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 Research

Volumn 59, Issue 20, 1999, Pages 5286-5293

  Montero, Lilian ^a   Nagamine, Yoshikuni ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ADENOSINE PHOSPHATE; GLOBIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; URIDINE PHOSPHATE; UROKINASE; UROKINASE RECEPTOR;

ANIMAL CELL; ARTICLE; BREAST TUMOR; CANCER INVASION; CELL INVASION; CELL LINE; ENZYME ACTIVITY; ENZYME REGULATION; GENE OVEREXPRESSION; GENETIC STABILITY; HALF LIFE TIME; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RNA DEGRADATION; RNA TRANSLATION;

3' UNTRANSLATED REGIONS; HUMANS; IMIDAZOLES; MITOGEN-ACTIVATED PROTEIN KINASES; NEOPLASM INVASIVENESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RECEPTORS, CELL SURFACE; RNA, MESSENGER; TUMOR CELLS, CULTURED; URINARY PLASMINOGEN ACTIVATOR;

EID: 0032697491     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. r 55,000 form of the human plasminogen activator, urokinase. J. Cell Biol., 100: 86-92, 1985.
2. Blasi, F. uPA, uPAR, PAI-I: key intersection of proteolytic, adhesive and chemotactic highways? Immunol. Today, 18: 415-417, 1997.
3. Kwaan, H. C. The plasminogen-plasmin system in malignancy. Cancer Metastasis Rev., 11: 291-311, 1992.
4. Duffy, M. J., Reilly, D., McDermott, E., O'Higgins, N., Fennelly, J. J., and Andreasen, P. A. Urokinase plasminogen activator as a prognostic marker in different subgroups of patients with breast cancer. Cancer (Phila.). 74: 2276-2280, 1994.
5. Ferno, M., Bendahl, P. O., Borg, A., Brundell, J., Hirschberg, L., Olsson, H., and Killander, D. Urokinase plasminogen activator, a strong independent prognostic factor in breast cancer, analysed in steroid receptor cytosols with a luminometric immunoassay. Eur. J. Cancer, 32A: 793-801, 1996.
6. Dano, K., Andreasen, P. A., Grondahl-Hansen, J., Kristensen, P., Nielsen, L. S., and Skriver, L. Plasminogen activators, tissue degradation, and cancer. Adv. Cancer Res., 44: 139-266, 1985.
7. Shapiro, R. L., Duquette, J. G., Roses, D. F., Nunes, I., Harris, M. N., Kamino, H., Wilson, E. L., and Rifkin, D. B. Induction of primary cutaneous melanocytic neoplasms in urokinase-type plasminogen activator (uPA)-deficient and wild-type mice: cellular blue nevi invade but do not progress to malignant melanoma in uPA-deficient animals. Cancer Res., 56: 3597-3604, 1996.
8. Besser, D., Verde, P., Nagamine, Y., and Blasi, F. Signal transduction and the uPA/uPAR system. Fibririolysis, 10: 215-237, 1996.
9. Irigoyen, J. P., Munoz-Canoves, P., Montero, L., Koziczak, M., and Nagamine, Y. The plasminogen activator system: biology and regulation. Cell. Mol. Life Sci., in press, 1999.
10. Nagamine, Y., Lee, J. S., Menoud, P-A., and Nambu, R. Structure, and function of the urokinase-type plasminogen activator gene. In: P. Glas-Greenwalt (ed.). Fibrinolysis in Disease, pp. 10-20. Boca Raton, FL: CRC Press, 1995.
11. Altus, M. S., and Nagamine, Y. Protein synthesis inhibition stabilizes urokinase-type plasminogen activator mRNA. Studies in vivo and in cell-free decay reactions. J. Biol. Chem., 266: 21190-21196, 1991.
12. Nanbu, R., Menoud, P. A., and Nagamine. Y. Multiple instability-regulating sites in the 3′ untranslated region of the urokinase-type plasminogen activator mRNA. Mol. Cell. Biol,14: 4920-4928, 1994.
13. Zubiaga, A. M., Belasco, J. G., Greenberg, M. E., and Wellington, C. L. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol., 15: 2219-2230, 1995.
14. Lagnado, C. A., Brown, C. Y., and Goodall, G. J. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A). Mol. Cell. Biol., 14: 7984-7995, 1994.
