Anticancer effects of an extract from the scallop Patinopecten yessoensis on MCF‑7 human breast carcinoma cells

Lee,Chu; Chun,Wonjoo; Zhao,Rongjie; Kim,Young  Dae; Nam,Myung  Mo; Jung,Dae  Hwa; Cho,Il  Je; Jegal,Kyung  Hwan; Lee,Tae  Hoon; Kim,Young  Woo; Park,Sang  Mi; Ju,Seong  A.; Lee,Chul  Won; Kim,Sang  Chan; An,Won  G.

doi:10.3892/ol.2017.6424

Anticancer effects of an extract from the scallop Patinopecten yessoensis on MCF‑7 human breast carcinoma cells

Authors:
- Chu Lee
- Wonjoo Chun
- Rongjie Zhao
- Young Dae Kim
- Myung Mo Nam
- Dae Hwa Jung
- Il Je Cho
- Kyung Hwan Jegal
- Tae Hoon Lee
- Young Woo Kim
- Sang Mi Park
- Seong A. Ju
- Chul Won Lee
- Sang Chan Kim
- Won G. An
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Affiliations: Aquaculture Industry Division, NFRDI, Gangneung 210‑809, Republic of Korea, Institute of Marine Biotechnology, Pusan National University, Busan 609‑735, Republic of Korea, School of Mental Health, Qiqihar Medical University, Qiqihar, Heilongjiang 161042, P.R. China, HaniBio Co., Ltd., Gyeongsan 712‑260, Republic of Korea, MRC‑GHF, College of Korean Medicine, Daegu Haany University, Gyeongsan 38610, Republic of Korea, Department of Biological Sciences, College of Biomedical Sciences and Engineering, Inje University, Gimhae 621‑749, Republic of Korea, School of Biological Sciences, University of Ulsan, Ulsan 680‑749, Republic of Korea
Published online on: June 20, 2017 https://doi.org/10.3892/ol.2017.6424
Pages: 2207-2217
Copyright: © Lee et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Patinopecten yessoensis, is a species of scallop and a marine bivalve mollusk. In traditional East Asian medicine, scallop meat is used as a drug for the treatment of diabetes, pollakisuria, and indigestion. The present study was conducted in order to examine the potential anticancer effects of scallop flesh extract (SE) on MCF‑7 human breast cancer cells. An MTT assay was used to evaluate cell viability and flow cytometry was used for the assessment of cell cycle distribution and apoptosis. The alteration in protein expression level was determined by western blot analysis, and the amounts of docosahexaenoic acid and eicosapentaenoic acid in the SE were measured by gas chromatography. SE inhibited the growth of MCF‑7 human breast cancer cells in a dose‑dependent manner by inducing G0/G1 phase arrest. The cell cycle arrest was associated with the upregulation of p53 and p21, and downregulation of G1 phase‑associated cyclin D1/cyclin‑dependent kinase (Cdk) 4 and cyclin E1/Cdk 2. In addition, SE‑mediated cell cycle arrest was associated with the promotion of apoptosis, as indicated by the expression of apoptosis‑associated proteins and changes in nuclear morphology. SE appeared to induce the mitochondrial apoptotic cascade, as indicated by a decreased expression of Bcl‑2, activation of Bcl‑2 associated X protein, release of cytochrome c, decrease in procaspase‑3, and an increase in cleaved‑poly (ADP‑ribose) polymerase (PARP). Furthermore, the expression levels of Fas‑associated via death domain and cleaved caspase‑8 were increased in a SE dose‑dependent manner. Taken together, these results suggest that the intrinsic and extrinsic pathways of apoptosis are associated with the anticancer effects of SE on MCF‑7 cells. Thus, SE may be a suitable candidate for the treatment and prevention of human breast cancer.

