ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR

Genes and Development

Volumn 16, Issue 23, 2002, Pages 3087-3099

  Kullmann, Michael ^a   Göpfert, Ulrich ^a   Siewe, Basile ^a   Hengst, Ludger ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Cell division cycle; ELAV; HuD; HuR; IRES; P27 Kip1; Translation

Indexed keywords

BINDING PROTEIN; COMPLEMENTARY DNA; EMBRYONIC LETHAL ABNORMAL VISION PROTEIN; HU PROTEIN; ISOPROTEIN; PROTEIN P27; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CELL CYCLE G1 PHASE; CONTROLLED STUDY; FEMALE; GROWTH INHIBITION; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; NERVE CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPORTER GENE; RNA CAPPING; TRANSLATION REGULATION;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; FIBROBLASTS; GENE EXPRESSION REGULATION; HELA CELLS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MOLECULAR SEQUENCE DATA; PROLIFERATING CELL NUCLEAR ANTIGEN; RIBONUCLEOPROTEINS; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, DNA;

EID: 0036894711     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.248902     Document Type: Article

References (42)

1. Agrawal, D., Hauser, P., McPherson, F., Dong, F., Garcia, A., and Pledger, W.J. 1996. Repression of p27kip1 synthesis by platelet-derived growth factor in BALB/c 3T3 cells. Mol. Cell. Biol. 16: 4327-4336.
2. Antic, D., Lu, N., and Keene, J.D. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes & Dev 13: 449-461.
3. Atasoy, U., Watson, J., Patel, D., and Keene, J.D. 1998. ELAV protein HuA (HuR) can redistribute between nucleus and cytoplasm and is upregulated during serum stimulation and T cell activation. J. Cell Sci. 111: 3145-3156.
4. Brennan, C.M. and Steitz, J.A. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58: 266-277.
5. Brennan, C.M., Gallouzi, I.E., and Steitz, J.A. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151: 1-14.
6. Campos, A.R., Grossman, D., and White, K. 1985. Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J. Neurogenet. 2: 197-218.
7. Chappell, S.A., LeQuesne, J.P., Paulin, F.E., deSchoolmeester, M.L., Stoneley, M., Soutar, R.L., Ralston, S.H., Helfrich, M.H., and Willis, A.E. 2000. A mutation in the c-myc-IRES leads to enhanced internal ribosome entry in multiple myeloma: A novel mechanism of oncogene de-regulation. Oncogene 19: 4437-4440.
8. Coldwell, M.J., Mitchell, S.A., Stoneley, M., MacFarlane, M., and Willis, A.E. 2000. Initiation of Apaf-1 translation by internal ribosome entry. Oncogene 19: 899-905.
9. 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.
10. Ekholm, S.V. and Reed, S.I. 2000. Regulation of G(1) cyclindependent kinases in the mammalian cell cycle. Curr. Opin. Cell Biol. 12: 676-684.
11. Elbashir, S.M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498.
12. Gallouzi, I.E. and Steitz, J.A. 2001. Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294: 1895-1901.
13. Gallouzi, I.E., Brennan, C.M., and Steitz, J.A. 2001. Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock. RNA 7: 1348-1361.
14. Gan, W., LaCelle, M., and Rhoads, R.E. 1998. Functional characterization of the internal ribosome entry site of eIF4G mRNA. J. Biol. Chem. 273:5006-5012.
15. Gardner, L.B., Li, Q., Park, M.S., Flanagan, W.M., Semenza, G.L., and Dang, C.V. 2001. Hypoxia inhibits G1/S transition through regulation of p27 expression. J. Biol. Chem. 276: 7919-7926.
16. Gingras, A.-C., Raught, B., and Sonenberg, N. 1999. eIF4 initiation factors: Effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68: 913-963.
17. Hengst, L. and Reed, S.I. 1996. Translational control of p27Kip1 accumulation during the cell cycle. Science 271: 1861-1864.
18. -. 1998. Inhibitors of the Cip/Kip family. Curr. Top. Microbiol. Immunol. 227: 25-41.
19. Ito, E., Iwahashi, Y., Yanagisawa, Y., Suzuki, Y., Sugano, S., Yuasa, Y., and Maruyama, K. 1999. Two short sequences have positive effects on the human p27Kip1 gene transcription. Gene 228: 93-100.
20. Jain, R.G., Andrews, L.G., McGowan, K.M., Pekala, P.H., and Keene, J.D. 1997. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol. 17: 954-962.
