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Suppressive Effect of Neoxanthin on the Differentiation of 3T3-L1 Adipose Cells

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Suppressive Effect of Neoxanthin on the Differentiation of 3T3-L1 Adipose Cells Journal of Oleo Science Copyright ©2008 by Japan Oil Chemists’ Society J. Oleo Sci. 57, (6) 345-351 (2008) Suppressive Effect of Neoxanthin on the Differentiation of 3T3-L1 Adipose Cells Tomoko Okada1, Miho Nakai1, Hayato Maeda1, Masashi Hosokawa1, Tokutake Sashima1,2 and Kazuo Miyashita1＊ 1 Laboratory of Biofunctional Material Chemistry, Division of Marine Bioscience, Faculty of Fisheries Sciences, Hokkaido University (Hakodate, Hokkaido 041-8611, JAPAN) 2 Creative Research Institute, Hokkaido University (Hakodate, Hokkaido 041-8611, JAPAN) Abstract: The objective of this study was to assess the suppressive effects of 13 naturally occurring carotenoids on the adipocyte differentiation of 3T3-L1. The relationship between carotenoid structure and suppressive effects was also examined. Treatment with neoxanthin significantly reduced lipid accumulation, as well as glycerol-3-phosphate dehydrogenase activity. This suppressive effect on adipose cell differentiation was not observed in the other 12 carotenoids used in this study. Neoxanthin treatment also decreased expression of CCAAT/enhancer binding protein a (C/EBPa) and peroxisome proliferator- activated receptor g (PPARg) mRNAs. An examination of structure and function suggested that carotenoids containing an allene bond and an additional hydroxyl substituent on the side group may show suppressive effects on adipocyte differentiation in 3T3-L1 cells. Key words: anti-obesity, neoxanthin, 3T3-L1 cells, carotenoids 1 INTRODUCTION lycopene, lutein, b-cryptxanthin and zeaxanthin. Most Carotenoids are a group of more than 700 naturally nutritional research studies have focused on these five occurring pigments that are biosynthesized de novo by carotenoids, although the major carotenoids occurring in plants, algae, fungi and bacteria. Animals are incapable of nature are fucoxanthin, lutein, violaxanthin and neoxan- producing carotenoids and must obtain them from the thin4,5). Among them, lutein has been thoroughly reviewed above sources. About 50 carotenoids are considered to be with respect to its biological functions and possible health provitamin A because they are precursors of retinol and benefits6,7). However, there have been a few studies on the retinoic acid. Numerous epidemiological, interventinal, and physiological effects or beneficial applications of other prospective human studies, as well as an incredible array carotenoids without their chemopreventive effect on the of fundamental research, are currently underway to eluci- growth of cancer cells8,9). date the role of vitamin A along with its stereoisomers and In previous studies, we have reported that fucoxanthin metabolites in biological processes and disease prevention. and its metabolite, fucoxanthinol, exhibit encouraging In addition to serving as a source of vitamin A, dietary antiobesity effects through suppression of adipocyte differ- carotenoids are considered to play an essential role in the entiation and both are considered to be promising thera- prevention of common chronic diseases, such as cardiovas- peutic compounds10,11). Fucoxanthin (Fig. 1) is a naturally cular disease, age-related macular degeneration and can- abundant pigment found in edible seaweed (Undaria pin- cer1,2). The nutritional functions of carotenoids depend on natifida) that contributes more than 10% of the estimated their chemical structures which differ depending on the total production of carotenoids in nature. Although fucox- length of the polyene, nature of the end group and various anthin has shown potential as an antiobesity agent, there substituents they contain3). Fifty to sixty different are many additional naturally occurring carotenoids whose carotenoids are typically present in the human diet, and biological effects have not been examined. The fundamen- the most abundant forms found in plasma are: b-carotene, tal question addressed in this study was whether a certain ＊Correspondence to: Kazuo Miyashita, Laboratory of Biofunctional Material Chemistry, Division of Marine Bioscience, Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido 041-8611, JAPAN E-mail: [email protected] (K. Miyashita) Accepted March 14, 2008 (recieved for review February 27, 2008) Journal of Oleo Science ISSN 1345-8957 print / ISSN 1347-3352 online http://www.jstage.jst.go.jp/browse/jos/ 345 T. Okada, M. Nakai, H. Maeda et al. Fig. 1 Structure of Fucoxanthin, Fucoxanthinol, and Carotenoids Used in This Experiment. structure of carotenoids is, either entirely or partially, 2 MATERIALS AND METHODS associated with suppressive effects on adipocyte differenti- 2.1 Materials ation. Further understanding of the essential structures