Stabilization of Urokinase and Urokinase Receptor mRNAs by HuR Is Linked to Its Cytoplasmic Accumulation Induced by Activated Mitogen-Activated Protein Kinase-Activated Protein Kinase 2

REFERENCES

• Andreasen, P. A., R. Egelund, and H. H. Petersen. 2000. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. Mol. Life Sci. 57: 25–40.
   PubMed Web of Science ®Google Scholar
• Andrews, G. K., M. A. Harding, J. P. Calvet, and E. D. Adamson. 1987. The heat shock response in HeLa cells is accompanied by elevated expression of the c-fos proto-oncogene. Mol. Cell. Biol. 7: 3452–3458.
   PubMed Web of Science ®Google Scholar
• Bakheet, T., B. R. Williams, and K. S. Khabar. 2003. ARED 2.0: an update of AU-rich element mRNA database. Nucleic Acids Res. 31: 421–423.
   PubMed Web of Science ®Google Scholar
• Ben-Levy, R., S. Hooper, R. Wilson, H. F. Paterson, and C. J. Marshall. 1998. Nuclear export of the stress-activated protein kinase p38 mediated by its substrate MAPKAP kinase-2. Curr. Biol. 8: 1049–1057.
   PubMed Web of Science ®Google Scholar
• Besser, D., P. Verde, Y. Nagamine, and F. Blasi. 1996. Signal transduction and the u-PA/u-PAR system. Fibrinolysis 10: 215–237.
   Google Scholar
• Blasi, F. 2001. u-PA and cell migration: urokinase receptor as a ligand for a chemotactic G-protein-coupled receptor. Haemostasis 31(Suppl. 1): 59.
   PubMedGoogle Scholar
• Blasi, F., and P. Carmeliet. 2002. uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell. Biol. 3: 932–943.
   PubMed Web of Science ®Google Scholar
• Brennan, C. M., I. E. Gallouzi, and J. A. Steitz. 2000. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151: 1–14.
   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
• Caruccio, L., and R. Banerjee. 1999. An efficient method for simultaneous isolation of biologically active transcription factors and DNA. J. Immunol. Methods 230: 1–10.
   PubMedGoogle Scholar
• Chen, C. Y., and A. B. Shyu. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20: 465–470.
   PubMed Web of Science ®Google Scholar
• Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351: 95–105.
   PubMed Web of Science ®Google Scholar
• Dean, J. L., R. Wait, K. R. Mahtani, G. Sully, A. R. Clark, and J. Saklatvala. 2001. The 3′ untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21: 721–730.
   PubMed Web of Science ®Google Scholar
• Degryse, B., S. Orlando, M. Resnati, S. A. Rabbani, and F. Blasi. 2001. Urokinase/urokinase receptor and vitronectin/alpha(v)beta(3) integrin induce chemotaxis and cytoskeleton reorganization through different signaling pathways. Oncogene 20: 2032–2043.
   PubMed Web of Science ®Google Scholar
• Dorion, S., and J. Landry. 2002. Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress Chaperones 7: 200–206.
   PubMed Web of Science ®Google Scholar
• Engel, K., A. Ahlers, M. A. Brach, F. Herrmann, and M. Gaestel. 1995. MAPKAP kinase 2 is activated by heat shock and TNF-alpha: in vivo phosphorylation of small heat shock protein results from stimulation of the MAP kinase cascade. J. Cell. Biochem. 57: 321–330.
   PubMedGoogle Scholar
• Engel, K., A. Kotlyarov, and M. Gaestel. 1998. Leptomycin B-sensitive nuclear export of MAPKAP kinase 2 is regulated by phosphorylation. EMBO J. 17: 3363–3371.
   PubMed Web of Science ®Google Scholar
• Engel, K., H. Schultz, F. Martin, A. Kotlyarov, K. Plath, M. Hahn, U. Heinemann, and M. Gaestel. 1995. Constitutive activation of mitogen-activated protein kinase-activated protein kinase 2 by mutation of phosphorylation sites and an A-helix motif. J. Biol. Chem. 270: 27213–27221.
   PubMedGoogle Scholar
• Fan, X. C., and J. A. Steitz. 1998. HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95: 15293–15298.
   PubMed Web of Science ®Google Scholar
• Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17: 3448–3460.
