Influence of the RNA-Binding Protein HuR in pVHL-Regulated p53 Expression in Renal Carcinoma Cells

REFERENCES

• An, W. G., M. Kanekal, M. C. Simon, E. Maltepe, M. V. Blagosklonny, and L. M. Neckers. 1998. Stabilization of wild-type p53 by hypoxia-inducible factor 1. Nature 392: 405–408.
   PubMed Web of Science ®Google Scholar
• Antic, D., N. Lu, and J. D. Keene. 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.
   PubMedGoogle Scholar
• Bhattacharya, S., T. Giordano, G. Brewer, and J. S. Malter. 1999. Identification of AUF-1 ligands reveals vast diversity of early response gene mRNAs. Nucleic Acids Res. 27: 1464–1472.
   PubMedGoogle Scholar
• Blankenship, C., J. Naglich, J. Whaley, B. Seizinger, and N. Kley. 1999. Alternate choice of initiation codon produces a biologically active product of the von Hippel-Lindau gene with tumor suppressor activity. Oncogene 18: 1529–1535.
   PubMed Web of Science ®Google Scholar
• Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58: 266–277.
   PubMed Web of Science ®Google Scholar
• Bunn, H. F., J. Gu, L. E. Huang, J. W. Park, and H. Zhu. 1998. Erythropoietin: a model system for studying oxygen-dependent gene regulation. J. Exp. Biol. 201: 1197–1201.
   PubMed Web of Science ®Google Scholar
• Caldwell, M. C., C. Hough, S. Fürer, W. M. Linehan, S., P. J. Morin, and M. Gorospe. 2002. Serial analysis of gene expression in renal carcinoma cells reveals VHL-dependent sensitivity to TNF-α cytotoxicity. Oncogene 21: 929–936.
   PubMed Web of Science ®Google Scholar
• Carballo, E., W. S. Lai, and P. J. Blackshear. 1998. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281: 1001–1005.
   PubMed Web of Science ®Google Scholar
• Chen, D., M. Li, J. Luo, and W. Gu. 2003. Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function. J. Biol. Chem. 278: 13595–13598.
   PubMed Web of Science ®Google Scholar
• Duan, D. R., A. Pause, W. Burgess, T. Aso, D. Y. T. Chen, K. P. Garrett, R. C. Conaway, J. W. Conaway, W. M. Linehan, R. D. Klausner, D. R. Duan, et al. 1995. Inhibition of transcriptional elongation by the VHL tumor suppressor protein. Science. 269: 1402–1406.
   PubMed Web of Science ®Google Scholar
• Elson, D. A., G. Thurston, L. E. Huang, D. G. Ginzinger, D. M. McDonald, R. S. Johnson, and J. M. Arbeit. 2001. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1alpha. Genes Dev. 15: 2520–2532.
   PubMed Web of Science ®Google Scholar
• Esteban-Barragan, M. A., P. Avila, M. Alvarez-Tejado, M. D. Gutierrez, A. Garcia-Pardo, F. Sanchez-Madrid, and M. O. Landazuri. 2002. Role of the von Hippel-Lindau tumor suppressor in the formation of β1-integrin fibrillar adhesions. Cancer Res. 62: 2929–2936.
   PubMed Web of Science ®Google Scholar
• Fan, J., X. Yang, W. Wang, W. H. Wood 3rd, K. G. Becker, and M. Gorospe. 2002. Global analysis of stress-regulated mRNA turnover by with cDNA arrays. Proc. Natl. Acad. Sci. USA 99: 10611–10616.
   PubMed Web of Science ®Google Scholar
• Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16: 4604–4613.
   PubMed Web of Science ®Google Scholar
• Foster, K., A. Prowse, A. van den Berg, S. Fleming, M. M. Hulsbeek, P. A. Crossey, F. M. Richards, P. Cairns, N. A. Affara, M. A. Ferguson-Smith, et al. 1994. Somatic mutations of the von Hippel-Lindau disease tumour suppressor gene in non-familial clear cell renal carcinoma. Hum. Mol. Genet. 3: 2169–2173.
   PubMed Web of Science ®Google Scholar
• Galbán, S., J. Fan, J. L. Martindale, C. Cheadle, B. Hoffman, M. P. Woods, G. Temeles, J. Brieger, J. Decker, and M. Gorospe. 2003. VHL-mediated repression of TNFα translation revealed through use of cDNA arrays. Mol. Cell. Biol. 23: 2316–2328.
