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Evidence-Based Complementary and Alternative Medicine
Volume 2017, Article ID 6793456, 10 pages
https://doi.org/10.1155/2017/6793456
Research Article

Induction of Cell Cycle Arrest and Apoptotic Response of Head and Neck Squamous Carcinoma Cells (Detroit 562) by Caffeic Acid and Caffeic Acid Phenethyl Ester Derivative

1Department of Conservative Dentistry with Endodontics, School of Medicine with the Division of Dentistry, Medical University of Silesia in Katowice, Pl. Akademicki 17, 41-902 Bytom, Poland
2Department of Pathology, School of Pharmacy and Division of Laboratory Medicine in Sosnowiec, Medical University of Silesia in Katowice, ul. Ostrogórska 30, 41-200 Sosnowiec, Poland

Correspondence should be addressed to Arkadiusz Dziedzic; lp.ude.mus@cizdeizda

Received 3 October 2016; Accepted 19 December 2016; Published 12 January 2017

Academic Editor: Vassya Bankova

Copyright © 2017 Arkadiusz Dziedzic 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. M. A. Ehara Watanabe, M. K. Amarante, B. J. Conti, and J. M. Sforcin, “Cytotoxic constituents of propolis inducing anticancer effects: a review,” Journal of Pharmacy and Pharmacology, vol. 63, no. 11, pp. 1378–1386, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. A. A. Righi, G. Negri, and A. Salatino, “Comparative chemistry of propolis from eight Brazilian localities,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 267878, 14 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Sforcin and V. Bankova, “Propolis: is there a potential for the development of new drugs?” Journal of Ethnopharmacology, vol. 133, no. 2, pp. 253–260, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. A. M. Gómez-Caravaca, M. Gómez-Romero, D. Arráez-Román, A. Segura-Carretero, and A. Fernández-Gutiérrez, “Advances in the analysis of phenolic compounds in products derived from bees,” Journal of Pharmaceutical and Biomedical Analysis, vol. 41, no. 4, pp. 1220–1234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. M. A. E. Watanabe, M. K. Amarante, B. J. Conti, and J. M. Sforcin, “Cytotoxic constituents of propolis inducing anticancer effects: a review,” Journal of Pharmacy and Pharmacology, vol. 63, no. 11, pp. 1378–1386, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. A. Nagappan, H. J. Lee, V. V. G. Saralamma et al., “Flavonoids isolated from Citrus platymamma induced G2/M cell cycle arrest and apoptosis in A549 human lung cancer cells,” Oncology Letters, vol. 12, no. 2, pp. 1394–1402, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Kakehashi, N. Ishii, M. Fujioka, K. Doi, M. Gi, and H. Wanibuchi, “Ethanol-extracted brazilian propolis exerts protective effects on tumorigenesis in wistar hannover rats,” PLoS ONE, vol. 11, no. 7, Article ID e0158654, 2016. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Demir, Y. Aliyazicioglu, I. Turan et al., “Antiproliferative and proapoptotic activity of Turkish propolis on human lung cancer cell line,” Nutrition and Cancer, vol. 68, no. 1, pp. 165–172, 2016. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Szliszka, G. Zydowicz, B. Janoszka, C. Dobosz, G. Kowalczyk-Ziomek, and W. Krol, “Ethanolic extract of Brazilian green propolis sensitizes prostate cancer cells to TRAIL-induced apoptosis,” International Journal of Oncology, vol. 38, no. 4, pp. 941–953, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. I. C. G. de Mendonça, I. C. C. M. Porto, T. G. do Nascimento et al., “Brazilian red propolis: phytochemical screening, antioxidant activity and effect against cancer cells,” BMC Complementary and Alternative Medicine, vol. 15, article 357, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Chirumbolo, “Anti-inflammatory property of propolis,” Journal of Clinical Biochemistry and Nutrition, vol. 56, no. 2, pp. 163–164, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. H. Xuan, Y. Wang, A. Li, C. Fu, Y. Wang, and W. Peng, “Bioactive components of Chinese propolis water extract on antitumor activity and quality control,” Evidence-Based Complementary and Alternative Medicine, vol. 2016, Article ID 9641965, 9 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Murtaza, A. Sajjad, Z. Mehmood, S. H. Shah, and A. R. Siddiqi, “Possible molecular targets for therapeutic applications of caffeic acid phenethyl ester in inflammation and cancer,” Journal of Food and Drug Analysis, vol. 23, no. 1, pp. 11–18, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. Y.-Y. Kuo, W.-T. Jim, L.