   PubMed Web of Science ®Google Scholar
• Ford, L. P., J. Watson, J. D. Keene, and J. Wilusz. 1999. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev. 13: 188–201.
   PubMed Web of Science ®Google Scholar
• Fritz, D. T., L. P. Ford, and J. Wilusz. 2000. An in vitro assay to study regulated mRNA stability. Sci. STKE 2000: PL1.
   PubMedGoogle Scholar
• Gallouzi, I. E., C. M. Brennan, and J. A. Steitz. 2001. Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock. RNA 7: 1348–1361.
   PubMed Web of Science ®Google 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
• Goldberg-Cohen, I., H. Furneauxb, and A. P. Levy. 2002. A 40-bp RNA element that mediates stabilization of vascular endothelial growth factor mRNA by HuR. J. Biol. Chem. 277: 13635–13640.
   PubMed Web of Science ®Google Scholar
• Gorospe, M., X. Wang, and N. J. Holbrook. 1998. p53-dependent elevation of p21Waf1 expression by UV light is mediated through mRNA stabilization and involves a vanadate-sensitive regulatory system. Mol. Cell. Biol. 18: 1400–1407.
   PubMedGoogle Scholar
• Guhaniyogi, J., and G. Brewer. 2001. Regulation of mRNA stability in mammalian cells. Gene 265: 11–23.
   PubMed Web of Science ®Google Scholar
• Han, Q., J. Leng, D. Bian, C. Mahanivong, K. A. Carpenter, Z. K. Pan, J. Han, and S. Huang. 2002. Rac1-MKK3-p38-MAPKAKPK2 pathway promotes urokinase plasminogen activator mRNA stability in invasive breast cancer cells. J. Biol. Chem. 107: 48379–48385.
   Google Scholar
• Hirsch, H. H., A. P. Nair, V. Backenstoss, and C. Moroni. 1995. Interleukin-3 mRNA stabilization by a trans-acting mechanism in autocrine tumors lacking interleukin-3 gene rearrangements. J. Biol. Chem. 270: 20629–20635.
   PubMed Web of Science ®Google Scholar
• Irigoyen, J. P., P. Munoz-Canoves, L. Montero, M. Koziczak, and Y. Nagamine. 1999. The plasminogen activator system: biology and regulation. Cell. Mol. Life Sci. 56: 104–132.
   PubMed Web of Science ®Google Scholar
• Jo, M., K. S. Thomas, A. V. Somlyo, A. P. Somlyo, and S. L. Gonias. 2002. Cooperativity between the Ras-ERK and Rho-Rho kinase pathways in urokinase-type plasminogen activator-stimulated cell migration. J. Biol. Chem. 277: 12479–12485.
   PubMedGoogle Scholar
• Kayyali, U. S., C. M. Pennella, C. Trujillo, O. Villa, M. Gaestel, and P. M. Hassoun. 2002. Cytoskeletal changes in hypoxic pulmonary endothelial cells are dependent on MAPK-activated protein kinase MK2. J. Biol. Chem. 277: 42596–42602.
   PubMed Web of Science ®Google Scholar
• Keene, J. D. 1999. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96: 5–7.
   PubMed Web of Science ®Google Scholar
• Kisielow, M., S. Kleiner, M. Nagasawa, A. Faisal, and Y. Nagamine. 2002. Isoform-specific knockdown and expression of adaptor protein ShcA using small interfering RNA. Biochem. J. 363: 1–5.
   PubMedGoogle Scholar
• Kontoyiannis, D., A. Kotlyarov, E. Carballo, L. Alexopoulou, P. J. Blackshear, M. Gaestel, R. Davis, R. Flavell, and G. Kollias. 2001. Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J. 20: 3760–3770.
   PubMed Web of Science ®Google Scholar
• Kotlyarov, A., and M. Gaestel. 2001. Is MK2 (mitogen-activated protein kinase-activated protein kinase 2) the key for understanding post-transcriptional regulation of gene expression? Biochem. Soc. Trans. 30: 959–963.
   Google Scholar
• Kotlyarov, A., A. Neininger, C. Schubert, R. Eckert, C. Birchmeier, H. D. Volk, and M. Gaestel. 1999. MAPKAP kinase 2 is essential for LPS-induced TNF-alpha biosynthesis. Nat. Cell Biol. 1: 94–97.
