Caffeic acid phenethyl ester: Inhibition of metastatic cell behaviours via voltage-gated sodium channel in human breast cancer in vitro

International Journal of Biochemistry and Cell Biology

Volumn 71, Issue , 2016, Pages 111-118

  Fraser, Scott P ^a   Hemsley, Faye ^a   Djamgoz, Mustafa B A ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b CYPRUS INTERNATIONAL UNIVERSITY   (Turkey)

Author keywords

Breast; Cancer; Colon; Non small cell lung; Voltage gated sodium channel

Indexed keywords

CAFFEIC ACID PHENETHYL ESTER; TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL; ANTINEOPLASTIC AGENT; CAFFEIC ACID DERIVATIVE; PHENETHYL ALCOHOL;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CELL FUNCTION; COLON CANCER; CONTROLLED STUDY; CURRENT DENSITY; ELECTROPHYSIOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; LONG TERM CARE; LUNG CANCER CELL LINE; NON SMALL CELL LUNG CANCER; STEADY STATE; ANALOGS AND DERIVATIVES; BREAST TUMOR; DRUG EFFECTS; METABOLISM; METASTASIS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CAFFEIC ACIDS; CELL LINE, TUMOR; ELECTROPHYSIOLOGICAL PHENOMENA; HUMANS; NEOPLASM METASTASIS; PHENYLETHYL ALCOHOL; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84953235743     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2015.12.012     Document Type: Article

References (68)