15. Chen, C. Y., and Shyu, A. B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci., 20: 465-470, 1995.
16. Xu, N., Loflin, P., Chen, C. Y., and Shyu, A. B. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res., 26: 558-565, 1998.
17. Nair, A. P., Hahn, S., Banholzer, R., Hirsch, H. H., and Moroni, C. Cyclosporin A inhibits growth of autocrine tumour cell lines by destabilizing interleukin-3 mRNA. Nature (Lond.), 369: 239-242, 1994.
18. Banholzer, R., Nair, A. P., Hirsch, H. H., Ming, X. F., and Moroni, C. Rapamycin destabilizes interleukin-3 mRNA in autocrine tumor cells by a mechanism requiring an intact 3' untranslated region. Mol. Cell. Biol., 17: 3254-3260, 1997.
19. Levy, N. S., Chung, S., Furneaux, H., and Levy, A. P. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem., 273: 6417-6423, 1998.
20. Peng, S. S., Chen. C. Y., Xu, N., and Shyu, A. B. RNA stabilization by the AU-rich element binding protein. HuR, an ELAV protein. EMBO J., 17: 3461-3470, 1998.
21. Fan, X. C., and Steitz, J. A. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J., 17: 3448-3460, 1998.
22. Danner, S., Frank, M., and Lohse, M. J. Agonist regulation of human β-adrenergic receptor mRNA stability occurs via a specific AU-rich element. J. Biol. Chem., 273: 3223-3229, 1998.
23. Nanbu, R., Montero, L., D'Orazio, D., and Nagamine, Y. 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, 1997.
24. Hull, R. N., Cherry, W. R., and Weaver, G. W. The origin and characteristics of a pig kidney cell strain, LLC-PK1. In Vitro (Rockville), 12: 670-677, 1976.
25. Cailleau, R., Young, R., Olive, M., and Reeves, W. J., Jr. Breast tumor cell lines from pleural effusions. J. Natl. Cancer Inst., 53: 661-674, 1974.
26. Herrin, D. L., and Schmidt, G. W. Rapid, reversible staining of northern blots prior to hybridization. Biotechniques, 6: 196-197, 199-200, 1988.
27. Andrus, L., Altus, M. S., Pearson, D., Grattan, M., and Nagamine, Y. hsp70 mRNA accumulates in LLC-PK1 pig kidney cells treated with calcitonin but not with 8-bromo-cAMP. J. Biol. Chem., 263: 6183-6187, 1988.
28. Medema, R. H., de Laat, W. L., Martin, G. A., McCormick, F., and Bos, J. L. GTPase-activating protein SH2-SH3 domains induce gene expression in a Ras-dependent fashion. Mol. Cell. Biol., 12: 3425-3430, 1992.
29. Moriguchi, T., Toyoshima, F., Masuyama, N., Hanafusa, H., Gotoh, Y., and Nishida, E. A novel SAPK/JNK kinase, MKK7, stimulated by TNFα and cellular stresses. EMBO J., 16: 7045-7053, 1997.
30. Raingeaud, J., Whitmarsh, A. J., Barrett, T., Derijard, B., and Davis, R. J. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol., 16: 1247-1255, 1996.
31. Ellis, V., Behrendt, N., and Dano, K. Plasminogen activation by receptor-bound urokinase. A kinetic study with both cell-associated and isolated receptor. J. Biol. Chem., 266: 12752-12758, 1991.
32. Heussen, C., and Dowdle, E. B. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulfate and copolymerized substrates. Anal. Biochem., 102: 196-202, 1980.
33. Vassalli, J. D., Hamilton, J., and Reich, E. Macrophage plasminogen activator: modulation of enzyme production by anti-inflammatory steroids, mitotic inhibitors, and cyclic nucleotides. Cell, 8: 271-281, 1976.
34. Rusciano, D., Lorenzoni, P., and Burger, M. M. Expression of constitutively activated hepatocyte growth factor/scatter factor receptor (c-met) in B16 melanoma cells selected for enhanced liver colonization. Oncogene, 11: 1979-1987, 1995.
35. Lee, J. C., Laydon, J. T., McDonnell, P. C., Gallagher, T. F., Kumar, S., Green, D., McNulty, D., Blumenthal, M. J., Keys, J. R., Landvatter, S. W., Strickler, J. E., McLaughlin, M. M., Siemens, I. R., Fisher, S. M., Livi, G. P., White, J. R., Adams, J. L., and Young, D. R. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature (Lond.), 372: 739-746, 1994.
