Apigenin Prevents UVB-Induced Cyclooxygenase 2 Expression: Coupled mRNA Stabilization and Translational Inhibition

REFERENCES

• Bachelor, M. A., A. L. Silvers, and G. T. Bowden. 2002. The role of p38 in UVA-induced cyclooxygenase-2 expression in the human keratinocyte cell line, HaCaT. Oncogene 21:7092–7099.
   PubMedGoogle Scholar
• Beck, A. R., I. J. Miller, P. Anderson, and M. Streuli. 1998. RNA-binding protein TIAR is essential for primordial germ cell development. Proc. Natl. Acad. Sci. USA 95:2331–2336.
   PubMed Web of Science ®Google Scholar
• Birt, D. F., D. Mitchell, B. Gold, P. Pour, and H. C. Pinch. 1997. Inhibition of ultraviolet light induced skin carcinogenesis in SKH-1 mice by apigenin, a plant flavonoid. Anticancer Res. 17:85–91.
   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
• Chan, G., J. O. Boyle, E. K. Yang, F. Zhang, P. G. Sacks, J. P. Shah, D. Edelstein, R. A. Soslow, A. T. Koki, B. M. Woerner, J. L. Masferrer, and A. J. Dannenberg. 1999. Cyclooxygenase-2 expression is up-regulated in squamous cell carcinoma of the head and neck. Cancer Res. 59:991–994.
   PubMed Web of Science ®Google Scholar
• Chaumontet, C., C. Droumaguet, V. Bex, C. Heberden, I. Gaillard-Sanchez, and P. Martel. 1997. Flavonoids (apigenin, tangeretin) counteract tumor promoter-induced inhibition of intercellular communication of rat liver epithelial cells. Cancer Lett. 114:207–210.
   PubMed Web of Science ®Google Scholar
• Cok, S. J., S. J. Acton, and A. R. Morrison. 2003. The proximal region of the 3′-untranslated region of cyclooxygenase-2 is recognized by a multimeric protein complex containing HuR, TIA-1, TIAR, and the heterogeneous nuclear ribonucleoprotein U. J. Biol. Chem. 278:36157–36162.
   PubMed Web of Science ®Google Scholar
• Cok, S. J., S. J. Acton, A. E. Sexton, and A. R. Morrison. 2004. Identification of RNA-binding proteins in RAW 264.7 cells that recognize a lipopolysaccharide-responsive element in the 3′-untranslated region of the murine cyclooxygenase-2 mRNA. J. Biol. Chem. 279:8196–8205.
   PubMedGoogle Scholar
• Cok, S. J., and A. R. Morrison. 2001. The 3′-untranslated region of murine cyclooxygenase-2 contains multiple regulatory elements that alter message stability and translational efficiency. J. Biol. Chem. 276:23179–23185.
   PubMed Web of Science ®Google Scholar
• Czeczot, H., B. Tudek, J. Kusztelak, T. Szymczyk, B. Dobrowolska, G. Glinkowska, J. Malinowski, and H. Strzelecka. 1990. Isolation and studies of the mutagenic activity in the Ames test of flavonoids naturally occurring in medical herbs. Mutat. Res. 240:209–216.
   PubMed Web of Science ®Google Scholar
• Derrigo, M., A. Cestelli, G. Savettieri, and I. Di Liegro. 2000. RNA-protein interactions in the control of stability and localization of messenger RNA. Int. J. Mol. Med. 5:111–123.
   PubMedGoogle Scholar
• Dixon, D. A. 2004. Dysregulated post-transcriptional control of COX-2 gene expression in cancer. Curr. Pharm. Des. 10:635–646.
   PubMed Web of Science ®Google Scholar
• Dixon, D. A., G. C. Balch, N. Kedersha, P. Anderson, G. A. Zimmerman, R. D. Beauchamp, and S. M. Prescott. 2003. Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1. J. Exp. Med. 198:475–481.
   PubMed Web of Science ®Google Scholar
• Dixon, D. A., N. D. Tolley, P. H. King, L. B. Nabors, T. M. McIntyre, G. A. Zimmerman, and S. M. Prescott. 2001. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Investig. 108:1657–1665.
   PubMed Web of Science ®Google Scholar
• Dreyfuss, G., V. N. Kim, and N. Kataoka. 2002. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3:195–205.
