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Published in: Chinese Medicine 1/2016

Open Access 01-12-2016 | Research

Inhibitory effect of trans-ferulic acid on proliferation and migration of human lung cancer cells accompanied with increased endogenous reactive oxygen species and β-catenin instability

Authors: Yao Fong, Chia-Chun Tang, Huei-Ting Hu, Hsin-Yu Fang, Bing-Hung Chen, Chang-Yi Wu, Shyng-Shiou Yuan, Hui-Min David Wang, Yen-Chun Chen, Yen-Ni Teng, Chien-Chih Chiu

Published in: Chinese Medicine | Issue 1/2016

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Abstract

Background

Trans-ferulic (FA) acid exhibits antioxidant effects in vitro. However, the underlying mechanism of trans-FA activity in cellular physiology, especially cancer physiology, remains largely unknown. This study investigated the cellular physiological effects of trans-FA on the H1299 human lung cancer cell line.

Methods

The 2,2-diphenyl-1-picrylhydrazyl assay was used to determine free radical scavenging capability. Assessment of intracellular reactive oxygen species (ROS) was evaluated using oxidized 2ʹ,7ʹ-dichlorofluorescin diacetate and dihydroethidium staining. Trypan blue exclusion, colony formation, and anchorage-independent growth assays were used to determine cellular proliferation. Annexin V staining assay was used to assess cellular apoptosis by flow cytometry. Wound healing and Boyden’s well assays were used to detect the migration and invasion of cells. Gelatin zymography was used to detect matrix metalloproteinase (MMP-2 and MMP-9) activity. Western blotting was used to detect expression levels of various signaling pathway proteins.

Results

DPPH assay results indicated that trans-FA exerted potent antioxidant effects. However, trans-FA increased intracellular ROS levels, including hydrogen peroxide and superoxide anion, in H1299 cells. Trans-FA treatment inhibited cellular proliferation and induced moderate apoptotic cell death at the highest concentration used (0.6 mM). Furthermore, trans-FA moderately inhibited the migration of H1299 cells at the concentrations of 0.3 and 0.6 mM and attenuated MMP-2 and MMP-9 activity. Trans-FA caused the phosphorylation of β-catenin, resulting in proteasomal degradation of β-catenin. Conversely, trans-FA treatment increased the expression of pro-apoptotic factor Bax and decreased the expression of pro-survival factor survivin.

Conclusion

Various concentrations (0.06–0.6 mM) of trans-FA exert both anti-proliferation and anti-migration effects in the human lung cancer cell line H1299.
Appendix
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Literature
1.
2.
go back to reference O’Rourke N, Roque IFM, Farre Bernado N, Macbeth F. Concurrent chemoradiotherapy in non-small cell lung cancer. Cochrane Database Syst Rev. 2010;16:CD002140. O’Rourke N, Roque IFM, Farre Bernado N, Macbeth F. Concurrent chemoradiotherapy in non-small cell lung cancer. Cochrane Database Syst Rev. 2010;16:CD002140.
3.
go back to reference Pirker R, Minar W. Chemotherapy of advanced non-small cell lung cancer. Front Radiat Ther Oncol. 2010;42:157–63.CrossRefPubMed Pirker R, Minar W. Chemotherapy of advanced non-small cell lung cancer. Front Radiat Ther Oncol. 2010;42:157–63.CrossRefPubMed
4.
go back to reference Wagner TD, Yang GY. The role of chemotherapy and radiation in the treatment of locally advanced non-small cell lung cancer (NSCLC). Curr Drug Targets. 2010;11:67–73.CrossRefPubMed Wagner TD, Yang GY. The role of chemotherapy and radiation in the treatment of locally advanced non-small cell lung cancer (NSCLC). Curr Drug Targets. 2010;11:67–73.CrossRefPubMed
5.
go back to reference Atagi S, Kawahara M, Tamura T, Noda K, Watanabe K, Yokoyama A, et al. Standard thoracic radiotherapy with or without concurrent daily low-dose carboplatin in elderly patients with locally advanced non-small cell lung cancer: a phase III trial of the Japan Clinical Oncology Group (JCOG9812). Jap J Clin Oncol. 2005;35:195–201.CrossRef Atagi S, Kawahara M, Tamura T, Noda K, Watanabe K, Yokoyama A, et al. Standard thoracic radiotherapy with or without concurrent daily low-dose carboplatin in elderly patients with locally advanced non-small cell lung cancer: a phase III trial of the Japan Clinical Oncology Group (JCOG9812). Jap J Clin Oncol. 2005;35:195–201.CrossRef
6.
