Induction of a ribotoxic stress response that stimulates stress-activated protein kinases by 13-deoxytedanolide, an antitumor marine macrolide

Bioscience, Biotechnology and Biochemistry

Volumn 70, Issue 1, 2006, Pages 161-171

  Lee, Kun Hyung ^a   Nishimura, Shinichi ^b   Matsunaga, Shigeki ^a   Fusetani, Nobuhiro ^a   Ichijo, Hidenori ^c   Horinouchi, Sueharu ^a   Yoshida, Minoru ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b RIKEN   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Anisomycin; Jun NH2 terminal protein kinase; p38 MAP kinase; p53; TGF beta

Indexed keywords

GENES; MUTAGENESIS; POLYPEPTIDES; STRESS ANALYSIS; SYNTHESIS (CHEMICAL); TUMORS; YEAST;

ANISOMYCIN; JUN NH2-TERMINAL PROTEIN KINASE; P38 MAP KINASE; P53; TGF-BETA;

ENZYMES;

13 DEOXYTEDANOLIDE; 13-DEOXYTEDANOLIDE; ANTINEOPLASTIC AGENT; MACROLIDE; MITOGEN ACTIVATED PROTEIN KINASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; RIBOSOME RNA;

ANIMAL; APOPTOSIS; ARTICLE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MINK; MOUSE; PROTEIN SYNTHESIS; SPONGE (PORIFERA);

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; MACROLIDES; MICE; MINK; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR STRUCTURE; PLASMINOGEN ACTIVATOR INHIBITOR 1; PORIFERA; PROTEIN BIOSYNTHESIS; RNA, RIBOSOMAL;

EID: 31444435888     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1271/bbb.70.161     Document Type: Article

References (42)

