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BMC Complementary Medicine and Therapies
Published in: BMC Complementary Medicine and Therapies 1/2019

Open Access 01-12-2019 | Colorectal Cancer | Research article

Extracts from Sageretia thea reduce cell viability through inducing cyclin D1 proteasomal degradation and HO-1 expression in human colorectal cancer cells

Authors: Ha Na Kim, Gwang Hun Park, Su Bin Park, Jeong Dong Kim, Hyun Ji Eo, Ho-Jun Son, Jeong Ho Song, Jin Boo Jeong

Published in: BMC Complementary Medicine and Therapies | Issue 1/2019

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Abstract

Background

Sageretia thea (S. thea) has been used as the medicinal plant for treating hepatitis and fevers in Korea and China. Recently, anticancer activity of S. thea has been reported, but the potential mechanism for the anti-cancer property of S. thea is still insufficient. Thus, we evaluated whether extracts from the leaves (STL) and branches (STB) of S. thea exert anticancer activity and elucidated its potential mechanism in SW480 cells.

Methods

MTT assay was performed for measuring cell viability. Western blot and RT-PCR were used for analyzing the level of protein and mRNA, respectively.

Results

Treatment of STL or STB decreased the cell viability and induced apoptosis in SW480 cells. Decreased level of cyclin D1 protein was observed in SW480 cells treated with STL or STB, but no change in cyclin D1 mRNA level was observed with the treatment of STL or STB. MG132 blocked downregulation of cyclin D1 protein by STL or STB. Thr286 phosphorylation of cyclin D1 by STL or STB occurred faster than downregulation of cyclin D1 protein in SW480 cells. When SW480 cells were transfected with T286A-cyclin D1, cyclin D1 degradation by STL or STB did not occur. Inhibition of GSK3β and cyclin D1 nuclear export attenuated STL or STB-mediated cyclin D1 degradation. In addition, STL or STB increased HO-1 expression, and the inhibition of HO-1 attenuated the induction of apoptosis by STL or STB. HO-1 expression by STL or STB resulted from Nrf2 activation through ROS-dependent p38 activation.

