Tetrandrine suppresses adhesion, migration and invasion of human colon cancer SW620 cells via inhibition of nuclear factor-κB, matrix metalloproteinase-2 and matrix metalloproteinase-9 signaling pathways

Juan,Ta‑Kuo; Liu,Kuo‑Ching; Kuo,Chao‑Lin; Yang,Mei‑Due; Chu,Yung‑Lin; Yang,Jiun‑Long; Wu,Ping‑Ping; Huang,Yi‑Ping; Lai,Kuang‑Chi; Chung,Jing‑Gung

doi:10.3892/ol.2018.8286

Tetrandrine suppresses adhesion, migration and invasion of human colon cancer SW620 cells via inhibition of nuclear factor-κB, matrix metalloproteinase-2 and matrix metalloproteinase-9 signaling pathways

Authors:
- Ta‑Kuo Juan
- Kuo‑Ching Liu
- Chao‑Lin Kuo
- Mei‑Due Yang
- Yung‑Lin Chu
- Jiun‑Long Yang
- Ping‑Ping Wu
- Yi‑Ping Huang
- Kuang‑Chi Lai
- Jing‑Gung Chung
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Affiliations: Department of Biological Science and Technology, China Medical University, Taichung 404, Taiwan, R.O.C., Department of Medical Laboratory Science and Biotechnology, China Medical University, Taichung 404, Taiwan, R.O.C., Department of Chinese Medicine Resources, China Medical University, Taichung 404, Taiwan, R.O.C., Department of Surgery, China Medical University Hospital, Taichung 404, Taiwan, R.O.C., International Master's Degree Program in Food Science, International College, National Pingtung University of Science and Technology, Pingtung 912, Taiwan, R.O.C., School of Pharmacy, China Medical University, Taichung 404, Taiwan, R.O.C., Department of Physiology, China Medical University, Taichung 404, Taiwan, R.O.C., School of Medicine, China Medical University, Taichung 404, Taiwan, R.O.C.
Published online on: March 16, 2018 https://doi.org/10.3892/ol.2018.8286
Pages: 7716-7724
Copyright: © Juan et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY_NC 4.0].

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Abstract

Tetrandrine (TET) exhibits biological activities, including anticancer activity. In Chinese medicine, TET has been used to treat hypertensive and arrhythmic conditions and has been demonstrated to induce cytotoxic effects on human cancer cell lines. However, to the best of the author's knowledge, no previous studies have revealed that TET affects cell metastasis in SW620 human colon cancer cells. The present study demonstrated that TET decreased the cell number and inhibited cell adhesion and mobility of SW620 cells. Furthermore, a wound healing assay was performed to demonstrate that TET suppressed cell movement, and Transwell chamber assays were used to reveal that TET suppressed the cell migration and invasion of SW620 cells. Western blotting demonstrated that TET significantly reduced protein expression levels of SOS Ras/Rac guanine nucleotide exchange factor 1, phosphatidylinositol 3‑kinase, growth factor receptor bound protein 2, phosphorylated (p)‑c Jun N‑terminal kinase 1/2, p‑p38, p38, 14‑3‑3, Rho A, β‑catenin, nuclear factor‑κB p65, signal transducer and activator of transcription‑1 and cyclooxygenase‑2, in comparison with untreated SW620 cells. Overall, the results of the present study suggested that TET may be used as a novel anti‑metastasis agent for the treatment of human colon cancer in the future.

