DOI QR코드

DOI QR Code

CYP1B1 Activates Wnt/β-Catenin Signaling through Suppression of Herc5-Mediated ISGylation for Protein Degradation on β-Catenin in HeLa Cells

  • 투고 : 2017.06.12
  • 심사 : 2017.06.19
  • 발행 : 2017.07.15

초록

Cytochrome P450 1B1 (CYP1B1) acts as a hydroxylase for estrogen and activates potential carcinogens. Moreover, its expression in tumor tissues is much higher than that in normal tissues. Despite this association between CYP1B1 and cancer, the detailed molecular mechanism of CYP1B1 on cancer progression in HeLa cells remains unknown. Previous reports indicated that the mRNA expression level of Herc5, an E3 ligase for ISGylation, is promoted by CYP1B1 suppression using specific small interfering RNA, and that ISGylation may be involved in ubiquitination related to ${\beta}-catenin$ degradation. With this background, we investigated the relationships among CYP1B1, Herc5, and ${\beta}-catenin$. RT-PCR and western blot analyses showed that CYP1B1 overexpression induced and CYP1B1 inhibition reduced, respectively, the expression of $Wnt/{\beta}-catenin$ signaling target genes including ${\beta}-catenin$ and cyclin D1. Moreover, HeLa cells were treated with the CYP1B1 inducer $7,12-dimethylbenz[{\alpha}]anthracene$ (DMBA) or the CYP1B1 specific inhibitor, tetramethoxystilbene (TMS) and consequently DMBA increased and TMS decreased ${\beta}-catenin$ and cyclin D1 expression, respectively. To determine the correlation between CYP1B1 expression and ISGylation, the expression of ISG15, a ubiquitin-like protein, was detected following CYP1B1 regulation, which revealed that CYP1B1 may inhibit ISGylation through suppression of ISG15 expression. In addition, the mRNA and protein expression levels of Herc5 were strongly suppressed by CYP1B1. Finally, an immunoprecipitation assay revealed a direct physical interaction between Herc5 and ${\beta}-catenin$ in HeLa cells. In conclusion, these data suggest that CYP1B1 may activate $Wnt/{\beta}-catenin$ signaling through stabilization of ${\beta}-catenin$ protein from Herc5-mediated ISGylation for proteosomal degradation.