Conclusions

These results indicate that STL or STB may induce GSK3β-dependent cyclin D1 degradation, and increase HO-1 expression through activating Nrf2 via ROS-dependent p38 activation, which resulted in the decrease of the viability in SW480 cells. These findings suggest that STL or STB may have great potential for the development of anti-cancer drug.
Literature
1.
2.
Arnold M, Sierra MS, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global patterns and trends in colorectal cancer incidence and mortality. Gut. 2017;66(4):683–91.PubMedCrossRef
3.
Meyerhardt JA, Mayer RJ. Systemic therapy for colorectal cancer. N Engl J Med. 2005;352(5):476–87.PubMedCrossRef
4.
Polachi N, Subramaniyan B, Nagaraja P, Rangiah K, Ganeshan M. Extract from Butea monosperma inhibits β-catenin/Tcf signaling in SW480 human colon cancer cells. Gene Rep. 2018;10:79–89.CrossRef
5.
Benarba B, Belabid L, Righi K, Bekkar AA, Elouissi M, Khaldi A, Hamimed A. Study of medicinal plants used by traditional healers in Mascara (north west of Algeria). J Ethnopharmacol. 2015;175:626–37.PubMedCrossRef
6.
Shukla S, Mehta A. Anticancer potential of medicinal plants and their phytochemicals: a review. Braz J Bot. 2015;38:199–210.CrossRef
7.
Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer. 2011;11:558–72.PubMedCrossRef
8.
9.
Yasui M, Yamamoto H, Ngan CY, Damdinsuren B, Sugita Y, Fukunaga H, Gu J, Maeda M, Takemasa I, Ikeda M, Fujio Y, Sekimoto M, Matsuura N, Weinstein IB, Monden M. Antisense to cyclin D1 inhibits vascular endothelial growth factor-stimulated growth of vascular endothelial cells: implication of tumor vascularization. Clin Cancer Rese. 2006;12(15):4720–9.CrossRef
10.
Zhang L, Fried FB, Guo H, Friedman AD. Cyclin-dependent kinase phosphorylation of RUNX1/AML1 on 3 sites increases transactivation potency and stimulates cell proliferation. Blood. 2008;111(3):1193–200.PubMedPubMedCentralCrossRef
11.
Roue G, Pichereau V, Lincet H, Colomer D, Sola B. Cyclin D1 mediates resistance to apoptosis through upregulation of molecular chaperones and consequent redistribution of cell death regulators. Oncogene. 2008;27(36):4909–20.PubMedCrossRef
12.
Driscoll B, Buckley S, Barsky L, Weinberg K, Anderson KD, Warburton D. Abrogation of cyclin D1 expression predisposes lung cancer cells to serum deprivation-induced apoptosis. Am J Phys. 1999;276:L679–87.
13.
Sauter ER, Nesbit M, Litwin S, Klein-Szanto AJ, Cheffetz S, Herlyn M. Antisense cyclin D1 induces apoptosis and tumor shrinkage in human squamous carcinomas. Cancer Res. 1999;59(19):4876–81.PubMed
14.
Albanese C, D'Amico M, Reutens AT, Fu M, Watanabe G, Lee RJ, Kitsis RN, Henglein B, Avantaggiati M, Somasundaram K, Thimmapaya B, Pestell RG. Activation of the cyclin D1 gene by the E1A-associated protein p300 through AP-1 inhibits cellular apoptosis. J Biol Chem. 1999;274(48):34186–95.PubMedCrossRef
15.
Bahnassy AA, Zekri AR, El-Houssini S, El-Shehaby AM, Mahmoud MR, Abdallah S, El-Serafi M. Cyclin a and cyclin D1 as significant prognostic markers in colorectal cancer patients. BMC Gastroenterol. 2004;23(4):22–4.CrossRef
16.
Balcerczak E, Pasz-Walczak G, Kumor P, Panczyk M, Kordek R, Wierzbicki R, Mirowski M. Cyclin D1 protein and CCND1 gene expression in colorectal cancer. Eur J Surg Oncol. 2005;31(7):721–6.PubMedCrossRef
17.
Podkalicka P, Mucha O, Jozkowicz A, Dulak J, Loboda A. Heme oxygenase inhibition in cancers: possible tools and targets. Contemp. Oncol. (Pozn) 2018;22(1A):23–32.