-C. Su et al., “Caffeic acid phenethyl ester is a potential therapeutic agent for oral cancer,” International Journal of Molecular Sciences, vol. 16, no. 5, pp. 10748–10766, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. J. T. Sanderson, H. Clabault, C. Patton et al., “Antiproliferative, antiandrogenic and cytotoxic effects of novel caffeic acid derivatives in LNCaP human androgen-dependent prostate cancer cells,” Bioorganic & Medicinal Chemistry, vol. 21, no. 22, pp. 7182–7193, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. F. Armutcu, S. Akyol, S. Ustunsoy, and F. F. Turan, “Therapeutic potential of caffeic acid phenethyl ester and its anti-inflammatory and immunomodulatory effects (Review),” Experimental and Therapeutic Medicine, vol. 9, no. 5, pp. 1582–1588, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Okutan, N. Ozcelik, H. R. Yilmaz, and E. Uz, “Effects of caffeic acid phenethyl ester on lipid peroxidation and antioxidant enzymes in diabetic rat heart,” Clinical Biochemistry, vol. 38, no. 2, pp. 191–196, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. J. F. Campos, U. P. dos Santos, P. S. da Rocha et al., “Antimicrobial, antioxidant, anti-inflammatory, and cytotoxic activities of propolis from the stingless bee Tetragonisca fiebrigi (Jataí),” Evidence-Based Complementary and Alternative Medicine, vol. 2015, Article ID 296186, 11 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  19. Z. S. Selamoglu, I. Ozdemir, O. Ciftci, M. F. Gulhan, and A. Savci, “Antioxidant effect of ethanolic extract of propolis in liver of L-NAME treated rats,” Advances in Clinical and Experimental Medicine, vol. 24, no. 2, pp. 227–232, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Shimizu, H. Ashida, Y. Matsuura, and K. Kanazawa, “Antioxidative bioavailability of artepillin C in Brazilian propolis,” Archives of Biochemistry and Biophysics, vol. 424, no. 2, pp. 181–188, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Dziedzic, R. Kubina, R. D. Wojtyczka, A. Kabała-Dzik, M. Tanasiewicz, and T. Morawiec, “The antibacterial effect of ethanol extract of polish propolis on mutans streptococci and lactobacilli isolated from saliva,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 681891, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. U. Czyżewska, K. Siemionow, I. Zaręba, and W. Miltyk, “Proapoptotic activity of propolis and their components on human tongue squamous cell carcinoma cell line (CAL-27),” PLoS ONE, vol. 11, no. 6, Article ID e0157091, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. H.-P. Lin, C.-Y. Lin, C. Huo et al., “Caffeic acid phenethyl ester induced cell cycle arrest and growth inhibition in androgen-independent prostate cancer cells via regulation of Skp2, p53, p21Cip1 and p27Kip1,” Oncotarget, vol. 6, no. 9, pp. 6684–6707, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Wu, C. Omene, J. Karkoszka et al., “Caffeic acid phenethyl ester (CAPE), derived from a honeybee product propolis, exhibits a diversity of anti-tumor effects in pre-clinical models of human breast cancer,” Cancer Letters, vol. 308, no. 1, pp. 43–53, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. M.-R. Ahn, K. Kunimasa, T. Ohta et al., “Suppression of tumor-induced angiogenesis by Brazilian propolis: major component artepillin C inhibits in vitro tube formation and endothelial cell proliferation,” Cancer Letters, vol. 252, no. 2, pp. 235–243, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Dziedzic, R. Kubina, A. Kabała-Dzik, R. D. Wojtyczka, T. Morawiec, and R. J. Bułdak, “Caffeic acid reduces the viability and migration rate of oral carcinoma cells (SCC-25) exposed to low concentrations of ethanol,” International Journal of Molecular Sciences, vol. 15, no. 10, pp. 18725–18741, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Li, Z. Sun, C. Han, and J. Chen, “The chemopreventive effects of tea on human oral precancerous mucosa lesions,” Proceedings of the Society for Experimental Biology and Medicine, vol. 220, no. 4, pp. 218–224, 2003. View at Google Scholar
