Apoptotic effect of hot water extract of Sanguisorba officinalis L. in human oral cancer cells

Shin,Ji-Ae; Kim,Jun-Sung; Kwon,Ki-Han; Nam,Jeong-Seok; Jung,Ji‑Youn; Cho,Nam-Pyo; Cho,Sung-Dae

doi:10.3892/ol.2012.748

Apoptotic effect of hot water extract of Sanguisorba officinalis L. in human oral cancer cells

Authors:
- Ji-Ae Shin
- Jun-Sung Kim
- Ki-Han Kwon
- Jeong-Seok Nam
- Ji‑Youn Jung
- Nam-Pyo Cho
- Sung-Dae Cho
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Affiliations: Department of Oral Pathology, School of Dentistry, Institute of Oral Bioscience, Chonbuk National University, Jeonju, Republic of Korea, R__AMB__D Center, Biterials Co. Ltd., Seoul, Republic of Korea, Department of Food Science and Nutrition, College of Health Welfare and Education, Gwangju University, Gwangju, Republic of Korea, Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Inchon, Republic of Korea, Department of Companion and Laboratory Animal Science, Kongju National University, Yesan, Republic of Korea
Published online on: June 8, 2012 https://doi.org/10.3892/ol.2012.748
Pages: 489-494

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Abstract

Sanguisorba officinalis L. has been used in traditional Asian medicine to treat diseases including diarrhea, chronic intestinal infections, duodenal ulcers and bleeding. This study examined the antiproliferative effects and apoptotic activity of hot water extract of S. officinalis L. (HESO) on HSC4 and HN22 human oral cancer cells. The effects of HESO were evaluated by the 3-(4,5-dimethylthiazol-20yl)-(3-carboxymethoxyphenyl)-2-(4-sulphophenyl)-2H-tetrazolium (MTS) assay, 4'-6-diamidino-2-phenylindole (DAPI) staining and western blot analysis. HESO was found to inhibit cell growth and induce apoptosis in HSC4 and HN22 oral cancer cells. HESO downregulated myeloid cell leukemia-1 (Mcl-1) in HSC4 cells and was associated with the activation of Bak, resulting in Bak oligomerization on the mitochondrial outer membrane. HESO did not alter Mcl-1 expression in HN22 cells, but it decreased Sp1 expression. The downregulation of Sp1 by HESO in HN22 cells resulted in a decrease in survivin, a downstream target protein of Sp1. These results suggested that HESO inhibited the growth of oral cancer through either Mcl-1 or Sp1, indicating that HESO may serve as a potential drug candidate against oral cancer.