18.
Castilho A, Aveleira CA, Leal EC, Simoes NF, Fernandes CR, Meirinhos RI, Baptista FI, Ambrosio AF. Heme oxygenase-1 protects retinal endothelial cells against high glucose- and oxidative/nitrosative stress-induced toxicity. PLoS One. 2012;7(8):e42428.PubMedPubMedCentralCrossRef
19.
Chen YC, Chow JM, Lin CW, Wu CY, Shen SC. Baicalein inhibition of oxidative-stress-induced apoptosis via modulation of ERKs activation and induction of HO-1 gene expression in rat glioma cells C6. Toxicol Appl Pharmacol. 2006;216(2):263–73.PubMedCrossRef
20.
Lee IT, Luo SF, Lee CW, Wang SW, Lin CC, Chang CC, Chen YL, Chau LY, Yang CM. Overexpression of HO-1 protects against TNF-alpha-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress. Am J Pathol. 2009;175(2):519–32.PubMedPubMedCentralCrossRef
21.
Lin HY, Shen SC, Lin CW, Yang LY, Chen YC. Baicalein inhibition of hydrogen peroxide-induced apoptosis via ROS-dependent heme oxygenase 1 gene expression. Biochim Biophys Acta. 2007;1773(7):1073–86.PubMedCrossRef
22.
Berberat PO, Dambrauskas Z, Gulbinas A, Giese T, Giese N, Kunzli B, Autschbach F, Meuer S, Buchler MW, Friess H. Inhibition of heme oxygenase-1 increases responsiveness of pancreatic cancer cells to anticancer treatment. Clin Cancer Res. 2005;11(10):3790–8.PubMedCrossRef
23.
Was H, Cichon T, Smolarczyk R, Rudnicka D, Stopa M, Chevalier C, Leger JJ, Lackowska B, Grochot A, Bojkowska K, Ratajska A, Kieda C, Szala S, Dulak J, Jozkowicz A. Overexpression of heme oxygenase-1 in murine melanoma: increased proliferation and viability of tumor cells, decreased survival of mice. Am J Pathol. 2006;169(6):2181–98.PubMedPubMedCentralCrossRef
24.
Ciesla M, Marona P, Kozakowska M, Jez M, Seczynska M, Loboda A, Bukowska-Strakova K, Szade A, Walawender M, Kusior M, Stepniewski J, Szade K, Krist B, Yagensky O, Urbanik A, Kazanowska B, Dulak J, Jozkowicz A. Heme Oxygenase-1 controls an HDAC4-miR-206 pathway of oxidative stress in rhabdomyosarcoma. Cancer Res. 2016;76(19):5707–18.PubMedCrossRef
25.
Hill M, Pereira V, Chauveau C, Zagani R, Remy S, Tesson L, Mazal D, Ubillos L, Brion R, Asghar K, Mashreghi MF, Kotsch K, Moffett J, Doebis C, Seifert M, Boczkowski J, Osinaga E, Anegon I. Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J. 2005;19(14):1957–68.PubMedCrossRef
26.
Gueron G, De Siervi A, Ferrando M, Salierno M, De Luca P, Elguero B, Meiss R, Navone N, Vazquez ES. Critical role of endogenous heme oxygenase 1 as a tuner of the invasive potential of prostate cancer cells. Mol Cancer Res. 2009;7(11):1745–55.PubMedCrossRef
27.
Yin H, Fang J, Liao L, Maeda H, Su Q. Upregulation of heme oxygenase-1 in colorectal cancer patients with increased circulation carbon monoxide levels, potentially affects chemotherapeutic sensitivity. BMC Cancer. 2014;14:436.PubMedPubMedCentralCrossRef
28.
Zou C, Zhang H, Li Q, Xiao H, Yu L, Ke S, Zhou L, Liu W, Wang W, Huang H, Ma N, Liu Q, Wang X, Zhao W, Zhou H, Gao X. Heme oxygenase-1: a molecular brake on hepatocellular carcinoma cell migration. Carcinogenesis. 2011;32(12):1840–8.PubMedCrossRef
29.
Chung SK, Chen CY, Blumberg JB. Flavonoid-rich fraction from Sageretia theezans leaves scavenges reactive oxygen radical species and increases the resistance of low-density lipoprotein to oxidation. J Med Food. 2009;12(6):1310–5.PubMedCrossRef
30.