   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
• Fischer, S. M., C. J. Conti, J. Viner, C. M. Aldaz, and R. A. Lubet. 2003. Celecoxib and difluoromethylornithine in combination have strong therapeutic activity against UV-induced skin tumors in mice. Carcinogenesis 24:945–952.
   PubMed Web of Science ®Google Scholar
• Fotsis, T., M. S. Pepper, E. Aktas, S. Breit, S. Rasku, H. Adlercreutz, K. Wahala, R. Montesano, and L. Schweigerer. 1997. Flavonoids, dietary-derived inhibitors of cell proliferation and in vitro angiogenesis. Cancer Res. 57:2916–2921.
   PubMed Web of Science ®Google Scholar
• Gueydan, C., L. Droogmans, P. Chalon, G. Huez, D. Caput, and V. Kruys. 1999. Identification of TIAR as a protein binding to the translational regulatory AU-rich element of tumor necrosis factor alpha mRNA. J. Biol. Chem. 274:2322–2326.
   PubMedGoogle Scholar
• Hall, E. J., M. Astor, J. Bedford, C. Borek, S. B. Curtis, M. Fry, C. Geard, T. Hei, J. Mitchell, N. Oleinick, et al. 1988. Basic radiobiology. Am. J. Clin. Oncol. 11:220–252.
   PubMedGoogle Scholar
• Hamilton, B. J., C. M. Burns, R. C. Nichols, and W. F. Rigby. 1997. Modulation of AUUUA response element binding by heterogeneous nuclear ribonucleoprotein A1 in human T lymphocytes. The roles of cytoplasmic location, transcription, and phosphorylation. J. Biol. Chem. 272:28732–28741.
   PubMedGoogle Scholar
• Kandasamy, K., K. Joseph, K. Subramaniam, J. R. Raymond, and B. G. Tholanikunnel. 2005. Translational control of β2-adrenergic receptor mRNA by T-cell-restricted intracellular antigen-related protein. J. Biol. Chem. 280:1931–1943.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kawai, T., J. Fan, K. Mazan-Mamczarz, and M. Gorospe. 2004. Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol. 24:6773–6787.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kawakami, A., Q. Tian, X. Duan, M. Streuli, S. F. Schlossman, and P. Anderson. 1992. Identification and functional characterization of a TIA-1-related nucleolysin. Proc. Natl. Acad. Sci. USA 89:8681–8685.
   PubMed Web of Science ®Google Scholar
• Kawamori, T., C. V. Rao, K. Seibert, and B. S. Reddy. 1998. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Res. 58:409–412.
   PubMed Web of Science ®Google Scholar
• Kedersha, N., and P. Anderson. 2002. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30:963–969.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kuo, M. L., and N. C. Yang. 1995. Reversion of v-H-ras-transformed NIH 3T3 cells by apigenin through inhibiting mitogen activated protein kinase and its downstream oncogenes. Biochem. Biophys. Res. Commun. 212:767–775.
   PubMedGoogle Scholar
• Kutchera, W., D. A. Jones, N. Matsunami, J. Groden, T. M. McIntyre, G. A. Zimmerman, R. L. White, and S. M. Prescott. 1996. Prostaglandin H synthase 2 is expressed abnormally in human colon cancer: evidence for a transcriptional effect. Proc. Natl. Acad. Sci. USA 93:4816–4820.
   PubMed Web of Science ®Google Scholar
• Lal, A., K. Abdelmohsen, R. Pullmann, T. Kawai, S. Galban, X. Yang, G. Brewer, and M. Gorospe. 2006. Posttranscriptional derepression of GADD45α by genotoxic stress. Mol. Cell 22:117–128.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Le Guiner, C., F. Lejeune, D. Galiana, L. Kister, R. Breathnach, J. Stevenin, and F. Del Gatto-Konczak. 2001. TIA-1 and TIAR activate splicing of alternative exons with weak 5′ splice sites followed by a U-rich stretch on their own pre-mRNAs. J. Biol. Chem. 276:40638–40646.
   PubMed Web of Science ®Google Scholar
• Lepley, D. M., and J. C. Pelling. 1997. Induction of p21/WAF1 and G1 cell-cycle arrest by the chemopreventive agent apigenin. Mol. Carcinog. 19:74–82.
