ARTICLE pubs.acs.org/JAFC
A Series of 190-Hexanoyloxyfucoxanthin Derivatives from the Sea Mussel, Mytilus galloprovincialis, Grown in the Black Sea, Ukraine Takashi Maoka,*,† Tetsuji Etoh,‡ Alexandra V. Borodina,§ and Alexander A. Soldatov§ †
Research Institute for Production Development, 15 Shimogamo-morimoto-cho, Sakyo-ku, Kyoto 606-0805, Japan Graduate School of Pharmaceutical Sciences, Kyoto University, Yoshida-shimoadachi-cho, Sakyo-ku, Kyoto 606-8501, Japan § Institute of Biology of the Southern Seas by A.O. Kovalevsky National Academy of Sciences of Ukraine, Nahimov Av. 2, Sevastopol 99011, Crimea, Ukraine ‡
ABSTRACT: A series of carotenoids with 19- or 190 -hexanoyloxy moieties, 190 -hexanoyloxyfucoxanthin (1), 190 -hexanoyloxyfucoxanthinol (2), 190 -hexanoyloxyhalocynthiaxanthin (3), 19-hexanoyloxycrassostreaxanthin A (4), 19-hexanoyloxymytiloxanthin (5), and 19-hexanoyloxyallenicmytiloxanthin (6) were isolated from the edible part of the sea mussel, Mytilus galloprovincialis, grown in the Black Sea, Ukraine. Among them, 3, 4, and 6 were new compounds. These structures were charcterized by UVvis, fast atom bombardment mass spectrometry, circular dichroism, and 1H NMR spectroscopic data. They were assumed to be metabolites of 190 -hexanoyloxyfucoxanthin (1). KEYWORDS: Carotenoids, sea mussel, Mytilus galloprovincialis, 19- or 190 -hexanoyloxy carotenoids
’ INTRODUCTION Marine bivalves contain various carotenoids that show structural diversity.14 Some marine carotenoids have reportedly exhibited biological functions such as antioxidative, antitumor, anticarcinogenic, and immune enhancement activities.5 Fucoxanthin and its metabolites, fucoxanthinol, halocynthiaxanthin, and mytiloxanthin, are widely distributed in marine bivalves.14 Edible mussels, belonging to Mytilidae, show bright orangecolored muscle due to the presence of carotenoids. In 1970, unique structural carotenoids, mytiloxanthin and isomytiloxanthin, were isolated as major carotenoids from Mytilus edulis.6 Later, some acetylenic and allenic carotenoids, including 190 hexanoyloxyfucoxanthin (1) and 190 -hexanoyloxyfucoxanthinol (2) (Figure 1), were reported from M. edulis.7,8 Furthermore, a series of oxidative metabolites of diatoxanthin and alloxanthin were isolated from the Japanese sea mussel, Mytilus coruscus.9 In the course of carotenoid studies of shellfish,915 carotenoids of the edible mussel Mytilus galloprovincialis were investigated. A series of carotenoids with 19- or 190 -hexanoyloxy moieties, 190 hexanoyloxyfucoxanthin (1), 190 -hexanoyloxyfucoxanthinol (2), 190 -hexanoyloxyhalocynthiaxanthin (3), 19-hexanoyloxycrassostreaxanthin A (4), 19-hexanoyloxymytiloxanthin (5), and 19hexanoyloxyallenicmytiloxanthin (6), were isolated from the edible part of M. galloprovincialis, grown in the Black Sea, Ukraine. Among them, 3, 4, and 6 were new carotenoids. Here, we describe the isolation and structural elucidation of these new carotenoids from M. galloprovincialis. Furthermore, metabolic pathways of 190 -hexanoyloxyfucoxanthin (1) in M. galloprovincialis are discussed. ’ MATERIALS AND METHODS Apparatus. The UVvisble (UVvis) spectra were recorded with a Hitachi U-2001 spectrophotometer in diethyl ether (Et2O). The positive ion fast atom bombardment mass spectrometry (FAB-MS) spectra were recorded using a JEOL JMS-HX 110A mass spectrometer r 2011 American Chemical Society
