Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2017, Article ID 3684581, 12 pages
https://doi.org/10.1155/2017/3684581
Research Article

Apigenin Inhibits Human SW620 Cell Growth by Targeting Polyamine Catabolism

1School of Chinese Herbology, Guangzhou University of Chinese Medicine, Guangdong Province, Guangzhou, China
2School of Pharmacy, Guangdong Pharmaceutical University, Guangdong Province, Guangzhou, China

Correspondence should be addressed to Guixiang Wang; moc.621@603gnaixiuggnaw

Received 26 January 2017; Revised 5 April 2017; Accepted 12 April 2017; Published 10 May 2017

Academic Editor: Kuzhuvelil B. Harikumar

Copyright © 2017 Jing Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. I. Choi, C. S. Jeong, S. Y. Cho, and Y. S. Lee, “Mechanism of apoptosis induced by apigenin in HepG2 human hepatoma cells: involvement of reactive oxygen species generated by NADPH oxidase,” Archives of Pharmacal Research, vol. 30, no. 10, pp. 1328–1335, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. C.-Y. Cheng, C.-C. Hu, H.-J. Yang, M.-C. Lee, and E.-S. Kao, “Inhibitory effects of scutellarein on proliferation of human lung cancer A549 cells through ERK and NFκB mediated by the EGFR pathway,” Chinese Journal of Physiology, vol. 57, no. 4, pp. 182–187, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. W. Lim, S. Park, F. W. Bazer, and G. Song, “Apigenin reduces survival of choriocarcinoma cells by inducing apoptosis via the PI3K/AKT and ERK1/2 MAPK pathways,” Journal of Cellular Physiology, vol. 231, no. 12, pp. 2690–2699, 2016. View at Publisher · View at Google Scholar · View at Scopus
  4. M. A. Hasnat, M. Pervin, J. H. Lim, and B. O. Lim, “Apigenin attenuates melanoma cell migration by inducing anoikis through integrin and focal adhesion kinase inhibition,” Molecules, vol. 20, no. 12, pp. 21157–21166, 2015. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Pham, M. Chen, H. Takahashi et al., “Apigenin inhibits NNK-induced focal adhesion kinase activation in pancreatic cancer cells,” Pancreas, vol. 41, no. 8, pp. 1306–1315, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. R. S. Sulaiman, H. D. Basavarajappa, and T. W. Corson, “Natural product inhibitors of ocular angiogenesis,” Experimental Eye Research, vol. 129, pp. 161–171, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Lee, B. Sung, Y. J. Kang et al., “Apigenin-induced apoptosis is enhanced by inhibition of autophagy formation in HCT116 human colon cancer cells,” International Journal of Oncology, vol. 44, no. 5, pp. 1599–1606, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. R. A. Casero and L. J. Marton, “Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases,” Nature Reviews Drug Discovery, vol. 6, no. 5, pp. 373–390, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Larqué, M. Sabater-Molina, and S. Zamora, “Biological significance of dietary polyamines,” Nutrition, vol. 23, no. 1, pp. 87–95, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. R. A. Casero Jr., B. Frydman, T. M. Stewart, and P. M. Woster, “Significance of targeting polyamine metabolism as an antineoplastic strategy: Unique targets for polyamine analogues,” Proceedings of the Western Pharmacology Society, vol. 48, pp. 24–30, 2005. View at Google Scholar · View at Scopus
  11. C. Moinard, L. Cynober, and J.-P. de Bandt, “Polyamines: metabolism and implications in human diseases,” Clinical Nutrition, vol. 24, no. 2, pp. 184–197, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Seiler and F. Dezeure, “Polyamine transport in mammalian cells,” International Journal of Biochemistry, vol. 22, no. 3, pp. 211–218, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. V. Battaglia, C. DeStefano Shields, T. Murray-Stewart, and R. A. Casero Jr., “Polyamine catabolism in carcinogenesis: potential targets for chemotherapy and chemoprevention,” Amino Acids, vol. 46, no. 3, pp. 511–519, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Mohammed, N. B. Janakiram, V. Madka et al., “Eflornithine (DFMO) prevents progression of pancreatic cancer by modulating ornithine decarboxylase signaling,” Cancer Prevention Research, vol. 7, no. 12, pp. 1198–1209, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. R. Burns, G. F. Graminski, R. S. Weeks, Y. Chen, and T. G. O'Brien, “Lipophilic lysine-spermine conjugates are potent polyamine transport inhibitors for use in combination with a