   PubMed Web of Science ®Google Scholar
• Liang, Y. C., Y. T. Huang, S. H. Tsai, S. Y. Lin-Shiau, C. F. Chen, and J. K. Lin. 1999. Suppression of inducible cyclooxygenase and inducible nitric oxide synthase by apigenin and related flavonoids in mouse macrophages. Carcinogenesis 20:1945–1952.
   PubMed Web of Science ®Google Scholar
• Lin, H. J., K. M. Lakkides, T. O. Keku, S. T. Reddy, A. D. Louie, I. H. Kau, H. Zhou, J. S. Gim, H. L. Ma, C. F. Matthies, A. Dai, H. F. Huang, A. M. Materi, J. H. Lin, H. D. Frankl, E. R. Lee, S. I. Hardy, H. R. Herschman, B. E. Henderson, L. N. Kolonel, L. Le Marchand, R. M. Garavito, R. S. Sandler, R. W. Haile, and W. L. Smith. 2002. Prostaglandin H synthase 2 variant (Val511Ala) in African Americans may reduce the risk for colorectal neoplasia. Cancer Epidemiol. Biomarkers Prev. 11:1305–1315.
   PubMed Web of Science ®Google Scholar
• Loflin, P., C. Y. Chen, and A. B. Shyu. 1999. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes Dev. 13:1884–1897.
   PubMed Web of Science ®Google Scholar
• Mahtani, K. R., M. Brook, J. L. Dean, G. Sully, J. Saklatvala, and A. R. Clark. 2001. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol. Cell. Biol. 21:6461–6469.
   PubMed Web of Science ®Google Scholar
• Mazan-Mamczarz, K., S. Galban, I. Lopez 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.
   PubMed Web of Science ®Google Scholar
• Mazan-Mamczarz, K., A. Lal, J. L. Martindale, T. Kawai, and M. Gorospe. 2006. Translational repression by RNA-binding protein TIAR. Mol. Cell. Biol. 26:2716–2727.
   PubMed Web of Science ®Google Scholar
• McVean, M., H. Xiao, K. Isobe, and J. C. Pelling. 2000. Increase in wild-type p53 stability and transactivational activity by the chemopreventive agent apigenin in keratinocytes. Carcinogenesis. 21:633–639.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Moos, P. J., D. T. Muskardin, and F. A. Fitzpatrick. 1999. Effect of taxol and taxotere on gene expression in macrophages: induction of the prostaglandin H synthase-2 isoenzyme. J. Immunol. 162:467–473.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay, D., C. W. Houchen, S. Kennedy, B. K. Dieckgraefe, and S. Anant. 2003. Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol. Cell 11:113–126.
   PubMed Web of Science ®Google Scholar
• Muller-Decker, K., G. Neufang, I. Berger, M. Neumann, F. Marks, and G. Furstenberger. 2002. Transgenic cyclooxygenase-2 overexpression sensitizes mouse skin for carcinogenesis. Proc. Natl. Acad. Sci. USA 99:12483–12488.
   PubMed Web of Science ®Google Scholar
• Oshima, M., J. E. Dinchuk, S. L. Kargman, H. Oshima, B. Hancock, E. Kwong, J. M. Trzaskos, J. F. Evans, and M. M. Taketo. 1996. Suppression of intestinal polyposis in Apc Δ716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell 87:803–809.
   PubMed Web of Science ®Google Scholar
• Otto, J. C., D. L. DeWitt, and W. L. Smith. 1993. N-glycosylation of prostaglandin endoperoxide synthases-1 and -2 and their orientations in the endoplasmic reticulum. J. Biol. Chem. 268:18234–18242.
   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
• Pentland, A. P., J. W. Schoggins, G. A. Scott, K. N. Khan, and R. Han. 1999. Reduction of UV-induced skin tumors in hairless mice by selective COX-2 inhibition. Carcinogenesis 20:1939–1944.
   PubMed Web of Science ®Google Scholar
• Piecyk, M., S. Wax, A. R. Beck, N. Kedersha, M. Gupta, B. Maritim, S. Chen, C. Gueydan, V. Kruys, M. Streuli, and P. Anderson. 2000. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J. 19:4154–4163.