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1	Xiao PG: Atlas of Chinese Herbs. The Commercial Press Ltd.; Hong Kong: 7. pp. 2021990
2	Nam M, Lee C, Moon TS and Huh MK: Genetic diversity and population structure of the scallop patinopecten yessoensis in Korea, China and Japan by random amplified polymorphic DNA markers. J Life Sci. 22:466–471. 2012. View Article : Google Scholar
3	Saad ED: Endpoints in advanced breast cancer: Methodological aspects & clinical implications. Indian J Med Res. 134:413–418. 2011.PubMed/NCBI
4	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
5	Tsao AS, Kim ES and Hong WK: Chemoprevention of cancer. CA Cancer J Clin. 54:150–180. 2004. View Article : Google Scholar : PubMed/NCBI
6	Hunter T and Pines J: Cyclins and cancer II Cyclin D and CDK inhibitors come of age. Cell. 79:573–582. 1994. View Article : Google Scholar : PubMed/NCBI
7	Harper JW and Elledge SJ: CDK inhibitors in development and cancer. Curr Opin Genet Dev. 6:56–64. 1996. View Article : Google Scholar : PubMed/NCBI
8	Sherr CJ: Cancer cell cycles. Science. 274:1672–1677. 1996. View Article : Google Scholar : PubMed/NCBI
9	Gartel AL and Tyner AL: The role of the cyclin-dependent kinase inhibitor p21 in apoptosis. Mol Cancer Ther. 1:639–649. 2002.PubMed/NCBI
10	Meek DW: The p53 response to DNA damage. DNA Repair (Amst). 3:1049–1056. 2004. View Article : Google Scholar : PubMed/NCBI
11	Weng MS, Ho YS and Lin JK: Chrysin induces G1 phase cell cycle arrest in C6 glioma cells through inducing p21Waf1/Cip1 expression: Involvement of p38 mitogen-activated protein kinase. Biochem Pharmacol. 69:1815–1827. 2005. View Article : Google Scholar : PubMed/NCBI
12	Muppidi J, Porter M and Siegel RM: Measurement of apoptosis and other forms of cell death. Curr Protoc Immunol. 3:3–17. 2004.
13	Evan GI and Vousden KH: Proliferation, cell cycle and apoptosis in cancer. Nature. 411:342–348. 2001. View Article : Google Scholar : PubMed/NCBI
14	MacKenzie SH and Clark AC: Targeting cell death in tumors by activating caspases. Curr Cancer Drug Targets. 8:98–109. 2008. View Article : Google Scholar : PubMed/NCBI
15	Repicky A, Jantova S and Milata V: Signal pathways of cell proliferation and death as targets of potential chemotherapeutics. Ceska Slov Farm. 57:4–10. 2008.(In Slovak). PubMed/NCBI
16	Ireland CM, Copp BR, Foster MP, et al: Biomedical potential of marine natural productsPharmaceutical and bioactive natural products. Attaway DH and Zaborsky OR: Springer US; New York, USA: 1. pp. 1–43. 1993, View Article : Google Scholar
17	Lv S, Gao J, Liu T, Zhu J, Xu J, Song L, Liang J and Yu R: Purification and partial characterization of a new antitumor protein from Tegillarca granosa. Mar Drugs. 13:1466–1480. 2015. View Article : Google Scholar : PubMed/NCBI
18	Sasaki T, Uchida H, Uchida NA, et al: Antitumor activity and immunomodulatory effect of glycoprotein fraction from scallop Patinopecten yessoensis. Nippon Suisan Gakkaishi. 53:267–272. 1987. View Article : Google Scholar
19	Zhang H, Wang K, Lin G and Zhao Z: Antitumor mechanisms of S-allyl mercaptocysteine for breast cancer therapy. BMC Complement Altern Med. 14:2702014. View Article : Google Scholar : PubMed/NCBI
20	Vermeulen K, Van Bockstaele DR and Berneman ZN: The cell cycle: A review of regulation, deregulation and therapeutic targets in cancer. Cell Prolif. 36:131–149. 2003. View Article : Google Scholar : PubMed/NCBI