with m-nitrobenzyl alcohol as a matrix. The 1H NMR (500 MHz) spectra were measured with a Varian UNITY INOVA 500 spectrometer in CDCl3 with TMS as an internal standard. The CD spectra were recorded in Et2O at room temperature with a Jasco J-500C spectropolarimeter. Preparative high-performance liquid chromatography (HPLC) was performed on a Shimadzu LC-6AD with a Shimadzu SPD-6AV spectrophotometer set at 450 nm. The column used was a 250 mm 10 mm i.d., 10 μm Cosmosil 5C18II (Nacalai Tesque, Kyoto, Japan) and a 250 mm 10 mm i.d., 10 μm Cosmosil 5SL-II (Nacalai Tesque, Kyoto, Japan). Animal Materials. M. galloprovincialis were collected from Sevastopol Bay (Martynova) in the Black Sea, Ukraine, from April to June, 2011. M. galloprovincialis grown in the Inland Sea of Seto, Japan, were purchased from a fish market in Kyoto, Japan, in June, 2011. Quantitation of Carotenoids. The total carotenoid content and amount of carotenoids eluted by column chromatography were calculated using the extinction coefficient of E1% cm = 2500 at λ max (450 nm) and 1600 in the case of fucoxanthin derivatives.16 In HPLC analysis, the relative amounts of individual carotenoids were calculated from the peak area detected at 450 nm. Isolation of Carotenoids. Procedures to isolate carotenoids from M. galloprovincialis, grown in the Black Sea, Ukraine, were as follows. The edible part (220 g) of M. galloprovincialis (from 1 kg of whole shellfish) was extracted with Me2CO at room temperature. The Me2CO extract was partitioned between Et2O and aqueous NaCl. The organic layer was dried over Na2SO4 and then concentrated to dryness and subjected to silica gel column chromatography (300 mm 10 mm). The fraction eluted with 100 mL of hexane from silica gel column chromatography contained β-carotene. The fraction eluted with 200 mL of Et2O:hexane (1:1) from silica gel column chromatography contained sterols and lipids. The fraction eluted with 200 mL of Et2O from silica gel column chromatography was further separated by preparative HPLC on Received: August 31, 2011 Accepted: November 10, 2011 Revised: November 9, 2011 Published: November 10, 2011 13059
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Figure 1. Structures of 190 -hexanolyoxyfucoxanthin derivatives from the sea mussel, M. galloprovincialis, grown in the Black Sea, Ukraine. silica gel with Me2CO:hexane (3:7), at a flow rate of 2.0 mL/min and successively ODS with methanol, flow rate of 2.0 mL/min, to yield 80 apoalloxanthinal, crassostreaxanthin A, 19-hexanoyloxycrassostreaxanthin A (4), pectenolone, diatoxanthin, alloxanthin, mytiloxanthin, and 19-hexanoyloxymytiloxanthin (5). The fraction eluted with 200 mL