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1	Siegel R, Desantis C and Jemal A: Colorectal cancer statistics, 2014. CA Cancer J Clin. 64:104–117. 2014. View Article : Google Scholar : PubMed/NCBI
2	Labianca R, Beretta GD, Kildani B, Milesi L, Merlin F, Mosconi S, Pessi MA, Prochilo T, Quadri A, Gatta G, et al: Colon cancer. Crit Rev Oncol Hematol. 74:106–133. 2010. View Article : Google Scholar : PubMed/NCBI
3	Ferlay J, Parkin DM and Steliarova-Foucher E: Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer. 46:765–781. 2010. View Article : Google Scholar : PubMed/NCBI
4	Li M and Gu J: Changing patterns of colorectal cancer in China over a period of 20 years. World J Gastroenterol. 11:4685–4688. 2005. View Article : Google Scholar : PubMed/NCBI
5	Ministry of Health and Welfare: The cancer mortality report of the Department of Health. Taiwan: 2014
6	Camp ER and Ellis LM: CCR 20th Anniversary Commentary: RAS as a Biomarker for EGFR-targeted therapy for colorectal cancer-from concept to practice. Clin Cancer Res. 21:3578–3580. 2015. View Article : Google Scholar : PubMed/NCBI
7	Siegel R, Ma J, Zou Z and Jemal A: Cancer statistics, 2014. CA Cancer J Clin. 64:9–29. 2014. View Article : Google Scholar : PubMed/NCBI
8	Hazan RB, Qiao R, Keren R, Badano I and Suyama K: Cadherin switch in tumor progression. Ann N Y Acad Sci. 1014:155–163. 2004. View Article : Google Scholar : PubMed/NCBI
9	Makrilia N, Kollias A, Manolopoulos L and Syrigos K: Cell adhesion molecules: Role and clinical significance in cancer. Cancer Invest. 27:1023–1037. 2009. View Article : Google Scholar : PubMed/NCBI
10	Babykutty S, Suboj P, Srinivas P, Nair AS, Chandramohan K and Gopala S: Insidious role of nitric oxide in migration/invasion of colon cancer cells by upregulating MMP-2/9 via activation of cGMP-PKG-ERK signaling pathways. Clin Exp Metastasis. 29:471–492. 2012. View Article : Google Scholar : PubMed/NCBI
11	Dung TD, Feng CC, Kuo WW, Pai P, Chung LC, Chang SH, Hsu HH, Tsai FJ, Lin YM and Huang CY: Suppression of plasminogen activators and the MMP-2/-9 pathway by a Zanthoxylum avicennae extract to inhibit the HA22T human hepatocellular carcinoma cell migration and invasion effects in vitro and in vivo via phosphatase 2A activation. Biosci Biotechnol Biochem. 77:1814–1821. 2013. View Article : Google Scholar : PubMed/NCBI
12	Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM and Shafie S: Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature. 284:67–68. 1980. View Article : Google Scholar : PubMed/NCBI
13	Lamouille S, Xu J and Derynck R: Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 15:178–196. 2014. View Article : Google Scholar : PubMed/NCBI
14	Kalluri R: EMT: When epithelial cells decide to become mesenchymal-like cells. J Clin. Invest. 119:1417–1419. 2009. View Article : Google Scholar
15	Acloque H, Adams MS, Fishwick K, Bronner-Fraser M and Nieto MA: Epithelial-mesenchymal transitions: The importance of changing cell state in development and disease. J Clin Invest. 119:1438–1449. 2009. View Article : Google Scholar : PubMed/NCBI
16	Kortylewski M, Xin H, Kujawski M, Lee H, Liu Y, Harris T, Drake C, Pardoll D and Yu H: Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell. 15:114–123. 2009. View Article : Google Scholar : PubMed/NCBI
17	Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI
18	Rieger-Christ KM, Lee P, Zagha R, Kosakowski M, Moinzadeh A, Stoffel J, Ben-Ze'ev A, Libertino JA and Summerhayes IC: Novel expression of N-cadherin elicits in vitro bladder cell invasion via the Akt signaling pathway. Oncogene. 23:4745–4753. 2004. View Article : Google Scholar : PubMed/NCBI
19	Tong W, Wang Q, Sun D and Suo J: Curcumin suppresses colon cancer cell invasion via AMPK-induced inhibition of NF-κB, uPA activator and MMP9. Oncol Lett. 12:4139–4146. 2016. View Article : Google Scholar : PubMed/NCBI
