RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1α

Molecular and Cellular Biology

Volumn 28, Issue 1, 2008, Pages 93-107

  Galbán, Stefanie ^a   Kuwano, Yuki ^a   Pullmann Jr , Rudolf ^a   Martindale, Jennifer L ^a   Hyeon, Ho Kim ^a   Lal, Ashish ^a   Abdelmohsen, Kotb ^a   Yang, Xiaoling ^a   Dang, Youngjun ^b   Liu, Jun O ^b   Lewis, Stephen M ^c   Holcik, Martin ^c   Gorospe, Myriam ^a,d  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COBALT CHLORIDE; HUR PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; POLYPYRIMIDINE TRACT BINDING PROTEIN; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CHIMERA; COMPLEX FORMATION; CONTROLLED STUDY; GENE OVEREXPRESSION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNAL RIBOSOME ENTRY SITE; POLYSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; RNA TRANSLATION; TRANSCRIPTION REGULATION; UPREGULATION; UTERINE CERVIX CARCINOMA;

ANTIGENS, SURFACE; CELL HYPOXIA; CELL LINE, TUMOR; COBALT; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RIBOSOMES; RNA INTERFERENCE; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC;

EID: 37549037125     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00973-07     Document Type: Article

References (67)

1. Abdelmohsen, K., R. Pullmann, Jr., A. Lal, H. H. Kim, S. Galban, X. Yang, J. D. Blethrow, M. Walker, J. Shubert, D. A. Gillespie, H. Furneaux, and M. Gorospe. 2007. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol. Cell 25:543-557.
2. Bhattacharyya, S. N., R. Habermacher, U. Martine, E. I. Closs, and W. Filipowicz. 2006. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125:1111-1124.
3. Blouin, C. C., E. L. Page, G. M. Soucy, and D. E. Richard. 2004. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1α. Blood 103:1124-1130.
4. Brennan, C. M., and J. A. Steitz. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266-277.
5. Carroll, V. A., and M. Ashcroft. 2006. Role of hypoxia-inducible factor (HIF)-1α versus HIF-2α in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res. 66:6264-6270.
6. Chachami, G., G. Simos, A. Hatziefthimiou, S. Bonanou, P. A. Molyvdas, and E. Paraskeva. 2004. Cobalt induces hypoxia-inducible factor-1α expression in airway smooth muscle cells by a reactive oxygen species- and PI3K-dependent mechanism. Am. J. Respir. Cell. Mol. Biol. 31:544-551.
7. Chan, D. A., P. D. Sutphin, N. C. Denko, and A. J. Giaccia. 2002. Role of prolyl hydroxylation in oncogenically stabilized hypoxia-inducible factor-1α. J. Biol. Chem. 277:40112-40117.
8. Connolly, E., S. Braunstein, S. Formenti, and R. J. Schneider. 2006. Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol. Cell. Biol. 26:3955-3965.
9. De Boeck, M., M. Kirsch-Volders, and D. Lison. 2003. Cobalt and antimony: genotoxicity and carcinogenicity. Mutat. Res. 533:135-152.
10. Déry, M.-A. C., M. D. Michaud, and D. E. Richard. 2005. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators Intl. J. Biochem. Cell. Biol. 37:535-540.
11. Dolt, K. S., M. K. Mishra, J. Karar, M. A. Baig, Z. Ahmed, and M. A. Pasha. 2007. cDNA cloning, gene organization and variant specific expression of HIF-1 alpha in high altitude yak (Bos grunniens). Gene 386:73-80.
12. Dong, Z., M. A. Venkatachalam, J. Wang, Y. Patel, P. Snikumar, G. L. Semenza, T. Force, and J. Nishiyama. 2001. Up-regulation of apoptosis inhibitory protein IAP-2 by hypoxia: Hif-1-independent mechanisms. J. Biol. Chem. 276:18702-18709.
13. Epstein, A. C., J. M. Gleadle, L. A. McNeill, K. S. Hewitson, J. O'Rourke, D. R. Mole, M. Mukherji, E. Metzen, M. I. Wilson, A. Dhanda, Y. M. Tian, N. Masson, D. L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P. H. Maxwell, C. W. Pugh, C. J. Schofield, and P. J. Ratcliffe. 2001. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107:43-54.
14. Fernandez, J., I. Yaman, P. Sarnow, M. D. Snider, and M. Hatzoglou. 2002. Regulation of internal ribosomal entry site-mediated translation by phosphorylation of the translation initiation factor eIF2α. J. Biol. Chem. 277:19198-19205.
15. Galbán, S., J. L. Martindale, K. Mazan-Mamczarz, I. López de Silanes, J. Fan, W. Wang, J. Decker, and M. Gorospe. 2003. Influence of the RNA-binding protein HuR in pVHL-regulated p53 expression in renal carcinoma cells. Mol. Cell. Biol. 23:7083-7095.
16. Gantt, K. R., J. Cherry, M. Richardson, V. Karschner, U. Atusoy, and P. H. Pekala. 2006. The regulation of glucose transporter (GLUT1) expression by the RNA binding protein HuR. J. Cell. Biochem. 99:565-574.
