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Generation of Tetracosahexaenoic Acid in Benthic Marine Organisms

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Generation of Tetracosahexaenoic Acid in Benthic Marine Organisms Journal of Oleo Science Copyright ©2015 by Japan Oil Chemists’ Society doi : 10.5650/jos.ess15079 J. Oleo Sci. 64, (7) 721-727 (2015) NOTE Generation of Tetracosahexaenoic Acid in Benthic Marine Organisms Rei Suo1, Haoqi Li1, Kazuaki Yoshinaga2, Toshiharu Nagai2, Hoyo Mizobe2, Koichi Kojima2, Koji Nagao3, Fumiaki Beppu1 and Naohiro Gotoh1＊ 1 Department of Food Science and Technology, Tokyo University of Marine Science and Technology (4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan) 2 Tsukishima Foods Industry Co. Ltd. (3-17-9, Higashi Kasai, Edogawa-ku, Tokyo 134-8520, Japan) 3 Department of Applied Biochemistry and Food Science, Saga University (1 Honjo-machi, Saga-shi, Saga 840-8502, Japan) Abstract: Tetracosahexaenoic acid (THA, 24:6n-3) has been shown to have the strongest ability to suppress accumulation of lipids in HepG2 cells among well-known n-3 highly unsaturated fatty acids, such as EPA and DHA. In this study, a method for mass production of THA was investigated using distributions of THA and DHA in thirty-two marine organisms, such as starfishes, right-eyed flounders, shellfishes, and sharks. The fatty acid composition of the marine organisms was analyzed using GC-FID and THA was detected in starfish, right-eyed flounder, and shark. Furthermore, the ratio of DHA and THA (DHA/THA) in each sample was calculated using chromatogram peak area of GC-FID, and the value was found to be lower than 1 in some starfishes. As a result, THA was thought to be synthesized in the starfishes. In contrast, the value of DHA/THA for right-eyed flounder and sharks was greater than 1. The THA accumulation in right-eyed flounder was considered to be because of the starfishes that the flounder consumes as part of its diet. DHA is synthesized from THA by beta-oxidation in peroxisomes, in the Sprecher’s shunt. The high accumulation of THA observed in the flounder would be caused by the decreasing enzyme activation due to beta-oxidation in the peroxisomes of the starfishes. Understanding the differences in THA between aquatic species could also potentially allow us to understand why THA is generated in marine animals. Key words: docosahexaenoic acid, lipid metabolism, N-3 highly unsaturated fatty acid, starfish, tetracosahexaenoic acid 1 INTRODUCTION and fishes do not produce Δ4 desaturase, which can direct- Docosahexaenoic acid（DHA; 22:6n-3）is an indispensable ly synthesize DHA from DPA. Consequently, many n-3HU- n-3 type highly unsaturated fatty acid（n-3HUFA）in the FAs appear during the process of DHA synthesis from EPA human body because it is a main component of the brain （Fig. 1）. DPA is one such, and it is reported that marine and nervous system. However, the human body cannot mammals contain high levels of DPA3, 4）. THA is also an synthesize DHA de novo. Humans primarily acquire DHA n-3HUFA found in marine organisms such as the Baltic from lipids in marine organisms, such as fishes and shell- herring（Clupea harengus）5）, flathead flounder（Hippo- fishes. Alternatively, the human body can synthesize DHA glossoides dubius）6）, brittle star（Amphiura elandifor- from eicosapentaenoic acid（EPA; 20:5n-3）via Sprecher’s mis7）, Asteronyx loveni8）, and Ophioplocus japonicas8））, shunt1）. During the synthesis process, EPA is firstly elon- jellyfish（Aurelia sp.）9）, sea lilies8（） Comanthus japonica, gated to form docosapentaenoic acid（DPA; 22:5n-3）. Later, Tropiometra afra macrodiscus）, and coelenterates（Pen- the formed DPA is elongated again to form tetracosapen- Abbreviations: DHA, docosahexaenoic acid; DPA, taenoic acid TPA; 24:5n-3 . The TPA is desaturated by 6 （ ） Δ docosapentaenoic acid; EPA, eicosapentaenoic acid; FAD, desaturase to form tetracosahexaenoic acid（THA; 24:6n- flavin adenine dinucleotide; GC-FID, gas chromatography- 3）. The THA is then beta-oxidized to form DHA in the per- flame ionization detector; n-3HUFA, n-3 highly unsaturated oxisome2）. This is a complicated process because animals fatty acid; THA, tetracosahexaenoic acid ＊Correspondence to: Naohiro Gotoh, Department of Food Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato-ku, Tokyo 108-8477, Japan E-mail: [email protected] Accepted April 13, 2015 (received for review April 5, 2015) 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 721 R. Suo, H. Li and K. Yoshinaga et al. Fig. 1 The structures of EPA, DPA, DHA, and THA. natularia: Pavonaria finmarchica10））. DPA and THA are 2 Materials and methods intermediate products in Sprecher’s shunt and do not have 2.1 Materials the necessary properties to accumulate in animal and fish All the reagents used in this study were purchased from bodies in high contents. THA, in particular, is an intermedi- Wako Pure Chemical Industries, Ltd.