21. Joseph, B., Orlian, M., and Furneaux, H. 1998. p21(waf1) mRNA contains a conserved element in its 3′-untranslated region that is bound by the Elav-like mRNA-stabilizing proteins. J. Biol. Chem. 273: 20511-20516.
22. Kamiyama, J., Inoue, T., Ohtani-Fujita, N., Minami, S., Yamagishi, H., and Sakai, T. 1999. The ubiquitous transcription factor NF-Y positively regulates the transcription of human p27Kip1 through a CCAAT box located in the 5-upstream region of the p27Kip1 gene. FEBS Lett. 455: 281-285.
23. Krtolica, A., Krucher, N.A., and Ludlow, J.W. 1998. Hypoxia-induced pRB hypophosphorylation results from downregulation of CDK and upregulation of PP1 activities. Oncogene 17: 2295-2304.
24. -. 1999. Molecular analysis of selected cell cycle regulatory proteins during aerobic and hypoxic maintenance of human ovarian carcinoma cells. Br. J. Cancer 80: 1875-1883.
25. Liu, J., Shen, X., Nguyen, V.A., Kunos, G., and Gao, B. 2000. α(1) adrenergic agonist induction of p21(waf1/cip1) mRNA stability in transfected HepG2 cells correlates with the increased binding of an AU-rich element binding factor. J. Biol. Chem. 275:11846-11851.
26. Millard, S.S., Yan, J.S., Nguyen, H., Pagano, M., Kiyokawa, H., and Koff, A. 1997. Enhanced ribosomal association of p27(Kip1) mRNA is a mechanism contributing to accumulation during growth arrest. J. Biol. Chem. 272: 7093-7098.
27. 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.
28. Minami, S., Ohtani-Fujita, N., Igata, E., Tamaki, T., and Sakai, T. 1997. Molecular cloning and characterization of the human p27Kip1 gene promoter. FEBS Lett. 411: 1-6.
29. Miskimins, W.K., Wang, G., Hawkinson, M., and Miskimins, R. 2001. Control of cyclin-dependent kinase inhibitor p27 expression by cap-independent translation. Mol. Cell. Biol. 21: 4960-4967.
30. Morgan, D.O. 1997. Cyclin-dependent kinases: Engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13: 261-291.
31. Nabors, L.B., Gillespie, G.Y., Harkins, L., and King, P.H. 2001. HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res. 61: 2154-2161.
32. Pagano, M., Tam, S.W., Theodoras, A.M., Beer-Romero, P., Del Sal, G., Chau, V., Yew, P.R., Draetta, G.F., and Rolfe, M. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269: 682-685.
33. Pe'ery, T. and Mathews, M.B. 2000. Viral translational strategies and host defense mechanisms. In Translational Control of Gene Expression (ed. M.B. Mathews), pp. 371-424. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Raught, B., Gingras, A.-C., and Sonenberg, N. 2000. Regulation of ribosomal recruitment in eukaryotes. In Translational Control of Gene Expression (ed. M.B. Mathews), pp. 245-293. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
35. 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.
36. Sherr, C.J. and Roberts, J.M. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes & Dev. 13: 1501-1512.
37. Stein, I., Itin, A., Einat, P., Skaliter, R., Grossman, Z., and Keshet, E. 1998. Translation of vascular endothelial growth factor mRNA by internal ribosome entry: Implications for translation under hypoxia. Mol. Cell. Biol. 18: 3112-3119.
38. Stoneley, M., Paulin, F.E., Le Quesne, J.P., Chappell, S.A., and Willis, A.E. 1998. C-Myc 5′ untranslated region contains an internal ribosome entry segment. Oncogene 16: 423-428.
39. Wang, W., Caldwell, M.C., Lin, S., Furneaux, H., and Gorospe, M. 2000a. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19: 2340-2350.
40. Wang, W., Furneaux, H., Cheng, H., Caldwell, M.C., Hutter, D., Liu, Y., Holbrook, N., and Gorospe, M. 2000b. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20: 760-769.
41. Wang, W., Yang, X., Cristofalo, V.J., Holbrook, N.J., and Gorospe, M. 2001. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol. Cell. Biol. 21: 5889-5898.
42. Yeap, B.B., Voon, D.C., Vivian, J.P., McCulloch, R.K., Thomson, A.M., Giles, K.M., Czyzyk-Krzeska, M.F., Furneaux, H., Wilce, M.C., Wilce, J.A., et al. 2002. Novel binding of HuR and poly(C)-binding protein to a conserved UC-rich motif within the 3′-untranslated region of the androgen receptor messenger RNA. J. Biol. Chem. 277: 27183-27192.