   PubMed Web of Science ®Google Scholar
• Kotlyarov, A., Y. Yannoni, S. Fritz, K. Laass, J. B. Telliez, D. Pitman, L. L. Lin, and M. Gaestel. 2002. Distinct cellular functions of MK2. Mol. Cell. Biol. 22: 4827–4835.
   PubMed Web of Science ®Google Scholar
• Lasa, M., K. R. Mahtani, A. Finch, G. Brewer, J. Saklatvala, and A. R. Clark. 2000. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell. Biol. 20: 4265–4274.
   PubMedGoogle Scholar
• Levy, N. S., S. Chung, H. Furneaux, and A. P. Levy. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273: 6417–6423.
   PubMed Web of Science ®Google Scholar
• 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. J. Biol. Chem. 277: 44623–44630.
   PubMed Web of Science ®Google Scholar
• Lindstein, T., C. H. June, J. A. Ledbetter, G. Stella, and C. B. Thompson. 1989. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244: 339–343.
   PubMed Web of Science ®Google Scholar
• Ma, W. J., S. Cheng, C. Campbell, A. Wright, and H. Furneaux. 1996. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem. 271: 8144–8151.
   PubMed Web of Science ®Google Scholar
• Milligan, J. F., D. R. Groebe, G. W. Witherell, and O. C. Uhlenbeck. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15: 8783–8798.
   PubMed Web of Science ®Google Scholar
• Ming, X. F., M. Kaiser, and C. Moroni. 1998. c-jun N-terminal kinase is involved in AUUUA-mediated interleukin-3 mRNA turnover in mast cells. EMBO J. 17: 6039–6048.
   PubMed Web of Science ®Google Scholar
• Montero, L., and Y. Nagamine. 1999. Regulation by p38 mitogen-activated protein kinase of adenylate- and uridylate-rich element-mediated urokinase-type plasminogen activator (uPA) messenger RNA stability and uPA-dependent in vitro cell invasion. Cancer Res. 59: 5286–5293.
   PubMed Web of Science ®Google Scholar
• Naderi, J., M. Hung, and S. Pandey. 2003. Oxidative stress-induced apoptosis in dividing fibroblasts involves activation of p38 MAP kinase and over-expression of Bax: resistance of quiescent cells to oxidative stress. Apoptosis 8: 91–100.
   PubMed Web of Science ®Google Scholar
• Nair, A. P., S. Hahn, R. Banholzer, H. H. Hirsch, and C. Moroni. 1994. Cyclosporin A inhibits growth of autocrine tumour cell lines by destabilizing interleukin-3 mRNA. Nature 369: 239–242.
   PubMed Web of Science ®Google Scholar
• Nanbu, R., P. A. Menoud, and Y. Nagamine. 1994. Multiple instability-regulating sites in the 3′ untranslated region of the urokinase-type plasminogen activator mRNA. Mol. Cell. Biol. 14: 4920–4928.
   PubMedGoogle Scholar
• Nanbu, R., L. Montero, D. D'Orazio, and Y. Nagamine. 1997. Enhanced stability of urokinase-type plasminogen activator mRNA in metastatic breast cancer MDA-MB-231 cells and LLC-PK1 cells down-regulated for protein kinase C—correlation with cytoplasmic heterogeneous nuclear ribonucleoprotein C. Eur. J. Biochem. 247: 169–174.
   PubMedGoogle Scholar
• Neininger, A., D. Kontoyiannis, A. Kotlyarov, R. Winzen, R. Eckert, H. D. Volk, H. Holtmann, G. Kollias, and M. Gaestel. 2002. MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277: 3065–3068.
   PubMed Web of Science ®Google Scholar
• New, L., Y. Jiang, M. Zhao, K. Liu, W. Zhu, L. J. Flood, Y. Kato, G. C. Parry, and J. Han. 1998. PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J. 17: 3372–3384.
   PubMed Web of Science ®Google Scholar
• Nguyen, D. H., D. J. Webb, A. D. Catling, Q. Song, A. Dhakephalkar, M. J. Weber, K. S. Ravichandran, and S. L. Gonias. 2000. Urokinase-type plasminogen activator stimulates the Ras/Extracellular signal-regulated kinase (ERK) signaling pathway and MCF-7 cell migration by a mechanism that requires focal adhesion kinase, Src, and Shc. Rapid dissociation of GRB2/Sps-Shc complex is associated with the transient phosphorylation of ERK in urokinase-treated cells. J. Biol. Chem. 275: 19382–19388.
