1,5-DI-O-Isoferuloylquinic acid and other phenolic compounds from pollen of calendula officinalis

Article abstract of DOI:10.1007/s10600-014-1030-9

A new phenylpropanoid that was identified as 1,5-di-O-isoferuloylquinic acid (1) and 17 known compounds including 1,5-di-O-feruloylquinic acid (2), which was obtained for the first time from a plant and was synthesized previously, were isolated from pollen of Calendula officinalis. Compounds 1 and 2 were the dominant phenolic compounds from pollen of C. officinalis. It was found that 1 possessed pronounced inhibitory activity against tyrosinase (IC50 11.26μg/mL).

Full text of DOI:10.1007/s10600-014-1030-9

Chemistry of Natural Compounds, Vol. 50, No. 4, September, 2014 [Russian original No. 4, July–August, 2014]
1
,5-DI-O-ISOFERULOYLQUINIC ACID AND OTHER PHENOLIC
COMPOUNDS FROM POLLEN OF Calendula officinalis
*
D. N. Olennikov and N. I. Kashchenko
A new phenylpropanoid that was identified as 1,5-di-O-isoferuloylquinic acid (1) and 17 known compounds
including 1,5-di-O-feruloylquinic acid (2), which was obtained for the first time from a plant and was
synthesized previously, were isolated from pollen of Calendula officinalis. Compounds 1 and 2 were the
dominant phenolic compounds from pollen of C. officinalis. It was found that 1 possessed pronounced
inhibitory activity against tyrosinase (IC50 11.26 ꢀg/mL).
Keywords: Calendula officinalis, Asteraceae, 1,5-di-O-isoferuloylquinic acid, anti-tyrosinase activity.
Pollen (pollen grain) is a morphologically specialized construct and plays an important role in plant reproduction.
Pollen is characterized by high contents of phenolic compounds, especially flavonoids, which regulate fertilization [1]. Early
research showed that pollen phenols are represented by various compound classes including flavonols, flavones, and
phenylpropanoids. Their composition is specific to each species [2].
Calendula officinalis L. (Asteraceae) is a well-known medicinal plant that is used in official medicine of most countries.
Despite the satisfactory knowledge level regarding C. officinalis, information on the chemical composition of its pollen indicates
only that it contains triterpenoids and carotinoids [3]. Phenolic compounds have not been reported from it. The goal of the
present work was to study the composition of phenolic compounds from pollen of C. officinalis cultivated in Buryatia.
Chromatographic separation of substances extracted from pollen of C. officinalis isolated 18 compounds including
the new phenylpropanoid 1 and 17 known compounds.
+
According to HR-MS-TOF, 1 had the formula C H O {m/z 567.411 ([M + Na] ; calc. 567.442)}. The UV
2
7 28 12
spectrum indicated that it was a phenylpropanoid formed from ferulic/isoferulic acid. ESI-MS/MS spectra taken in negative
–
mode contained peaks for the molecular ion with m/z 543 [M – H] and a characteristic ferulic/isoferulic acid fragment with
m/z 193 [4]. The alkaline hydrolysis products included isoferulic and quinic acids and provided a final identification of the
acyl group. The results established that 1 was di-O-isoferuloylquinic acid.
The PMR spectrum of 1 exhibited four doublets with SSCC J = 16.1 Hz that were due to the influence of
trans-olefinic protons H-7ꢁ/H-8ꢁ and H-7ꢂ/H-8ꢂ (Table 1). The aromatic protons gave resonances for two aromatic systems
with 1,3,4-substitution (ABX-type) at 7.10 (1H, d, J = 1.9), 6.82 (1H, d, J = 8.0), and 7.05 (1H, dd, J = 8.0, 1.9) and 7.14 (1H,
1
3
d, J = 1.9), 6.78 (1H, d, J = 8.0), and 7.00 (1H, dd, J = 8.0, 1.9). Weak-field shifts of C-4ꢁ and C-4ꢂ in the C NMR spectrum
149.4 and 149.1 ppm) compared with those of 1,5-di-O-caffeoylquinic acid (147.0 and 146.6 ppm) were due to the influence
of the methoxy group. Correlations in the HMBC spectrum between methoxy protons (3.90 and 3.87 ppm) and C-4ꢁ and C-4ꢂ
(
(
149.4 and 149.1 ppm, respectively) confirmed that the acyl substituents were isoferulic acids.
Quinic acid in 1 gave characteristic resonances in the 13C NMR spectrum for three oxymethines (69.7, 70.6, 72.8 ppm)
and two methylenes (34.5 and 35.4 ppm), one oxidized quaternary C atom (80.9 ppm), and one carboxylic C atom
174.7 ppm). The PMR spectrum showed resonances for three oxymethine protons (3.75, 4.27, 5.35 ppm) and two pairs of
(
1
3
methylene protons (H -2 and H -6) [5]. A comparison of C NMR spectra of unsubstituted quinic acid and 1 found that the
2
2
C-1 and C-5 resonances were shifted to weak field (75.4ꢃ80.9 and 67.4ꢃ70.6 ppm), which was characteristic of 1,5-acylquinic
acids [6], and indicated that these positions were substituted. Despite the similar chemical shifts of the quinic acid H-3 and
H-5 resonances [7], the location of the second isoferuloyl residue on C-5 was confirmed by the strong weak-field shift of the
H-5 resonance (4.10ꢃ5.35 ppm) and correlations in the HMBC spectrum between H-5 (5.35 pm) and C-9ꢂ (167.9 ppm).
Institute of General and Experimental Biology, Siberian Branch, Russian Academy of Sciences, 670047, Ulan-Ude,
Ul. Sakhꢁyanovoi, 6, fax: 7(3012) 43 47 43, e-mail: oldaniil@rambler.ru. Translated from Khimiya Prirodnykh Soedinenii,
No. 4, July–August, 2014, pp. 513–517. Original article submitted April 20, 2014.
0
009-3130/14/5004-0589 ©2014 Springer Science+Business Media New York
589