21	Schwartz GK and Shah MA: Targeting the cell cycle: A new approach to cancer therapy. J Clin Oncol. 23:9408–9421. 2005. View Article : Google Scholar : PubMed/NCBI
22	Nagle AA, Gan FF, Jones G, So CL, Wells G and Chew EH: Induction of tumor cell death through targeting tubulin and evoking dysregulation of cell cycle regulatory proteins by multifunctional cinnamaldehydes. PLoS One. 7:e501252012. View Article : Google Scholar : PubMed/NCBI
23	Bellamy CO: p53 and apoptosis. Br Med Bull. 53:522–538. 1997. View Article : Google Scholar : PubMed/NCBI
24	Levine AJ: p53, the cellular gatekeeper for growth and division. Cell. 88:323–331. 1997. View Article : Google Scholar : PubMed/NCBI
25	Pucci B, Kasten M and Giordano A: Cell cycle and apoptosis. Neoplasia. 2:291–299. 2000. View Article : Google Scholar : PubMed/NCBI
26	Harris SL and Levine AJ: The p53 pathway: Positive and negative feedback loops. Oncogene. 24:2899–2908. 2005. View Article : Google Scholar : PubMed/NCBI
27	Didenko VV, Wang X, Yang L and Hornsby PJ: Expression of p21(WAF1/CIP1/SDI1) and p53 in apoptotic cells in the adrenal cortex and induction by ischemia/reperfusion injury. J Clin Invest. 97:1723–1731. 1996. View Article : Google Scholar : PubMed/NCBI
28	Yang L, Zhang HW, Hu R, Yang Y, Qi Q, Lu N, Liu W, Chu YY, You QD and Guo QL: Wogonin induces G1 phase arrest through inhibiting CDK4 and cyclin D1 concomitant with an elevation in p21Cip1 in human cervical carcinoma HeLa cells. Biochem Cell Biol. 87:933–942. 2009. View Article : Google Scholar : PubMed/NCBI
29	Zorn JA, Wolan DW, Agard NJ and Wells JA: Fibrils colocalize caspase-3 with procaspase-3 to foster maturation. J Biol Chem. 287:33781–33795. 2012. View Article : Google Scholar : PubMed/NCBI
30	Donepudi M and Grütter MG: Structure and zymogen activation of caspases. Biophys Chem 101–102. 145–153. 2002. View Article : Google Scholar
31	Stennicke HR and Salvesen GS: Caspases. Controlling intracellular signals by protease zymogen activation. Biochim Biophys Acta. 1477:299–306. 2000. View Article : Google Scholar : PubMed/NCBI
32	Gray DC, Mahrus S and Wells JA: Activation of specific apoptotic caspases with an engineered small molecule-activated protease. Cell. 142:637–646. 2010. View Article : Google Scholar : PubMed/NCBI
33	Putt KS, Chen GW, Pearson JM, Sandhorst JS, Hoagland MS, Kwon JT, Hwang SK, Jin H, Churchwell MI, Cho MH, et al: Small-molecule activation of procaspase-3 to caspase-3 as a personalized anticancer strategy. Nat Chem Biol. 2:543–550. 2006. View Article : Google Scholar : PubMed/NCBI
34	Fulda S and Debatin KM: Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene. 25:4798–4811. 2006. View Article : Google Scholar : PubMed/NCBI
35	Salvesen GS and Riedl SJ: Caspase mechanisms. Adv Exp Med Biol. 615:13–23. 2008. View Article : Google Scholar : PubMed/NCBI
36	McIlwain DR, Berger T and Mak TW: Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol. 5:a0086562013. View Article : Google Scholar : PubMed/NCBI
37	Kroemer G and Reed JC: Mitochondrial control of cell death. Nat Med. 6:513–519. 2000. View Article : Google Scholar : PubMed/NCBI
38	Gross A, McDonnell JM and Korsmeyer SJ: Bcl-2 family members and the mitochondria in apoptosis. Genes Dev. 13:1899–1911. 1999. View Article : Google Scholar : PubMed/NCBI
39	Li H, Wang LJ, Qiu GF, Yu JQ, Liang SC and Hu XM: Apoptosis of Hela cells induced by extract from Cremanthodium humile. Food Chem Toxicol. 45:2040–2046. 2007. View Article : Google Scholar : PubMed/NCBI