of Mouse 3T3-L1 (CCL-92.1) preadipocytes were obtained active carotenoids may allow for the elucidation of more from the American Type Culture Collection (Rockville, CT, comprehensive mechanisms, as well as the development of USA). Fetal bovine serum (FBS) and Dulbecco’s modified novel therapeutic compounds that possess antiobesity Eagle’s medium (DMEM) were purchased from Asahi Tech- activity due to their structural characteristics. no Glass Co., Ltd. (Funabashi, Chiba, Japan) and Nissui The objective of the present study was to investigate Pharmaceutical Co., Ltd. (Ueno, Tokyo, Japan), respectively. whether 13 naturally occurring carotenoids found in veg- The following 13 carotenoids were obtained from Carote- etables, fruits, and flowers (Fig. 1) possess suppressive Nature (Lupsingen, Switzerland): neoxanthin, lutein, vio- effects on the differentiation of 3T3-L1 preadipocyte cells. laxanthin, (rac)-a-carotene, b-carotene 5, 6-epoxide, (13Z)- The 3T3-L1 preadipocyte/adipocyte cell system was cho- canthaxanthin, (9Z)-canthaxanthin, citranaxanthin, rho- sen because this method has been well-characterized as a doxanthin, b-cryptoxanthin, capsorubin, antheraxanthin, reliable model for studying adipogenesis12). The suppres- lutein epoxide. sive effect was evaluated by determining lipid accumula- tion, glycerol-3-phosphate dehydrogenase (GPDH) activity, 2.23T3-L1 culture adipocyte protein 2 (aP2) expression and nuclear hormone 3T3-L1 cells were cultured in DMEM with 10% FBS, 100 receptors mRNA expression with or without the presence U/mL penicillin and 100 mg/mL streptomycin at 37℃ in a of the carotenoid during the cell differentiation. humidified atmosphere of 95% air and 5% CO2. After 3T3- L1 cells reached confluence, cells were incubated for an additional 24 h. Then, adipocyte differentiation of 3T3-L1 preadipocytes was initiated with the differentiation medi- um I, which contained 10 mg/mL insulin, 0.5 mM isobutyl- 346 J. Oleo Sci. 57, (6) 345-351 (2008) Suppressive Effect of Neoxanthin on the Adipocyte Differentiation methylxanthine, 0.1 mM dexamethazone, for 48 h. After cycles of 95℃ for 15 s, then 60℃ for 1 min. Primers used this time period, medium I was replaced with differentia- for PCR (PPARg, Mm00440945-m1; C/EBPa, Mm00514283- tion medium II (DMEM with 5 mg/ml insulin), which was s1; C/EBPb, Mm00843434-s1; aP2, Mm00445880-m1) were thereafter exchanged every 48 h for fresh medium II. purchased from Applied Biosystems Japan Ltd. (Haccho- Carotenoids were added into differentiation medium II in bori, Tokyo, Japan). an ethanol solution. The final concentration of ethanol in the medium was adjusted to 0.1% so as not to affect cell 2.6 Statistical analysis growth. The results were expressed as mean ± standard devia- tion (S.D.). Statistical comparisons were made between 2.3 Oil Red O staining treatments by ANOVA and Scheffe’s F-test. Intercellular lipid accumulation was measured by Oil Red O staining during adipocyte differentiation13). 3T3-L1 cells were incubated in carotenoid-containing differentia- tion medium II for 144 h. After incubation, cells were 3 RESULTS washed twice with PBS and fixed in a 10% formalin-con- 3.1 Effect of neoxanthin on lipid accumulation in 3T3-L1 taining PBS solution at 4℃ for 1 h. The fixed cells were adipose cell washed twice with distilled water and then stained using Oil red O staining revealed a promising effect of neoxan- 0.3% Oil Red O for 15 min at room temperature. The excess thin on prevention of lipid accumulation of 3T3-L1 cells; Oil Red O dye was then washed off with distilled water. A however, lutein did not show significant effects. As shown blank was also run that consisted of 3T3-L1 cell extracts in Fig. 2A, the addition of neoxanthin during adipocyte dif- that had undergone incubation with the carotenoid treat- ferentiation caused a significant reduction of intercellular ment above, but were not stained with Oil Red O dye. lipid accumulation expressed as relative value (%), with the Stained oil droplets in 3T3-L1 cells were extracted with control adipocyte being 100% (positive control). Differentia- isopropanol and their absorbance was measured at 490 nm. tion-induced cells plus 5 mM of neoxanthin accumulated The absorbance of the blank was then subtracted from the only 68% of the intracellular lipid contained in the control. absorbance of each treatment. Results were represented as Moreover, treatment with 20 mM neoxanthin resulted in a a relative percentage of differentiated 3T3-L1 cells without further reduction to approximately 36% of the lipid accu- carotenoid treatment (control). mulation of the control. In contrast, lutein at both 5 mM and 20 mM concentration did not attenuate lipid accumula- 2.4 Measurement of GPDH activity tion levels. GPDH (EC 1.1.1.8) activity was measured with a com- mercial assay kit (Hokudo Co., Ltd, Sapporo, Hokkaido, 3.2
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