   PubMedGoogle Scholar
• Gallouzi, I. E., C. M. Brennan, M. G. Stenberg, M. S. Swanson, A. Eversole, N. Maizels, and J. A. Steitz. 2000. HuR binding to cytoplasmic mRNA is perturbed by heat shock. Proc. Natl. Acad. Sci. USA 97: 3073–3078.
   PubMedGoogle Scholar
• Gnarra, J. R., K. Tory, Y. Weng, L. Schmidt, M. H. Wei, H. Li, F. Latif, S. Liu, F. Chen, F. M. Duh, et al. 1994. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat. Genet. 7: 85–90.
   PubMed Web of Science ®Google Scholar
• Gnarra, J. R., S. Zhou, M. J. Merrill, J. R. Wagner, A. Krumm, E. Papavassiliou, E. H. Oldfield, R. D. Klausner, and W. M. Linehan. 1996. Post-transcriptional regulation of vascular endothelial growth factor mRNA by the product of the VHL tumor suppressor gene. Proc. Natl. Acad. Sci. USA 93: 10589–10594.
   PubMed Web of Science ®Google Scholar
• Gorospe, M., and N. J. Holbrook. 1996. Role of p21 in prostaglandin A2-mediated cellular arrest and death. Cancer Res. 55: 475–479.
   Google Scholar
• Gorospe, M., Y. Liu, Q. Xu, F. J. Chrest, and N. J. Holbrook. 1996. Inhibition of G1 cyclin-dependent kinase activity during growth arrest of human breast carcinoma cells by prostaglandin A2. Mol. Cell. Biol. 16: 762–770.
   PubMed Web of Science ®Google Scholar
• Gorospe, M., J. M. Egan, B. Zbar, M. Lerman, L. Geil, I. Kuzmin, and N. J. Holbrook. 1999. Protective function of von Hippel-Lindau protein against impaired protein processing in renal carcinoma cells. Mol. Cell. Biol. 19: 1289–1300.
   PubMedGoogle Scholar
• Hansen, W. J., M. Ohh, J. Moslehi, K. Kondo, W. G. Kaelin, and W. J. Welch. 2002. Diverse effects of mutations in exon II of the von Hippel-Lindau (VHL) tumor suppressor gene on the interaction of pBHL with the cytosolic chaperonin and pVHL-dependent ubiquitin ligase activity. Mol. Cell. Biol. 22: 1947–1960.
   PubMed Web of Science ®Google Scholar
• Hansson, L. O., A. Friedler, S. Freund, S. Rudiger, and A. R. Fersht. 2002. Two sequence motifs from HIF-1alpha bind to the DNA-binding site of p53. Proc. Natl. Acad. Sci. USA 99: 10305–10309.
   PubMed Web of Science ®Google Scholar
• Hardie, D. G., I. P. Salt, and S. P. Davies. 2000. Analysis of the role of the AMP-activated protein kinase in the response to cellular stress. Methods Mol. Biol. 99: 63–74.
   PubMedGoogle Scholar
• Iliopoulos, O., A. Kibel, S. Gray, and W. G. Kaelin. 1995. Tumor suppression by the human von Hippel-Lindau gene product. Nat. Med. 1: 822–866.
   PubMed Web of Science ®Google Scholar
• Iliopoulos, O., A. P. Levy, C. Jiang, W. C. Kaelin, Jr., and M. A. Goldberg. 1996. Negative regulation of hypoxia-inducible genes by the von Hippel-Lindau protein. Proc. Natl. Acad. Sci. USA 93: 10595–10599.
   PubMed Web of Science ®Google Scholar
• Iliopoulos, O., M. Ohh, and W. G. Kaelin. 1998. pVHL19 is a biologically active product of the von Hippel-Lindau gene arising from internal translation initiation. Proc. Natl. Acad. Sci. USA 95: 11661–11666.
   PubMedGoogle Scholar
• Ivan, M., and W. G. Kaelin. 2001. The von Hippel-Lindau tumor suppressor protein. Curr. Opin. Genet. Dev. 11: 27–34.
   PubMed Web of Science ®Google Scholar
• Ivan, M., K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J. M. Asara, W. S. Lane, and W. G. Kaelin, Jr. 2001. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464–468.
   PubMed Web of Science ®Google Scholar
• Johannes, G., M. S. Carter, M. B. Eisen, P. O. Brown, and P. Sarnow. 1999. Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations with a cDNA microarray. Proc. Natl. Acad. Sci. USA 96: 13118–13123.
   PubMed Web of Science ®Google Scholar
• Kaelin, W. G. 2002. Molecular basis of the VHL hereditary cancer syndrome. Nat. Rev. Cancer 2: 673–682.
   PubMed Web of Science ®Google Scholar
• Keene, J. D. 2001. Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. USA 98: 7018–7024.