go back to reference Guo S, Liang Y, Zhou Q. Complement and correction for meta-analysis of patients with extensive-stage small cell lung cancer managed with irinotecan/cisplatin versus etoposide/cisplatin as first-line chemotherapy. J Thorac Oncol. 2011;6:406–8.CrossRefPubMed Guo S, Liang Y, Zhou Q. Complement and correction for meta-analysis of patients with extensive-stage small cell lung cancer managed with irinotecan/cisplatin versus etoposide/cisplatin as first-line chemotherapy. J Thorac Oncol. 2011;6:406–8.CrossRefPubMed
7.
go back to reference Corbaux C, Marie J, Meraud JP, Lacroix S, Delhoume JY, Jouary T, et al. Pemetrexed-induced scleroderma-like changes in the lower legs. Ann Dermatol Venereol. 2015;142:115–20.CrossRefPubMed Corbaux C, Marie J, Meraud JP, Lacroix S, Delhoume JY, Jouary T, et al. Pemetrexed-induced scleroderma-like changes in the lower legs. Ann Dermatol Venereol. 2015;142:115–20.CrossRefPubMed
8.
go back to reference Sun Y, Chen J, Rigas B. Chemopreventive agents induce oxidative stress in cancer cells leading to COX-2 overexpression and COX-2-independent cell death. Carcinogenesis. 2009;30:93–100.CrossRefPubMed Sun Y, Chen J, Rigas B. Chemopreventive agents induce oxidative stress in cancer cells leading to COX-2 overexpression and COX-2-independent cell death. Carcinogenesis. 2009;30:93–100.CrossRefPubMed
9.
go back to reference Setia S, Nehru B, Sanyal SN. The PI3K/Akt pathway in colitis associated colon cancer and its chemoprevention with celecoxib, a Cox-2 selective inhibitor. Biomed Pharmacother. 2014;68:721–7.CrossRefPubMed Setia S, Nehru B, Sanyal SN. The PI3K/Akt pathway in colitis associated colon cancer and its chemoprevention with celecoxib, a Cox-2 selective inhibitor. Biomed Pharmacother. 2014;68:721–7.CrossRefPubMed
10.
go back to reference Madka V, Mohammed A, Li Q, Zhang Y, Patlolla JM, Biddick L, et al. Chemoprevention of urothelial cell carcinoma growth and invasion by the dual COX-LOX inhibitor licofelone in UPII-SV40T transgenic mice. Cancer Prev Res (Phila). 2014;7:708–16.CrossRefPubMedCentral Madka V, Mohammed A, Li Q, Zhang Y, Patlolla JM, Biddick L, et al. Chemoprevention of urothelial cell carcinoma growth and invasion by the dual COX-LOX inhibitor licofelone in UPII-SV40T transgenic mice. Cancer Prev Res (Phila). 2014;7:708–16.CrossRefPubMedCentral
11.
go back to reference Wang Y, Ma W, Zheng W. Deguelin, a novel anti-tumorigenic agent targeting apoptosis, cell cycle arrest and anti-angiogenesis for cancer chemoprevention. Mol Clin Oncol. 2013;1:215–9.PubMed Wang Y, Ma W, Zheng W. Deguelin, a novel anti-tumorigenic agent targeting apoptosis, cell cycle arrest and anti-angiogenesis for cancer chemoprevention. Mol Clin Oncol. 2013;1:215–9.PubMed
12.
go back to reference Zhu B, Liu GT, Wu RS, Strada SJ. Chemoprevention of bicyclol against hepatic preneoplastic lesions. Cancer Biol Ther. 2006;5:1665–73.CrossRefPubMed Zhu B, Liu GT, Wu RS, Strada SJ. Chemoprevention of bicyclol against hepatic preneoplastic lesions. Cancer Biol Ther. 2006;5:1665–73.CrossRefPubMed
13.
go back to reference Tanaka T, Shnimizu M, Moriwaki H. Cancer chemoprevention by carotenoids. Molecules. 2012;17:3202–42.CrossRefPubMed Tanaka T, Shnimizu M, Moriwaki H. Cancer chemoprevention by carotenoids. Molecules. 2012;17:3202–42.CrossRefPubMed
14.
go back to reference Tanaka T, Makita H, Ohnishi M, Hirose Y, Wang A, Mori H, et al. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary curcumin and hesperidin: comparison with the protective effect of β-carotene. Cancer Res. 1994;54:4653–9.PubMed Tanaka T, Makita H, Ohnishi M, Hirose Y, Wang A, Mori H, et al. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary curcumin and hesperidin: comparison with the protective effect of β-carotene. Cancer Res. 1994;54:4653–9.PubMed
15.