1. S. Akyol, Z. Ginis, F. Armutcu, G. Ozturk, M.R. Yigitoglu, and O. Akyol The potential usage of caffeic acid phenethyl ester (CAPE) against chemotherapy-induced and radiotherapy-induced toxicity Cell Biochem. Funct. 30 5 2012 438 443 10.1002/cbf.2817
2. D.T. Baptista-Hon, F.M. Robertson, G.B. Robertson, S.J. Owen, G.W. Rogers, E.L. Lydon, and et al. Potent inhibition by ropivacaine of metastatic colon cancer SW620 cell invasion and Nav1.5 channel function Br. J. Anaesth. 113 Suppl. 1 2014 i39 i48 10.1093/bja/aeu104
3. I. Ben-Porath, M.W. Thomson, V.J. Carey, R. Ge, G.W. Bell, A. Regev, and et al. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors Nat. Genet. 40 5 2008 499 507 10.1038/ng.127
4. J.C. Berger, D. Vander-Griend, W.M. Stadler, and C. Rinker-Schaeffer Metastasis suppressor genes: signal transduction, cross-talk and the potential for modulating the behavior of metastatic cells Anticancer Drugs 15 6 2004 559 568
5. W.J. Brackenbury Voltage-gated sodium channels and metastatic disease Channels (Austin) 6 5 2012 352 361 10.4161/chan.21910
6. W.J. Brackenbury, A.-M. Chioni, J.K.J. Diss, and M.B.A. Djamgoz The neonatal splice variant of Nav1.5 potentiates in vitro invasive behaviour of MDA-MB-231 human breast cancer cells Breast Cancer Res. Treat. 101 2 2007 149 160 10.1007/s10549-006-9281-1
7. + efflux in caveolae Oncogene 30 17 2011 2070 2076 10.1038/onc.2010.574
8. M.K. Burgazli, N. Aydogdu, A. Rafiq, M. Mericliler, R. Chasan, and A. Erdogan Effects of caffeic acid phenethyl ester (CAPE) on membrane potential and intracellular calcium in human endothelial cells Eur. Rev. Med. Pharmacol. Sci. 17 6 2013 720 728
9. +-channel Nav1.7 is necessary for EGF-mediated invasion in human non-small cell lung cancer cells J. Cell Sci. 126 Pt 21 2013 4939 4949 10.1242/jcs.130013
10. N. Celli, L.K. Dragani, S. Murzilli, T. Pagliani, and A. Poggi In vitro and in vivo stability of caffeic acid phenethyl ester, a bioactive compound of propolis J. Agric. Food Chem. 55 9 2007 3398 3407
11. G.C. Chan, K.W. Cheung, and D.M. Sze The immunomodulatory and anticancer properties of propolis Clin. Rev. Allergy Immunol. 44 3 2013 262 273 10.1007/s12016-012-8322-2
12. P. Chevrier, K. Vijayaragavan, and M. Chahine Differential modulation of Nav1.7 and Nav1.8 peripheral nerve sodium channels by the local anesthetic lidocaine Br. J. Pharmacol. 142 3 2004 576 584
13. E-P.I. Chiang, S.-Y. Tsai, Y.-H. Kuo, M.-H. Pai, H.L. Chiu, R.L. Rodriguez, and et al. Caffeic acid derivatives inhibit the growth of colon cancer: involvement of the PI3-K/Akt and AMPK signaling pathways PLOS ONE 9 6 2014 e99631 10.1371/journal.pone.0099631
14. + current by NVP-AUY922 in the human pancreatic duct cell line (PANC-1) possibly independent of heat shock protein 90 inhibition J. Pharmacol. Sci. 127 4 2015 404 413 10.1016/j.jphs.2015.02.009
15. A.M. Chioni, D. Shao, R. Grose, and M.B.A. Djamgoz Protein kinase A and regulation of neonatal Nav1.5 expression in human breast cancer cells: activity-dependent positive feedback and cellular migration Int. J. Biochem. Cell Biol. 42 2 2010 346 358 10.1016/j.biocel.2009.11.021
16. + channel by caffeic acid phenethyl ester (CAPE) and curcumin Pflugers Arch. 465 8 2013 1121 1134 10.1007/s00424-013-1239-7
17. D. Diaz, D.M. Delgadillo, E. Hernandez-Gallegos, M.E. Ramirez-Dominguez, L.M. Hinojosa, C.S. Ortiz, and et al. Functional expression of voltage-gated sodium channels in primary cultures of human cervical cancer J. Cell. Physiol. 210 2 2007 469 478
18. M.B.A. Djamgoz, and R. Onkal Persistent current blockers of voltage-gated sodium channels: a clinical opportunity for controlling metastatic disease Recent Pat. Anticancer Drug Discov. 8 1 2013 66 84
19. V. Driffort, L. Gillet, E. Bon, S. Marionneau-Lambot, T. Oullier, V. Joulin, and et al. Ranolazine inhibits Nav1.5-mediated breast cancer cell invasiveness and lung colonization Mol. Cancer 13 2014 264 10.1186/1476-4598-13-264
20. S.P. Fraser, Y. Ding, A. Liu, C.S. Foster, and M.B.A. Djamgoz Tetrodotoxin suppresses morphological enhancement of the metastatic MAT-LyLu rat prostate cancer cell line Cell Tissue Res. 295 3 1999 505 512
21. + channel expression to cell behaviours involved in the metastatic cascade in rat prostate cancer: I. Lateral motility J. Cell. Physiol. 195 3 2003 479 487
22. + channel subunit in rat prostate cancer cell lines: electrophysiological, pharmacological and molecular characterisation Pflugers Arch. 446 5 2003 559 571