   PubMedGoogle Scholar
• Parry, M. A., X. C. Zhang, and I. Bode. 2000. Molecular mechanisms of plasminogen activation: bacterial cofactors provide clues. Trends Biochem. Sci. 25: 53–59.
   PubMed Web of Science ®Google Scholar
• Peng, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17: 3461–3470.
   PubMed Web of Science ®Google Scholar
• Ross, J. 1996. Control of messenger RNA stability in higher eukaryotes. Trends Genet. 12: 171–175.
   PubMed Web of Science ®Google Scholar
• Rousseau, S., N. Morrice, M. Peggie, D. G. Campbell, M. Gaestel, and P. Cohen. 2002. Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J. 21: 6505–6514.
   PubMed Web of Science ®Google Scholar
• Saunders, L. R., D. J. Perkins, S. Balachandran, R. Michaels, R. Ford, A. Mayeda, and G. N. Barber. 2001. Characterization of two evolutionarily conserved, alternatively spliced nuclear phosphoproteins, NFAR-1 and -2, that function in mRNA processing and interact with the double-stranded RNA-dependent protein kinase, PKR. J. Biol. Chem. 276: 32300–32312.
   PubMed Web of Science ®Google Scholar
• Shaw, G., and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659–667.
   PubMed Web of Science ®Google Scholar
• Shim, J., H. Lim, J. R. Yates, and M. Karin. 2002. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell 10: 1331–1344.
   PubMed Web of Science ®Google Scholar
• Ulitzur, N., C. Rancano, and S. R. Pfeffer. 1997. Biochemical characterization of mapmodulin, a protein that binds microtubule-associated proteins. J. Biol. Chem. 272: 30577–30582.
   PubMed Web of Science ®Google Scholar
• Walensky, L. D., D. S. Coffey, T. H. Chen, T. C. Wu, and G. R. Pasternack. 1993. A novel M(r) 32,000 nuclear phosphoprotein is selectively expressed in cells competent for self-renewal. Cancer Res. 53: 4720–4726.
   PubMedGoogle Scholar
• Wang, G. J., M. Collinge, F. Blasi, R. Pardi, and J. R. Bender. 1998. Posttranscriptional regulation of urokinase plasminogen activator receptor messenger RNA levels by leukocyte integrin engagement. Proc. Natl. Acad. Sci. USA 95: 6296–6301.
   PubMedGoogle Scholar
• Wang, W., M. C. Caldwell, S. Lin, H. Furneaux, and M. Gorospe. 2000. HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19: 2340–2350.
   PubMed Web of Science ®Google Scholar
• Wang, W., J. Fan, X. Yang, S. Furer-Galban, 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
• Wang, W., H. Furneaux, H. Cheng, M. C. Caldwell, D. Hutter, Y. Liu, N. 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, Z., N. Day, P. Trifillis, and M. Kiledjian. 1999. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol. Cell. Biol. 19: 4552–4560.
   PubMed Web of Science ®Google Scholar
• Webb, D. J., D. H. Nguyen, and S. L. Gonias. 2000. Extracellular signal-regulated kinase functions in the urokinase receptor-dependent pathway by which neutralization of low density lipoprotein receptor-related protein promotes fibrosarcoma cell migration and matrigel invasion. J. Cell Sci. 113: 123–134.
   PubMed Web of Science ®Google Scholar
• Winzen, R., M. Kracht, B. Ritter, A. Wilhelm, C. Y. Chen, A. B. Shyu, M. Muller, M. Gaestel, K. Resch, and H. Holtmann. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18: 4969–4980.
   PubMed Web of Science ®Google Scholar
• Xi, X., J. Han, and J. Z. Zhang. 2001. Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase. J. Biol. Chem 276: 41029–41034.
   PubMed Web of Science ®Google Scholar
• Yaman, I., J. Fernandez, B. Sarkar, R. J. Schneider, M. D. Snider, L. E. Nagy, and M. Hatzoglou. 2002. Nutritional control of mRNA stability is mediated by a conserved AU-rich element that binds the cytoplasmic shuttling protein HuR. J. Biol. Chem. 277: 41539–41546.
   PubMedGoogle Scholar