키워드

참고문헌

  1. Nelson, D.R., Koymans, L., Kamataki, T., Stegeman, J.J., Feyereisen, R., Waxman, D.J., Waterman, M.R., Gotoh, O., Coon, M.J., Estabrook, R.W., Gunsalus, I.C. and Nebert, D.W. (1996) P450 superfamily: update on new sequences, gene mapping, accession numbers and nomenclature. Pharmacogenetics, 6, 1-42. https://doi.org/10.1097/00008571-199602000-00002
  2. Yang, X., Zhang, B., Molony, C., Chudin, E., Hao, K., Zhu, J., Gaedigk, A., Suver, C., Zhong, H., Leeder, J.S., Guengerich, F.P., Strom, S.C., Schuetz, E., Rushmore, T.H., Ulrich, R.G., Slatter, J.G., Schadt, E.E., Kasarskis, A. and Lum, P.Y. (2010) Systematic genetic and genomic analysis of cytochrome P450 enzyme activities in human liver. Genome Res., 20, 1020-1036. https://doi.org/10.1101/gr.103341.109
  3. Shimada, T. (2017) Inhibition of carcinogen-activating cytochrome P450 enzymes by xenobiotic chemicals in relation to antimutagenicity and anticarcinogenicity. Toxicol. Res., 33, 79-96. https://doi.org/10.5487/TR.2017.33.2.079
  4. Saini, S., Hirata, H., Majid, S. and Dahiya, R. (2009) Functional significance of cytochrome P450 1B1 in endometrial carcinogenesis. Cancer Res., 69, 7038-7045. https://doi.org/10.1158/0008-5472.CAN-09-1691
  5. Delvoux, B., Groothuis, P., D'Hooghe, T., Kyama, C., Dunselman, G. and Romano, A. (2009) Increased production of $17{\beta}$-estradiol in endometriosis lesions is the result of impaired metabolism. J. Clin. Endocrinol. Metab., 94, 876-883. https://doi.org/10.1210/jc.2008-2218
  6. Piotrowska, H., Kucinska, M. and Murias, M. (2013) Expression of CYP1A1, CYP1B1 and MnSOD in a panel of human cancer cell lines. Mol. Cell. Biochem., 383, 95-102. https://doi.org/10.1007/s11010-013-1758-8
  7. Barnett, J.A., Urbauer, D.L., Murray, G.I., Fuller, G.N. and Heimberger, A.B. (2007) Cytochrome P450 1B1 expression in glial cell tumors: an immunotherapeutic target. Clin. Cancer Res., 13, 3559-3567. https://doi.org/10.1158/1078-0432.CCR-06-2430
  8. Akiyama, T. (2000) Wnt/${\beta}$-catenin signaling. Cytokine Growth Factor Rev., 11, 273-282. https://doi.org/10.1016/S1359-6101(00)00011-3
  9. Clevers, H. (2006) Wnt/${\beta}$-catenin signaling in development and disease. Cell, 127, 469-480. https://doi.org/10.1016/j.cell.2006.10.018
  10. Konigshoff, M. and Eickelberg, O. (2010) WNT signaling in lung disease: a failure or a regeneration signal? Am. J. Respir. Cell Mol. Biol., 42, 21-31. https://doi.org/10.1165/rcmb.2008-0485TR
  11. Kim, W., Kim, M. and Jho, E.H. (2013) Wnt/${\beta}$-catenin signalling: from plasma membrane to nucleus. Biochem. J., 450, 9-21. https://doi.org/10.1042/BJ20121284
  12. Lee, J., Li, L., Gretz, N., Gebert, J. and Dihlmann, S. (2012) Absent in Melanoma 2 (AIM2) is an important mediator of interferon-dependent and -independent HLA-DRA and HLADRB gene expression in colorectal cancers. Oncogene, 31, 1242-1253. https://doi.org/10.1038/onc.2011.320
  13. Narasimhan, J., Wang, M., Fu, Z., Klein, J.M., Haas, A.L. and Kim, J.J. (2005) Crystal structure of the interferon-induced ubiquitin-like protein ISG15. J. Biol. Chem., 280, 27356-27365. https://doi.org/10.1074/jbc.M502814200
  14. Dastur, A., Beaudenon, S., Kelley, M., Krug, R.M. and Huibregtse, J.M. (2006) Herc5, an interferon-induced HECT E3 enzyme, is required for conjugation of ISG15 in human cells. J. Biol. Chem., 281, 4334-4338. https://doi.org/10.1074/jbc.M512830200
  15. Shi, H.X., Yang, K., Liu, X., Liu, X.Y., Wei, B., Shan, Y.F., Zhu, L.H. and Wang, C. (2010) Positive regulation of interferon regulatory factor 3 activation by Herc5 via ISG15 modification. Mol. Cell. Biol., 30, 2424-2436. https://doi.org/10.1128/MCB.01466-09
  16. Skaug, B. and Chen, Z.J. (2010) Emerging role of ISG15 in antiviral immunity. Cell, 143, 187-190. https://doi.org/10.1016/j.cell.2010.09.033
  17. Durfee, L.A., Lyon, N., Seo, K. and Huibregtse, J.M. (2010) The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell, 38, 722-732. https://doi.org/10.1016/j.molcel.2010.05.002
  18. Hochrainer, K., Mayer, H., Baranyi, U., Binder, B., Lipp, J. and Kroismayr, R. (2005) The human HERC family of ubiquitin ligases: novel members, genomic organization, expression profiling, and evolutionary aspects. Genomics, 85, 153-164. https://doi.org/10.1016/j.ygeno.2004.10.006
  19. Cruz, C., Ventura, F., Bartrons, R. and Rosa, J.L. (2001) HERC3 binding to and regulation by ubiquitin. FEBS Lett., 488, 74-80. https://doi.org/10.1016/S0014-5793(00)02371-1
  20. Wong, J.J., Pung, Y.F., Sze, N.S. and Chin, K.C. (2006) HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc. Natl. Acad. Sci. U.S.A., 103, 10735-10740. https://doi.org/10.1073/pnas.0600397103
  21. Kroismayr, R., Baranyi, U., Stehlik, C., Dorfleutner, A., Binder, B.R. and Lipp, J. (2004) HERC5, a HECT E3 ubiquitin ligase tightly regulated in LPS activated endothelial cells. J. Cell Sci., 117, 4749-4756. https://doi.org/10.1242/jcs.01338
  22. Liu, C., Kato, Y., Zhang, Z., Do, V.M., Yankner, B.A. and He, X. (1999) ${\beta}$-Trcp couples ${\beta}$-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc. Natl. Acad. Sci. U.S.A., 96, 6273-6278. https://doi.org/10.1073/pnas.96.11.6273
  23. Lee, J.H., Bae, J.A., Lee, J.H., Seo, Y.W., Kho, D.H., Sun, E.G., Lee, S.E., Cho, S.H., Joo, Y.E., Ahn, K.Y., Chung, I.J. and Kim, K.K. (2010) Glycoprotein 90K, downregulated in advanced colorectal cancer tissues, interacts with CD9/CD82 and suppresses the Wnt/${\beta}$-catenin signal via ISGylation of ${\beta}$-catenin. Gut, 59, 907-917. https://doi.org/10.1136/gut.2009.194068
  24. Gribben, J.G., Ryan, D.P., Boyajian, R., Urban, R.G., Hedley, M.L., Beach, K., Nealon, P., Matulonis, U., Campos, S., Gilligan, T.D., Richardson, P.G., Marshall, B., Neuberg, D. and Nadler, L.M. (2005) Unexpected association between induction of immunity to the universal tumor antigen CYP1B1 and response to next therapy. Clin. Cancer Res., 11, 4430-4436. https://doi.org/10.1158/1078-0432.CCR-04-2111
  25. Shimada, T., Hayes, C.L., Yamazaki, H., Amin, S., Hecht, S.S., Guengerich, F.P. and Sutter, T.R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res., 56, 2979-2984.
  26. Murray, G.I., Taylor, M.C., McFadyen, M.C., McKay, J.A., Greenlee, W.F., Burke, M.D. and Melvin, W.T. (1997) Tumorspecific expression of cytochrome P450 CYP1B1. Cancer Res., 57, 3026-3031.
  27. Tsuchiya, Y., Nakajima, M., Kyo, S., Kanaya, T., Inoue, M. and Yokoi, T. (2004) Human CYP1B1 is regulated by estradiol via estrogen receptor. Cancer Res., 64, 3119-3125. https://doi.org/10.1158/0008-5472.CAN-04-0166
  28. Goodin, M.G., Fertuck, K.C., Zacharewski, T.R. and Rosengren, R.J. (2002) Estrogen receptor-mediated actions of polyphenolic catechins in vivo and in vitro. Toxicol. Sci., 69, 354-361. https://doi.org/10.1093/toxsci/69.2.354
  29. Nakajima, M., Iwanari, M. and Yokoi, T. (2003) Effects of histone deacetylation and DNA methylation on the constitutive and TCDD-inducible expressions of the human CYP1 family in MCF-7 and HeLa cells. Toxicol. Lett., 144, 247-256. https://doi.org/10.1016/S0378-4274(03)00216-9
  30. Heidel, S.M., Czuprynski, C.J. and Jefcoate, C.R. (1998) Bone marrow stromal cells constitutively express high levels of cytochrome P4501B1 that metabolize 7,12-dimethylbenz[a]anthracene. Mol. Pharmacol., 54, 1000-1006. https://doi.org/10.1124/mol.54.6.1000
  31. Chun, Y.J. and Kim, S. (2003) Discovery of cytochrome P450 1B1 inhibitors as new promising anti-cancer agents. Med. Res. Rev., 23, 657-668. https://doi.org/10.1002/med.10050
  32. Chun, Y.J., Lee, S.K. and Kim, M.Y. (2005) Modulation of human cytochrome P450 1B1 expression by 2,4,3',5'-tetramethoxystilbene. Drug Metab. Dispos., 33, 1771-1776.
  33. Zou, W., Papov, V., Malakhova, O., Kim, K.I., Dao, C., Li, J. and Zhang, D.E. (2005) ISG15 modification of ubiquitin E2 Ubc13 disrupts its ability to form thioester bond with ubiquitin. Biochem. Biophys. Res. Commun., 336, 61-68. https://doi.org/10.1016/j.bbrc.2005.08.038