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1	Siegel R, Ward E, Brawley O and Jemal A: Cancer statistics: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin. 61:212–236. 2011. View Article : Google Scholar : PubMed/NCBI
2	Mashberg A, Boffetta P, Winkelman R and Garfinkel L: Tobacco smoking, alcohol drinking, and cancer of the oral cavity and oropharynx among U.S. veterans. Cancer. 72:1369–1375. 1993. View Article : Google Scholar : PubMed/NCBI
3	Neville BW and Day TA: Oral cancer and precancerous lesions. CA Cancer J Clin. 52:195–215. 2002. View Article : Google Scholar : PubMed/NCBI
4	Michels J, Johnson PW and Packham G: Mcl-1. Int J Biochem Cell Biol. 37:267–271. 2005. View Article : Google Scholar
5	Liu XS, Jiang J, Jiao XY, Wu YE, Lin JH and Cai YM: Lycorine induces apoptosis and down-regulation of Mcl-1 in human leukemia cells. Cancer Lett. 274:16–24. 2009. View Article : Google Scholar : PubMed/NCBI
6	Battle TE, Arbiser J and Frank DA: The natural product honokiol induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia (B-CLL) cells. Blood. 106:690–697. 2005. View Article : Google Scholar : PubMed/NCBI
7	Lee NH, Lee MY, Lee JA, Jung DY, Seo CS, Kim JH and Shin HK: Anti-asthmatic effect of Sanguisorba officinalis L. and potential role of heme oxygenase-1 in an ovalbumin-induced murine asthma model. Int J Mol Med. 26:201–208. 2010.
8	Van Delft MF and Huang DC: How the Bcl-2 family of proteins interact to regulate apoptosis. Cell Res. 16:203–213. 2006.PubMed/NCBI
9	Dash R, Richards JE, Su ZZ, Bhutia SK, Azab B, Rahmani M, Dasmahapatra G, Yacoub A, Dent P, Dmitriev IP, et al: Mechanism by which Mcl-1 regulates cancer-specific apoptosis triggered by mda-7/IL-24, an IL-10-related cytokine. Cancer Res. 70:5034–5045. 2010. View Article : Google Scholar : PubMed/NCBI
10	Okumura K, Huang S and Sinicrope FA: Induction of Noxa sensitizes human colorectal cancer cells expressing Mcl-1 to the small-molecule Bcl-2/Bcl-xL inhibitor, ABT-737. Clin Cancer Res. 14:8132–8142. 2008. View Article : Google Scholar : PubMed/NCBI
11	Chen S, Dai Y, Harada H, Dent P and Grant S: Mcl-1 down-regulation potentiates ABT-737 lethality by cooperatively inducing Bak activation and Bax translocation. Cancer Res. 67:782–791. 2007. View Article : Google Scholar : PubMed/NCBI
12	Lee NH, Lee MY, Lee JA, Jung DY, Seo CS, Kim JH and Shin HK: Anti-asthmatic effect of Sanguisorba officinalis L. and potential role of heme oxygenase-1 in an ovalbumin-induced murine asthma model. Int J Mol Med. 26:201–208. 2010.
13	Shin TY, Lee KB and Kim SH: Anti-allergic effects of Sanguisorba officinalis on animal models of allergic reactions. Immunopharmacol Immunotoxicol. 24:455–468. 2002.PubMed/NCBI
14	Yu T, Lee YJ, Yang HM, Han S, Kim JH, Lee Y, Kim C, Han MH, Kim MY, Lee J and Cho JY: Inhibitory effect of Sanguisorba officinalis ethanol extract on NO and PGE production is mediated by suppression of NF-kappaB and AP-1 activation signaling cascade. J Ethnopharmacol. 134:11–17. 2011.
15	Hachiya A, Kobayashi A, Ohuchi A, Kitahara T and Takema Y: The inhibitory effect of an extract of Sanguisorba officinalis L. on ultraviolet B-induced pigmentation via the suppression of endothelin-converting enzyme-1alpha. Biol Pharm Bull. 24:688–692. 2001.PubMed/NCBI
16	Liu X, Cui Y, Yu Q and Yu B: Triterpenoids from Sanguisorba officinalis. Phytochemistry. 66:1671–1679. 2005. View Article : Google Scholar : PubMed/NCBI
17	Nijhawan D, Fang M, Traer E, Zhong Q, Gao W, Du F and Wang X: Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 17:1475–1486. 2003. View Article : Google Scholar : PubMed/NCBI
18	Choi KH, Shim JH, Huong LD, Cho NP and Cho SD: Inhibition of myeloid cell leukemia-1 by tolfenamic acid induces apoptosis in mucoepidermoid carcinoma. Oral Dis. 17:469–475. 2011. View Article : Google Scholar : PubMed/NCBI
19	Gul O, Basaga H and Kutuk O: Apoptotic blocks and chemotherapy resistance: strategies to identify Bcl-2 protein signatures. Brief Funct Genomic Proteomic. 7:27–34. 2008. View Article : Google Scholar : PubMed/NCBI
20	Chetoui N, Sylla K, Gagnon-Houde JV, Alcaide-Loridan C, Charron D, Al-Daccak R and Aoudjit F: Down-regulation of mcl-1 by small interfering RNA sensitizes resistant melanoma cells to fas-mediated apoptosis. Mol Cancer Res. 6:42–52. 2008. View Article : Google Scholar : PubMed/NCBI
21	Ma Y, Cress WD and Haura EB: Flavopiridol-induced apoptosis is mediated through up-regulation of E2F1 and repression of Mcl-1. Mol Cancer Ther. 2:73–81. 2003.PubMed/NCBI