   PubMed Web of Science ®Google Scholar
• Koochekpour, S., M. Jeffers, P. H. Wang, C. Gong, G. A. Taylor, L. M. Roessler, R. Stearman, J. R. Vasselli, W. G. Stetler-Stevenson, W. G. Kaelin, Jr., W. M. Linehan, R. D. Klausner, J. R. Gnarra, and G. F. Vande Woude. 1999. The von Hippel-Lindau tumor suppressor gene inhibits hepatocyte growth factor/scatter factor-induced invasion and branching morphogenesis in renal carcinoma cells. Mol. Cell. Biol. 19: 5902–5912.
   PubMed Web of Science ®Google Scholar
• Kroll, S. L., W. R. Paulding, P. O. Schnell, M. C. Barton, J. W. Conaway, R. C. Conaway, and M. F. Czyzyk-Krzeska. 1999. von Hippel-Lindau protein induces hypoxia-regulated arrest of tyrosine hydroxylase transcript elongation in pheochromocytoma cells. J. Biol. Chem. 274: 30109–30114.
   PubMedGoogle Scholar
• Kullmann, M., U. Gopfert, B. Siewe, L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev. 16: 3087–3099.
   PubMed Web of Science ®Google Scholar
• Kuznetsova, A. V., J. Meller, P. O. Schnell, J. A. Nash, M. L. Ignacak, Y. Sanchez, J. W. Conaway, R. C. Conaway, and M. F. Czyzyk-Krzeska. 2003. von Hippel-Lindau protein binds hyperphosphorylated large subunit of RNA polymerase II through a proline hydroxylation motif and targets it for ubiquitination. Proc. Natl. Acad. Sci. USA 100: 2706–2711.
   PubMed Web of Science ®Google Scholar
• Latif, F. et al. 1993. Identification of the von Hippel-Lindau disease tumor suppressor gene. Science 260: 1317–1320.
   PubMed Web of Science ®Google Scholar
• Lee, J. Y., S. M. Dong, W. S. Park, N. J. Yoo, C. S. Kim, J. J. Jang, J. G. Chi, B. Zbar, I. A. Lubensky, W. M. Linehan, A. O. Vortmeyer, and Z. Zhuang. 1998. Loss of heterozygosity and somatic mutations of the VHL tumor suppressor gene in sporadic cerebellar hemangioblastomas. Cancer Res. 58: 504–508.
   PubMed Web of Science ®Google Scholar
• Los, M., G. H. Jansen, W. G. Kaelin, C. J. Lips, G. H. Blijham, and E. E. Voest. 1996. Expression pattern of the von Hippel-Lindau protein in human tissues. Lab. Investig. 75: 231–238.
   PubMed Web of Science ®Google Scholar
• Mazan-Mamczarz, K., S. Galbán, I. López de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100: 8354–8359.
   PubMed Web of Science ®Google Scholar
• Maxwell, P. H., M. S. Wiesener, G.-W. Chang, S. C. Clifford, E. C. Vaux, M. E. Cockman, C. C. Wykoff, C. W. Pugh, E. R. Maher, and P. J. Ratcliffe. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271–275.
   PubMed Web of Science ®Google Scholar
• Millard, S. S., A. Vidal, M. Markus, and A. Koff. 2000. A U-rich element in the 5′ untranslated region is necessary for the translation of p27 mRNA. Mol. Cell. Biol. 20: 5947–5959.
   PubMed Web of Science ®Google Scholar
• Ohh, M., R. L. Yauch, K. M. Lonergan, J. M. Whaley, A. O. Stemmer-Rachamimov, D. N. Louis, B. J. Gavin, N. Kley, W. G. Kaelin, Jr., and O. Iliopoulos. 1998. The von Hippel-Lindau tumor suppressor protein is required for proper assembly of an extracellular fibronectin matrix. Mol. Cell 1: 959–968.
   PubMed Web of Science ®Google Scholar
• Ohh, M., C. W. Park, M. Ivan, M. A. Hoffman, L. E. Huang, V. Chau, and W. G. Kaelin. 2000. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. J. Biol. Chem. 275: 25733–25741.
   PubMedGoogle Scholar
• Pioli, P. A., and W. F. C. Rigby. 2001. The von Hippel-Lindau protein interacts with heteronuclear ribonucleoprotein A2 and regulates its expression. J. Biol. Chem. 276: 40346–40352.
   PubMedGoogle Scholar
• Prives, C., and P. A. Hall. 1999. The p53 pathway. J. Pathol. 187: 112–126.
