaction between iron regulatory proteins and the ferritin mRNA iron-responsive element. J. Biol. Chem. 271:12017-12023.
37. Levine, T. D., F. Gao, P. H. King, L. G. Andrews, and J. D. Keene. 1993. Hcl-Nl: an autoimmune RNA-binding protein with specificity for 3′ uridylate-rich untranslated regions of growth factor mRNAs. Mol. Cell. Biol. 13:3494-3504.
38. Levy, N. S., S. Chung, H. Furneaux, and A. P. Levy. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417-6423.
39. Libermann, T. A., H. R. Nusbaum, N. Razon, K. Kris, I. Lax, H. Soreq, N. Whittle, M. D. Waterfield, A. Ullrich, and J. Schlessinger. 1985. Amplification, enhanced expression and possible rearrangement of EGF receptor gene in primary human brain tumors of glial organ. Nature 313:144-147.
40. Lin, C. R., W. S. Chen, W. Kruiger, L. S. Stolarsky, W. Weber, R. M. Evans, I. M. Verma, G. N. Gill, and M. G. Rosenfield. 1984. Expression cloning of human EGF receptor complementary DNA: gene amplification and three related messenger RNA products in A431 cells. Science 224:843-848.
41. Ma, W. J., S. Cheng, C. Campbell, A. Wright, and H. Furneaux. 1996. Cloning and characterization of HuR, a ubiquilously expressed Elav-like protein. J. Biol. Chem. 271:8144-8151.
42. Malter, J. S. 1989. Identitication of an AUUUA-specific messenger RNA binding protein. Science 2-46:664-666.
43. Malter, J. S., and Y. Hong. 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.
44. Maurer, F., M. Tierney, and R. L. Medcalf. 1999. An AU-rich sequence in the 3′-UTR of plasminogen activator inhibitor type 2 (PAI-2) mRNA promotes PAI-2 mRNA decay and provides a binding site for nuclear HuR. Nucleic Acids Res. 27:1664-1673.
45. McCulloch, R. K., C. E. Walker, A. Chakera, J. Jazayeri, and P. J. Leedman. 1998. Regulation of EGF-receptor expression by EGF and TGF alpha in epidermoid cancer cells is cell type-specific. Int. J. Biochem. Cell. Biol. 30:1265-1278.
46. Merlino, G. T., Y. H. Xu, S. Ishii, A. J. Clark, K. Semba, K. Toyoshima, T. Yamamolo, and I. Pastan. 1984. Amplification and enhanced expression of the epidermal growth factor receptor gene in A431 human carcinoma cells. Science 224:417-419.
47. Morris, G. L., and J. D. Dodd. 1990. Epidermal growth factor receptor mRNA levels in human prostatic tumors and cell lines. J. Urol. 143:1272-1274.
48. Myer, V. E., X. C. Fan, and J. A. Steitz. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16:2130-2139.
49. Nakagawa, J., H. Waldner, S. Meyer-Monard, J. Hofsteenge, P. Jeno, and C. Moroni. 1994. AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity. Proc. Natl. Acad. Sci. USA 92:2051-2055.
50. Nakamaki, T., J. Imamura, G. Brewer, N. Tsuruoka, and H. P. Koeffler. 1995. Characterization of adenosine-uridine-rich RNA binding factors. J. Cell. Physiol. 165:484-492.
51. Peltz, S. W., G. Brewer, P. Bernstein, P. A. Hart, and J. Ross. 1991. Regulation of mRNA turnover in eukaryotic cells. Crit. Rev. Eukaryot. Gene Expr. 1:99-126.
52. Rosenthal, N. 1987. Identification of regulatory elements of cloned genes with functional assays. Methods Enzymol. 152:704-720.
53. Sainsbury, J. R., J. R. Farndon, G. V. Sherbet, and A. L. Harris. 1985. Epidermal-growth-factor receptors and oestrogen receptors in human breast cancer. Lancet i:364-366.
54. Schalinske, K. L., and R. S. Eisenstein. 1996. Phosphorylation and activation of both iron regulatory proteins 1 and 2 in HL-60 cells. J. Biol. Chem. 271:7168-7176.
55. Seth, D., K. Shaw, J. Jazayeri, and P. J. Leedman. 1999. Complex post-transcriptional regulation of EGF-receptor expression by EGF and TGF-alpha in human prostate cancer cells. Br. J. Cancer 80:657-669.
56. 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.
57. Sheikh, M. S., Z. M. Shao, J. C. Chen, X. S. Li, A. Hussain, and J. A. Fontana. 1994. Expression of estrogen receptors in estrogen receptor-negative human breast carcinoma cells: modulation of epidermal growth factor-receptor (EGF-R) and transforming growth factor alpha (TGF alpha) gene expression. J. Cell. Biochem. 54:289-298.
58. Thomson, A. M., J. T. Rogers, C. E. Walker, J. M. Staton, and P. J. Leedman. 1994. Optimized RNA gel-shift and UV cross-linking assays for characterization of cytoplasmic RNA-protein interactions. BioTechniques 27:1032-1042.
59. Toi, M., T. Tominaga, A. Osaki, and T. Toge. 1994. Role of epidermal growth factor receptor expression in primary breast cancer: results of a biochemical study and an immunocytochemical study. Breast Cancer Res. Treat. 29:51-59.
60. Vakalopoulou, E., J. Schaack, and T. Shenk. 1991. A 32-kilodalton protein binds to AU-rich domains in the 3′ untranslated regions of rapidly degraded m RNAs. Mol. Cell. Biol. 11:3355-3364.
61. Wilson, G. M., and G. Brewer. 1999. Identification and characterization of proteins binding A + U-rich elements. Methods 17:74-83.
62. Wittor, H., H. Leying, A. Hochhaus, and R. V. Miltenburg. 2000. Real-time quantitation of BCR-ABL mRNA transcripts using the LightCycler -t(9;22) Quantification Kit. Biochemica, no. 2, Roche Diagnostics Corp., Indianapolis, Ind.
63. Xu, Y. H., S. Ishii, A. J. Clark, M. Sullivan, R. K. Wilson, D. P. Ma, B. A. Roe, G. T. Merlino, and I. Pastan. 1984. Human epidermal growth factor receptor cDNA is homologous to a variety of RNAs overproduced in A431 carcinoma cells. Nature 309:806-810.
64. Yamamoto, T., T. Nishida, N. Miyajima, S. Kawai, T. Ooi, and K. Toyoshima. 1983. The erbB gene of avian erythroblastosis virus is a member of the src gene family. Cell 35:71-78.
65. Yeap, B. B., R. G. Krueger, and P. J. Leedman. 1999. Differential posttranscriptional regulation of androgen receptor gene expression by androgen in prostate and breast cancer cells. Endocrinology 140:3282-3291.
66. You, Y., C. Y. Chen, and A. B. Shyu. 1992. U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleolide 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.
67. Zhang, W., B. J. Wagner, K. Ehrenman, A. W. Schaefer, C. T. De-Maria, D. Crater, K. DeHaven, L. Long, and G. Brewer. 1993. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 12:7652-7665.
68. Zubiaga, A. M., J. G. Belasco, and M. E. Greenberg. 1995. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15:2219-2230.