17. Gdaniec, Z., H. Sierzputowska-Gracz, and E. C. Theil. 1998. Iron regulatory element and internal loop/bulge structure for ferritin mRNA studied by cobalt(III) hexammine binding, molecular modeling, and NMR spectroscopy. Biochemistry 37:1505-1512.
18. Gorospe, M. 2003. HuR in the mammalian genotoxic response: post-transcriptional multitasking. Cell Cycle 2:412-414.
19. Heinonen, M., P. Bono, K. Narko, S. H. Chang, J. Lundin, H. Joensuu, H. Furneaux, T. Hla, C. Haglund, and A. Ristimaki. 2005. Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res. 65:2157-2161.
20. Holcik, M., C. Lefebvre, C. Yeh, T. Chow, and R. G. Korneluk. 1999. A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1:190-192.
21. Huez, I., L. Creancier, S. Audigier, M. C. Gensac, A. C. Prats, and H. Prats. 1998. Two independent internal ribosome entry sites are involved in translation initiation of vascular endothelial growth factor mRNA. Mol. Cell. Biol. 18:6178-6190.
22. Hui, A. S., A. L. Bauer, J. B. Striet, P. O. Schnell, and M. F. Czyzyk-Krzeska. 2006. Calcium signaling stimulates translation of HIF-alpha during hypoxia. FASEB J. 20:466-475.
23. Hunt, S. L., and R. J. Jackson. 1999. Polypyrimidine-tract binding protein (PTB) is necessary, but not sufficient, for efficient internal initiation of translation of human rhinovirus-2 RNA. RNA 5:344-359.
24. Hunt, S. L., J. J. Hsuan, N. Totty, and R. J. Jackson. 1999. Unr, a cellular cytoplasmic RNA-binding protein with five cold-shock domains, is required for internal initiation of translation of human rhinovirus RNA. Genes Dev. 13:437-448.
25. Katsanou, V., O. Papadaki, S. Milatos, P. J. Blackshear, P. Anderson, G. Kollias, and D. L. Kontoyiannis. 2005. HuR as a negative posttranscriptional modulator in inflammation. Mol. Cell 19:777-789.
26. Kawai, T., A. Lal, X. Yang, S. Galban, K. Mazan-Mamczarz, and M. Gorospe. 2006. Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol. Cell. Biol. 26:3295-3307.
27. Ke, Y., H. Sierzputowska-Gracz, Z. Gdaniec, and E. C. Theil. 2000. Internal loop/bulge and hairpin loop of the iron-responsive element of ferritin mRNA contribute to maximal iron regulatory protein 2 binding and translational regulation in the iso-iron-responsive element/iso-iron regulatory protein family. Biochemistry 39:6235-6242.
28. Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963-969.
29. 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.
30. Kim, W. Y., and W. G. Kaelin. 2004. Role of VHL gene mutation in human cancer. J. Clin. Oncol. 22:4991-5004.
31. Kullmann, M., U. Gopfert, B. Siewe, and L. Hengst. 2002. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev. 16:3087-3099.
32. Lal, A., K. Mazan-Mamczarz, T. Kawai, X. Yang, J. L. Martindale, and M. Gorospe. 2004. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23:3092-3102.
33. Lal, A., T. Kawai, X. Yang, K. Mazan-Mamczarz, and M. Gorospe. 2005. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24:1852-1862.
34. Lang, K. J., A. Kappel, and G. J. Goodall. 2002. Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia. Mol. Biol. Cell 13:1792-1801.
35. Li, H., S. Park, B. Kilburn, M. A. Jelinek, A. Henschen-Edman, D. W. Aswad, M. R. Stallcup, and I. A. Laird-Offringa. 2002. Lipopolysaccharide- induced methylation of HuR, an mRNA-stabilizing protein, by CARM1. Coactivator-associated arginine methyltransferase. J. Biol. Chem. 277:44623-44630.
36. Li, Q. F., X. R. Wang, Y. W. Yang, and H. Lin. 2006. Hypoxia upregulates hypoxia inducible factor (HIF)-3α expression in lung epithelial cells: characterization and comparison with HIF-1α. Cell. Res. 16:548-558.
37. Li, Z., D. Wang, E. M. Messing, and G. Wu. 2005. VHL protein-interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF-1alpha. EMBO Rep. 6:373-378.
38. López de Silanes, I., M. Zhan, A. Lal, X. Yang, and M. Gorospe. 2004. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101:2987-2992.
39. López de Silanes, I., A. Lal, and M. Gorospe. 2005. HuR: post-transcriptional paths to malignancy. RNA Biol. 2:11-13.
40. MacGregor, G. R., G. P. Nolan, S. Fiering, M. Roederer, and L. A. Herzenberg. 1991. Use of the E. coli lacZ (β-galactosidase) as a reporter gene. Methods Mol. Biol. 7:217-235.
41. Maxwell, P., and K. Salnikow. 2004. HIF-1: an oxygen and metal responsive transcription factor. Cancer Biol Ther. 3:29-35.
42. Mazan-Mamczarz, K., S. Galban, I. López de Silanes, J. L. Martindale, U. Atasoy, J. D. Keene, and M. Gorospe. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100:8354-8359.