go back to reference Chiu CC, Liu PL, Huang KJ, Wang HM, Chang KF, Chou CK, et al. Goniothalamin inhibits growth of human lung cancer cells through DNA damage, apoptosis, and reduced migration ability. J Agric Food Chem. 2011;59:4288–93.CrossRefPubMed Chiu CC, Liu PL, Huang KJ, Wang HM, Chang KF, Chou CK, et al. Goniothalamin inhibits growth of human lung cancer cells through DNA damage, apoptosis, and reduced migration ability. J Agric Food Chem. 2011;59:4288–93.CrossRefPubMed
16.
go back to reference Fang HY, Wang HM, Chang KF, Hu HT, Hwang LJ, Fu TF, et al. Feruloyl-l-arabinose attenuates migration, invasion and production of reactive oxygen species in H1299 lung cancer cells. Food Chem Toxicol. 2013;58:459–66.CrossRefPubMed Fang HY, Wang HM, Chang KF, Hu HT, Hwang LJ, Fu TF, et al. Feruloyl-l-arabinose attenuates migration, invasion and production of reactive oxygen species in H1299 lung cancer cells. Food Chem Toxicol. 2013;58:459–66.CrossRefPubMed
17.
go back to reference Pai HC, Chang LH, Peng CY, Chang YL, Chen CC, Shen CC, et al. Moscatilin inhibits migration and metastasis of human breast cancer MDA-MB-231 cells through inhibition of Akt and Twist signaling pathway. J Mol Med (Berl). 2013;91:347–56.CrossRef Pai HC, Chang LH, Peng CY, Chang YL, Chen CC, Shen CC, et al. Moscatilin inhibits migration and metastasis of human breast cancer MDA-MB-231 cells through inhibition of Akt and Twist signaling pathway. J Mol Med (Berl). 2013;91:347–56.CrossRef
18.
go back to reference Kowitdamrong A, Chanvorachote P, Sritularak B, Pongrakhananon V. Moscatilin inhibits lung cancer cell motility and invasion via suppression of endogenous reactive oxygen species. Biomed Res Int. 2013;2013:765894.CrossRefPubMedPubMedCentral Kowitdamrong A, Chanvorachote P, Sritularak B, Pongrakhananon V. Moscatilin inhibits lung cancer cell motility and invasion via suppression of endogenous reactive oxygen species. Biomed Res Int. 2013;2013:765894.CrossRefPubMedPubMedCentral
19.
go back to reference Buanafina MM, Langdon T, Hauck B, Dalton S, Timms-Taravella E, Morris P. Targeting expression of a fungal ferulic acid esterase to the apoplast, endoplasmic reticulum or golgi can disrupt feruloylation of the growing cell wall and increase the biodegradability of tall fescue (Festuca arundinacea). Plant Biotechnol J. 2010;8:316–31.CrossRefPubMed Buanafina MM, Langdon T, Hauck B, Dalton S, Timms-Taravella E, Morris P. Targeting expression of a fungal ferulic acid esterase to the apoplast, endoplasmic reticulum or golgi can disrupt feruloylation of the growing cell wall and increase the biodegradability of tall fescue (Festuca arundinacea). Plant Biotechnol J. 2010;8:316–31.CrossRefPubMed
20.
21.
go back to reference Pan GX, Spencer L, Leary GJ. Reactivity of ferulic acid and its derivatives toward hydrogen peroxide and peracetic acid. J Agric Food Chem. 1999;47:3325–31.CrossRefPubMed Pan GX, Spencer L, Leary GJ. Reactivity of ferulic acid and its derivatives toward hydrogen peroxide and peracetic acid. J Agric Food Chem. 1999;47:3325–31.CrossRefPubMed
22.
go back to reference Hartley RD, Jones EC. Phenolic components and degradability of cell walls of grass and legume species. Phytochemistry. 1977;16:1531–4.CrossRef Hartley RD, Jones EC. Phenolic components and degradability of cell walls of grass and legume species. Phytochemistry. 1977;16:1531–4.CrossRef
23.
go back to reference Das U, Manna K, Sinha M, Datta S, Das DK, Chakraborty A, et al. Role of ferulic acid in the amelioration of ionizing radiation induced inflammation: a murine model. PLoS One. 2014;9:e97599.CrossRefPubMedPubMedCentral Das U, Manna K, Sinha M, Datta S, Das DK, Chakraborty A, et al. Role of ferulic acid in the amelioration of ionizing radiation induced inflammation: a murine model. PLoS One. 2014;9:e97599.CrossRefPubMedPubMedCentral
24.
