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The Anti-Tumor Activities of Cerebrosides Derived from Sea

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The Anti-Tumor Activities of Cerebrosides Derived from Sea Journal of Oleo Science Copyright ©2012 by Japan Oil Chemists’ Society J. Oleo Sci. 61, (6) 321-330 (2012) The anti-tumor activities of cerebrosides derived from sea cucumber Acaudina molpadioides and starfi sh Asterias amurensis in vitro and in vivo Lei Du1, a, Zhao-Jie Li1, a, Jie Xu1, Jing-Feng Wang1, Yong Xue1, Chang-Hu Xue1, Koretaro Takahashi2 and Yu-Ming Wang1＊ 1 College of Food Science and Engineering, Ocean University of China (No.5 Yushan Road, Qingdao, Shandong Province, 266003, P.R.China) 2 Division of Marine Life Science, Faculty of Fisheries Sciences, Hokkaido University (Hakodate, 041-8611, Japan) a Lei Du and Zhao-Jie Li contributed equally to this work. Abstract: The present study was undertaken to examine the effect of cerebrosides derived from the sea cucumber Acaudina molpadioides and the starfi sh Asterias amurensis on the anti-tumor activity in vitro and in vivo. The results indicated that both Acaudina molpadioides cerebrosides (AMC) and Asterias amurensis cerebrosides (AAC) exhibited an inhibitory effect on cell proliferation through induction of apoptosis in S180 cells. Moreover, administration of AMC and AAC (50 mg/kg BW) on S180 tumor bearing mice reduced the tumor weight by 45.24 % and 35.71 %, respectively. In S180 ascites tumor model, AMC and AAC (50 mg/kg BW) treatment exhibited a signifi cant ascites fl uid growth inhibition of 31.23 % and 22.72 %. Furthermore, the ascites tumor cell viability ratio in AMC and AAC groups reduced to 50.89 % and 51.69 %, respectively. The life span of AMC and AAC administrated groups increased by 55.28 % and 35.77 % compared to control. Quantitative real-time PCR analysis demonstrated that the administration of AMC and AAC down-regulated the expression of Bcl-2, Bcl-xL, while on the other hand, up-regulated Bax, Cytochrome c, caspase-9 and caspase-3 mRNA level of the S180 ascites tumor cells. It was concluded that AMC and AAC should have potential anti-tumor activity both in vitro and in vivo by inducing apoptosis through the mitochondria-mediated apoptosis pathway. AAC seemed to be more effective than AMC in vitro but less potent in vivo. It may depend on the structural differences in their fatty acid groups and sphingoid bases. Key words: Acaudina molpadioides, Asterias amurensis, cerebrosides, anti-tumor, S180 cells, mitochondria-mediated apoptosis pathway 1 INTRODUCTION species, and many are still undiscovered. Various second- The marine echinoderms mainly include sea cucumber ary metabolites including steroids, steroidal glycosides, an- （Holothuroidea）, starfi sh（Asteroidea）and sea urchin（Echi- thraquinones, alkaloids, phospholipids, peptides, and fatty noidea）. They occur in various habitats from intertidal acids were reported from starfi sh. These chemical constitu- zone down to the bottom of the deep sea trenches and ents exhibit cytotoxic, hemolytic, antiviral, antifungal, and from sand to rubble coral reefs through cold and tropical antimicrobial activities4）. Acaudina molpadioides is an seas. Sea cucumbers have been used as a traditional tonic abundant low valued sea cucumber widely distributed in food in China and other Asian countries for thousands of sandy coastal regions of China. However it has not been years1, 2）. The major edible part of sea cucumber is the body fully exploited nor utilized. Asterias amurensis is a widely wall, which contains numerous bioactive substances, in- distributed starfish in the Northern Pacific and causes cluding collagen, acidic polysaccharides, triterpenoid sapo- severe damage to the fi shery and aquacultural grounds for nins, gangliosides and cerebrosides3）. Except a few species benthic shellfi sh5）. Therefore, suffi cient exploiting and uti- that inhabit in brackish water, starfi sh are bascially benthic lization of Acaudina molpadioides and Asterias amu- organisms found in all oceans. There are over 1,500 known rensis is aspired. ＊Correspondence to: Yu-Ming Wang, College of Food Science and Engineering, Ocean University of China, No.5 Yushan Road, Qingdao, Shandong Province, 266003, P.R. China E-mail: [email protected] Accepted December 23, 2011 (received for review December 2, 2011) Journal of Oleo Science ISSN 1345-8957 print / ISSN 1347-3352 online http://www.jstage.jst.go.jp/browse/jos/ http://mc.manusriptcentral.com/jjocs 321 L. Du, Z. J. Li, J. Xu et al. Cerebrosides are one of the simplest lipid classes of gly- investigate the anti-tumor molecule mechanism of AMC cosphingolipids and consist of monosaccharides（such as and AAC, we assayed the gene expression of Bcl-2, Bcl-xL, glucose and galactose）, an amide-linked fatty acid and Bax, cytochrome c, caspase-9 and caspase-3, which are sphingoid base which is also called long-chain base6）. Cere- strongly associated with the mitochondrial apoptotic brosides have been shown to display variety of biological pathway. activities such as anti-tumor, immunomodulatory, and anti- microbial activities7－10）. The studies of prominent anti-tu- mor activities of marine-derived cerebrosides and their sphingoid bases during the past two decades have been at- 2 EXPERIMENTAL PROCEDURES tracted our attention. The glycosphingolipids of marine in- 2.1 Materials vertebrates, including sea cucumber and starfish, have Sea cucumber（Acaudina molpadioides）was purchased unique sphingoid bases with a conjugated diene such as from the Zhou-Shan Fishery Company（Zhejiang Province, 2-amino-1, 3-dihydroxy-4-heptadecene（d17:1）, 2-amino-1, China）in September, 2008. Starfi sh（Asterias amurensis） 3-dihydroxy-4, 8, 10-octadecatriene（d18:3）or 2-amino-1, material was collected in southern Hokkaido in April, 2007. 