22	Gojo I, Zhang B and Fenton RG: The cyclin-dependent kinase inhibitor flavopiridol induces apoptosis in multiple myeloma cells through transcriptional repression and down-regulation of Mcl-1. Clin Cancer Res. 8:3527–3538. 2002.
23	MacCallum DE, Melville J, Frame S, Watt K, Anderson S, Gianella-Borradori A, Lane DP and Green SR: Seliciclib (CYC202, R-Roscovitine) induces cell death in multiple myeloma cells by inhibition of RNA polymerase II-dependent transcription and down-regulation of Mcl-1. Cancer Res. 65:5399–5407. 2005. View Article : Google Scholar : PubMed/NCBI
24	Konopleva M, Contractor R, Tsao T, Samudio I, Ruvolo PP, Kitada S, Deng X, Zhai D, Shi YX, Sneed T, et al: Mechanisms of apoptosis sensitivity and resistance to the BH3 mimetic ABT-737 in acute myeloid leukemia. Cancer Cell. 10:375–388. 2006. View Article : Google Scholar : PubMed/NCBI
25	Lin X, Morgan-Lappe S, Huang X, Li L, Zakula DM, Vernetti LA, Fesik SW and Shen Y: ‘Seed’ analysis of off-target siRNAs reveals an essential role of Mcl-1 in resistance to the small-molecule Bcl-2/Bcl-XL inhibitor ABT-737. Oncogene. 26:3972–3979. 2007.
26	Fulda S, Scaffidi C, Susin SA, Krammer PH, Kroemer G, Peter ME and Debatin KM: Activation of mitochondria and release of mitochondrial apoptogenic factors by betulinic acid. J Biol Chem. 273:33942–33948. 1998. View Article : Google Scholar : PubMed/NCBI
27	Li Y, He K, Huang Y, Zheng D, Gao C, Cui L and Jin YH: Betulin induces mitochondrial cytochrome c release associated apoptosis in human cancer cells. Mol Carcinog. 49:630–640. 2010.PubMed/NCBI
28	Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J and Thompson CB: Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J Cell Biol. 162:59–69. 2003. View Article : Google Scholar : PubMed/NCBI
29	Germain M, Milburn J and Duronio V: MCL-1 inhibits BAX in the absence of MCL-1/BAX Interaction. J Biol Chem. 283:6384–6392. 2008. View Article : Google Scholar : PubMed/NCBI
30	Shankar S and Srivastava RK: Bax and Bak genes are essential for maximum apoptotic response by curcumin, a polyphenolic compound and cancer chemopreventive agent derived from turmeric, Curcuma longa. Carcinogenesis. 28:1277–1286. 2007. View Article : Google Scholar
31	Labi V, Erlacher M, Kiessling S and Villunger A: BH3-only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ. 13:1325–1338. 2006. View Article : Google Scholar : PubMed/NCBI
32	Leber B, Lin J and Andrews DW: Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis. 12:897–911. 2007. View Article : Google Scholar : PubMed/NCBI
33	Upreti M, Chu R, Galitovskaya E, Smart SK and Chambers TC: Key role for Bak activation and Bak-Bax interaction in the apoptotic response to vinblastine. Mol Cancer Ther. 7:2224–2232. 2008. View Article : Google Scholar : PubMed/NCBI
34	Heath-Engel HM and Shore GC: Regulated targeting of Bax and Bak to intracellular membranes during apoptosis. Cell Death Differ. 13:1277–1280. 2006. View Article : Google Scholar : PubMed/NCBI
35	Wang L, Wei D, Huang S, Peng Z, Le X, Wu TT, Yao J, Ajani J and Xie K: Transcription factor Sp1 expression is a significant predictor of survival in human gastric cancer. Clin Cancer Res. 9:6371–6380. 2003.PubMed/NCBI
36	Shi Q, Le X, Abbruzzese JL, Peng Z, Qian CN, Tang H, Xiong Q, Wang B, Li XC and Xie K: Constitutive Sp1 activity is essential for differential constitutive expression of vascular endothelial growth factor in human pancreatic adenocarcinoma. Cancer Res. 61:4143–4154. 2001.
37	Shim JH, Shin JA, Jung JY, Choi KH, Choi ES, Cho NP, Kong G, Ryu MH, Chae JI and Cho SD: Chemopreventive effect of tolfenamic acid on KB human cervical cancer cells and tumor xenograft by downregulating specificity protein 1. Eur J Cancer Prev. 20:102–111. 2011. View Article : Google Scholar : PubMed/NCBI
38	Choi ES, Shim JH, Jung JY, Kim HJ, Choi KH, Shin JA, Nam JS, Cho NP and Cho SD: Apoptotic effect of tolfenamic acid in androgen receptor-independent prostate cancer cell and xenograft tumor through specificity protein 1. Cancer Sci. 102:742–748. 2011. View Article : Google Scholar : PubMed/NCBI
39	Shin JA, Shim JH, Jeon JG, Choi KH, Choi ES, Cho NP and Cho SD: Apoptotic effect of Polygonum Cuspidatum in oral cancer cells through the regulation of specificity protein 1. Oral Dis. 17:162–170. 2011. View Article : Google Scholar : PubMed/NCBI
40	Li F and Altieri DC: Transcriptional analysis of human survivin gene expression. Biochem J. 344(Pt 2): 305–311. 1999. View Article : Google Scholar
41	Chun JY, Hu Y, Pinder E, Wu J, Li F and Gao AC: Selenium inhibition of survivin expression by preventing Sp1 binding to its promoter. Mol Cancer Ther. 6:2572–2580. 2007. View Article : Google Scholar : PubMed/NCBI