go back to reference Manikandan R, Beulaja M, Thiagarajan R, Pandi M, Arulvasu C, Prabhu NM, et al. Ameliorative effect of ferulic acid against renal injuries mediated by nuclear factor-κB during glycerol-induced nephrotoxicity in Wistar rats. Ren Fail. 2014;36:154–65.CrossRefPubMed Manikandan R, Beulaja M, Thiagarajan R, Pandi M, Arulvasu C, Prabhu NM, et al. Ameliorative effect of ferulic acid against renal injuries mediated by nuclear factor-κB during glycerol-induced nephrotoxicity in Wistar rats. Ren Fail. 2014;36:154–65.CrossRefPubMed
25.
go back to reference Panneerselvam L, Subbiah K, Arumugam A, Senapathy JG. Ferulic acid modulates fluoride-induced oxidative hepatotoxicity in male Wistar rats. Biol Trace Elem Res. 2013;151:85–91.CrossRefPubMed Panneerselvam L, Subbiah K, Arumugam A, Senapathy JG. Ferulic acid modulates fluoride-induced oxidative hepatotoxicity in male Wistar rats. Biol Trace Elem Res. 2013;151:85–91.CrossRefPubMed
26.
go back to reference Yuan X, Wang J, Yao H. Antioxidant activity of feruloylated oligosaccharides from wheat bran. Food Chem. 2005;90:759–64.CrossRef Yuan X, Wang J, Yao H. Antioxidant activity of feruloylated oligosaccharides from wheat bran. Food Chem. 2005;90:759–64.CrossRef
27.
go back to reference Roy S, Metya SK, Sannigrahi S, Rahaman N, Ahmed F. Treatment with ferulic acid to rats with streptozotocin-induced diabetes: effects on oxidative stress, pro-inflammatory cytokines, and apoptosis in the pancreatic beta cell. Endocrine. 2013;44:369–79.CrossRefPubMed Roy S, Metya SK, Sannigrahi S, Rahaman N, Ahmed F. Treatment with ferulic acid to rats with streptozotocin-induced diabetes: effects on oxidative stress, pro-inflammatory cytokines, and apoptosis in the pancreatic beta cell. Endocrine. 2013;44:369–79.CrossRefPubMed
28.
go back to reference Ramar M, Manikandan B, Raman T, Priyadarsini A, Palanisamy S, Velayudam M, et al. Protective effect of ferulic acid and resveratrol against alloxan-induced diabetes in mice. Eur J Pharmacol. 2012;690:226–35.CrossRefPubMed Ramar M, Manikandan B, Raman T, Priyadarsini A, Palanisamy S, Velayudam M, et al. Protective effect of ferulic acid and resveratrol against alloxan-induced diabetes in mice. Eur J Pharmacol. 2012;690:226–35.CrossRefPubMed
29.
go back to reference Janicke B, Hegardt C, Krogh M, Onning G, Akesson B, Cirenajwis HM, et al. The antiproliferative effect of dietary fiber phenolic compounds ferulic acid and p-coumaric acid on the cell cycle of Caco-2 cells. Nutr Cancer. 2011;63:611–22.CrossRefPubMed Janicke B, Hegardt C, Krogh M, Onning G, Akesson B, Cirenajwis HM, et al. The antiproliferative effect of dietary fiber phenolic compounds ferulic acid and p-coumaric acid on the cell cycle of Caco-2 cells. Nutr Cancer. 2011;63:611–22.CrossRefPubMed
30.
go back to reference Jayaprakasam B, Vanisree M, Zhang Y, Dewitt DL, Nair MG. Impact of alkyl esters of caffeic and ferulic acids on tumor cell proliferation, cyclooxygenase enzyme, and lipid peroxidation. J Agric Food Chem. 2006;54:5375–81.CrossRefPubMed Jayaprakasam B, Vanisree M, Zhang Y, Dewitt DL, Nair MG. Impact of alkyl esters of caffeic and ferulic acids on tumor cell proliferation, cyclooxygenase enzyme, and lipid peroxidation. J Agric Food Chem. 2006;54:5375–81.CrossRefPubMed
31.
go back to reference Karthikeyan S, Kanimozhi G, Prasad NR, Mahalakshmi R. Radiosensitizing effect of ferulic acid on human cervical carcinoma cells in vitro. Toxicol In Vitro. 2011;25:1366–75.CrossRefPubMed Karthikeyan S, Kanimozhi G, Prasad NR, Mahalakshmi R. Radiosensitizing effect of ferulic acid on human cervical carcinoma cells in vitro. Toxicol In Vitro. 2011;25:1366–75.CrossRefPubMed
32.