1. Laskin, J. D., Heck, D. E., and Laskin, D. L., The ribotoxic stress response as a potential mechanism for MAP kinase activation in xenobiotic toxicity. Toxicol. Sci., 69, 289-291 (2002).
2. Bogoyevitch, M. A., Ketterman, A. J., and Sugden, P. H., Cellular stresses differentially activate c-Jun N-terminal protein kinases and extracellular signal-regulated protein kinases in cultured ventricular myocytes. J. Biol. Chem., 270, 29710-29717 (1995).
3. Hazzalin, C. A., Cano, E., Cuenda, A., Barratt, M. J., Cohen, P., and Mahadevan, L. C., p38/RK is essential for stress-induced nuclear responses: JNK/SAPKs and c-Jun/ATF-2 phosphorylation are insufficient. Curr. Biol., 6, 1028-1031 (1996).
4. Iordanov, M. S., Pribnow, D., Magun, J. L., Dinh, T. H., Pearson, J. A., Chen, S. L., and Magun, B. E., Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol. Cell. Biol., 17, 3373-3381 (1997).
5. Cano, E., Hazzalin, C. A., and Mahadevan, L. C., Anisomycin-activated protein kinases p45 and p55 but not mitogen-activated protein kinases ERK-1 and -2 are implicated in the induction of c-fos and c-jun. Mol. Cell. Biol., 14, 7352-7362 (1994).
6. Zinck, R., Cahill, M. A., Kracht, M., Sachsenmaier, C., Hipskind, R. A., and Nordheim, A., Protein synthesis inhibitors reveal differential regulation of mitogen-activated protein kinase and stress-activated protein kinase pathways that converge on Elk-1. Mol. Cell. Biol., 15, 4930-4938 (1995).
7. Iordanov, M. S., Pribnow, D., Magun, J. L., Dinh, T. H., Pearson, J. A., and Magun, B. E., Ultraviolet radiation triggers the ribotoxic stress response in mammalian cells. J. Biol. Chem., 273, 15794-15803 (1998).
8. Kochi, S. K., and Collier, R. J., DNA fragmentation and cytolysis in U937 cells treated with diphtheria toxin or other inhibitors of protein synthesis. Exp. Cell. Res., 208, 296-302 (1993).
9. Polverino, A. J., and Patterson, S. D., Selective activation of caspases during apoptotic induction in HL-60 cells: Effects of a tetrapeptide inhibitor. J. Biol. Chem., 272, 7013-7021 (1997).
10. Shifrin, V. I., and Anderson, P., Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. J. Biol. Chem., 274, 13985-13992 (1999).
11. Davis, R. J., Signal transduction by the JNK group of MAP kinases. Cell, 103, 239-252 (2000).
12. Matsuzawa, A., and Ichijo, H., Molecular mechanisms of the decision between life and death: regulation of apoptosis by apoptosis signal-regulating kinase 1. J. Biochem., 130, 1-8 (2001).
13. Fusetani, N., Sugawara, T., Matsunaga, S., and Hirota, H., Cytotoxic metabolites of the marine sponge Mycale adhaerens Lambe. J. Org. Chem., 56, 4971-4974 (1991).
14. Nishimura, S., Matsunaga, S., Yoshida, M., Hirota, H., Yokoyama, S., and Fusetani, N., 13-Deoxytedanolide, a marine sponge-derived antitumor macrolide, binds to 60S large ribosomal subunit. Bioorg. Med. Chem., 13, 449-454 (2005).
15. Massague, J., Blain, S. W., and Lo, R. S., TGFbeta signaling in growth control, cancer, and heritable disorders. Cell, 103, 295-309 (2000).
16. Nishimura, S., Matsunaga, S., Yoshida, S., Nakao, Y., Hirota, H., and Fusetani, N., Structure-activity relationship study on 13-deoxytedanolide, a highly antitumor macrolide from the marine sponge Mycale adhaerens. Bioorg. Med. Chem., 13, 455-462 (2005).
17. Gannon, J. V., and Lane, D. P., Protein synthesis required to anchor a mutant p53 protein which is temperature-sensitive for nuclear transport. Nature, 349, 802-806 (1991).
18. Val135). J. Biol. Chem., 276, 14649-14657 (2001).
19. Masuoka, Y., Shin-Ya, K., Kim, Y. B., Yoshida, M., Nagai, K., Suzuki, K., Hayakawa, Y., and Seto, H., Diheteropeptin, a new substance with TGF-beta-like activity, produced by a fungus, Diheterospora chlamydosporia. I. Production, isolation and biological activities. J. Antibiotics, 53, 788-792 (2000).
20. Hannigan, M., Zhan, L., Ai, Y., and Huang, C. K., The role of p38 MAP kinase in TGF-beta1-induced signal transduction in human neutrophils. Biochem. Biophys. Res. Commun., 246, 55-58 (1998).
21. Hanafusa, H., Ninomiya-Tsuji, J., Masuyama, N., Nishita, M., Fujisawa, J., Shibuya, H., Matsumoto, K., and Nishida, E., Involvement of the p38 mitogen-activated protein kinase pathway in transforming growth factor-beta-induced gene expression. J. Biol. Chem., 274, 27161-22167 (1999).