of Me2COEt2O (1:1) from silica gel column chromatography was further separated by preparative HPLC on silica gel with Me2COhexane (3:7), at a flow rate of 2.0 mL/min and successively ODS with methanol (MeOH), at a flow rate of 2.0 mL/min, to yield fucoxanthin, 190 -hexanoyloxyfucoxanthin (1), halocynthiaxanthin, 190 hexanoyloxyhalocynthiaxanthin (3), pectenol A, hetertoxanthin, fucoxanthinol, 190 -hexaoyloxyfucoxanthinol (2), and 19-hexanoyloxyallenicmytiloxanthin (6). Carotenoids from M. galloprovincialis, grown in the Inland Sea of Seta, Japan, were analyzed in the same manner. Identification and Characterization of Carotenoids. 190 Hexanoyloxyfucoxanthin (1). Yield: 20 μg. UVvis: λmax 445 and 470 nm (Et2O). HR FAB-MS m/z: 772.4880 [M+] (calcd for C48H68O8, 772.4896). CD (Et2O) λmax (Δε): 218 (0.4), 271 (0.5), 332 (+0.5). These data were identical with reported values of previous literatures.1719 190 -Hexanoyloxyfucoxanthinol (2). Yield: 200 μg. UVvis: λmax 445 and 470 nm (Et2O). HR FAB-MS m/z: 730.4780 [M+] (calcd for C46H66O7, 730.4808). 1H NMR: δ (CDCl3) Table 1. CD (Et2O) λmax (Δε): 218 (0.4), 271 (0.5), 332 (+0.5). 190 -Hexanoyloxyhalocynthiaxanthin (3). Yield: 100 μg. UVvis: λmax 450 and 470 nm (Et2O). HR FAB-MS m/z: 712.4696 [M+] (calcd for C46H64O6, 712.4704). 1H NMR: δ (CDCl3) Table 1. CD (Et2O) λmax (Δε): 247 (0.2), 263 (1.1), 350 (1.5). 19-Hexanoyloxycrassostreaxanthin A (4). Yield: 50 μg. UVvis: λmax 450 and 470 nm (Et2O). HR FAB-MS m/z: 712.4698 [M+] (calcd for C46H64O6, 712.4704). 1H NMR: δ (CDCl3) Table 1. CD (Et2O) λmax (Δε): 210 (2.8), 276 (2.2), 335 (+1.0). 19-Hexanoyloxymytiloxanthin (5). Yield: 100 μg. UVvis: 470 nm (Et2O). FAB-MS m/z: 712. CD (Et2O) λmax (Δε): 216 (1.3), 254 (1.7), 298 (+1.0). 1H NMR: δ (CDCl3) spectral data were the same as previous published values.20 190 -Hexanoyloxyallenicmytiloxanthin (6). Yield: 100 μg. UVvis: λmax 465 nm (Et2O). HR FAB-MS m/z: 730.4783 [M+] (calcd for C46H66O7, 730.4808). 1H NMR: δ (CDCl3) Table 1. CD (Et2O) λmax (Δε): 227 (1.5), 290 (3.0), 370 (1.0). The identification of other carotenoids was carried out according to our usual methods.915
Table 1. Carotenoids Content and Compositions of Edible Part of the Sea Mussel, M. galloprovincialis, Grown in the Black Sea, Ukraine, and Inland Sea of Seto, Japan
total carotenoid content
Black Sea,
Inland Sea
Ukraine
of Seto, Japan
3.6
1.2
carotenoid composition
%
%
β-carotene
0.5
0.5
80 -apoalloxanthinol crassostreaxanrhin A
0.5 4.5
0.8 6.5 NDa
(mg/100 g edible part)
19-hexanoyloxycrassostreaxanrhin A (4)
1.0
pectenolone
3.5
6.0
diatoxanthin
4.4
4.4
4.5
4.5
alloxanthin mytiloxanthin
11.5
18.4
2.5
ND
17.6 2.2
17.6 ND
pectenol A
6.4
8.6
fucoxanthin
3.1
4.0
190 -hexanoyloxyfucoxanthin (1)
0.5
ND
19-hexanoyloxymytiloxanthin (5) halocynthiaxanthin 190 -hexanoyloxyhalocynthiaxanthin (3)
a
heteroxanthin
17.2
15.0
fucoxanthinol
7.2
8.2
190 -hexanoyloxyfucoxanthinol (2)
6.9
ND
19-hexanoyloxyallenicmytiloxanthin (6) peridinin
2.5 1.5
ND 1.8
pyrrhoxanthinol
1.5
1.2
others
0.5
2.5
ND, not detected.