23. S.P. Fraser, J.K.J. Diss, A.-M. Chioni, M.E. Mycielska, H. Pan, R.F. Yamaci, and et al. Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis Clin. Cancer Res. 11 15 2005 5381 5389
24. S.P. Fraser, I. Özerlat-Gunduz, W.J. Brackenbury, E.M. Fitzgerald, T. Campbell, R.C. Coombes, and et al. Regulation of voltage-gated sodium channel expression in cancer: hormones, growth factors and auto-regulation Philos. Trans. R. Soc. Lond. B: Biol. Sci. 369 1638 2014 20130105 10.1098/rstb.2013.0105
25. + channel activity in rat prostate cancer in vitro Nutr. Cancer 66 6 2014 1047 1058 10.1080/01635581.2014.939291
26. L. Gillet, S. Roger, P. Besson, F. Lecaille, J. Gore, P. Bougnoux, and et al. Voltage-gated sodium channel activity promotes cysteine cathepsin-dependent invasiveness and colony growth of human cancer cells J. Biol. Chem. 284 13 2009 8680 8691 10.1074/jbc.M806891200
27. + currents in two prostatic tumour cell lines: contribution to invasiveness in vitro FEBS Lett. 369 2-3 1995 290 294
28. H. Han, B. Du, X. Pan, J. Liu, Q. Zhao, X. Lian, and et al. CADPE inhibits PMA-stimulated gastric carcinoma cell invasion and matrix metalloproteinase-9 expression by FAK/MEK/ERK-mediated AP-1 activation Mol. Cancer Res. 8 11 2010 1477 1488 10.1158/1541-7786.MCR-10-0114
29. D. Hanahan, and R.A. Weinberg The hallmarks of cancer Cell 100 1 2000 57 70
30. E. Hernandez-Plata, C.S. Ortiz, B. Marquina-Castillo, I. Medina-Martinez, A. Alfaro, J. Berumen, and et al. Overexpression of Nav1.6 channels is associated with the invasion capacity of human cervical cancer Int. J. Cancer 130 9 2012 2013 2023 10.1002/ijc.26210
31. + channel SCN5A is a key regulator of a gene transcriptional network that controls colon cancer invasion Cancer Res. 70 17 2010 6957 6967 10.1158/0008-5472.CAN-10-1169
32. H.I. Ingólfsson, P. Thakur, K.F. Herold, E.A. Hobart, N.B. Ramsey, X. Periole, and et al. Phytochemicals perturb membranes and promiscuously alter protein function ACS Chem. Biol. 9 8 2014 1788 1798 10.1021/cb500086e
33. B. Isbilen, S.P. Fraser, and M.B.A. Djamgoz Docosahexaenoic Acid (Omega-3) blocks voltage-gated sodium channel activity and migration of MDA-MB-231 human breast cancer cells Int. J. Biochem. Cell Biol. 38 12 2006 2173 2182
34. + currents in rat dorsal root ganglion neurons Brain Res. 1045 1-2 2005 134 141
35. + channels Mol. Pharmacol. 64 3 2003 741 752
36. + channels in human prostate cancer cell lines and their contribution to invasiveness in vitro Am. J. Pathol. 150 4 1997 1213 1221
37. + channel activity in human prostate cancer cell lines of markedly different metastatic potential: distinguishing characteristics of PC-3 and LNCaP cells Prostate 46 4 2001 262 274
38. K.W. Lee, N.J. Kang, J.H. Kim, K.M. Lee, D.E. Lee, H.J. Hur, and et al. Caffeic acid phenethyl ester inhibits invasion and expression of matrix metalloproteinase in SK-Hep1 human hepatocellular carcinoma cells by targeting nuclear factor kappa B Genes Nutr. 2 4 2008 319 322 10.1007/s12263-007-0067-9
39. H.P. Lin, C.Y. Lin, C. Huo, P.H. Hsiao, L.C. Su, S.S. Jiang, and 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 6 9 2015 6684 6707
40. C. Manach, G. Williamson, C. Morand, A. Scalbert, and C. Rémésy Bioavailability and bioefficacy of polyphenols in humans, I. Review of 97 bioavailability studies Am. J. Clin. Nutr. 81 1 Suppl. 2005 230S 242S
41. + channel Nav1.5 by post-translational modifications J. Mol. Cell. Cardiol. 82 2015 36 47 10.1016/j.yjmcc.2015.02.013
42. M. Monk, and C. Holding Human embryonic genes re-expressed in cancer cells Oncogene 20 56 2001 8085 8091
43. + channel expression to cell behaviours involved in the metastatic cascade in rat prostate cancer: II. Secretory membrane activity J. Cell. Physiol. 195 3 2003 461 469
44. M. Nelson, M. Yang, A.A. Dowle, J.R. Thomas, and W.J. Brackenbury The sodium channel-blocking antiepileptic drug phenytoin inhibits breast tumour growth and metastasis Mol. Cancer 14 1 2015 13 10.1186/s12943-014-0277-x
45. M. Nelson, M. Yang, R. Millican-Slater, and W.J. Brackenbury Nav1.5 regulates breast tumor growth and metastatic dissemination in vivo Oncotarget 6 32 2015 32914 32929 10.18632/oncotarget.5441
46. v1.5: an electrophysiological comparison of 'neonatal' and 'adult' isoforms, and critical involvement of a lysine residue J. Cell. Physiol. 216 3 2008 716 726 10.1002/jcp.21451
47. H.C. Pal, S. Sharma, L.R. Strickland, S.K. Katiyar, M.E. Ballestas, M. Athar, and et al. Fisetin inhibits human melanoma cell invasion through promotion of mesenchymal to epithelial transition and by targeting MAPK and NFκB signaling pathways PLOS ONE 9 1 2014 e86338 10.1371/journal.pone.0086338