36. Singer, R. H., and Penman, S. Stability of HeLa cell mRNA in actinomycin. Nature (Lond.), 240: 100-102, 1972.
37. Maurer, F., and Medcalf, R. L. Plasminogen activator inhibitor type 2 gene induction by tumor necrosis factor and phorbol ester involves transcriptional and post transcriptional events. Identification of a functional nonameric AU- rich motif in the 3′-untranslated region. J. Biol. Chem., 271: 26074-26080, 1996.
38. Besser, D., Presta, M., and Nagamine, Y. Elucidation of a signaling pathway induced by FGF-2 leading to uPA gene expression in NIH 3T3 fibroblasts. Cell Growth Differ., 6: 1009-1017, 1995.
39. Besser, D., Urich, M., Sakaue, M., Messerschmitt, A., Ballmer-Hofer, K., and Nagamine, Y. Urokinase-type plasminogen activator gene regulation by polyomavirus middle-T antigen. Oncogene, 11: 2383-2391, 1995.
40. Besser, D., Bardelli, A., Didichenko, S., Thelen, M., Comoglio, P. M., Ponzetto, C., and Nagamine, Y. Regulation of the urokinase-type plasminogen activator gene by the oncogene Tpr-Met involves GRB2. Oncogene, 14: 705-711, 1997.
41. Irigoyen, J. P., Besser, D., and Nagamine, Y. Cytoskeleton reorganization induces the urokinase-type plasminogen activator gene via the Ras/extracellular signal-regulated kinase (ERK) signaling pathway. J. Biol. Chem., 272: 1904-1909, 1997.
42. D'Orazio, D., Besser, D., Marksitzer, R., Kunz, C., Hume, D. A., Kiefer, B., and Nagamine, Y Cooperation of two PEA3/AP1 sites in uPA gene induction by TPA and FGF- 2. Gene, 201: 179-187, 1997.
43. Whitmarsh, A. J., Yang, S. H., Su, M. S., Sharrocks, A. D., and Davis, R. J. Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol. Cell. Biol., 17: 2360-2371, 1997.
44. Han, J., Lee, J. D., Jiang, Y., Li, Z., Feng, L., and Ulevitch, R. J. Characterization of the structure and function of a novel MAP kinase kinase (MKK6). J. Biol. Chem., 271: 2886-2891, 1996.
45. Moriguchi, T., Kuroyanagi, N., Yamaguchi, K., Gotoh, Y., Irie, K., Kano, T., Shirakabe, K., Muro, Y., Shibuya, H., Matsumoto, K., Nishida, E., and Haglwara, M. A novel kinase cascade mediated by mitogen-aclivated protein kinase kinase 6 and MKK3. J. Biol. Chem., 271: 13675-13679, 1996.
46. Raingeaud, J., Gupta, S., Rogers, J. S., Dickens, M., Han, J., Ulevitch, R. J., and Davis, R. J. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem., 270: 7420-7426, 1995.
47. Zanke, B. W., Rubie, E. A., Winnett, E., Chan, J., Randall, S., Parsons, M., Boudreau, K., McInnis, M., Yan, M., Templeton, D. J., and Woodgett, J. R. Mammalian mitogen-activated protein kinase pathways are regulated through formation of specific kinase-activator complexes. J. Biol. Chem., 271: 29876-29881, 1996.
48. Toyoshima, F., Moriguchi, T., and Nishida, E. Fas induces cytoplasmic apoptotic responses and activation of the MKK7- JNK/SAPK and MKK6-p38 pathways independent of CPP32-like proteases. J. Cell Biol., 139: 1005-1015, 1997.
49. Vassalli, J. D., and Belin, D. Amiloride selectively inhibits the urokinase-type plasminogen activator. FEBS Lett., 214: 187-191, 1987.
50. Holst-Hansen, C., Johannessen, B., Hoyer-Hansen, G., Romer. J., Ellis, V., and Brunner, N. Urokinase-type plasminogen activation in three human breast cancer cell lines correlates with their in vitro invasiveness. Clin. & Exp. Metastasis, 14: 297-307, 1996.