   PubMed Web of Science ®Google Scholar
• Raso, G. M., R. Meli, G. Di Carlo, M. Pacilio, and R. Di Carlo. 2001. Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 expression by flavonoids in macrophage J774A.1. Life Sci. 68:921–931.
   PubMed Web of Science ®Google Scholar
• Sengupta, S., B. C. Jang, M. T. Wu, J. H. Paik, H. Furneaux, and T. Hla. 2003. The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J. Biol. Chem. 278:25227–25233.
   PubMedGoogle Scholar
• Smith, W. L., R. M. Garavito, and D. L. DeWitt. 1996. Prostaglandin endoperoxide H synthases (cyclooxygenases)-1 and -2. J. Biol. Chem. 271:33157–33160.
   PubMed Web of Science ®Google Scholar
• Spirio, L. N., D. A. Dixon, J. Robertson, M. Robertson, J. Barrows, E. Traer, R. W. Burt, M. F. Leppert, R. White, and S. M. Prescott. 1998. The inducible prostaglandin biosynthetic enzyme, cyclooxygenase 2, is not mutated in patients with attenuated adenomatous polyposis coli. Cancer Res. 58:4909–4912.
   PubMed Web of Science ®Google Scholar
• Strickland, J. E., D. A. Greenhalgh, A. Koceva-Chyla, H. Hennings, C. Restrepo, M. Balaschak, and S. H. Yuspa. 1988. Development of murine epidermal cell lines which contain an activated ras Ha oncogene and form papillomas in skin grafts on athymic nude mouse hosts. Cancer Res. 48:165–169.
   PubMedGoogle Scholar
• Subbaramaiah, K., T. P. Marmo, 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.
   PubMed Web of Science ®Google Scholar
• Taupin, J. L., Q. Tian, N. Kedersha, M. Robertson, and P. Anderson. 1995. The RNA-binding protein TIAR is translocated from the nucleus to the cytoplasm during Fas-mediated apoptotic cell death. Proc. Natl. Acad. Sci. USA 92:1629–1633.
   PubMedGoogle Scholar
• Thun, M. J., M. M. Namboodiri, and C. W. Heath, Jr. 1991. Aspirin use and reduced risk of fatal colon cancer. N. Engl. J. Med. 325:1593–1596.
   PubMed Web of Science ®Google Scholar
• Tiano, H. F., C. D. Loftin, J. Akunda, C. A. Lee, J. Spalding, A. Sessoms, D. B. Dunson, E. G. Rogan, S. G. Morham, R. C. Smart, and R. Langenbach. 2002. Deficiency of either cyclooxygenase (COX)-1 or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res. 62:3395–3401.
   PubMed Web of Science ®Google Scholar
• Ulrich, C. M., J. Bigler, and J. D. Potter. 2006. Non-steroidal anti-inflammatory drugs for cancer prevention: promise, perils and pharmacogenetics. Nat. Rev. Cancer 6:130–140.
   PubMed Web of Science ®Google Scholar
• Van Dross, R., X. Hong, S. Essengue, S. M. Fischer, and J. C. Pelling. Modulation of UVB-induced and basal cyclooxygenase-2 (COX-2) expression by apigenin in mouse keratinocytes: role of USF transcription factors. Mol. Carcinog., in press.
   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
• Wei, H., L. Tye, E. Bresnick, and D. F. Birt. 1990. Inhibitory effect of apigenin, a plant flavonoid, on epidermal ornithine decarboxylase and skin tumor promotion in mice. Cancer Res. 50:499–502.
   PubMed Web of Science ®Google Scholar
• Williams, C. S., M. Mann, and R. N. DuBois. 1999. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18:7908–7916.
   PubMed Web of Science ®Google Scholar
• Yu, Q., S. J. Cok, C. Zeng, and A. R. Morrison. 2003. Translational repression of human matrix metalloproteinases-13 by an alternatively spliced form of T-cell-restricted intracellular antigen-related protein (TIAR). J. Biol. Chem. 278:1579–1584.
   PubMed Web of Science ®Google Scholar
• Zhang, W., B. J. Wagner, K. Ehrenman, A. W. Schaefer, C. T. DeMaria, D. Crater, K. DeHaven, L. Long, and G. Brewer. 1993. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13:7652–7665.
   PubMed Web of Science ®Google Scholar