The RNA-binding protein RNPC1 stabilizes the mRNA encoding the RNA-binding protein HuR and cooperates with HuR to suppress cell proliferation

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14535-14544

  Cho, Seong Jun ^a   Jung, Yong Sam ^a   Zhang, Jin ^a   Chen, Xinbin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; BIOLOGICAL SIGNIFICANCE; CELLULAR PROCESS; GROWTH SUPPRESSIONS; INFLAMMATORY RESPONSE; KNOCK OUTS; MRNA STABILITY; OVER-EXPRESSION; PROTEIN FAMILY; RNA BINDING; RNA-BINDING PROTEIN; UNTRANSLATED REGIONS;

CELL PROLIFERATION; RNA;

PROTEINS;

HUR PROTEIN; MESSENGER RNA; MYC PROTEIN; RNA BINDING PROTEIN; RNPC1 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; GROWTH INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA BINDING; RNA STABILITY;

3' UNTRANSLATED REGIONS; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; MICE; RNA STABILITY; RNA-BINDING PROTEINS;

EID: 84860366769     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.326827     Document Type: Article

References (36)

1. 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
2. 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
3. Yang, X., Wang, W., Fan, J., Lal, A., Yang, D., Cheng, H., and Gorospe, M. (2004) Prostaglandin A2-mediated stabilization of p21 mRNA through an ERK-dependent pathway requiring the RNA-binding protein HuR. J. Biol. Chem. 279, 49298-49306
4. 1/S checkpoint. Mol. Cell. Biol. 29, 4341-4351
5. Zou, T., Rao, J. N., Liu, L., Xiao, L., Yu, T. X., Jiang, P., Gorospe, M., and Wang, J. Y. (2010) Polyamines regulate the stability of JunD mRNA by modulating the competitive binding of its 3′ untranslated region to HuR and AUF1. Mol. Cell. Biol. 30, 5021-5032
6. Kuwano, Y., Kim, H. H., Abdelmohsen, K., Pullmann, R., Jr., Martindale, J. L., Yang, X., and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol. 28, 4562-4575
7. Talwar, S., Jin, J., Carroll, B., Liu, A., Gillespie, M. B., and Palanisamy, V. (2011) Caspase-mediated cleavage of RNA-binding protein HuR regulates c-Myc protein expression after hypoxic stress. J. Biol. Chem. 286, 32333-32343
8. Kim, H. H., Kuwano, Y., Srikantan, S., Lee, E. K., Martindale, J. L., and Gorospe, M. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 23, 1743-1748
9. Peng, S. S., Chen, C. Y., Xu, N., and Shyu, A. B. (1998)RNAstabilization by the AU-rich element binding protein, HuR, an ELAV protein.EMBOJ. 17, 3461-3470
10. 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. U.S.A. 100, 8354-8359
11. 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, 2340-2350
12. Guo, X., and Hartley, R. S. (2006) HuR contributes to cyclin E1 deregulation in MCF-7 breast cancer cells. Cancer Res. 66, 7948-7956
13. Lal, A., Mazan-Mamczarz, K., Kawai, T., Yang, X., Martindale, J. L., and Gorospe, M. (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102
14. 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
15. Datta, K., Mondal, S., Sinha, S., Li, J., Wang, E., Knebelmann, B., Karumanchi, S. A., and Mukhopadhyay, D. (2005) Role of elongin-binding domain of von Hippel Lindau gene product on HuR-mediated VPF/VEGF mRNA stability in renal cell carcinoma. Oncogene 24, 7850-7858
16. Doller, A., Winkler, C., Azrilian, I., Schulz, S., Hartmann, S., Pfeilschifter, J., and Eberhardt, W. (2011) High-constitutive HuR phosphorylation at Ser 318 by PKCδ propagates tumor relevant functions in colon carcinoma cells. Carcinogenesis 32, 676-685
17. Doller, A., Huwiler, A., Müller, R., Radeke, H. H., Pfeilschifter, J., and Eberhardt, W. (2007) Protein kinase Cα-dependent phosphorylation of the mRNA-stabilizing factor HuR. Implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell 18, 2137-2148
