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Induction of Cyclin D1 Proteasomal Degradation by Branch Extracts from Abeliophyllum distichum Nakai in Human Colorectal Cancer Cells

  • Park, Gwang Hun ;
  • Park, Jae Ho ;
  • Jeong, Jin Boo
  • Received : 2015.06.12
  • Accepted : 2015.09.20
  • Published : 2015.12.31

Abstract

Abeliophyllum distichum Nakai (A. distichum) has been reported to exert the inhibitory effect on angiotensin converting enzyme and aldose reductase. Recently, our group found that branch extracts of A. distichum (EAFAD-B) induce apoptosis through ATF3 activation in human colon cancer cells. However, anti-cancer reagents exert their activity through the regulation of various molecular targets. Therefore, the elucidation of potential mechanisms of EAFAD-B for anti-cancer activity may be necessary. To elucidate the potential mechanism of EAFAD-B for anti-cancer activity, we evaluated the regulation of cyclin D1 in human colon cancer cells. EAFAD-B decreased cellular accumulation of cyclin D1 protein. However, cyclin D1 mRNA was not changed by EAFAD-B. Inhibition of proteasomal degradation by MG132 attenuated EAFAD-B-mediated cyclin D1 downregulation and the half-life of cyclin D1 was decreased in the cells treated with EAFAD-B. In addition, EAFAD-B induced cyclin D1 phosphorylation at threonine-286 and the point mutation of threonine-286 to alanine attenuated EAFAD-B-mediated cyclin D1 proteasomal degradation. Inhibitions of both ERK1/2 by PD98059 and NF-κB by a selective inhibitor, BAY 11-7082 suppressed cyclin D1 downregulation by EAFAD-B. From these results, we suggest that EAFAD-B-mediated cyclin D1 downregulation may result from proteasomal degradation through its threonine-286 phosphorylation via ERK1/2-dependent NF-κB activation. The current study provides new mechanistic link between EAFAD-B and anti-cancer activity in human colon cancer cells.

Keywords

Abeliophyllum distichum Nakai;Cyclin D1;Proteasomal degradation;Cancer prevention;Colon cancer