’ RESULTS AND DISCUSSION The carotenoids content and composition in M. galloprovncialis, grown in Sevastopol Bay, the Black Sea, Ukraine, are shown in Table 1. As with other sea mussels,69 mytlioxanthin, halocymthiaxanthin, 13060
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Table 2. 1H NMR (CDCl3, 500 MHz) Data for Compounds 24 and 6a 2 δ
position
4
δ
mult (J Hz)
6
δ
mult (J Hz)
δ
mult (J Hz)
mult (J Hz)
H-2α
1.50
dd (12, 12)
1.50
dd (12, 12)
1.84
ddd (13,4,2)
1.94
H-2β
1.36
overlapped
1.36
overlapped
1.45
dd (13, 13)
1.34
dd (12, 12)
H-3
3.82
m
3.82
m
3.99
m
4.30
m
H-4α
2.32
ddd (18, 6, 2)
2.32
ddd (18, 6, 2)
2.43
ddd (18, 6, 2)
2.26
ddd (13, 4, 2)
H-4β
1.76
dd (18, 9)
1.76
dd (18, 9)
2.07
dd (18, 9)
1.41
dd (13, 13)
H-7
2.06
d (18)
2.06
d (18)
H-7
3.66
d (18)
3.66
d (18)
H-8 H-10
7.15
d (11)
7.15
d (11)
6.42
d (11)
6.04 6.30
s d (11)
H-11
6.59
dd (15, 11)
6.59
dd (15, 11)
6.60
dd (15, 11)
6.72
dd (15, 11)
H-12
6.68
d (15)
6.68
d (15)
6.64
d (15)
6.41
d (15)
H-14
6.41
d (11)
6.41
d (11)
6.31
d (11)
6.31
d (11)
H-15
6.65
dd (14, 11)
6.65
dd (14, 11)
6.75
dd (14, 11)
6.75
dd (14, 11)
CH3-16
1.04
s
1.04
s
1.15
s
1.34
s
CH3-17
0.97
s
0.97
s
1.20
s
1.08
s
CH3-18 19
1.23 CH3 1.95
s s
1.23 CH3 1.95
s s
1.93 CH2 4.85
s s
1.36 H 4.75
s d (12)
H 4.81
d (12)
CH3-20
2.00
s
2.00
s
1.98
s
1.96
s
H-20 α
1.94
ddd (12, 4, 2)
1.84
ddd (13,4,2)
2.69
dd (15, 7)
2.19
dd (14, 8)
H-20 β
1.34
dd (12, 12)
1.45
dd (13, 13)
2.52
dd (15, 5)
1.72
dd (14, 5)
H-30
4.30
m
3.99
m
4.21
m
4.53
m
H-40 α
2.26
ddd (13, 4, 2)
2.43
ddd (18, 6, 2)
n.a.
2.88
dd (15, 9)
H-40 β H-50
1.41
dd (13, 13)
2.07
dd (18, 9)
n.a. n.a.
1.55
dd (15,3)
H-70
2.86
d (14)
H-70
2.93
d (14)
ddd (12, 4, 2)
H-80
6.04
s
5.86
s
H-100
6.30
d (11)
6.42
d (11)
7.26
d (11)
7.24
d (11)
H-110
6.72
dd (15, 11)
6.60
dd (15, 11)
6.59
d (15, 11)
6.60
d (15, 11)
H-120
6.41
d (15)
6.64
d (15)
6.68
d (15)
6.66
d (15)
H-140 H-150
6.31 6.75
d (11) dd (14, 11)
6.31 6.75
d (11) dd (14, 11)
6.42 6.66
d (11) dd (14, 11)
6.38 6.63
d (11) dd (14, 11)
CH3-160
1.34
s
1.15
s
2.14
s
1.19
s
CH3-170
1.08
s
1.20
s
1.10
s
0.85
s
CH3-180
1.36
s
1.93
s
0.99
d (7)
1.35
s
190
H 4.75
d (12)
CH2 4.85
s
CH3 1.93
s
CH3 1.99
s
H 4.81
d (12)
1.96
s
1.98
s
1.99
s
1.99
s
2.28
t (7.5)
16.30 2.28
s t (7.5)
CH3-200
a
3
80 -OH Ac-CH2
2.28
Ac-CH2
1.261.29
m
1.261.29
m
1.261.29
m
1.261.29
m
Ac-CH3
0.88
t (7.5)
0.88
t (7.5)
0.88
t (7.5)
0.88
t (7.5)
t (7.5)
2.28
t (7.5)
Ac, acyloxy moiety; s, singlet; d, doublet; t, triplet; m, multiplet.