18. Kim, H. H., Abdelmohsen, K., Lal, A., Pullmann, R., Jr., Yang, X., Galban, S., Srikantan, S., Martindale, J. L., Blethrow, J., Shokat, K. M., and Gorospe, M. (2008) Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev. 22, 1804-1815
19. Abdelmohsen, K., Pullmann, R., Jr., Lal, A., Kim, H. H., Galban, S., Yang, X., Blethrow, J. D., Walker, M., Shubert, J., Gillespie, D. A., Furneaux, H., and Gorospe, M. (2007) Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell 25, 543-557
20. Mazroui, R., Di Marco, S., Clair, E., von Roretz, C., Tenenbaum, S. A., Keene, J. D., Saleh, M., and Gallouzi, I. E. (2008) Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. J. Cell Biol. 180, 113-127
21. Dai, W., Zhang, G., and Makeyev, E. V. (2012) RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res. 40, 787-800
22. Xu, F., Zhang, X., Lei, Y., Liu, X., Liu, Z., Tong, T., and Wang, W. (2010) Loss of repression of HuR translation by miR-16 may be responsible for the elevation of HuR in human breast carcinoma. J. Cell. Biochem. 111, 727-734
23. Abdelmohsen, K., Kim, M. M., Srikantan, S., Mercken, E. M., Brennan, S. E., Wilson, G. M., Cabo, R., and Gorospe, M. (2010) miR-519 suppresses tumor growth by reducing HuR levels. Cell Cycle 9, 1354-1359
24. Guo, X., Wu, Y., and Hartley, R. S. (2009) MicroRNA-125a represses cell growth by targeting HuR in breast cancer. RNA Biol. 6, 575-583
25. Shu, L., Yan, W., and Chen, X. (2006) RNPC1, an RNA-binding proteinand a target of the p53 family, is required for maintaining the stability of the basal and stress-induced p21 transcript. Genes Dev. 20, 2961-2972
26. Miyamoto, S., Hidaka, K., Jin, D., and Morisaki, T. (2009) RNA-binding proteins Rbm38 and Rbm24 regulate myogenic differentiation via p21-dependent and -independent regulatory pathways. Genes Cells 14, 1241-1252
27. Léveillé, N., Elkon, R., Davalos, V., Manoharan, V., Hollingworth, D., Oude Vrielink, J., le Sage, C., Melo, C. A., Horlings, H. M., Wesseling, J., Ule, J., Esteller, M., Ramos, A., and Agami, R. (2011) Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity. Nat. Commun. 2, 513
28. Cho, S. J., Zhang, J., and Chen, X. (2010) RNPC1 modulates the RNA-binding activity of, and cooperates with, HuR to regulate p21 mRNA stability. Nucleic Acids Res. 38, 2256-2267
29. Zhang, J., Cho, S. J., Shu, L., Yan, W., Guerrero, T., Kent, M., Skorupski, K., Chen, H., and Chen, X. (2011) Translational repression of p53 by RNPC1, a p53 target overexpressed in lymphomas. Genes Dev. 25, 1528-1543
30. Harms, K. L., and Chen, X. (2007) Histone deacetylase 2 modulates p53 transcriptional activities through regulation of p53-DNA binding activity. Cancer Res. 67, 3145-3152
31. Peritz, T., Zeng, F., Kannanayakal, T. J., Kilk, K., Eirí ksdóttir, E., Langel, U., and Eberwine, J. (2006) Immunoprecipitation of mRNA-protein complexes. Nat. Protoc. 1, 577-580
32. Adams, D. J., Beveridge, D. J., van der Weyden, L., Mangs, H., Leedman, P. J., and Morris, B. J. (2003) HADHB, HuR, and CP1 bind to the distal 3′-untranslated region of human renin mRNA and differentially modulate renin expression. J. Biol. Chem. 278, 44894-44903
33. Sully, G., Dean, J. L., Wait, R., Rawlinson, L., Santalucia, T., Saklatvala, J., and Clark, A. R. (2004) Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1], AUF-2, tristetraprolin, HuR (Hu antigen R) or FBP1 (far-upstream-sequence- element-binding protein 1). Biochem. J. 377, 629-639
34. Liu, L., Rao, J. N., Zou, T., Xiao, L., Wang, P. Y., Turner, D. J., Gorospe, M., and Wang, J. Y. (2009) Polyamines regulate c-Myc translation through Chk2-dependent HuR phosphorylation. Mol. Biol. Cell 20, 4885-4898
35. 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. U.S.A. 105, 20297-20302
36. Lal, A., Kawai, T., Yang, X., Mazan-Mamczarz, K., and Gorospe, M. (2005) Antiapoptotic function of RNA-binding protein HuR effected through prothymosin α. EMBO J. 24, 1852-1862