3-dihydroxy-9-methyl-4, 8, 10-octadecatriene（d19:3）11, 12）. The sample of AAC was provided by Professor Takahashi Recent significant progress in biochemical and molecular from the Hokkaido University. Roswell Park Memorial Insti- studies of cerebrosides metabolism and function revealed tute-1640 Medium（RPMI-1640）, newborn calf serum（NCS） that these cerebroside metabolites regulate many cellular were all obtained from Gibco（Grand Island, NY）. Trypsin, processes including apoptosis13－15）. Sugawara et al report- 3-（4, 5-Dimethylthiazol-2-yl）-2,5-diphenyl-tetrazolium ed that sea cucumber（Stichopus variegates）sphingoid bromide（MTT）and Trypan blue were purchased from bases e.g. d17:1, 4, 8-sphingadienine（d18:2）, d18:3 and Sigma（St. Louis, MO, USA）. Tissue culture plates were ob- d19:3 have strong cytotoxicity against some colon cancer tained from Corning（NY, USA）. Acridine orange（AO）, cell lines via induction of apoptosis16）. A novel identified ethidium bromide（EB）and Moloney murine leukemia virus glycosphingolipid, ophidiacerebroside C was isolated from reverse transcriptase（MMLV）were obtained from Promega Ophidiaster ophidiamus. The major component of that （Madison, WI）. TRIzol reagent was obtained from Invitro- cerebrosides was（2S, 3R, 4E, 8E, 10E）-1-（β-D- gen（Carlsbad, CA, USA）. Maxima SYBR Green qPCR glucopyranosyloxy）-2-hudrocy-2-［（（R）-2-hydroxydoco- Master mix was purchased from Fermentas（Glen Burnie, sanoy）amino］-9-methyl-4, 8, 10-octadecatriene. And this Maryland）. showed strong cytotoxicity on L1210 leukemia cells in vitro17）. It is demonstrated that the marine-derived cere- 2.2 Preparation and analysis of AMC and AAC brosides and their sphingoid bases have signifi cant anti-tu- AMC were prepared and analyzed using the procedure mor activity. And it is considered that the antitumor activi- described by Xu et al6）. The preparation of AMC and AAC ty rests on the sphingoid base structure. solution was followed by the liposome preparation done by Apoptosis is the process of programmed cell death that Z. Hossain et al25）, and diluted to the desired concentra- occurs in multicellular organisms. It is physiologically and tions by medium before use. pathologically involved in cellular homeostasis18）. In the recent years, apoptosis has become an important area for 2.3 Cell lines and cell culture cancer research because most anti-cancer strategies, in- Murine sarcoma cells（S180）were obtained from Shang- cluding radiation therapy, immunotherapy, or targeted hai Cell Bank（Shanghai, China）. S180 cells were main- therapies, activate apoptosis signal pathways19－21）. Apopto- tained in RPMI-1640 medium, supplemented with 10％ sis occurs through two main pathways. The fi rst, referred heat-inactivated NCS, 100 U/mL penicillin, and 100 U/mL to as the extrinsic or cytoplasmic pathway, is triggered streptomycin at 37℃ in a humidifi ed atmosphere contain- 22） through the Fas death receptor . The second pathway is ing 5％ CO2. the intrinsic or mitochondrial pathway that when stimulat- ed leads to the release of cytochrome c from the mitochon- 2.4 Animals dria and activation of the death signal23）. Bcl-2 family genes BALB/c male mice（18-22 g, 8-10 weeks）were purchased comprise one of the most important regulators of this from Vital River Laboratory Animal Laboratory Animal pathway. Both pathways converge to a final common Center（Beijing, China）. The animals were provided with pathway involving the activation of a cascade of proteases standard laboratory food and water, and were kept at 24℃, called caspases that cleave regulatory and structural mole- relative humidity at 65±15％ and under 12 h light-dark cules, culminating in the death of the cell24）. cycle. All experiments were carried out according to the The aim of this work is to assess the anti-tumor activi- P.R. China legislation regarding the use and care of labora- ties, in particular, the structure-activity relationships of tory animals and were approved by the Bioethics Commit- AMC and AAC both in vitro and in vivo. Furthermore, to tee of Ocean University of China. 322 J. Oleo Sci. 61, (6) 321-330 (2012) The anti-tumor activities of cerebrosides from sea cucumber and starfi sh 2.5 Cell viability assay saline）and AMC-treated or AAC-treated groups（AMC or Cell viability was determined by the MTT assay26）. S180 AAC, 50 mg/kg BW）. After 24 h, the animals in each group cells（2×104 cells/well）were seeded in 96-well plates.
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