diatoxanthin, alloxanthin, pectinol A, and heteroxanthin were found to be major carotenoids in M. galloprovincialis. A series of carotenoids with 19- or 190 -hexanoyloxy moieties, 16, were isolated. 190 -Hexanoyloxyfucoxanthin (1) was identified from UVvis and FAB-MS data.1719 190 -Hexanoyloxyfucoxanthinol (2) and 19-hexanoyloxymytiloxanthin (5) were identified by UVvis, FAB-MS, CD, and 1H NMR data. 190 -Hexanoyloxyfucoxanthinol (2) was once characterized by
only UVvis and EI-MS data.7,8 In the present study, 190 hexanoyloxyfucoxanthinol was completely characterized by 1 H NMR and CD spectroscopic data. The stereostructure of 19-hexanoyloxymytiloxanthin was postulated to be (3R,30 S, 50 R), as shown in Figure 1, on CD spectral data comparison with mytiloxanthin.21 Compound 3 was isolated as a minor component. HR FAB-MS revealed the molecular formula of C46H64O6 for 3. 13061
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Figure 2. Possible metabolic pathways of 190 -hexanoyloxyfucoxanthin in the sea mussel, M. galloprovincialis, grown in the Black Sea, Ukraine.
Compound 3 showed the same UVvis spectrum as that of halocynthiaxanthin.21 1H NMR of 3 showed almost the same spectra as that of halocynthiaxanthin 21 except for the disappearance of the methyl signal at 190 , which was replaced by an oxymethylene signal at 4.85 ppm and the presence of a saturated acyloxy moiety (Table 2). This suggested that compound 3 was a 190 -acyloxy derivative of halocynthiaxanthin. This structure was confirmed by COSY and ROESY experiments. From the HR FAB-MS data, the acyloxy moiety was assigned as hexanoyl. Therefore, the structure of this compound was determined to be 190 -hexanoyloxyhalocynthiaxanthin (3). CD of 3 showed the same spectra as that of halocynthiaxanthin.21 Thus, the (3S,5R,6S,30 S) configuration was postulated for 3 as shown in Figure 1. Compound 4 showed the same UVvis and FAB-MS spectra as those of 3. This compound revealed almost the same 1H NMR spectrum as that of crassostreaxanthin A,22 except for the disappearance of a methyl signal at 19 instead of the presence of an oxymethylene signal at 4.85 ppm and the presence of a saturated acyloxy moiety (Table 2). From the results of COSY and CD data, the structure of this compound was determined to be 19-hexanoyloxycrassostreaxanthin A (4), as shown in Figure 1. Compound 6 showed an absorption maximum at 465 nm. The molecular formula of 6 was determined to be C46H66O7 by HR FAB-MS. 1H NMR of 3 showed almost the same spectra as that of 3,5,30 ,80 -tetrahydro-6,7-didehydro-5,6-dihydro-β,k-caroten60 -one,10 named allenicmytiloxanthin,4 except for the disappearance of a methyl signal at 19, which was replaced by AB type coupled oxymethylene signals at 4.75 and 4.81 ppm and the presence of a saturated acyloxy moiety (Table 1). This suggested that compound 6 was a 19-acyloxy derivative of allenicmytiloxanthin. This structure was confirmed by COSY and ROESY experiments. Because of the anisotropic effect of an allenic bond,