20	Han M, Song Y and Zhang X: Quercetin suppresses the migration and invasion in human colon cancer Caco-2 cells through regulating toll-like receptor 4/nuclear factor-kappa B Pathway. Pharmacogn Mag. 12 Suppl 2:S237–S244. 2016. View Article : Google Scholar : PubMed/NCBI
21	Yun JH, Kim KA, Yoo G, Kim SY, Shin JM, Kim JH, Jung SH, Kim J and Nho CW: Phenethyl isothiocyanate suppresses cancer stem cell properties in vitro and in a xenograft model. Phytomedicine. 30:42–49. 2017. View Article : Google Scholar : PubMed/NCBI
22	Kuo PL and Lin CC: Tetrandrine-induced cell cycle arrest and apoptosis in Hep G2 cells. Life Sci. 73:243–252. 2003. View Article : Google Scholar : PubMed/NCBI
23	Lee JH, Kang GH, Kim KC, Kim KM, Park DI, Choi BT, Kang HS, Lee YT and Choi YH: Tetrandrine-induced cell cycle arrest and apoptosis in A549 human lung carcinoma cells. Int J Oncol. 21:1239–1244. 2002.PubMed/NCBI
24	Meng LH, Zhang H, Hayward L, Takemura H, Shao RG and Pommier Y: Tetrandrine induces early G1 arrest in human colon carcinoma cells by down-regulating the activity and inducing the degradation of G1-S-specific cyclin-dependent kinases and by inducing p53 and p21Cip1. Cancer Res. 64:9086–9092. 2004. View Article : Google Scholar : PubMed/NCBI
25	Chen XL, Ren KH, He HW and Shao RG: Involvement of PI3K/AKT/GSK3beta pathway in tetrandrine-induced G1 arrest and apoptosis. Cancer Biol Ther. 7:1073–1078. 2008. View Article : Google Scholar : PubMed/NCBI
26	McCubrey JA, Basecke J, Cervello M, Martelli AM and Franklin RA: GSK-3beta is a critical mediator of tetrandrine induced cell cycle arrest and cytotoxicity. Cancer Biol Ther. 7:10792008. View Article : Google Scholar : PubMed/NCBI
27	Liu W, Kou B, Ma ZK, Tang XS, Lv C, Ye M, Chen JQ, Li L, Wang XY and He DL: Tetrandrine suppresses proliferation, induces apoptosis, and inhibits migration and invasion in human prostate cancer cells. Asian J Androl. 17:850–853. 2015.PubMed/NCBI
28	Gao JL, Ji X, He TC, Zhang Q, He K, Zhao Y, Chen SH and Lv GY: Tetrandrine suppresses cancer angiogenesis and metastasis in 4T1 tumor bearing mice. Evid Based Complement. Alternat Med. 2013:2650612013.
29	Horng CT, Yang JS, Chiang JH, Lu CC, Lee CF, Chiang NN and Chen FA: Inhibitory effects of tetrandrine on epidermal growth factor-induced invasion and migration in HT29 human colorectal adenocarcinoma cells. Mol Med Rep. 13:1003–1009. 2016. View Article : Google Scholar : PubMed/NCBI
30	Xu H, Hou Z, Zhang H, Kong H, Li X, Wang H and Xie W: An efficient Trojan delivery of tetrandrine by poly(N-vinylpyrrolidone)-block-poly(ε-caprolactone) (PVP-b-PCL) nanoparticles shows enhanced apoptotic induction of lung cancer cells and inhibition of its migration and invasion. Int J Nanomedicine. 9:231–242. 2014.PubMed/NCBI
31	Zhang JS, Li DM, Ma Y, He N, Gu Q, Wang FS, Jiang SQ, Chen BQ and Liu JR: γ-Tocotrienol induces paraptosis-like cell death in human colon carcinoma SW620 cells. PLoS One. 8:e577792013. View Article : Google Scholar : PubMed/NCBI
32	Chang YM, Velmurugan BK, Kuo WW, Chen YS, HO TJ, Tsai CT, Ye CX, Tsai CH, Tsai FJ and Huang CY: Inhibitory effect of alpinate Oxyphyllae fructus extracts on Ang II-induced cardiac pathological remodeling-related pathways in H9c2 cardiomyoblast cells. Biomedicine. 3:148–152. 2013. View Article : Google Scholar
33	Park WH, Seol JG, Kim ES, Hyun JM, Jung CW, Lee CC, Kim BK and Lee YY: Arsenic trioxide-mediated growth inhibition in MC/CAR myeloma cells via cell cycle arrest in association with induction of cyclin-dependent kinase inhibitor, p21, and apoptosis. Cancer Res. 60:3065–3071. 2000.PubMed/NCBI
34	Lai KC, Hsu SC, Yang JS, Yu CC, Lein JC and Chung JG: Diallyl trisulfide inhibits migration, invasion and angiogenesis of human colon cancer HT-29 cells and umbilical vein endothelial cells, and suppresses murine xenograft tumour growth. J Cell Mol Med. 19:474–484. 2015. View Article : Google Scholar : PubMed/NCBI