（Osaka, Japan）. A ary product formed prior to the formation of DHA in Spre- fatty acid methyl ester standard solution（Supelco 37 Com- cher’s shunt. The accumulation of DHA is thought to be as- ponent FAME Mix）was purchased from Sigma-Aldrich cribed to the inactivation of the beta-oxidation activity in Japan K.K.（Tokyo, Japan）. THA methyl ester was obtained the peroxisome7）. Interestingly, most of the reported from Tsukishima Foods Industry Co., Ltd（Tokyo, Japan） marine organisms containing high amounts of THA are with purity greater than 98％. Sample marine organisms benthic organisms. For example, brittle stars and sea lilies were collected during May 2013 to Dec 2013, and the accumulate a large quantity of THA; however, their food details are shown in Table 1. sources, such as the sea cucumber, do not contain THA within their bodies8）. Therefore, it is thought that the high 2.2 Extraction of the lipids from samples content of THA in such benthic organisms might be as- The samples were weighed and homogenized with two- cribed to the decreasing beta-oxidation activity required to fold weight of normal saline. Each homogenate was placed form DHA from THA and elongation of DHA to THA that in a test tube with a screw cap, and a two-fold volume of a would yield extremely high levels of THA11）. It is now chloroform and methanol mixture（2:/1, v/v）was added to thought that decreasing levels of beta-oxidation activity in the homogenate14）. The solution was mixed vigorously with the peroxisome might be the main cause of high THA accu- a vortex mixer and centrifuged at 700×g for 10 min. The mulation7）. Incidentally, the high level of THA found in the bottom layer was carefully removed with a Pasteur pipette, flathead flounder（H. dubius）is thought to be because of transferred to a new test tube, and dried using nitrogen its position in the food chain with the brittle star is part of stream. The dried lipid samples were weighed, purged with the flathead flounder diet11）. argon gas, and stored at －40℃ until use. Two studies concerning the health functions of THA were recently conducted. Ishihara et al. reported that THA 2.3 Analyses of fatty acid composition isolated from brittle star could reduce histamine content Methyl esterification of the extracted lipids was per- and inhibit antigen-stimulated production of leukotriene- formed using the following procedure. Approximately 10 related compounds in MC/9 cells12）. Nagao et al. recently mg extracted lipids from the sample and 1 mL 0.5 M compared lipid metabolism effects among 4 types of sodium hydroxide methanol solution were mixed in a 10 n-3HUFAs（EPA, DPA, DHA, and THA）by using HepG2 mL screw-capped tube. A 14％ boron trifluoride methanol cells13）. These researchers found that THA exerted the solution（2 mL）was added to the mixture and heated at strongest suppression on the synthesis of triacylglycerol 100℃ for 20 s. The heated tube was cooled to 40℃ under and cholesteryl ester in the following order: THA＞DHA＞ air, and 1 mL hexane was added to the solution. Saturated DPA＞EPA. Nagao et al. concluded that both the number sodium chloride solution（3 mL）was added to the mixture of carbon atoms and double bonds in an n-3HUFA structure and shaken vigorously. The tube was left undisturbed for a affects lipid metabolism in HepG2 cells. According to these few minutes to allow the hexane and water layers to sepa- results, THA might act as a valuable health functional com- rate. The 1 μL hexane layer was introduced to a gas chro- ponent to decrease accumulation of hepatic lipids and matography-flame ionization detector（GC-FID）system possess high potential as a food functional ingredient. （GC14B, Shimadzu Corporation, Tokyo, Japan）equipped However, THA is a rare n-3HUFA, even in marine organ- with a capillary column（Omegawax320, 30 m×0.32 mm isms. Here, we discuss a method for the mass production ID, 0.25 μm thickness, Sigma-Aldrich Japan K.K.）and a of THA based on the distributions of THA and DHA in thir- Chromatopac integrator（C-R6A; Shimadzu Corporation）to ty-two marine organisms. analyze the fatty acid composition and relative ratio. The 722 J. Oleo Sci. 64, (7) 721-727 (2015) Generation of THA in benthic marine organisms Table 1 Samples used in this study. Name Origin Sampling/Purchase Starfish 1 Ophiura sarsii (N.E.N#) A¢ Sampling 2 Certonardoa semiregularis (Red starfish) B£ Sampling 3 Macrophiothrix longipeda (N.E.N#) A Sampling 4 Ophiura sarsi Lütken (N.E.N#) A Sampling 5 Luidia quinaria (N.E.N#) A Sampling 6 Solaster paxillatus (N.E.N#) A Sampling 7 Asterias amurensis (Northern Pacific seastar) 1 A Sampling 8 Ophiozonella longispina (brittle star) A Sampling 9 Astropecten (comb star) A Sampling 10 Asterias amurensis (Northern
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