TABLE 1. PMR (500 MHz) and 13C NMR (125 MHz) Spectra of 1 and 2 (MeOH-d , ꢄ, ppm, J/Hz)
4
1
2
C atom
DEPT
ꢄH
ꢄÑ
ꢄH
ꢄÑ
Quinyl
1
2
3
4
5
6
C
CH
CH
CH
CH
80.9
34.5
69.7
72.8
70.6
35.4
80.3
34.4
69.4
72.6
70.3
35.1
2
2.38–2.42 (2Í, m)
4.27 (1Í, ddd, J = 4.5, 4.0, 3.2)
3.75 (1Í, dd, J = 8.0, 3.2)
2.35–2.40 (2Í, m)
4.24 (1Í, ddd, J = 4.4, 4.0, 3.1)
3.70 (1Í, dd, J = 8.1, 3.3)
5.35 (1Í, ddd, J = 9.0, 8.1, 3.9)
2.46 (1Í, m, Í ),
À
2.01 (1Í, dd, J = 14.0, 8.9, Í
5.35 (1Í, ddd, J = 9.1, 8.0, 3.9)
CH
2
2.51 (1Í, m, Í
A
),
2
.07 (1Í, dd, J = 13.9, 9.0, Í
B
)
Â
)
ÑÎÎÍ
C
174.7
174.5
1
-O-Isoferuloyl
7.10 (1Í, d, J = 1.9)
1-O-Feruloyl
1
2
3
4
5
6
7
8
9
ꢁ
ꢁ
ꢁ
ꢁ
ꢁ
ꢁ
ꢁ
ꢁ
ꢁ
C
CH
C
128.3
112.7
144.9
149.4
110.2
121.7
140.1
115.9
168.4
56.1
127.5
109.7
147.2
148.4
114.3
122.7
144.0
115.4
168.9
55.9
7.02 (1Í, d, J = 1.9)
C
CH
CH
CH
CH
C
6.82 (1Í, d, J = 8.0)
7.05 (1Í, dd, J = 8.0, 1.9)
7.60 (1Í, d, J = 16.1)
6.24 (1Í, d, J = 16.1)
6.92 (1Í, d, J = 8.0)
7.10 (1Í, dd, J = 8.0, 1.9)
7.64 (1Í, d, J = 16.1)
6.25 (1Í, d, J = 16.1)
CH3
3.90 (3Í, s)
3.88 (3Í, s)
OCH
3
5
-O-Isoferuloyl
5-O-Feruloyl
1
2
3
4
5
6
7
8
9
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
ꢁꢁ
C
CH
C
128.0
111.7
144.2
149.1
109.4
121.5
139.7
115.6
167.9
55.8
127.3
109.4
146.8
148.0
113.7
122.1
143.5
114.9
167.1
55.4
7.14 (1Í, d, J = 1.9)
7.00 (1Í, d, J = 1.9)
C
CH
CH
CH
CH
C
6.78 (1Í, d, J = 8.0)
7.00 (1Í, dd, J = 8.0, 1.9)
7.58 (1Í, d, J = 16.1)
6.20 (1Í, d, J = 16.1)
6.87 (1Í, d, J = 8.0)
7.05 (1Í, dd, J = 8.0, 1.9)
7.52 (1Í, d, J = 16.1)
6.22 (1Í, d, J = 16.1)
OCH
3
CH
3
3.87 (3Í, s)
3.86 (3Í, s)
Thus, the results showed that 1 was 1,5-di-O-isoferuloylquinic acid, a new natural product. Four conjugates of
i
i
isoferulic and quinic acids ( FQA) (1-O-, 3-O-, 4-O-, and 5-O- FQA) are now known [4]. Compound 1 was the first
di-O-isoferuloylquinic acid isolated from a plant.
2
OH
OH
O
1
HOOC
O
5
O
O
7
'
7''
1''
1
'
3
'
3''
R
2
R
2
4
'
4''
R
1
R
1
1
, 2
1
2
: R = OCH , R = OH
1
3
2
: R = OH, R = OCH
1
2
3
+
The formula C H O {m/z 567.417 ([M + Na] ; calc. 567.442)} was determined for 2 using HR-MS-TOF. The
2
7 28 12
spectral properties were similar to those of 1. However, the alkaline hydrolysis products were ferulic and quinic acids. The
1
3
C NMR spectrum had weak-field shifts (147.2 and 146.8 ppm) for C-3ꢁ and C-3ꢂ. The HMBC spectrum showed correlations
between the methoxy protons (3.88 and 3.86 ppm) and C-3ꢁ and C-3ꢂ (147.2 and 146.8 ppm, respectively). These data
confirmed that the acyl substituents in 2 were two ferulic acids.
590