go back to reference Stagos D, Kazantzoglou G, Magiatis P, Mitaku S, Anagnostopoulos K, Kouretas D. Effects of plant phenolics and grape extracts from Greek varieties of Vitis vinifera on mitomycin C and topoisomerase I-induced nicking of DNA. Int J Mol Med. 2005;15:1013–22.PubMed Stagos D, Kazantzoglou G, Magiatis P, Mitaku S, Anagnostopoulos K, Kouretas D. Effects of plant phenolics and grape extracts from Greek varieties of Vitis vinifera on mitomycin C and topoisomerase I-induced nicking of DNA. Int J Mol Med. 2005;15:1013–22.PubMed
33.
go back to reference Tanaka T, Kojima T, Kawamori T, Wang A, Suzui M, Okamoto K, et al. Inhibition of 4-nitroquinoline-1-oxide-induced rat tongue carcinogenesis by the naturally occurring plant phenolics caffeic, ellagic, chlorogenic and ferulic acids. Carcinogenesis. 1993;14:1321–5.CrossRefPubMed Tanaka T, Kojima T, Kawamori T, Wang A, Suzui M, Okamoto K, et al. Inhibition of 4-nitroquinoline-1-oxide-induced rat tongue carcinogenesis by the naturally occurring plant phenolics caffeic, ellagic, chlorogenic and ferulic acids. Carcinogenesis. 1993;14:1321–5.CrossRefPubMed
34.
go back to reference Blois MS. Antioxidant determinations by the use of a stable free radical. Nature. 1958;181:1199–200.CrossRef Blois MS. Antioxidant determinations by the use of a stable free radical. Nature. 1958;181:1199–200.CrossRef
35.
go back to reference Barreto JC, Trevisan MT, Hull WE, Erben G, de Brito ES, Pfundstein B, et al. Characterization and quantitation of polyphenolic compounds in bark, kernel, leaves, and peel of mango (Mangifera indica L.). J Agric Food Chem. 2008;56:5599–610.CrossRefPubMed Barreto JC, Trevisan MT, Hull WE, Erben G, de Brito ES, Pfundstein B, et al. Characterization and quantitation of polyphenolic compounds in bark, kernel, leaves, and peel of mango (Mangifera indica L.). J Agric Food Chem. 2008;56:5599–610.CrossRefPubMed
36.
go back to reference Tseng CN, Hong YR, Chang HW, Yu TJ, Hung TW, Hou MF, et al. Brefeldin A reduces anchorage-independent survival, cancer stem cell potential and migration of MDA-MB-231 human breast cancer cells. Molecules. 2014;19:17464–77.CrossRefPubMed Tseng CN, Hong YR, Chang HW, Yu TJ, Hung TW, Hou MF, et al. Brefeldin A reduces anchorage-independent survival, cancer stem cell potential and migration of MDA-MB-231 human breast cancer cells. Molecules. 2014;19:17464–77.CrossRefPubMed
37.
go back to reference Chiu CC, Li CH, Fuh TS, Chen WL, Huang CS, Chen LJ, et al. The suppressed proliferation and premature senescence by ganciclovir in p53-mutated human non-small-lung cancer cells acquiring herpes simplex virus-thymidine kinase cDNA. Cancer Detect Prev. 2005;29:286–93.CrossRefPubMed Chiu CC, Li CH, Fuh TS, Chen WL, Huang CS, Chen LJ, et al. The suppressed proliferation and premature senescence by ganciclovir in p53-mutated human non-small-lung cancer cells acquiring herpes simplex virus-thymidine kinase cDNA. Cancer Detect Prev. 2005;29:286–93.CrossRefPubMed
38.
go back to reference Chiu CC, Chen JY, Lin KL, Huang CJ, Lee JC, Chen BH, et al. p38 MAPK and NF-κB pathways are involved in naphtho[1,2-b] furan-4,5-dione induced anti-proliferation and apoptosis of human hepatoma cells. Cancer Lett. 2010;295:92–9.CrossRefPubMed Chiu CC, Chen JY, Lin KL, Huang CJ, Lee JC, Chen BH, et al. p38 MAPK and NF-κB pathways are involved in naphtho[1,2-b] furan-4,5-dione induced anti-proliferation and apoptosis of human hepatoma cells. Cancer Lett. 2010;295:92–9.CrossRefPubMed
39.