43. Meng, Z., P. H. King, L. B. Nabors, N. L. Jackson, C. Y. Chen, P. D. Emanuel, and S. W. Blume. 2005. The ELAV RNA-stability factor HuR binds the 5′-untranslated region of the human IGF-IR transcript and differentially represses cap-dependent and IRES-mediated translation. Nucleic Acids Res. 33:2962-2979.
44. Ming, X. F., G. Stoecklin, M. Lu, R. Looser, and C. Moroni. 2001. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell. Biol. 21:5778-5789.
45. Mitchell, S. A., K. A. Spriggs, M. J. Coldwell, R. J. Jackson, and A. E. Willis. 2003. The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol. Cell 11:757-771.
46. Mitchell, S. A., K. A. Spriggs, M. Bushell, J. R. Evans, M. Stoneley, J. P. Le Quesne, R. V. Spriggs, and A. E. Willis. 2005. Identification of a motif that mediates polypyrimidine tract-binding protein-dependent internal ribosome entry. Genes Dev. 19:1556-1571.
47. Pagé, E. L., G. A. Robitaille, J. Pouyssegur, and D. E. Richard. 2002. Induction of hypoxia-inducible factor-1α by transcriptional and translational mechanisms. J. Biol. Chem. 277:48403-48409.
48. -/- mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24:3112-3124.
49. Pore, N., Z. Jiang, H. K. Shu, E. Bernhard, G. D. Kao, and A. Maity. 2006. Akt1 activation can augment hypoxia-inducible factor-1α expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol. Cancer Res. 4:471-479.
50. Pouyssegur, J., F. Dayan, and N. M. Mazure. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437-443.
51. Rossignol, F., E. de Laplanche, R. Mounier, J. Bonnefont, A. Cayre, C. Godinot, H. Simonnet, and W. Clottes. 2004. Natural antisense transcripts of HIF-1α are conserved in rodents. Gene 339:121-130.
52. Ruvinsky, I., N. Sharon, T. Lerer, H. Cohen, M. Stolovich-Rain, T. Nir, Y. Dor, P. Zisman, and O. Meyuhas. 2005. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev. 19:2199-2211.
53. Ruvinsky, I., and O. Meyuhas. 2006. Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem. Sci. 31:342-348.
54. Schepens, B., S. A. Tinton, Y. Bruynooghe, R. Beyaert, and S. Cornells. 2005. The polypyrimidine tract-binding protein stimulates HIF-1alpha IRES-mediated translation during hypoxia. Nucleic Acids Res. 33:6884-6894.
55. Schofield, C. J., and P. J. Ratclifie. 2004. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:343-354.
56. Semenza, G. L. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721-732.
57. Sheflin, L. G., A. P. Zou, and S. W. Spaulding. 2004. Androgens regulate the binding of endogenous HuR to the AU-rich 3′UTRs of HIF-1α and EGF mRNA. Biochem. Biophys. Res. Commun. 322:644-651.
58. Subbaramaiah, K., T. P. Marino, D. A. Dixon, and A. J. Dannenberg. 2003. Regulation of cyclooxgenase-2 mRNA stability by taxanes: evidence for involvement of p38, MAPKAPK-2, and HuR. J. Biol. Chem. 278:37637-37647.
59. Uchida, T., F. Rossignol, M. A. Matthay, R. Mounier, S. Couette, E. Clottes, and C. Clerici. 2004. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1α and HIF-2α expression in lung epithelial cells: implication of natural antisense HIF-1α. J. Biol. Chem. 279:14871-14878.
60. Vaupel, P., F. Kallinowski, and P. Okunielf. 1989. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 49:6449-6465.
61. Vengellur, A., and J. J. LaPres. 2004. The role of hypoxia inducible factor 1α in cobalt chloride induced cell death in mouse embryonic fibroblasts, Toxicol. Sci. 82:638-646.
62. Vogelstein, B., and K. W. Kinzler. 2004. Cancer genes and the pathways they control. Nat. Med. 10:789-799.
63. Vos, S., D. J. Berrisford, and J. M. Avis. 2002. Effect of magnesium ions on the tertiary structure of the hepatitis C virus IRES and its affinity for the cyclic peptide antibiotic viomycin. Biochemistry 41:5383-5396.
64. Wenger, R. H., D. P. Stiehl, and G. Camenisch. 2005. Integration of oxygen signaling at the consensus HRE. Sci. STKE 306:re12.
65. Yang, S. J., J. Pyen, I. Lee, H. Lee, Y. Kim, and T. Kim. 2004. Cobalt chloride-induced apoptosis and extracellular signal-regulated protein kinase 1/2 activation in rat C6 glioma cells. J. Biochem. Mol. Biol. 37:480-486.
66. 2-mediated stabilization of p21 mRNA through an ERK-dependent pathway requiring the RNA-binding protein HuR. J. Biol. Chem. 279:49298-49306.
67. Zhou, J., and B. Brune. 2006. Cytokines and hormones in the regulation of hypoxia inducible factor-1α (HIF-1α). Cardiovasc. Hematol. Agents Med. Chem. 4:189-197.