40	Elmore S: Apoptosis: A review of programmed cell death. Toxicol Pathol. 35:495–516. 2007. View Article : Google Scholar : PubMed/NCBI
41	Nagata S: Apoptosis by death factor. Cell. 88:355–365. 1997. View Article : Google Scholar : PubMed/NCBI
42	Schwartsmann G, da Rocha A Brondani, Berlinck RG and Jimeno J: Marine organisms as a source of new anticancer agents. Lancet Oncol. 2:221–225. 2001. View Article : Google Scholar : PubMed/NCBI
43	Mitsiades CS, Ocio EM, Pandiella A, Maiso P, Gajate C, Garayoa M, Vilanova D, Montero JC, Mitsiades N, McMullan CJ, et al: Aplidin, a marine organism-derived compound with potent antimyeloma activity in vitro and in vivo. Cancer Res. 68:5216–5225. 2008. View Article : Google Scholar : PubMed/NCBI
44	Suarez-Jimenez GM, Burgos-Hernandez A and Ezquerra-Brauer JM: Bioactive peptides and depsipeptides with anticancer potential: Sources from marine animals. Mar Drugs. 10:963–986. 2012. View Article : Google Scholar : PubMed/NCBI
45	Chapkin RS, Seo J, McMurray DN and Lupton JR: Mechanisms by which docosahexaenoic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids. 153:14–23. 2008. View Article : Google Scholar : PubMed/NCBI
46	Fukui M, Kang KS, Okada K and Zhu BT: EPA, an omega-3 fatty acid, induces apoptosis in human pancreatic cancer cells: Role of ROS accumulation, caspase-8 activation, and autophagy induction. J Cell Biochem. 114:192–203. 2013. View Article : Google Scholar : PubMed/NCBI
47	Maleek MI: Omega-3 fatty acids decrease the proliferation of Rhabdomyosarcoma (RD) and Vero cell lines. J Cancer Sci Ther. 5:85–88. 2013. View Article : Google Scholar
48	Park JM, Kwon SH, Han YM, Hahm KB and Kim EH: Omega-3 polyunsaturated fatty acids as potential chemopreventive agent for gastrointestinal cancer. J Cancer Prev. 18:201–208. 2013. View Article : Google Scholar : PubMed/NCBI
49	Yang P, Cartwright C, Chan D, Ding J, Felix E, Pan Y, Pang J, Rhea P, Block K, Fischer SM, et al: Anticancer activity of fish oils against human lung cancer is associated with changes in formation of PGE2 and PGE3 and alteration of Akt phosphorylation. Mol Carcinog. 53:566–577. 2014. View Article : Google Scholar : PubMed/NCBI
50	Kato T, Hancock RL, Mohammadpour H, McGregor B, Manalo P, Khaiboullina S, Hall MR, Pardini L and Pardini RS: Influence of omega-3 fatty acids on the growth of human colon carcinoma in nude mice. Cancer Lett. 187:169–177. 2002. View Article : Google Scholar : PubMed/NCBI
51	Wu M, Harvey KA, Ruzmetov N, Welch ZR, Sech L, Jackson K, Stillwell W, Zaloga GP and Siddiqui RA: Omega-3 polyunsaturated fatty acids attenuate breast cancer growth through activation of a neutral sphingomyelinase-mediated pathway. Int J Cancer. 117:340–348. 2005. View Article : Google Scholar : PubMed/NCBI
52	Shaikh IA, Brown I, Schofield AC, Wahle KW and Heys SD: Docosahexaenoic acid enhances the efficacy of docetaxel in prostate cancer cells by modulation of apoptosis: The role of genes associated with the NF-kappaB pathway. Prostate. 68:1635–1646. 2008. View Article : Google Scholar : PubMed/NCBI
53	Hawcroft G, Volpato M, Marston G, Ingram N, Perry SL, Cockbain AJ, Race AD, Munarini A, Belluzzi A, Loadman PM, et al: The omega-3 polyunsaturated fatty acid eicosapentaenoic acid inhibits mouse MC-26 colorectal cancer cell liver metastasis via inhibition of PGE2-dependent cell motility. Br J Pharmacol. 166:1724–1737. 2012. View Article : Google Scholar : PubMed/NCBI