go back to reference Geback T, Schulz MM, Koumoutsakos P, Detmar M. TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques. 2009;46:265–74.PubMed Geback T, Schulz MM, Koumoutsakos P, Detmar M. TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques. 2009;46:265–74.PubMed
40.
go back to reference Tu B, Ma TT, Peng XQ, Wang Q, Yang H, Huang XL. Targeting of COX-2 expression by recombinant adenovirus shRNA attenuates the malignant biological behavior of breast cancer cells. Asian Pac J Cancer Prev. 2014;15:8829–36.CrossRefPubMed Tu B, Ma TT, Peng XQ, Wang Q, Yang H, Huang XL. Targeting of COX-2 expression by recombinant adenovirus shRNA attenuates the malignant biological behavior of breast cancer cells. Asian Pac J Cancer Prev. 2014;15:8829–36.CrossRefPubMed
41.
go back to reference Chu SC, Yang SF, Liu SJ, Kuo WH, Chang YZ, Hsieh YS. In vitro and in vivo antimetastatic effects of Terminalia catappa L. leaves on lung cancer cells. Food Chem Toxicol. 2007;45:1194–201.CrossRefPubMed Chu SC, Yang SF, Liu SJ, Kuo WH, Chang YZ, Hsieh YS. In vitro and in vivo antimetastatic effects of Terminalia catappa L. leaves on lung cancer cells. Food Chem Toxicol. 2007;45:1194–201.CrossRefPubMed
42.
go back to reference Wu WS. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 2006;25:695–705.CrossRefPubMed Wu WS. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 2006;25:695–705.CrossRefPubMed
43.
go back to reference Liu J, Ping W, Zu Y, Sun W. Correlations of lysyl oxidase with MMP2/MMP9 expression and its prognostic value in non-small cell lung cancer. Int J Clin Exp Pathol. 2014;7:6040–7.PubMedPubMedCentral Liu J, Ping W, Zu Y, Sun W. Correlations of lysyl oxidase with MMP2/MMP9 expression and its prognostic value in non-small cell lung cancer. Int J Clin Exp Pathol. 2014;7:6040–7.PubMedPubMedCentral
45.
go back to reference Chang CJ, Chiu JH, Tseng LM, Chang CH, Chien TM, Wu CW, et al. Modulation of HER2 expression by ferulic acid on human breast cancer MCF7 cells. Eur J Clin Invest. 2006;36:588–96.CrossRefPubMed Chang CJ, Chiu JH, Tseng LM, Chang CH, Chien TM, Wu CW, et al. Modulation of HER2 expression by ferulic acid on human breast cancer MCF7 cells. Eur J Clin Invest. 2006;36:588–96.CrossRefPubMed
46.
go back to reference Yabe T, Hirahara H, Harada N, Ito N, Nagai T, Sanagi T, et al. Ferulic acid induces neural progenitor cell proliferation in vitro and in vivo. Neuroscience. 2010;165:515–24.CrossRefPubMed Yabe T, Hirahara H, Harada N, Ito N, Nagai T, Sanagi T, et al. Ferulic acid induces neural progenitor cell proliferation in vitro and in vivo. Neuroscience. 2010;165:515–24.CrossRefPubMed
47.
go back to reference Koyama M, Sowa Y, Hitomi T, Iizumi Y, Watanabe M, Taniguchi T, et al. Perillyl alcohol causes G1 arrest through p15(INK4b) and p21(WAF1/Cip1) induction. Oncol Rep. 2013;29:779–84.PubMed Koyama M, Sowa Y, Hitomi T, Iizumi Y, Watanabe M, Taniguchi T, et al. Perillyl alcohol causes G1 arrest through p15(INK4b) and p21(WAF1/Cip1) induction. Oncol Rep. 2013;29:779–84.PubMed
48.
49.
go back to reference Clerkin JS, Naughton R, Quiney C, Cotter TG. Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer Lett. 2008;266:30–6.CrossRefPubMed Clerkin JS, Naughton R, Quiney C, Cotter TG. Mechanisms of ROS modulated cell survival during carcinogenesis. Cancer Lett. 2008;266:30–6.CrossRefPubMed
50.
go back to reference Wu XJ, Hua X. Targeting ROS: selective killing of cancer cells by a cruciferous vegetable derived pro-oxidant compound. Cancer Biol Ther. 2007;6:646–7.CrossRefPubMed Wu XJ, Hua X. Targeting ROS: selective killing of cancer cells by a cruciferous vegetable derived pro-oxidant compound. Cancer Biol Ther. 2007;6:646–7.CrossRefPubMed
51.