48. + channel expression Eur. Biophys. J. 37 4 2008 359 368
49. C.Y. Peng, H.W. Yang, Y.H. Chu, Y.C. Chang, M.J. Hsieh, M.Y. Chou, and et al. Caffeic acid phenethyl ester inhibits oral cancer cell metastasis by regulating matrix metalloproteinase-2 and the mitogen-activated protein kinase pathway Evid. Based Complement. Altern. Med. 2012 2012 732578 10.1155/2012/732578
50. + channels by local anesthetics Science 265 5179 1994 1724 1728
51. S. Roger, P. Besson, and J.Y. Le Guennec Involvement of a novel fast inward sodium current in the invasion capacity of a breast cancer cell line Biochim. Biophys. Acta 1616 2 2003 107 111
52. L.L. Shang, S. Sanyal, A.E. Pfahnl, Z. Jiao, J. Allen, H. Liu, and et al. NF-kappaB-dependent transcriptional regulation of the cardiac scn5a sodium channel by angiotensin II Am. J. Physiol. Cell Physiol. 294 1 2008 C372 C379
53. Y. Shigeoka, T. Igishi, S. Matsumoto, H. Nakanishi, M. Kodani, K. Yasuda, and et al. Sulindac sulfide and caffeic acid phenethyl ester suppress the motility of lung adenocarcinoma cells promoted by transforming growth factor-beta through Akt inhibition J. Cancer Res. Clin. Oncol. 130 3 2004 146 152
54. 2+ channel (CRAC) by curcumin and caffeic acid phenethyl ester (CAPE) via electrophilic addition to a cysteine residue of Orai1 Biochem. Biophys. Res. Commun. 428 1 2012 56 61 10.1016/j.bbrc.2012.10.005
55. R. Silva-Carvalho, V. Miranda-Goncalves, A.M. Ferreira, S.M. Cardoso, A.J.F.N. Sobral, C. Almeida-Aguiar, and et al. Antitumoural and antiangiogenic activity of Portuguese propolis in in vitro and in vivo models J. Funct. Foods 11 2014 160 171 10.1016/j.jff.2014.09.009
56. M.F. Tolba, S.S. Azab, A.E. Khalifa, S.Z. Abdel-Rahman, and A.B. Abdel-Naim Caffeic acid phenethyl ester, a promising component of propolis with a plethora of biological activities: a review on its anti-inflammatory, neuroprotective, hepatoprotective, and cardioprotective effects IUBMB Life 65 8 2013 699 709 10.1002/iub.1189
57. K.S. Vaidya, and D.R. Welch Metastasis suppressors and their roles in breast carcinoma J. Mammary Gland Biol. Neoplasia 12 2-3 2007 175 190
58. C.H.R. Wallace, I. Baczko, L. Jones, M. Fercho, and P.E. Light Inhibition of cardiac voltage-gated sodium channels by grape polyphenols Br. J. Pharmacol. 149 6 2006 657 665
59. X. Wang, J. Pang, J.A. Maffucci, D.S. Pade, R.A. Newman, S.M. Kerwin, and et al. Pharmacokinetics of caffeic acid phenethyl ester and its catechol-ring fluorinated derivative following intravenous administration to rats Biopharm. Drug Dispos. 30 5 2009 221 228 10.1002/bdd.657
60. M.A. Watanabe, M.K. Amarante, B.J. Conti, and J.M. Sforcin Cytotoxic constituents of propolis inducing anticancer effects: a review J. Pharm. Pharmacol. 63 11 2011 1378 1386 10.1111/j.2042-7158.2011.01331.x
61. B. Weigelt, Z. Hu, X. He, C. Livasy, L.A. Carey, M.G. Ewend, and et al. Molecular portraits and 70-gene prognosis signature are preserved throughout the metastatic process of breast cancer Cancer Res. 65 20 2005 9155 9158
62. C.-J. Weng, and G.-C. Yen Chemopreventive effects of dietary phytochemicals against cancer invasion and metastasis: phenolic acids, monophenol, polyphenol, and their derivatives Cancer Treat. Rev. 38 1 2012 76 87 10.1016/j.ctrv.2011.03.001
63. J. Wu, C. Omene, J. Karkoszka, M. Bosland, J. Eckard, C.B. Klein, and 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 Lett. 308 1 2011 43 53 10.1016/j.canlet.2011.04.012
64. M. Yang, D.J. Kozminski, L.A. Wold, R. Modak, J.D. Calhoun, L.L. Isom, and et al. Therapeutic potential for phenytoin: targeting Nav1.5 sodium channels to reduce migration and invasion in metastatic breast cancer Breast Cancer Res. Treat. 134 2 2012 603 615 10.1007/s10549-012-2102-9
65. G. Yang, Y. Fu, M. Malakhova, I. Kurinov, F. Zhu, K. Yao, H. Li, and et al. Caffeic acid directly targets ERK1/2 to attenuate solar UV-induced skin carcinogenesis Cancer Prev. Res. (Phila.) 7 10 2014 1056 1066 10.1158/1940-6207
66. + channel alpha subunit in voltage-dependent gating and drug block J. Biol. Chem. 277 38 2002 35393 35401
67. S. Yildirim, S. Altun, H. Gumushan, A. Patel, and M.B.A. Djamgoz Voltage-gated sodium channel activity promotes prostate cancer metastasis in vivo Cancer Lett. 323 1 2012 58 61 10.1016/j.canlet.2012.03.036
68. P. Zhang, Y. Tang, N.-G. Li, Y. Zhu, and J.-A. Duan Bioactivity and chemical synthesis of caffeic acid phenethyl ester and its derivatives Molecules 19 10 2014 16458 16476 10.3390/molecules191016458