two oxymethylene protons at 19 in 6 showed different chemical shifts (4.75 and 4.81 ppm) and AB type-coupled signals in 1H NMR.19 CD of 6 was the same as that of allenicmytiloxanthin, exhibiting a (3S,5R,6R,30 S,50 R) configuration.10 Therefore, the structure of 6 was determined to be 190 -hexanoyloxyallenicmytiloxanthin (6), as shown in Figure 1. 190 -Hexanoyloxyfucoxanthin (1) is a major characteristic carotenoid in Emilina (Coccolithus) huxleyi,17,18 and it was also found in several algae belonging to Prymnesiophyceae 23,24 and toxic dinoflagellates belonging to the genera genus Gymnodinium and Gyrodinium.24 190 -Hexanoyloxyfucoxanthinol (2) was isolated from M. edulis after feeding with E. huxleyi.7,8 19-Hexanoyloxymytiloxanthin (5) was isolated from the marine sponge Phakellia stelliderma.20 Bivalves accumulate carotenoids obtained from their dietary microalgae and modify them through metabolic reactions.14 The salinity of Sevastopol Bay in the Black Sea is 17 ppm, which is almost two times lower than that of the ocean.25 Therefore, phytoplankton blooms in Sevastopol Bay are characteristic and different from the ocean. Marked sewage pollution leads to periodic blooms of toxic blue-green algae and dinoflagellates.26 Furthermore, blooming of E. huxleyi, which contains 190 -hexanoyloxyfucoxanthin (1) as a major carotenoid, was frequently found in Sevastopol Bay.27 Therefore, 190 -hexanoyloxyfucoxanthin (1) in M. galloprovincialis was assumed to originate from E. huxleyi and/or dinoflagellates, belonging to the genera Gymnodinium and Gyrodinium, which mussels feed on. Concerning the metabolic pathway of fucoxanthin in marine invertebrtates14 and the results of previous studies,7,8,20 the metabolic pathways of 190 -hexanoyloxyfucoxanthin (1) in M. galloprovincialis were proposed as shown in Figure 2. We also investigated the carotenoids of M. galloprovincialis, grown in the Inland Sea of Seto, Japan. Fucoxanthin, fucoxanthinol, halocynthiaxanthin, crrasostreaxanthin A, mytiloxanthin, and 13062
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Journal of Agricultural and Food Chemistry allenicmytiloxanthin were also isolated. However, their corresponding 19- or 190 -hexanoyloxy derivatives (16) were not found in Japanese M. galloprovincialis (Table 1). These differences might reflect the diversity of algae consumed by Ukrainan and Japanese mussels. From the carotenoids composition, the major diets of Japanese M. galloprovincialis were assumed to be diatoms whose major carotenoids are not 190 -hexanoyloxyfucoxanthin but fucoxanthin and diatoxanthin. Carotenoids in bivalves well reflect the carotenoids of their dietary algae. Because available amounts of samples were less than 200 μg, biological activities of compounds 16 could not be examined. Recently, fucoxanthin and its metabolites were noted to exhibit radical scavenging,28 singlet oxygen quenching,28 anticarcinogenic,29,30 antidiabetic,31 and antiobesity.32 Therefore, it was assumed that compounds 16 might have similar activities as those of fucoxanthin. Furthermore, some microalgal carotenoids, such as diatoxanthin and alloxanthin, were found to exhibit anticarcinogenic33,34 and anti-inflammatory activities.35 Sea mussels accumulate microalgal carotenoids, fucoxanthin, diatoxanthin, and alloxanthin in their bodies. Therefore, sea mussels are good dietary sources of carotenoids originating from microalgae for humans. In conclusion, 190 -hexanolyoxyfucoxanthin (1), 190 -hexanolyoxyfucoxanthinol (2), 190 -hexanolyoxyhalocynthiaxanthin (3), 19-hexanolyoxycrrasostreaxanthin A (4), 19-hexanolyoxymytiloxanthin (5), and 19-hexanolyoxyallenicmytiloxanthin (6) were isolated from the edible part of M. galloprovincialis, grown in the Black Sea, Ukraine.
’ AUTHOR INFORMATION Corresponding Author
*Tel: +81-75-781-1107. Fax: +81-75-791-7659. E-mail: maoka@ mbox.kyoto-inet.or.jp.
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