  28. P. E. Petersen, “Oral cancer prevention and control—the approach of the World Health Organization,” Oral Oncology, vol. 45, no. 4-5, pp. 454–460, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Siegel, D. Naishadham, and A. Jemal, “Cancer statistics, 2013,” CA: A Cancer Journal for Clinicians, vol. 63, no. 1, pp. 11–30, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Iriti and E. M. Varoni, “Chemopreventive potential of flavonoids in oral squamous cell carcinoma in human studies,” Nutrients, vol. 5, no. 7, pp. 2564–2576, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. C. F. G. De Moura, J. Noguti, G. P. P. De Jesus et al., “Polyphenols as a chemopreventive agent in oral carcinogenesis: putative mechanisms of action using in-vitro and in-vivo test systems,” European Journal of Cancer Prevention, vol. 22, no. 5, pp. 467–472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Tanaka and M. Tanaka, “Oral carcinogenesis and oral cancer chemoprevention: a review,” Pathology Research International, vol. 2011, Article ID 431246, 10 pages, 2011. View at Publisher · View at Google Scholar
  33. Y.-J. Surh, “Cancer chemoprevention with dietary phytochemicals,” Nature Reviews Cancer, vol. 3, no. 10, pp. 768–780, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. E. Lucenteforte, W. Garavello, C. Bosetti, and C. La Vecchia, “Dietary factors and oral and pharyngeal cancer risk,” Oral Oncology, vol. 45, no. 6, pp. 461–467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Rossi, W. Garavello, R. Talamini et al., “Flavonoids and the risk of oral and pharyngeal cancer: a case-control study from Italy,” Cancer Epidemiology, Biomarkers & Prevention, vol. 16, no. 8, pp. 1621–1625, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Majchrzak, B. Szybiak, A. Wegner et al., “Oral cavity and oropharyngeal squamous cell carcinoma in young adults: a review of the literature,” Radiology and Oncology, vol. 48, no. 1, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. K. B. Jadhav and N. Gupta, “Clinicopathological prognostic implicators of oral squamous cell carcinoma: need to understand and revise,” North American Journal of Medical Sciences, vol. 5, no. 12, pp. 671–679, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. M. L. Khalil, “Biological activity of bee propolis in health and disease,” Asian Pacific Journal of Cancer Prevention, vol. 7, no. 1, pp. 22–31, 2006. View at Google Scholar · View at Scopus
  39. S. Patel, “Emerging adjuvant therapy for cancer: propolis and its constituents,” Journal of Dietary Supplements, vol. 13, no. 3, pp. 245–268, 2015. View at Publisher · View at Google Scholar
  40. S.-F. Chen, S. Nien, C.-H. Wu, C.-L. Liu, Y.-C. Chang, and Y.-S. Lin, “Reappraisal of the anticancer efficacy of quercetin in oral cancer cells,” Journal of the Chinese Medical Association, vol. 76, no. 3, pp. 146–152, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. C.-L. Lin, R.-F. Chen, J. Y.-F. Chen et al., “Protective effect of caffeic acid on paclitaxel induced anti-proliferation and apoptosis of lung cancer cells involves NF-κb pathway,” International Journal of Molecular Sciences, vol. 13, no. 5, pp. 6236–6245, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Kimoto, M. Aga, K. Hino et al., “Apoptosis of human leukemia cells induced by Artepillin C, an active ingredient of Brazilian propolis,” Anticancer Research, vol. 21, no. 1, pp. 221–228, 2001. View at Google Scholar · View at Scopus
  43. K. J. Woo, Y.-J. Jeong, J.-W. Park, and T. K. Kwon, “Chrysin-induced apoptosis is mediated through caspase activation and Akt inactivation in U937 leukemia cells,” Biochemical and Biophysical Research Communications, vol. 325, no. 4, pp. 1215–1222, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. E. Pichichero, R. Cicconi, M. Mattei, M. G. Muzi, and A. Canini, “Acacia honey and chrysin reduce proliferation of melanoma cells through alterations in cell cycle progression,” International Journal of Oncology, vol. 37, no. 4, pp. 973–981, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. C.-N. Chen, C.-L. Wu, and J.-K. Lin, “Propolin C from propolis induces apoptosis through activating caspases, Bid and cytochrome c release in human melanoma cells,” Biochemical Pharmacology, vol. 67, no. 1, pp. 53–66, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Kubina, A. Kabała-Dzik, A. Dziedzic et al., “The ethanol extract of polish propolis exhibits anti-proliferative and/or pro-apoptotic effect on HCT 116 colon cancer and Me45 Malignant melanoma cells in vitro conditions,” Advances in Clinical and Experimental Medicine, vol. 24, no. 2, pp. 203–212, 2015. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Luo, J.-W. Soh, W.-Q. Xing, Y. Mao, T. Matsuno, and I. B. Weinstein, “PM-3, a benzo-γ-pyran derivative isolated from propolis, inhibits growth of MCF-7 human breast cancer cells,” Anticancer Research, vol. 21, no. 3, pp. 1665–1671, 2001. View at Google Scholar · View at Scopus