22. Sano, Y., Harada, J., Tashiro, S., Gotoh-Mandeville, R., Maekawa, T., and Ishii, S., ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-beta signaling. J. Biol. Chem., 274, 8949-8957 (1999).
23. Liao, J. H., Chen, J. S., Chai, M. Q., Zhao, S., and Song, J. G., The involvement of p38 MAPK in transforming growth factor betal-induced apoptosis in murine hepatocytes. Cell Res., 11, 89-94 (2001).
24. Wang, L., Ma, R., Flavell, R. A., and Choi, M. E., Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for activation of p38alpha and p38delta MAPK isoforms by TGF-beta 1 in murine mesangial cells. J. Biol. Chem., 277, 47257-47262 (2002).
25. Engel, M. E., McDonnell, M. A., Law, B. K., and Moses, H. L., Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J. Biol. Chem., 274, 37413-37420 (1999).
26. Hocevar, B. A., Brown, T. L., and Howe, P. H., TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J., 18, 1345-1356 (1999).
27. Ichijo, H., Nishida, E., Irie, K., ten Dijke, P., Saitoh, M., Moriguchi, T., Takagi, M., Matsumoto, K., Miyazono, K., and Gotoh, Y., Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science, 275, 90-94 (1997).
28. Matsukawa, J., Matsuzawa, A., Takeda, K., and Ichijo, H., The ASK1-MAP kinase cascades in mammalian stress response. J. Biochem., 136, 261-265 (2004).
29. Chang, L., and Karin, M., Mammalian MAP kinase signalling cascades. Nature, 410, 37-40 (2001).
30. Laping, N. J., Grygielko, E., Mathur, A., Butter, S., Bomberger, J., Tweed, C., Martin, W., Fornwald, J., Lehr, R., Harling, J., Gaster, L., Callahan, J. F., and Olson, B. A., Inhibition of transforming growth factor (TGF)-betal-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol. Pharmacol., 62, 58-64 (2002).
31. Konkle, B. A., Schuster, S. J., Kelly, M. D., Harjes, K., Hassett, D. E., Bohrer, M., and Tavassoli, M., Plasminogen activator inhibitor-1 messenger RNA expression is induced in rat hepatocytes in vivo by dexamethasone. Blood, 79, 2636-2642 (1992).
32. Zhao, W., Spitz, D. R., Oberley, L. W., and Robbins, M. E., Redox modulation of the pro-fibrogenic mediator plasminogen activator inhibitor-1 following ionizing radiation. Cancer Res., 61, 5537-5543 (2001).
33. Yamamoto, K., Takeshita, K., Shimokawa, T., Yi, H., Isobe, K., Loskutoff, D. J., and Saito, H., Plasminogen activator inhibitor-1 is a major stress-regulated gene: implications for stress-induced thrombosis in aged individuals. Proc. Natl. Acad. Sci. U.S.A., 99, 890-895 (2002).
34. Vulin, A. I., and Stanley, F. M., Oxidative stress activates the plasminogen activator inhibitor type 1 (PAI-1) promoter through an AP-1 response element and cooperates with insulin for additive effects on PAI-1 transcription. J. Biol. Chem., 279, 25172-25178 (2004).
35. Tournier, C., Hess, P., Yang, D. D., Xu, J., Turner, T. K., Nimnual, A., Bar-Sagi, D., Jones, S. N., Flavell, R. A., and Davis, R. J., Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science, 288, 870-874 (2000).
36. Mizumura, Y., Matsumura, Y., Yokoyama, M., Okano, T., Kawaguchi, T., Moriyasu, F., and Kakizoe, T., Incorporation of the anticancer agent KRN5500 into polymeric micelles diminishes the pulmonary toxicity. Jpn. J. Cancer Res., 93, 1237-1243 (2002).
37. Kucuk, O., Young, M. L., Habermann, T. M., Wolf, B. C., Jimeno, J., and Cassileth, P. A., Phase II trial of didemnin B in previously treated non-Hodgkin's lymphoma: an Eastern Cooperative Oncology Group (ECOG) Study. Am. J. Clin. Oncol., 23, 273-277 (2000).
38. Semb, K. A., Aamdal, S., Mette, E., Ingvar, C., Gullaksen, N., and Osmundsen, K., Zilascorb (2H), a low-toxicity protein synthesis inhibitor that exhibits signs of anticancer activity in malignant melanoma. Anticancer Drugs, 9, 797-802 (1998).
39. Caraglia, M., Budillon, A., Vitale, G., Lupoli, G., Tagliaferri, P., and Abbruzzese, A., Modulation of molecular mechanisms involved in protein synthesis machinery as a new tool for the control of cell proliferation. Eur. J. Biochem., 267, 3919-3936 (2000).
40. Meric, F., and Hunt, K. K., Translation initiation in cancer: a novel target for therapy. Mol. Cancer Ther., 1, 971-979 (2002).
41. Smith, A. B., 3rd, Adams, C. M., Barbosa, S. A., and Degnan, A. P., A unified approach to the tedanolides: total synthesis of (+)-13-deoxytedanolide. Proc. Natl. Acad. Sci. U.S.A., 101, 12042-12047 (2004).
42. Julian, L. D., Newcom, J. S., and Roush, W. R., Total synthesis of (+)-13-deoxytedanolide. J. Am. Chem. Soc., 127, 6186-6187 (2005).