피인용 문헌

  1. Volasertib Enhances Sensitivity to TRAIL in Renal Carcinoma Caki Cells through Downregulation of c-FLIP Expression vol.18, pp.12, 2017, https://doi.org/10.3390/ijms18122568
  2. Angelicin potentiates TRAIL-induced apoptosis in renal carcinoma Caki cells through activation of caspase 3 and down-regulation of c-FLIP expression pp.02724391, 2017, https://doi.org/10.1002/ddr.21414
  3. Maritoclax Enhances TRAIL-Induced Apoptosis via CHOP-Mediated Upregulation of DR5 and miR-708-Mediated Downregulation of cFLIP vol.23, pp.11, 2018, https://doi.org/10.3390/molecules23113030
  4. HSP70 Acetylation Prevents Combined mTORC1/2 Inhibitor and Curcumin Treatment-Induced Apoptosis vol.23, pp.11, 2018, https://doi.org/10.3390/molecules23112755
  5. Cepharanthine Enhances TRAIL-Mediated Apoptosis Through STAMBPL1-Mediated Downregulation of Survivin Expression in Renal Carcinoma Cells vol.19, pp.10, 2018, https://doi.org/10.3390/ijms19103280
  6. Interferon-stimulated gene 15 enters posttranslational modifications of p53 pp.00219541, 2018, https://doi.org/10.1002/jcp.27347
  7. mTORC1/2 inhibitor and curcumin induce apoptosis through lysosomal membrane permeabilization-mediated autophagy vol.37, pp.38, 2018, https://doi.org/10.1038/s41388-018-0345-6
  8. Z-FL-COCHO, a cathepsin S inhibitor, enhances oxaliplatin-mediated apoptosis through the induction of endoplasmic reticulum stress vol.50, pp.8, 2018, https://doi.org/10.1038/s12276-018-0138-6
  9. Involvement of Up-Regulation of DR5 Expression and Down-Regulation of c-FLIP in Niclosamide-Mediated TRAIL Sensitization in Human Renal Carcinoma Caki Cells vol.23, pp.9, 2018, https://doi.org/10.3390/molecules23092264
  10. Garcinol Enhances TRAIL-Induced Apoptotic Cell Death through Up-Regulation of DR5 and Down-Regulation of c-FLIP Expression vol.23, pp.7, 2018, https://doi.org/10.3390/molecules23071614