35	Verhoeff JJ, van Tellingen O, Claes A, Stalpers LJ, van Linde ME, Richel DJ, Leenders WP and van Furth WR: Concerns about anti-angiogenic treatment in patients with glioblastoma multiforme. BMC Cancer. 9:4442009. View Article : Google Scholar : PubMed/NCBI
36	Cheng SH, Jian JJ, Tsai SY, Chan KY, Yen LK, Chu NM, Tan TD, Tsou MH and Huang AT: Prognostic features and treatment outcome in locoregionally advanced nasopharyngeal carcinoma following concurrent chemotherapy and radiotherapy. Int J Radiat Oncol Biol Phys. 41:755–762. 1998. View Article : Google Scholar : PubMed/NCBI
37	Gupta GP and Massague J: Cancer metastasis: Building a framework. Cell. 127:679–695. 2006. View Article : Google Scholar : PubMed/NCBI
38	Huang YL, Chu YL, Ho CT, Chung JG, Lai CI, Su YC, Kuo YH and Sheen LY: Antcin K, an active triterpenoid from the fruiting bodies of basswood-cultivated antrodia cinnamomea, inhibits metastasis via suppression of integrin-mediated adhesion, migration, and invasion in human hepatoma cells. J Agric Food Chem. 63:4561–4569. 2015. View Article : Google Scholar : PubMed/NCBI
39	Park SJ, Kong HK, Kim YS, Lee YS and Park JH: Inhibition of S-adenosylhomocysteine hydrolase decreases cell mobility and cell proliferation through cell cycle arrest. Am J Cancer Res. 5:2127–2138. 2015.PubMed/NCBI
40	Wu ZY, Lien JC, Huang YP, Liao CL, Lin JJ, Fan MJ, Ko YC, Hsiao YP, Lu HF and Chung JG: Casticin inhibits A375.S2 human melanoma cell migration/invasion through downregulating NF-κB and matrix metalloproteinase-2 and −1. Molecules. 21:3842016. View Article : Google Scholar : PubMed/NCBI
41	Ji BC, Hsiao YP, Tsai CH, Chang SJ, Hsu SC, Liu HC, Huang YP, Lien JC and Chung JG: Cantharidin impairs cell migration and invasion of A375.S2 human melanoma cells by suppressing MMP-2 and −9 through PI3K/NF-κB signaling pathways. Anticancer Res. 35:729–738. 2015.PubMed/NCBI
42	Liao CL, Lai KC, Huang AC, Yang JS, Lin JJ, Wu SH, Wood Gibson W, Lin JG and Chung JG: Gallic acid inhibits migration and invasion in human osteosarcoma U-2 OS cells through suppressing the matrix metalloproteinase-2/-9, protein kinase B (PKB) and PKC signaling pathways. Food Chem Toxicol. 50:1734–1740. 2012. View Article : Google Scholar : PubMed/NCBI
43	Kessenbrock K, Plaks V and Werb Z: Matrix metalloproteinases: Regulators of the tumor microenvironment. Cell. 141:52–67. 2010. View Article : Google Scholar : PubMed/NCBI
44	Shia CS, Suresh G, Hou YC, Lin YC, Chao PD and Juang SH: Suppression on metastasis by rhubarb through modulation on MMP-2 and uPA in human A549 lung adenocarcinoma: An ex vivo approach. J Ethnopharmacol. 133:426–433. 2011. View Article : Google Scholar : PubMed/NCBI
45	Bauvois B: New facets of matrix metalloproteinases MMP-2 and MMP-9 as cell surface transducers: Outside-in signaling and relationship to tumor progression. Biochim Biophys Acta. 1825:29–36. 2012.PubMed/NCBI
46	Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A and Engler JA: Matrix metalloproteinases: A review. Crit Rev Oral Biol Med. 4:197–250. 1993. View Article : Google Scholar : PubMed/NCBI
47	Dutta A, Li J, Lu H, Akech J, Pratap J, Wang T, Zerlanko BJ, FitzGerald TJ, Jiang Z, Birbe R, et al: Integrin αvβ6 promotes an osteolytic program in cancer cells by upregulating MMP2. Cancer Res. 74:1598–1608. 2014. View Article : Google Scholar : PubMed/NCBI
48	Lai KC, Hsu SC, Kuo CL, Ip SW, Yang JS, Hsu YM, Huang HY, Wu SH and Chung JG: Phenethyl isothiocyanate inhibited tumor migration and invasion via suppressing multiple signal transduction pathways in human colon cancer HT29 cells. J Agric Food Chem. 58:11148–11155. 2010. View Article : Google Scholar : PubMed/NCBI
49	Matsumura T, Sugimachi K, Takahashi Y, Uchi R, Sawada G, Ueda M, Hirata H, Sakimura S, Ueo H, Takano Y, et al: Clinical significance of GAB2, a scaffolding/docking protein acting downstream of EGFR in human colorectal cancer. Ann Surg Oncol. 21 Suppl 4:S743–S749. 2014. View Article : Google Scholar : PubMed/NCBI