go back to reference Geest CR, Buitenhuis M, Groot Koerkamp MJ, Holstege FC, Vellenga E, Coffer PJ. Tight control of MEK-ERK activation is essential in regulating proliferation, survival, and cytokine production of CD34+ -derived neutrophil progenitors. Blood. 2009;114:3402–12.CrossRefPubMed Geest CR, Buitenhuis M, Groot Koerkamp MJ, Holstege FC, Vellenga E, Coffer PJ. Tight control of MEK-ERK activation is essential in regulating proliferation, survival, and cytokine production of CD34+ -derived neutrophil progenitors. Blood. 2009;114:3402–12.CrossRefPubMed
52.
go back to reference Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol. 2010;594:57–72.CrossRefPubMed Eruslanov E, Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol. 2010;594:57–72.CrossRefPubMed
53.
go back to reference Svensk AM, Soini Y, Paakko P, Hiravikoski P, Kinnula VL. Differential expression of superoxide dismutases in lung cancer. Am J Clin Pathol. 2004;122:395–404.CrossRefPubMed Svensk AM, Soini Y, Paakko P, Hiravikoski P, Kinnula VL. Differential expression of superoxide dismutases in lung cancer. Am J Clin Pathol. 2004;122:395–404.CrossRefPubMed
54.
go back to reference Zechner D, Fujita Y, Hulsken J, Muller T, Walther I, Taketo MM, et al. β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol. 2003;258:406–18.CrossRefPubMed Zechner D, Fujita Y, Hulsken J, Muller T, Walther I, Taketo MM, et al. β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol. 2003;258:406–18.CrossRefPubMed
55.
go back to reference Kim SI, Park CS, Lee MS, Kwon MS, Jho EH, Song WK. Cyclin-dependent kinase 2 regulates the interaction of axin with β-catenin. Biochem Biophys Res Commun. 2004;317:478–83.CrossRefPubMed Kim SI, Park CS, Lee MS, Kwon MS, Jho EH, Song WK. Cyclin-dependent kinase 2 regulates the interaction of axin with β-catenin. Biochem Biophys Res Commun. 2004;317:478–83.CrossRefPubMed
56.
go back to reference Garcia-Florez LJ, Gomez-Alvarez G, Frunza AM, Barneo-Serra L, Martinez-Alonso C, Fresno-Forcelledo MF. Predictive markers of response to neoadjuvant therapy in rectal cancer. J Surg Res. 2015;194:120–6.CrossRefPubMed Garcia-Florez LJ, Gomez-Alvarez G, Frunza AM, Barneo-Serra L, Martinez-Alonso C, Fresno-Forcelledo MF. Predictive markers of response to neoadjuvant therapy in rectal cancer. J Surg Res. 2015;194:120–6.CrossRefPubMed
57.
go back to reference Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, et al. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science. 1997;275:1787–90.CrossRefPubMed Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, et al. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science. 1997;275:1787–90.CrossRefPubMed
58.
go back to reference Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, et al. A Wnt-Axin2-GSK3β cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol. 2006;8:1398–406.CrossRefPubMed Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, et al. A Wnt-Axin2-GSK3β cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol. 2006;8:1398–406.CrossRefPubMed
59.
go back to reference Verras M, Sun Z. Roles and regulation of Wnt signaling and β-catenin in prostate cancer. Cancer Lett. 2006;237:22–32.CrossRefPubMed Verras M, Sun Z. Roles and regulation of Wnt signaling and β-catenin in prostate cancer. Cancer Lett. 2006;237:22–32.CrossRefPubMed
60.
go back to reference Pu P, Zhang Z, Kang C, Jiang R, Jia Z, Wang G, et al. Downregulation of Wnt2 and β-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther. 2009;16:351–61.CrossRefPubMed Pu P, Zhang Z, Kang C, Jiang R, Jia Z, Wang G, et al. Downregulation of Wnt2 and β-catenin by siRNA suppresses malignant glioma cell growth. Cancer Gene Ther. 2009;16:351–61.CrossRefPubMed
61.
go back to reference Stewart DJ. Wnt signaling pathway in non-small cell lung cancer. J Natl Cancer Inst. 2014;106:djt356.CrossRefPubMed Stewart DJ. Wnt signaling pathway in non-small cell lung cancer. J Natl Cancer Inst. 2014;106:djt356.CrossRefPubMed
62.
go back to reference Tetsu O, McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999;398:422–6.CrossRefPubMed Tetsu O, McCormick F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999;398:422–6.CrossRefPubMed
63.