TABLE 2. Quantitative Contents of Phenolic Compounds in Pollen from Three Varieties of C. officinalis, mg/g
Compound
Geisha
Fiesta Gitana
Radio
1
1
,5-Di-O-isoferuloylquinic acid (1)
,5-Di-O-feruloylquinic acid (2)
32.12
25.44
0.05
2.28
0.53
Tr.
33.63
27.12
0.09
2.59
0.41
Tr.
30.10
24.82
0.18
3.19
0.27
0.05
0.74
1.28
0.25
2.15
2.04
3.11
2.52
Caffeic acid (5)
3
4
4
-O-Caffeoylquinic acid (6)
-O-Caffeoylquinic acid (7)
,5-Di-O-caffeoylquinic acid (8)
Manghaslin (10)
Calendoflavobioside (11)
Rutin (12)
Isoquercitrin (13)
Typhaneoside (14)
Calendoflavoside (15)
Narcissin (16)
Isorhamnetin-3-O-glucoside (17)
Isorhamnetin-3-O-(6ꢁꢁ-acetyl)glucoside (18)
Identified, including:
phenylpropanoids, including:
feruloyl/isoferuloylquinic acids
caffeoylquinic acids
0.49
0.97
0.11
1.40
2.76
4.74
2.61
0.65
18.60
92.75
60.42
57.56
2.81
32.33
2.97
29.36
0.52
1.14
0.14
1.24
2.43
5.16
2.39
0.78
19.40
97.04
63.84
60.75
3.00
33.20
3.04
30.16
0.27
14.67
85.64
58.61
54.92
3.51
27.03
4.42
flavonoids, including:
quercetin derivatives
isorhamnetin derivatives
22.61
_
_____
Tr.: trace (< 0.005 mg/g).
TABLE 3. Tyrosinase Inhibition by 1–4, IC , ꢀg/mL
5
0
Activity
Compound
monophenolase
diphenolase
1
2
3
11.26 ꢆ 0.39
24.32 ꢆ 0.82
37.08 ꢆ 1.33
21.14 ꢆ 0.61
> 100
50.34 ꢆ 1.56
12.52 ꢆ 0.30
39.68 ꢆ 1.12
73.16 ꢆ 2.56
89.63 ꢆ 3.04
65.29 ꢆ 2.22
> 100
70.42 ꢆ 2.39
14.62 ꢆ 0.35
4
Quinic acid*
Arbutin*
Kojic acid*
_
*
_____
Reference compounds.
These features indicated that 2 was 1,5-di-O-feruloylquinic acid, which was synthesized previously [8]. We did not
find information on the observation of this compound in plants. Other disubstituted conjugates of ferulic and quinic acids
(
(
(
di-O-FQA) were isolated earlier from Brachiaria ruziziensis Germ. & C. M. Evrard and B. decumbens Stapf (Poaceae)
3,4- and 1,3-di-O-FQA [6]); Coffea arabica L. (Rubiaceae) (3,4-di-O-FQA [9]); Scorzonera divaricata Turcz. (Asteraceae)
3,5-di-O-FQA [10]); and Aster ageratoides Turcz. and Artemisia annua L. (Asteraceae) (3,4-, 3,5-, and 4,5-di-O-FQA [11]).
Known compounds isolated from pollen of C. officinalis were identified as the phenylpropanoids ferulic (3), isoferulic
4), caffeic (5), 3-O- (6), 4-O- (7), and 4,5-di-O-caffeoylquinic acids (8); 6ꢁ-O-vanilloyl-ꢅ-D-glucopyranose (9); quercetin
(
derivatives manghaslin (10), calendoflavobioside (11), rutin (12), and isoquercitrin (13); and isorhamnetin derivatives
typhaneoside (14), calendoflavoside (15), narcissin (16), isorhamnetin-3-O-glucoside (17), and isorhamnetin-3-O-(6ꢂ-
acetyl)glucoside (18). The pollen phenolic compounds were similar to those of the inflorescences [12] with the exception of
6
ꢁ-O-vanilloyl-ꢅ-D-glucopyranose (9), which was isolated earlier from C. officinalis leaves [13].
Quantitative analysis of pollen from the three varieties of C. officinalis cultivated in Buryatia showed that the dominant
compounds were feruloyl/isoferuloylquinic acids including 1 (30.10–33.63 mg/g) and 2 (24.82–27.12 mg/g) (Table 2).
The contents of caffeoylquinic acids were 2.81–3.51 mg/g. Isorhamnetin derivatives 18 (14.67–19.40 mg/g) and 15
(
3.11–5.16 mg/g) were also dominant flavonoids.
591