50	Waseem T, Duxbury M, Ashley SW and Robinson MK: Ghrelin promotes intestinal epithelial cell proliferation through PI3K/Akt pathway and EGFR trans-activation both converging to ERK 1/2 phosphorylation. Peptides. 52:113–121. 2014. View Article : Google Scholar : PubMed/NCBI
51	Hsu HH, Hu WS, Lin YM, Kuo WW, Chen LM, Chen WK, Hwang JM, Tsai FJ, Liu CJ and Huang CY: JNK suppression is essential for 17β-estradiol inhibits prostaglandin E2-induced uPA and MMP-9 expressions and cell migration in human LoVo colon cancer cells. J Biomed Sci. 18:612011. View Article : Google Scholar : PubMed/NCBI
52	Xiang T, Fei R, Wang Z, Shen Z, Qian J and Chen W: Nicotine enhances invasion and metastasis of human colorectal cancer cells through the nicotinic acetylcholine receptor downstream p38 MAPK signaling pathway. Oncol Rep. 35:205–210. 2016. View Article : Google Scholar : PubMed/NCBI
53	Zhao GY, Ding JY, Lu CL, Lin ZW and Guo J: The overexpression of 14-3-3ζ and Hsp27 promotes non-small cell lung cancer progression. Cancer. 120:652–663. 2014. View Article : Google Scholar : PubMed/NCBI
54	Jeong D, Park S, Kim H, Kim CJ, Ahn TS, Bae SB, Kim HJ, Kim TH, Im J and Lee MS: RhoA is associated with invasion and poor prognosis in colorectal cancer. Int J Oncol. 48:714–722. 2016. View Article : Google Scholar : PubMed/NCBI
55	Clevers H: Wnt/β-catenin signaling in development and disease. Cell. 127:469–480. 2006. View Article : Google Scholar : PubMed/NCBI
56	White BD, Chien AJ and Dawson DW: Dysregulation of Wnt/β-catenin signaling in gastrointestinal cancers. Gastroenterology. 142:219–232. 2012. View Article : Google Scholar : PubMed/NCBI
57	Norwood MG, Bailey N, Nanji M, Gillies RS, Nicholson A, Ubhi S, Darnton JJ, Steyn RS, Womack C, Hughes A, et al: Cytoplasmic beta-catenin accumulation is a good prognostic marker in upper and lower gastrointestinal adenocarcinomas. Histopathology. 57:101–111. 2010. View Article : Google Scholar : PubMed/NCBI
58	Kobayashi M, Honma T, Matsuda Y, Suzuki Y, Narisawa R, Ajioka Y and Asakura H: Nuclear translocation of beta-catenin in colorectal cancer. Br J Cancer. 82:1689–1693. 2000.PubMed/NCBI
59	Guttridge DC, Albanese C, Reuther JY, Pestell RG and Baldwin AS Jr: NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol. 19:5785–5799. 1999. View Article : Google Scholar : PubMed/NCBI
60	Yamamoto Y and Gaynor RB: Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer. J Clin Invest. 107:135–142. 2001. View Article : Google Scholar : PubMed/NCBI
61	Fryknas M, Dhar S, Oberg F, Rickardson L, Rydåker M, Göransson H, Gustafsson M, Pettersson U, Nygren P, Larsson R and Isaksson A: STAT1 signaling is associated with acquired crossresistance to doxorubicin and radiation in myeloma cell lines. Int J Cancer. 120:189–195. 2007. View Article : Google Scholar : PubMed/NCBI
62	Roberts D, Schick J, Conway S, Biade S, Laub PB, Stevenson JP, Hamilton TC, O'Dwyer PJ and Johnson SW: Identification of genes associated with platinum drug sensitivity and resistance in human ovarian cancer cells. Br J Cancer. 92:1149–1158. 2005. View Article : Google Scholar : PubMed/NCBI
63	Hasegawa K, Ichikawa W, Fujita T, Ohno R, Okusa T, Yoshinaga K and Sugihara K: Expression of cyclooxygenase-2 (COX-2) mRNA in human colorectal adenomas. Eur J Cancer. 37:1469–1474. 2001. View Article : Google Scholar : PubMed/NCBI
64	Peek RM Jr: Prevention of colorectal cancer through the use of COX-2 selective inhibitors. Cancer Chemother Pharmacol. 54 Suppl 1:S50–S56. 2004.PubMed/NCBI
65	Dempke W, Rie C, Grothey A and Schmoll HJ: Cyclooxygenase-2: A novel target for cancer chemotherapy? J Cancer Res Clin Oncol. 127:411–417. 2001. View Article : Google Scholar : PubMed/NCBI
66	Giercksky KE: COX-2 inhibition and prevention of cancer. Best Pract Res Clin Gastroenterol. 15:821–833. 2001. View Article : Google Scholar : PubMed/NCBI
67	Zhang H and Sun XF: Overexpression of cyclooxygenase-2 correlates with advanced stages of colorectal cancer. Am J Gastroenterol. 97:1037–1041. 2002. View Article : Google Scholar : PubMed/NCBI