go back to reference Li TW, Peng H, Yang H, Kurniawidjaja S, Panthaki P, Zheng Y, et al. S-Adenosylmethionine and methylthioadenosine inhibit β-catenin signaling by multiple mechanisms in liver and colon cancer. Mol Pharmacol. 2015;87:77–86.CrossRefPubMedPubMedCentral Li TW, Peng H, Yang H, Kurniawidjaja S, Panthaki P, Zheng Y, et al. S-Adenosylmethionine and methylthioadenosine inhibit β-catenin signaling by multiple mechanisms in liver and colon cancer. Mol Pharmacol. 2015;87:77–86.CrossRefPubMedPubMedCentral
64.
go back to reference Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science. 2007;317:803–6.CrossRefPubMed Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, et al. Augmented Wnt signaling in a mammalian model of accelerated aging. Science. 2007;317:803–6.CrossRefPubMed
65.
go back to reference Yoon JC, Ng A, Kim BH, Bianco A, Xavier RJ, Elledge SJ. Wnt signaling regulates mitochondrial physiology and insulin sensitivity. Genes Dev. 2010;24:1507–18.CrossRefPubMedPubMedCentral Yoon JC, Ng A, Kim BH, Bianco A, Xavier RJ, Elledge SJ. Wnt signaling regulates mitochondrial physiology and insulin sensitivity. Genes Dev. 2010;24:1507–18.CrossRefPubMedPubMedCentral
66.
go back to reference Zhang DY, Pan Y, Zhang C, Yan BX, Yu SS, Wu DL, et al. Wnt/β-catenin signaling induces the aging of mesenchymal stem cells through promoting the ROS production. Mol Cell Biochem. 2013;374:13–20.CrossRefPubMed Zhang DY, Pan Y, Zhang C, Yan BX, Yu SS, Wu DL, et al. Wnt/β-catenin signaling induces the aging of mesenchymal stem cells through promoting the ROS production. Mol Cell Biochem. 2013;374:13–20.CrossRefPubMed
67.
go back to reference Wu B, Crampton SP, Hughes CC. Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity. 2007;26:227–39.CrossRefPubMedPubMedCentral Wu B, Crampton SP, Hughes CC. Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity. 2007;26:227–39.CrossRefPubMedPubMedCentral
68.
go back to reference Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, bax, that accelerates programmed cell death. Cell. 1993;74:609–19.CrossRefPubMed Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, bax, that accelerates programmed cell death. Cell. 1993;74:609–19.CrossRefPubMed
69.
go back to reference Sah NK, Khan Z, Khan GJ, Bisen PS. Structural, functional and therapeutic biology of survivin. Cancer Lett. 2006;244:164–71.CrossRefPubMed Sah NK, Khan Z, Khan GJ, Bisen PS. Structural, functional and therapeutic biology of survivin. Cancer Lett. 2006;244:164–71.CrossRefPubMed
70.
go back to reference Ito T, Shiraki K, Sugimoto K, Yamanaka T, Fujikawa K, Ito M, et al. Survivin promotes cell proliferation in human hepatocellular carcinoma. Hepatology. 2000;31:1080–5.CrossRefPubMed Ito T, Shiraki K, Sugimoto K, Yamanaka T, Fujikawa K, Ito M, et al. Survivin promotes cell proliferation in human hepatocellular carcinoma. Hepatology. 2000;31:1080–5.CrossRefPubMed
71.
go back to reference Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I. Bistability in apoptosis: roles of bax, bcl-2, and mitochondrial permeability transition pores. Biophys J. 2006;90:1546–59.CrossRefPubMed Bagci EZ, Vodovotz Y, Billiar TR, Ermentrout GB, Bahar I. Bistability in apoptosis: roles of bax, bcl-2, and mitochondrial permeability transition pores. Biophys J. 2006;90:1546–59.CrossRefPubMed
72.
go back to reference Noel A, Jost M, Maquoi E. Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol. 2008;19:52–60.CrossRefPubMed Noel A, Jost M, Maquoi E. Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol. 2008;19:52–60.CrossRefPubMed
Metadata
Title
Inhibitory effect of trans-ferulic acid on proliferation and migration of human lung cancer cells accompanied with increased endogenous reactive oxygen species and β-catenin instability
Authors
Yao Fong
Chia-Chun Tang
Huei-Ting Hu
Hsin-Yu Fang
Bing-Hung Chen
Chang-Yi Wu
Shyng-Shiou Yuan
Hui-Min David Wang
Yen-Chun Chen
Yen-Ni Teng
Chien-Chih Chiu
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Chinese Medicine / Issue 1/2016
Electronic ISSN: 1749-8546
DOI
https://doi.org/10.1186/s13020-016-0116-7

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