   PubMed Web of Science ®Google Scholar
• Sato, K., K. Terada, T. Sugiyama, S. Takahashi, M. Saito, M. Moriyama, H. Kakinuma, Y. Suzuki, M. Kato, and T. Kato. 1994. Frequent overexpression of vascular endothelial growth factor gene in human renal cell carcinoma. J. Tohoku Exp. Med. 173: 355–360.
   PubMedGoogle Scholar
• Schoenfeld, A. R., E. J. Davidowitz, and R. D. Burk. 2001. Endoplasmic reticulum/cytosolic localization of von Hippel-Lindau gene products is mediated by a 64-amino acid region. Int. J. Cancer 91: 457–467.
   PubMedGoogle Scholar
• Schoenfeld, A., E. Davidowitz, and R. A. Burk. 1998. A second major native von Hippel-Lindau gene product, initiated from an internal translation start site, functions as a tumor suppressor. Proc. Natl. Acad. Sci. USA 95: 8817–8822.
   PubMed Web of Science ®Google Scholar
• Semenza, G. L., and G. L. Wang. 1992. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12: 5447–5454.
   PubMed Web of Science ®Google Scholar
• Shuin, T., K. Kondo, S. Ashida, H. Okuda, M. Yoshida, H. Kanno, and M. Yao. 1999. Germline and somatic mutations in von Hippel-Lindau disease gene and its significance in the development of kidney cancer. Contrib. Nephrol. 128: 1–10.
   PubMedGoogle Scholar
• Tenenbaum, S. A., P. J. Lager, C. C. Carson, and J. D. Keene. 2002. Ribonomics: identifying mRNA subsets in mRNP complexes with antibodies to RNA-binding proteins and genomic arrays. Methods 26: 191–198.
   PubMed Web of Science ®Google Scholar
• Vawter, M. P., T. Barrett, C. Cheadle, B. P. Sokolov, W. H. Wood, D. Donovan, M. Webster, W. J. Freed, and K. G. Becker. 2001. Application of cDNA microarrays to examine gene expression differences in schizophrenia. Brain Res. Bull. 55: 641–650.
   PubMed Web of Science ®Google Scholar
• Wang, W., S. Lin, C. M. Caldwell, H. Furneaux, and M. Gorospe. 2000. HuR regulates cyclin A and cyclin B1 mRNA stability during the cell division cycle. EMBO J. 19: 2340–2350.
   PubMed Web of Science ®Google Scholar
• Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. J. Holbrook, and M. Gorospe. 2000. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20: 760–769.
   PubMed Web of Science ®Google Scholar
• Wang, W., J. Fan, X. Yang, S. Fürer, I. Lopez de Silanes, C. von Kobbe, J. Guo, S. N. Georas, F. Foufelle, D. G. Hardie, D. Carling, and M. Gorospe. 2002. AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol. 22: 3425–3436.
   PubMed Web of Science ®Google Scholar
• Wizigmann-Voos, S., G. Breier, W. Risau, and K. Plate. 1995. Up-regulation of vascular endothelial growth factor and its receptors in von Hippel-Lindau disease-associated and sporadic hemangioblastomas. Cancer Res. 55: 1358–1364.
   PubMed Web of Science ®Google Scholar
• Wykoff, C., C. Pugh, P. Maxwell, A. Harris, and P. Ratcliffe. 2000. Identification of novel hypoxia-dependent and -independent target genes of the von Hippel-Lindau (VHL) tumor suppressor by mRNA differential expression profiling. Oncogene 19: 6297–6305.
   PubMed Web of Science ®Google Scholar
• Zatyka, M., N. F. da Silva, S. C. Clifford, M. R. Morris, M. S. Wiesener, K. U. Eckardt, R. S. Houlston, F. M. Richards, F. Latif, and E. R. Maher. 2002. Identification of cyclin D1 and other novel targets for the von Hippel-Lindau tumor suppressor gene by expression array analysis and investigation of cyclin D1 genotype as a modifier in von Hippel-Lindau disease. Cancer Res. 62: 3803–3811.
   PubMed Web of Science ®Google Scholar
• Zhou, M. I., H. Wang, J. J. Ross, I. Kuzmin, C. Xu, and H. T. Cohen. 2002. The von Hippel-Lindau (VHL) tumor suppressor stabilizes novel PHD protein Jade-1. J. Biol. Chem. 277: 39887–39898.
   PubMed Web of Science ®Google Scholar
• Zong, Q., M. Schummer, L. Hood, and D. R. Morris. 1999. Messenger RNA translation state: the second dimension of high-throughput expression screening. Proc. Natl. Acad. Sci. USA 96: 10632–10636.
   PubMedGoogle Scholar