polyamine biosynthesis inhibitor,” Journal of Medicinal Chemistry, vol. 52, no. 7, pp. 1983–1993, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. A. E. Pegg and R. A. Casero Jr., “Current status of the polyamine research field,” in Polyamines, vol. 720 of Methods and Protocols, pp. 3–35, Humana Press, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Igarashi and K. Kashiwagi, “Modulation of cellular function by polyamines,” International Journal of Biochemistry and Cell Biology, vol. 42, no. 1, pp. 39–51, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. N. Lopatin, E. N. Makhina, and C. G. Nichols, “Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification,” Nature, vol. 372, no. 6504, pp. 366–369, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Williams, “Modulation and block of ion channels: a new biology of polyamines,” Cellular Signalling, vol. 9, no. 1, pp. 1–13, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. H. C. Ha, N. S. Sirisoma, P. Kuppusamy, J. L. Zweier, P. M. Woster, and R. A. Casero Jr., “The natural polyamine spermine functions directly as a free radical scavenger,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 19, pp. 11140–11145, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. H. T. Kurata, L. J. Marton, and C. G. Nichols, “The polyamine binding site in inward rectifier K+ channels,” Journal of General Physiology, vol. 127, no. 5, pp. 467–480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Kidd, L. H. Tang, S. W. Schmid et al., “A polyamine pathway-mediated mitogenic mechanism in enterochromaffin-like cells of Mastomys,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 275, no. 2, pp. G370–G376, 1998. View at Google Scholar · View at Scopus
  23. T. D. Johnson, “Modulation of channel function by polyamines,” Trends in Pharmacological Sciences, vol. 17, no. 1, pp. 22–26, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Seiler, “Thirty years of polyamine-related approaches to cancer therapy. Retrospect and prospect. Part 1. Selective enzyme inhibitors,” Current Drug Targets, vol. 4, no. 7, pp. 537–564, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Seiler, “Thirty years of polyamine-related approaches to cancer therapy. Retrospect and prospect. Part 2. Structural analogues and derivatives,” Current Drug Targets, vol. 4, no. 7, pp. 565–585, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. T. S. Weiss, G. Bernhardt, A. Buschauer et al., “Polyamine levels of human colorectal adenocarcinomas are correlated with tumor stage and grade,” International Journal of Colorectal Disease, vol. 17, no. 6, pp. 381–387, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. F. L. Meyskens and E. W. Gerner, “Development of difluoromethylornithine as a chemoprevention agent for the management of colon cancer,” Journal of Cellular Biochemistry, vol. 59, supplement 22, pp. 126–131, 1995. View at Publisher · View at Google Scholar · View at Scopus
  28. V. A. Levin, J. H. Uhm, K. A. Jaeckle et al., “Phase III randomized study of postradiotherapy chemotherapy with α-difluoromethylornithine-procarbazine, N-(2-chloroethyl)-N′-cyclohexyl-N-nitrosurea, vincristine (DFMO-PCV) versus PCV for glioblastoma multiforme,” Clinical Cancer Research, vol. 6, no. 10, pp. 3878–3884, 2000. View at Google Scholar · View at Scopus
  29. V. A. Levin, K. R. Hess, A. Choucair et al., “Phase III randomized study of postradiotherapy chemotherapy with combination α-difluoromethylornithine-PCV versus PCV for anaplastic gliomas,” Clinical Cancer Research, vol. 9, no. 3, pp. 981–990, 2003. View at Google Scholar · View at Scopus
  30. F. L. Meyskens Jr., C. E. McLaren, D. Pelot et al., “Difluoromethylornithine plus sulindac for the prevention of sporadic colorectal adenomas: a randomized placebo-controlled, double-blind trial,” Cancer Prevention Research, vol. 1, no. 1, pp. 32–38, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. A. E. Pegg, R. Madhubala, T. Kameji, and R. J. Bergeron, “Control of ornithine decarboxylase activity in α-difluoromethylornithine-resistant L1210 cells by polyamines and synthetic analogues,” Journal of Biological Chemistry, vol. 263, no. 22, pp. 11008–11014, 1988. View at Google Scholar · View at Scopus
  32. D. H. Russell, “Clinical relevance of polyamines as biochemical markers of tumor kinetics,” Clinical Chemistry, vol. 23, no. 1, pp. 22–27, 1977. View at Google Scholar · View at Scopus
