Reduced nuclear export of HuR mRNA by HuR is linked to the loss of HuR in replicative senescence

Nucleic Acids Research

Volumn 38, Issue 5, 2009, Pages 1547-1558

  Yi, Jie ^a   Chang, Na ^a   Liu, Xinwen ^a   Guo, Gaier ^b   Xue, Lixiang ^a   Tong, Tanjun ^a   Gorospe, Myriam ^c   Wang, Wengong ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b CHANGZHI MEDICAL COLLEGE   (China)

^c NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; HUR PROTEIN; LEPTOMYCIN B; LUCIFERASE; MESSENGER RNA; ELAV-LIKE PROTEIN 1; MEMBRANE ANTIGEN; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; CELL AGING; CHIMERA; CONTROLLED STUDY; CYTOPLASM; DIPLOIDY; ENZYME ACTIVITY; FIBROBLAST; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NUCLEAR EXPORT SIGNAL; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REPORTER GENE; RNA REPLICATION; SENESCENCE; TRANSLATION REGULATION; UTERINE CERVIX CARCINOMA; ACTIVE TRANSPORT; BIOSYNTHESIS; CELL CULTURE; CELL NUCLEUS; DNA REPLICATION; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; HOMEOSTASIS; METABOLISM; PROTEIN SYNTHESIS;

3' UNTRANSLATED REGIONS; ACTIVE TRANSPORT, CELL NUCLEUS; ANTIGENS, SURFACE; CELL AGING; CELL NUCLEUS; CELLS, CULTURED; CYTOPLASM; DNA REPLICATION; GENE EXPRESSION REGULATION; GENES, REPORTER; HELA CELLS; HOMEOSTASIS; HUMANS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 77950482789     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1114     Document Type: Article

References (36)