51. Brunner, N., Moser, C., Clarke, R., and Cullen, K. IGF-I, and IGF-II expression in human breast cancer xenografts: relationship to hormone independence. Breast Cancer Res. Treat., 22: 39-45, 1992
52. 3 binding to vitronectin. Nature (Lond.), 383: 441-443, 1996.
53. Planus, E., Barlovalz-Meimon, G., Rogers, R. A., Bonavaud, S., Ingber, D. E., and Wang, N. Binding of urokinase to plasminogen activator inhibitor type-1 mediates cell adhesion and spreading. J. Cell Sci., 110: 1091-1098, 1997.
54. Beyaert, R., Cuenda, A., Vanden Berghe, W., Plaisance, S., Lee, J. C., Haegeman, G., Cohen, P., and Fiers, W. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J., 15: 1914-1923, 1996.
55. Kramer, R. M., Roberts, E. F., Um, S. L., Borsch-Haubold, A. G., Watson, S. P., Fisher, M. J., and Jakubowski, J. A. p38 mitogen-activated protein kinase phosphorylates cytosolic phospholipase A2 (cPLA2) in thrombin-stimulated platelets. Evidence that proline-directed phosphorylation is not required for mobilization of arachidonic acid by cPLA2. J. Biol. Chem., 271: 27723-27729, 1996.
56. Lee, J. C., and Young, P. R. Role of CSB/p38/RK stress response kinase in LPS and cytokine signaling mechanisms. J. Leukocyte Biol., 59: 152-157, 1996.
57. Derijard, B., Raingeaud, J., Barrett, T., Wu, I. H., Han, J., Ulevitch, R. J., and Davis, R. J. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science (Washington DC), 267: 682-685, 1995.
58. Enslen, H., Raingeaud, J., and Davis, R. J. Selective activation of p38 mitogen-activated protein (MAP) kinase isoforms by the MAP kinase kinases MKK3 and MKK6. J. Biol. Chem., 273: 1741-1748, 1998.
59. Cuenda, A., Rouse, J., Doza, Y. N., Meier, R., Cohen, P., Gallagher, T. F., Young, P. R., and Lee, J. C. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett., 364: 229-233, 1995.
60. Tran-Thang, C., Kruithof, E., Lahm, H., Schuster, W. A., Tada, M., and Sordat, B. Modulation of the plasminogen activation system by inflammatory cytokines in human colon carcinoma cells. Br. J. Cancer, 74: 846-852, 1996.
61. Takahashi, K., Uwabe, Y., Sawasaki, Y., Kiguchi, T., Nakamura, H., Kashiwabara, K., Yagyu, H., and Matsuoka, T. Increased secretion of urokinase-type plasminogen activator by human lung microvascular endothelial cells. Am. J. Physiol., 275: L47-L54, 1998.
62. Cohen, P. The search for physiological substrates of MAP and SAP kinases. Trends Cell Biol., 7: 353-361, 1997.
63. Miyazawa, K., Mori, A., Miyata, H., Akahane, M., Ajisawa, Y., and Okudaira, H. Regulation of interleukin-1β-induced interleukin-6 gene expression in human fibroblast-like synoviocytes by p38 mitogen-activated protein kinase. J. Biol. Chem., 273: 24832-24838, 1998.
64. Chen, C. Y., Del Gatto-Konczak, F., Wu, Z., and Karin, M. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science (Washington DC), 280: 1945-1949, 1998.
65. Ming, X-F., Kaiser, M., and Moroni, C. JNK is involved in AUUUA-mediated 1L-3 mRNA turnover in mast cells. EMBO J., 17: 6039-6048, 1998.
66. Prichett, W., Hand, A., Sheilds, J., and Dunnington, D. Mechanism of action of bicyclic imidazoles defines a translational regulatory pathway for tumor necrosis factor alpha. J. Inflamm., 45: 97-105, 1995.
67. Simon, C., Goepfert, H., and Boyd, D. Inhibition of the p38 mitogen-activated protein kinase by SB 203580 blocks PMA-induced Mr 92,000 type IV collagenase secretion and in vitro invasion. Cancer Res., 58: 1135-1139, 1998.
68. Wang, G. J., Collinge, M., Blasi, F., Pardi, R., and Bender, J. R. Posttranscriptional regulation of urokinase plasminogen activator receptor messenger RNA levels by leukocyte integrin engagement. Proc. Natl. Acad. Sci. USA, 95, 6296-6301, 1998.