  33. S. Sarhan, B. Knödgen, and N. Seiler, “Polyamine deprivation, malnutrition and tumor growth,” Anticancer Research, vol. 12, no. 2, pp. 457–466, 1991. View at Google Scholar · View at Scopus
  34. N. Seiler, S. Sarhan, C. Grauffel et al., “Endogenous and exogenous polyamines in support of tumor growth,” Cancer Research, vol. 50, no. 16, pp. 5077–5083, 1990. View at Google Scholar · View at Scopus
  35. A. Ask, L. Persson, and O. Heby, “Increased survival of L1210 leukemic mice by prevention of the utilization of extracellular polyamines. Studies using a polyamineuptake mutant, antibiotics and a polyamine-deficient diet,” Cancer Letters, vol. 66, no. 1, pp. 29–34, 1992. View at Publisher · View at Google Scholar · View at Scopus
  36. A. E. Pegg, “Polyamine metabolism and its importance in neoplastic growth and as a target for chemotherapy,” Cancer Research, vol. 48, no. 4, pp. 759–774, 1988. View at Google Scholar · View at Scopus
  37. B. Toursarkissian, E. D. Endean, and S. M. Aziz, “Characterization of polyamine transport in rat aortic smooth muscle cells,” Journal of Surgical Research, vol. 57, no. 3, pp. 401–407, 1994. View at Publisher · View at Google Scholar · View at Scopus
  38. A. E. Pegg, “Spermidine/spermine-N1-acetyltransferase: a key metabolic regulator,” American Journal of Physiology—Endocrinology and Metabolism, vol. 294, no. 6, pp. E995–E1010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. S.-Q. Xie, Y.-H. Zhang, Q. Li et al., “COX-2-independent induction of apoptosis by celecoxib and polyamine naphthalimide conjugate mediated by polyamine depression in colorectal cancer cell lines,” International Journal of Colorectal Disease, vol. 27, no. 7, pp. 861–868, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. R. G. Schipper, L. C. Penning, and A. A. J. Verhofstad, “Involvement of polyamines in apoptosis. Facts and controversies: Effectors or protectors?” Seminars in Cancer Biology, vol. 10, no. 1, pp. 55–68, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Chopra and H. M. Wallace, “Induction of spermidine/spermine N1-acetyltransferase in human cancer cells in response to increased production of reactive oxygen species,” Biochemical Pharmacology, vol. 55, no. 7, pp. 1119–1123, 1998. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Schreck, P. Rieber, and P. A. Baeuerle, “Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1,” EMBO Journal, vol. 10, no. 8, p. 2247, 1991. View at Google Scholar · View at Scopus
  43. R. E. Parchment, “The implications of a unified theory of programmed cell death, polyamines, oxyradicals and histogenesis in the embryo,” International Journal of Developmental Biology, vol. 37, no. 1, pp. 75–83, 2003. View at Google Scholar
  44. Y. Wang, W. Devereux, P. M. Woster et al., “Cloning and characterization of a human polyamine oxidase that is inducible by polyamine analogue exposure,” Cancer Research, vol. 61, no. 14, pp. 5370–5373, 2001. View at Google Scholar
  45. I. Matsui, L. Wiegand, and A. E. Pegg, “Properties of spermidine N-acetyltransferase from livers of rats treated with carbon tetrachloride and its role in the conversion of spermidine into putrescine,” Journal of Biological Chemistry, vol. 256, no. 5, pp. 2454–2459, 1981. View at Google Scholar
  46. F. Dai, W. Yu, J. Song, Q. Li, C. Wang, and S. Xie, “Extracellular polyamines-induced proliferation and migration of cancer cells by ODC, SSAT, and Akt1-mediated pathway,” Anti-Cancer Drugs, vol. 28, no. 4, pp. 457–464, 2017. View at Publisher · View at Google Scholar
  47. S. Erdogan, O. Doganlar, Z. B. Doganlar et al., “The flavonoid apigenin reduces prostate cancer CD44+ stem cell survival and migration through PI3K/Akt/NF-κB signaling,” Life Sciences, vol. 162, pp. 77–86, 2016. View at Publisher · View at Google Scholar
  48. H. M. Wallace, D. E. Ball, and C. S. Coleman, “Evidence for a cytosolic N8-spermidine acetyltransferase in human colonic carcinoma cells,” in Polyamines in the Gastrointestinal Tract, pp. 87–93, Kluwer Academic Publishers, Dordrecht, South Holland, The Netherlands, 1992. View at Google Scholar
  49. V. G. Brunton, M. H. Grant, and H. M. Wallace, “Mechanisms of spermine toxicity in baby-hamster kidney (BHK) cells: The role of amine oxidases and oxidative stress,” Biochemical Journal, vol. 280, no. 1, pp. 193–198, 1991. View at Publisher · View at Google Scholar · View at Scopus