  48. A. Rzepecka-Stojko, A. Kabała-Dzik, A. Moździerz et al., “Caffeic acid phenethyl ester and ethanol extract of propolis induce the complementary cytotoxic effect on triple-negative breast cancer cell lines,” Molecules, vol. 20, no. 5, pp. 9242–9262, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. M.-W. Hung, M.-S. Shiao, L.-C. Tsai, G.-G. Chang, and T.-C. Chang, “Apoptotic effect of caffeic acid phenenyl ester and its ester and amide analogues in human cervical cancer ME180 cells,” Anticancer Research, vol. 23, no. 6, pp. 4773–4780, 2003. View at Google Scholar · View at Scopus
  50. C. O. Omene, J. Wu, and K. Frenkel, “Caffeic Acid Phenethyl Ester (CAPE) derived from propolis, a honeybee product, inhibits growth of breast cancer stem cells,” Investigational New Drugs, vol. 30, no. 4, pp. 1279–1288, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. M. G. Dilshara, R. G. P. T. Jayasooriya, S. R. Park, Y.-H. Choi, I.-W. Choi, and G.-Y. Kim, “Caffeic acid phenethyl ester enhances TRAIL-mediated apoptosis via CHOP-induced death receptor 5 upregulation in hepatocarcinoma Hep3B cells,” Molecular and Cellular Biochemistry, vol. 418, no. 1-2, pp. 13–20, 2016. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Rossi, A. Ligresti, R. Longo, A. Russo, F. Borrelli, and L. Sautebin, “The inhibitory effect of propolis and caffeic acid phenethyl ester on cyclooxygenase activity in J774 macrophages,” Phytomedicine, vol. 9, no. 6, pp. 530–535, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Michaluart, J. L. Masferrer, A. M. Carothers et al., “Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation,” Cancer Research, vol. 59, no. 10, pp. 2347–2352, 1999. View at Google Scholar · View at Scopus
  54. Y. Shigeoka, T. Igishi, S. Matsumoto et al., “Sulindac sulfide and caffeic acid phenethyl ester suppress the motility of lung adenocarcinoma cells promoted by transforming growth factor-β through Akt inhibition,” Journal of Cancer Research and Clinical Oncology, vol. 130, no. 3, pp. 146–152, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. Z.-H. Jiao, M. Li, Y.-X. Feng, J.-C. Shi, J. Zhang, and B. Shao, “Hormesis effects of silver nanoparticles at non-cytotoxic doses to human hepatoma cells,” PLoS ONE, vol. 9, no. 7, Article ID e102564, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. Y.-Y. Kuo, H.-P. Lin, C. Huo et al., “Caffeic acid phenethyl ester suppresses proliferation and survival of TW2.6 human oral cancer cells via inhibition of akt signaling,” International Journal of Molecular Sciences, vol. 14, no. 5, pp. 8801–8817, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. Y.-T. Lee, M.-J. Don, P.-S. Hung et al., “Cytotoxicity of phenolic acid phenethyl esters on oral cancer cells,” Cancer Letters, vol. 223, no. 1, pp. 19–25, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Ciftci-Yilmaz, S. Yilmaz, A. Gurel et al., “Caffeic Acid Phenethyl Ester (CAPE) inhibits growth of head and neck squamous cancer stem cells,” Clinical and Investigative Medicine, vol. 38, no. 4, pp. E206–E209, 2015. View at Google Scholar · View at Scopus
  59. Y.-C. Chang, P.-N. Chen, S.-C. Chu, C.-Y. Lin, W.-H. Kuo, and Y.-S. Hsieh, “Black tea polyphenols reverse epithelial-to-mesenchymal transition and suppress cancer invasion and proteases in human oral cancer cells,” Journal of Agricultural and Food Chemistry, vol. 60, no. 34, pp. 8395–8403, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. K. McEleny, R. Coffey, C. Morrissey, J. M. Fitzpatrick, and R. W. G. Watson, “Caffeic acid phenethyl ester-induced PC-3 cell apoptosis is caspase-dependent and mediated through the loss of inhibitors of apoptosis proteins,” BJU International, vol. 94, no. 3, pp. 402–406, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. Y.-J. Lee, P.-H. Liao, W.-K. Chen, and C.-C. Yang, “Preferential cytotoxicity of caffeic acid phenethyl ester analogues on oral cancer cells,” Cancer Letters, vol. 153, no. 1-2, pp. 51–56, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. A. Khan, K. Gillis, J. Clor, and K. Tyagarajan, “Simplified evaluation of apoptosis using the Muse cell analyzer,” Postepy Biochemii, vol. 58, no. 4, pp. 492–496, 2012. View at Google Scholar · View at Scopus
  63. A. S. Holpuch, K. H. Desai, S. P. Schwendeman, and S. R. Mallery, “Optimizing therapeutic efficacy of chemopreventive agents: a critical review of delivery strategies in oral cancer chemoprevention clinical trials,” Journal of Carcinogenesis, vol. 10, article 23, 2011. View at Publisher · View at Google Scholar