Hyun TK, Song SC, Song CK, Kim JS. Nutritional and nutraceutical characteristics of Sageretia theezans fruit. J Food Drug Anal. 2015;23(4):742–9.PubMedCrossRef
31.
Ko GA, Shrestha S, Kim CS. Sageretia thea fruit extracts rich in methyl linoleate and methyl linolenate downregulate melanogenesis via the Akt/GSK3beta signaling pathway. Nutr Res Pract. 2018;12(1):3–12.PubMedPubMedCentralCrossRef
32.
Park JC, Hur JM, Park JG, Hatano T, Yoshida T, Miyashiro H, Min BS, Hattori M. Inhibitory effects of Korean medicinal plants and camelliatannin H from Camellia japonica on human immunodeficiency virus type 1 protease. Phytother Res. 2002;16(5):422–6.PubMedCrossRef
33.
Ko GA, Son M, Cho SK. Comparative evaluation of free radical scavenging activities and cytotoxicity of various solvent fractions of Sandong Sageretia thea (Osbeck) M.C. Johnst. Branches. Food Sci. Biotechnol. 2016;25(6):1683–91.
34.
Balaji C, Muthukumaran J, Vinothkumar R, Nalini N. Anticancer effects of sinapic acid on human colon cancer cell lines HT-29 and SW480. Int J Pharm Biol Arch. 2014;5(3):176–83.
35.
Li Y, Wei J, Xu C, Zhao Z, You T. Prognostic significance of cyclin D1 expression in colorectal cancer: a meta-analysis of observational studies. PLoS One. 2014;9(4):e94508.PubMedPubMedCentralCrossRef
36.
37.
Okabe H, Lee SH, Phuchareon J, Albertson DG, McCormick F, Tetsu O. A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PLoS One. 2006;1:e128.PubMedPubMedCentralCrossRef
38.
Casanovas O, Miro F, Estanyol JM, Itarte E, Agell N, Bachs O. Osmotic stress regulates the stability of cyclin D1 in a p38SAPK2-dependent manner. J Biol Chem. 2000;275(45):35091–7.PubMedCrossRef
39.
Thoms HC, Dunlop MG, Stark LA. p38-mediated inactivation of cyclin D1/cyclin-dependent kinase 4 stimulates nucleolar translocation of RelA and apoptosis in colorectal cancer cells. Cancer Res. 2007;67(4):1660–9.PubMedCrossRef
40.
Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998;12(22):3499–511.PubMedPubMedCentralCrossRef
41.
Becker JC, Fukui H, Imai Y, Sekikawa A, Kimura T, Yamagishi H, Yoshitake N, Pohle T, Domschke W, Fujimori T. Colonic expression of heme oxygenase-1 is associated with a better long-term survival in patients with colorectal cancer. Scand J Gastroenterol. 2007;42(7):852–8.PubMedCrossRef
42.
Kang KA, Maeng YH, Zhang R, Yang YR, Piao MJ, Kim KC, Kim GY, Kim YR, Koh YS, Kang HK, Hyun CL, Chang WY, Hyun JW. Involvement of heme oxygenase-1 in Korean colon cancer. Tumour Biol. 2012;33(4):1031–8.PubMedCrossRef
43.
Andrés NC, Fermento ME, Gandini NA, Romero AL, Ferro A, Donna LG, Curino AC, Facchinetti MM. Heme oxygenase-1 has antitumoral effects in colorectal cancer: involvement of p53. Exp Mol Pathol. 2014;97(3):321–31.PubMedCrossRef
44.
Park EJ, Lim JH, Nam SI, Park JW, Kwon TK. Rottlerin induces heme oxygenase-1 (HO-1) up-regulation through reactive oxygen species (ROS) dependent and PKC delta-independent pathway in human colon cancer HT29 cells. Biochimie. 2010;92(1):110–5.PubMedCrossRef
45.
Nicco C, Batteux F. ROS modulator molecules with therapeutic potential in cancers treatments. Molecules. 2017;23(1):E84.PubMedCrossRef
46.
Gillett C, Fantl V, Smith R, Fisher C, Bartek J, Dickson C, Barnes D, Peters G. Amplification and overexpression of cyclin D1 in breast cancer detected by immunohistochemical staining. Cancer Res. 1994;54(7):1812–7.PubMed
47.
Barbash O, Diehl JA. SCF(Fbx4/alphaB-crystallin) E3 ligase: when one is not enough. Cell Cycle. 2008;7:2983–6.PubMedCrossRef