References

  1. Diehl, J.A., F. Zindy and C.J. Sherr. 1997. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 11:957-972. https://doi.org/10.1101/gad.11.8.957
  2. Diehl, J.A., M. Cheng, M.F. Roussel and C.J. Sherr. 1998. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 12:3499-3511. https://doi.org/10.1101/gad.12.22.3499
  3. Benzeno, S., F. Lu, M. Guo, O. Barbash, F. Zhang, J.G. Herman, P.S. Klein, A. Rustgi and J.A. Diehl. 2006. Identification of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene 25:6291-6303. https://doi.org/10.1038/sj.onc.1209644
  4. Bahnassy, A.A., A.R.N. Zekri, S. El-Houssini, A.M.R. El-Shehaby, M.R. Mahmoud, S. Abdallah and M. El-Serafi. 2004. Cyclin A and cyclin D1 as significant prognostic markers in colorectal cancer patients. BMC Gastroenterol. 4:22. https://doi.org/10.1186/1471-230X-4-22
  5. Alao, J.P., A.V. Stavropoulou, E.W. Lam, R.C. Coombes and D.M. Vigushin. 2006. Histone deacetylase inhibitor, trichostatin A induces ubiquitin-dependent cyclin D1 degradation in MCF-7 breast cancer cells. Mol. Cancer 5:8.
  6. Alao, J.P., E.W. Lam, S. Ali, L. Buluwela, W. Bordogna, P. Lockey, R. Varshochi, A.V. Stavropoulou, R.C. Coombes and D.M. Vigushin. 2004. Histone deacetylase inhibitor trichostatin A represses estrogen receptor alpha-dependent transcription and promotes proteasomal degradation of cyclin D1 in human breast carcinoma cell lines. Clin. Cancer Res. 10:8094-8104. https://doi.org/10.1158/1078-0432.CCR-04-1023
  7. Alao, J.P. 2007. The regulation of cyclin D1 degradation: roles in cancer development and the potential for therapeutic invention. Mol. Cancer 6:24.
  8. Li, H.M., J.K. Kim, J.M. Jang, C.B. Cui and S.S. Lim. 2013. Analysis of the inhibitory activity of Abeliophyllum distichum leaf constituents against aldose reductase by using high-speed counter current chromatography. Arch. Pharm. Res. 36:1104-1112. https://doi.org/10.1007/s12272-013-0127-1
  9. Lee, K.W., H.J. Kim, Y.S. Lee, H.J. Park, J.W. Choi, J. Ha and K.T. Lee. 2007. Acteoside inhibits human promyelocytic HL-60 leukemia cell proliferation via inducing cell cycle arrest at G0/G1 phase and differentiation into monocyte. Carcinogenesis 28:1928-1936. https://doi.org/10.1093/carcin/bgm126
  10. Langenfeld, J., H. Kiyokawa, D. Sekula, J. Boyle and E. Dmitrovsky. 1997. Posttranslational regulation of cyclin D1 by retinoic acid: a chemoprevention mechanism. Proc. Natl. Acad. Sci. USA. 94:12070-12074. https://doi.org/10.1073/pnas.94.22.12070
  11. Kwak, Y.T., R. Li, C.R. Becerra, D. Tripathy, E.P. Frenkel and U.N. Verma. 2005. IkappaB kinase alpha regulates subcellular distribution and turnover of cyclin D1 by phosphorylation. J. Biol. Chem. 280:33945-33952. https://doi.org/10.1074/jbc.M506206200
  12. Kim, H.J., N. Hawke and A.S. Baldwin. 2006. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ. 13:738-747. https://doi.org/10.1038/sj.cdd.4401877
  13. Kato, J., H. Matsushime, S.W. Hiebert, M.E. Ewen and C.J. Sherr. 1993. Direct binding of cyclin D to the retinoblastoma gene product (pRb) and pRb phosphorylation by the cyclin D-dependent kinase CDK4. Genes Dev. 7:331-342. https://doi.org/10.1101/gad.7.3.331
  14. Jeong, J.B., X. Yang, C. Ruth, J. Choi, S.J. Baek and S.H. Lee. 2013. A mechanistic study of the proapoptotic effect of tolfenamic acid: involvement of NF-κB activation. Carcinogenesis 34:2350-2360. https://doi.org/10.1093/carcin/bgt224
  15. Holland, T.A., J. Elder, J.M. McCloud, C. Hall, M. Deakin, A.A. Fryer, J.B. Elder and P.R. Hoban. Subcellular localisation of cyclin D1 protein in colorectal tumours is associated with p21 (WAF1/CIP1) expression and correlates with patient survival. Int. J. Cancer 95:302-306. https://doi.org/10.1002/1097-0215(20010920)95:5<302::AID-IJC1052>3.0.CO;2-#
  16. Thoms, H.C., M.G. Dunlop and L.A. Stark. 2007. p38-mediated inactivation of cyclin D1/cyclin-dependent kinase 4 stimulates nucleolar translocation of RelA and apoptosis in colorectal cancer cells. Cancer Res. 67:1660-1669. https://doi.org/10.1158/0008-5472.CAN-06-1038
  17. Stark, L.A., F.V. Din, R.M. Zwacka and M.G. Dunlop. 2001. Aspirin-induced activation of the NF-kappaB signaling pathway: a novel mechanism for aspirin-mediated apoptosis in colon cancer cells. FASEB J. 15:1273-1275. https://doi.org/10.1096/fj.00-0529fje
  18. Spinella, M.J., S.J. Freemantle, D. Sekula, J.H. Chang, A.J. Christie and E. Dmitrovsky. 1999. Retinoic acid promotes ubiquitination and proteolysis of cyclin D1 during induced tumor cell differentiation. J. Biol. Chem. 274:22013-22018. https://doi.org/10.1074/jbc.274.31.22013
  19. Shao, H.J., Z. Lou, J.B. Jeong, K.J. Kim, J. Lee and S.H. Lee. 2015. Tolfenamic acid suppresses inflammatory-mediated activation of NF-κB signaling. Biomol. Ther. 23:39-44. https://doi.org/10.4062/biomolther.2014.088
  20. Park, G.H., J.H. Park, H.J. Eo, H.M. Song, M.H. Lee, J.R. Lee and J.B. Jeong. 2014b. Anti-inflammatory effect of the extracts from Abeliophyllum distichum Nakai in LPSstimulated RAW264.7 cells. Korean J. Plant Res. 27:209-214. https://doi.org/10.7732/kjpr.2014.27.3.209
  21. Park, G.H., J.H. Park, H.J. Eo, H.M. Song, S.H. Woo, M.K. Kim, J.W. Lee, M.H. Lee, J.R. Lee, J.S. Koo and J.B. Jeong. 2014a. The induction of activating transcription factor 3 (ATF3) contributes to anti-cancer activity of Abeliophyllum distichum Nakai in human colorectal cancer cells. BMC Complementary Alt. Med. 14:487. https://doi.org/10.1186/1472-6882-14-487
  22. Okabe, H., S.H. Lee, J. Phuchareon, D.G. Albertson, F. McCormick and O. Tetsu. 2006 A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PloS One 1:e128. https://doi.org/10.1371/journal.pone.0000128
  23. Oh, H., D.G. Kang, T.O. Kwon, K.K. Jang, K.Y. Chai, Y.G. Yun, H.T. Chung and H.S. Lee. 2003. Four glycosides from the leaves of Abeliophyllum distichum with inhibitory effects on angiotensin converting enzyme. Phytother. Res. 17:811-819. https://doi.org/10.1002/ptr.1199
  24. Weinberg, R.A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330. https://doi.org/10.1016/0092-8674(95)90385-2
  25. Verma, I.M. 2004. Nuclear factor (NF)-kappaB proteins: therapeutic targets. Ann. Rheum. Dis. 63:57-61.