1. Abdelmohsen, K., Pullmann, R. Jr, Lal, A., Kim, H.H., Galban, S., Yang, X., Blethrow, J.D., Walker, M., Shubert, J., Gillespie, D.A. et al. (2007) Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell, 25, 543-557.
2. Dormoy-Raclet, V., Ménard, I., Clair, E., Kurban, G., Mazroui, R., Di Marco, S., von Roretz, C., Pause, A. and Gallouzi, I.E. (2007) The RNA-binding protein HuR promotes cell migration and cell invasion by stabilizing the beta-actin mRNA in a U-rich-element-dependent manner. Mol. Cell. Biol., 27, 5365-5380.
3. Figueroa, A., Cuadrado, A., Fan, J., Atasoy, U., Muscat, G.E., Muñoz-Canoves, P., Gorospe, M. and Muñoz, A. (2003) Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol. Cell. Biol., 23, 4991-5004.
4. Levy, N.S., Chung, S., Furneaux, H., Levy, A.P. and Levy, N.S. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem., 273, 6417-6423.
5. Sengupta, S., Jang, B.C., Wu, M.T., Paik, J.H., Furneaux, H. and Hla, T. (2003) The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J. Biol. Chem., 278, 25227-25233.
6. Wang, W., Furneaux, H., Cheng, H., Caldwell, M.C., Hutter, D., Liu, Y., Holbrook, N. and Gorospe, M. (2000) HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol., 20, 760-769.
7. Wang, W., Caldwell, M.C., Lin, S., Furneaux, H. and Gorospe, M. (2000) HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J., 19, 2340-23450.
8. Fries, B., Heukeshoven, J., Hauber, I., Grüttner, C., Stocking, C., Kehlenbach, R.H., Hauber, J. and Chemnitz, J. (2007) Analysis of nucleocytoplasmic trafficking of the HuR ligand APRIL and its influence on CD83 expression. J. Biol. Chem., 282, 4504-4515.
9. Kullmann, M., Göpfert, U., Siewe, B. and Hengst, L. (2002) ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev., 16, 3087-3099.
10. Ma, W., Cheng, S., Campbell, C., Wright, A. and Furneaux, H.M. (1996) Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem., 271, 8144-8151.
11. Mazan-Mamczarz, K., Galbán, S., López de Silanes, I., Martindale, J.L., Atasoy, U., Keene, J.D. and Gorospe, M. (2003) RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl Acad. Sci. USA, 100, 8354-8359.
12. Peng, S.S., Chen, C.Y., 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.
13. 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.
14. Doller, A., Akool, el-S., Huwiler, A., Müller, R., Radeke, H.H., Pfeilschifter, J. and Eberhardt, W. (2008) Posttranslational modification of the AU-rich element binding protein HuR by protein kinase C delta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol. Cell. Biol., 28, 2608-2625.
15. Li, H., Park, S., Kilburn, B., Jelinek, M.A., Henschen-Edman, A., Aswad, D.W., Stallcup, M.R. and Laird-Offringa, I.A. (2002) Lipopolysaccharide-induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated argininemethyltransferase. J. Biol. Chem., 277, 44623-44630.
16. Denkert, C., Weichert, W., Winzer, K.J., Müller, B.M., Noske, A., Niesporek, S., Kristiansen, G., Guski, H., Dietel, M. and Hauptmann, S. (2004) Expression of the ELAV-like protein HuR is associated with higher tumor grade and increased cyclooxygenase-2 expression in human breast carcinoma. Clin. Cancer Res., 10, 5580-5586.
17. Erkinheimo, T.L., Lassus, H., Sivula, A., Sengupta, S., Furneaux, H., Hla, T., Haglund, C., Butzow, R. and Ristimäki, A. (2003) Cytoplasmic HuR expression correlates with poor outcome and with cyclooxygenase 2 expression in serous ovarian carcinoma. Cancer Res., 63, 7591-7594.
18. Heinonen, M., Bono, P., Narko, K., Chang, S.H., Lundin, J., Joensuu, H., Furneaux, H., Hla, T., Haglund, C. and Ristimäki, A. (2005) Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res., 65, 2157-2161.
19. 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.
20. Denkert, C., Weichert, W., Pest, S., Koch, I., Licht, D., Köbel, M., Reles, A., Sehouli, J., Dietel, M. and Hauptmann, S. (2004) Overexpression of the embryonic-lethal abnormal vision-like protein HuR in ovarian carcinoma is a prognostic factor and is associated with increased cyclooxygenase 2 expression. Cancer Res., 64, 189-195.
21. Wang, W., Fan, J., Yang, X., Fürer-Galban, S., Lopez de Silanes, I., von Kobbe, C., Guo, J., Georas, S.N., Foufelle, F., Hardie, D.G. et al. (2002) AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol., 22, 3425-3436.
22. Wang, W., Yang, X., Kawai, T., López de Silanes, I., Mazan-Mamczarz, K., Chen, P., Chook, Y.M., Quensel, C., Köhler, M. and Gorospe, M. (2004) AMP-activated protein kinase-regulated phosphorylation and acetylation of importin alpha1: involvement in the nuclear import of RNA-binding protein HuR. J. Biol. Chem., 279, 48376-48388.
23. 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.
24. 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.
25. Young, L.E., Sanduja, S., Bemis-Standoli, K., Pena, E.A., Price, R.L. and Dixon, D.A. (2009) The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology, 136, 1669-1679.
26. Abdelmohsen, K., Srikantan, S., Kuwano, Y. and Gorospe, M. (2008) miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proc. Natl Acad. Sci. USA, 105, 20297-20302.
27. Chemnitz, J., Pieper, D., Grüttner, C. and Hauber, J. (2009) Phosphorylation of the HuR ligand APRIL by casein kinase 2 regulates CD83 expression. Eur. J. Immunol., 39, 267-279.
28. Higashino, F., Aoyagi, M., Takahashi, A., Ishino, M., Taoka, M., Isobe, T., Kobayashi, M., Totsuka, Y., Kohgo, T. and Shindoh, M. (2005) Adenovirus E4orf6 targets pp32/LANP to control the fate of ARE-containing mRNAs by perturbing the CRM1-dependent mechanism. J. Cell Biol., 170, 15-20.
29. Prechtel, A.T., Chemnitz, J., Schirmer, S., Ehlers, C., Langbein-Detsch, I., Stülke, J., Dabauvalle, M.C., Kehlenbach, R.H. and Hauber, J. (2006) Expression of CD83 is regulated by HuR via a novel cis-active coding region RNA element. J. Biol. Chem., 281, 10912-10925.
30. Wright, W.E., Pereira-Smith, O.M. and Shay, J.W. (1989) Reversible cellular senescence: implications for immortalization of normal human diploid fibroblasts. Mol. Cell. Biol., 9, 3088-3092.
31. Ma, L., Chang, N., Guo, S., Li, Q., Zhang, Z., Wang, W. and Tong, T. (2008) CSIG inhibits PTEN translation in replicative senescence. Mol. Cell. Biol., 28, 6290-6301.
32. Wijdan, A., Al-Ghamdi, M., Al-Haj, L., Al-Saif, M. and Khabar, K.S.A. (2009) Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-Regulation. Nucleic Acids Res., 37, 3612-3624.
33. Hutten, S. and Kehlenbach, R.H. (2007) CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol., 17, 193-201.
34. Jang, B.C., Muñoz-Najar, U., Paik, J.H., Claffey, K., Yoshida, M. and Hla, T. (2003) Leptomycin B, an inhibitor of the nuclear export receptor CRM1, inhibits COX-2 expression. J. Biol. Chem., 278, 2773-2776.
35. Kimura, T., Hashimoto, I., Nagase, T. and Fujisawa, J. (2004) CRM1-dependent, but not ARE-mediated, nuclear export of IFN-alpha1 mRNA. J. Cell Sci., 117(Pt 11), 2259-2270.
36. Culjkovic, B., Topisirovic, I., Skrabanek, L., Ruiz-Gutierrez, M. and Borden, K.L. (2006) eIF4E is a central node of an RNA regulon that governs cellular proliferation. J. Cell Biol., 175, 415-426.