48.
Yu XJ, Han QB, Wen ZS, Ma L, Gao J, Zhou GB. Gambogenic acid induces G1 arrest via GSK3beta-dependent cyclin D1 degradation and triggers autophagy in lung cancer cells. Cancer Lett. 2012;322(2):185–94.PubMedCrossRef
49.
Cheng YH, Li LA, Lin P, Cheng LC, Hung CH, Chang NW, Lin C. Baicalein induces G1 arrest in oral cancer cells by enhancing the degradation of cyclin D1 and activating AhR to decrease Rb phosphorylation. Toxicol Appl Pharmacol. 2012;263(3):360–7.PubMedCrossRef
50.
Park GH, Song HM, Jeong JB. The coffee diterpene kahweol suppresses the cell proliferation by inducing cyclin D1 proteasomal degradation via ERK1/2, JNK and GKS3beta-dependent threonine-286 phosphorylation in human colorectal cancer cells. Food Chem Toxicol. 2016;95:142–8.PubMedCrossRef
51.
Cornblatt BS, Ye L, Dinkova-Kostova AT, Erb M, Fahey JW, Singh NK, Chen MS, Stierer T, Garrett-Mayer E, Argani P, Davidson NE, Talalay P, Kensler TW, Visvanathan K. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast. Carcinogenesis. 2007;28(7):1485–90.PubMedCrossRef
52.
Keum YS, Yu S, Chang PP, Yuan X, Kim JH, Xu C, Han J, Agarwal A, Kong AN. Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res. 2006;66(17):8804–13.PubMedCrossRef
53.
Xu L, Yang X, Li B. Chemical constituents of Sageretia theezans Brongn. Zhongguo Zhong yao za zhi. 1994;19:675–6.PubMed
54.
Chung SK, Kim YC, Takaya Y, Terashima K, Niwa M. Novel flavonol glycoside, 7-O-methyl mearnsitrin, from Sageretia theezans and its antioxidant effect. J Agric Food Chem. 2004;52(15):4664–8.PubMedCrossRef
55.
Shen CJ, Chen CK, Lee SS. Polar constituents from Sageretia thea leaf characterized by HPLC-SPE-NMR assisted approaches. J Chin Inst Chem. 2009;56:1002–9.CrossRef
56.
Hong JF, Song YF, Liu Z, Zheng ZC, Chen HJ, Wang SS. Anticancer activity of taraxerol acetate in human glioblastoma cells and a mouse xenograft model via induction of autophagy and apoptotic cell death, cell cycle arrest and inhibition of cell migration. Mol Med Rep. 2016;13(6):4541–8.PubMedPubMedCentralCrossRef
57.
Rauf A, Imran M, Khan IA, Ur-Rehman M, Gilani SA, Mehmood Z, Mubarak MS. Anticancer potential of quercetin: a comprehensive review. Phytother Res. 2018;32(11):2109–30.PubMedCrossRef
58.
Abaza MS, Al-Attiyah R, Bhardwaj R, Abbadi G, Koyippally M, Afzal M. Syringic acid from Tamarix aucheriana possesses antimitogenic and chemo-sensitizing activities in human colorectal cancer cells. Pharm Biol. 2013;51(9):1110–24.PubMedCrossRef
59.
Kim SH, Choi KC. Anti-cancer effect and underlying mechanism(s) of kaempferol, a phytoestrogen, on the regulation of apoptosis in diverse cancer cell models. Toxicol Res. 2013;29(4):229–34.PubMedPubMedCentralCrossRef
60.
Zhao C, She T, Wang L, Su Y, Qu L, Gao Y, Xu S, Cai S, Shou C. Daucosterol inhibits cancer cell proliferation by inducing autophagy through reactive oxygen species-dependent manner. Life Sci. 2015;137:37–43.PubMedCrossRef
Metadata
Title
Extracts from Sageretia thea reduce cell viability through inducing cyclin D1 proteasomal degradation and HO-1 expression in human colorectal cancer cells
Authors
Ha Na Kim
Gwang Hun Park
Su Bin Park
Jeong Dong Kim
Hyun Ji Eo
Ho-Jun Son
Jeong Ho Song
Jin Boo Jeong
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2019
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-019-2453-4

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