It was found earlier that isoferulic acid possessed pronounced inhibitory activity against mushroom tyrosinase [14].
The present investigation examined the influence of 1–4 and quinic acid on tyrosinase activity (Table 3). It was found that
1
–4 inhibited tyrosinase activity with the monophenolase activity inhibited more strongly. Quinic acid was inactive
(
IC50 > 100 ꢀg/mL). This indicated that the phenylpropanoid substituents played the lead role in the activity. Compound 1
was the most active with IC50 of 11.26 ꢀg/mL. This value was better than those of reference compounds arbutin (50.34 ꢀg/mL)
and kojic acid (12.52 ꢀg/mL). The activities of 3 (ferulic acid) and 2 were less than those of the isoferuloyl analogs. This
indicated that the C-4 methoxy of the phenylpropanoid group affected significantly the tyrosinase activity.
EXPERIMENTAL
Pollen from C. officinalis (Geisha Girl, Fiesta Gitana, and Radio varieties) was collected from flowering plants that
were grown in the open at experimental plantations of the IGEB, SB, RAS (July-August 2012) from authenticated seeds
obtained from N. V. Tsitsin Main Botanical Garden, RAS (Moscow, Russia). Central flower heads were collected in plastic
containers. Then, pollen was dried to <5% moisture using microwaves.
Column chromatography (CC) used silica gel (SiO , Sigma), Sephadex LH-20 (Pharmacia), and polyamide (Woelm).
2
Spectrophotometry was carried out on an SF-2000 spectrophotometer (OKB Spektr) and a Uniplan microplate spectrophotometer
(
Pikon Corp.). Mass spectra were recorded on a MAT 8200 high-resolution mass spectrometer (Finnigan). NMR spectra were
taken on a VXR 500S NMR spectrometer (Varian).
Extraction and Fractionation. A weighed portion of dry pollen (20 g) was extracted (3ꢇ) by EtOH (60%, 1:20) in
an ultrasonic bath at 45°C for 30 min. The resulting extract was concentrated in vacuo and dried to afford dry extract (9.5 g)
that was mostly (9 g) suspended in H O and fractionated using hexane and n-BuOH. The BuOH fraction was concentrated
2
and separated over polyamide (CC, 2 ꢇ 80 cm, H O–EtOH eluent, 100:0ꢃ0:100), silica gel (CC, 3 ꢇ 60 cm, hexane–EtOAc
2
eluent, 100:0ꢃ30:70), and Sephadex LH-20 (CC, 3 ꢇ 90 cm, EtOH–H O eluent, 100:0ꢃ50:50) to isolate 18 compounds that
2
were identified based on UV, MS, and NMR spectroscopy as ferulic acid (3, 6 mg), isoferulic acid (4, 8 mg) [15], caffeic acid
(
[
(
5, 2 mg) [16], 3-O-caffeoylquinic acid (6, 16 mg), 4-O-caffeoylquinic acid (7, 4 mg), 4,5-di-O-caffeoylquinic acid (8, 1 mg)
17], 6ꢁ-O-vanilloyl-ꢅ-D-glucopyranose (9, 2 mg) [13], manghaslin (10, 2 mg) [18], calendoflavobioside (11, 6 mg) [19], rutin
12, 2 mg), isoquercitrin (13, 9 mg) [20], typhaneoside (14, 20 mg) [21], calendoflavoside (15, 21 mg) [19], narcissin (16,
7 mg), isorhamnetin-3-O-glucoside (17, 4 mg) [20], and isorhamnetin-3-O-(6ꢂ-acetyl)glucoside (18, 28 gm) [22]. Compounds
1 and 2 were separated by preparative HPLC (conditions 1). Fractions with retention times 39–39 min (subfraction A) and
41–42 min (subfraction B) were collected. The subfractions were concentrated and recrystallized from MeOH to afford 1
(
18 mg from B) and 2 (21 mg from A).
,5-Di-O-isoferuloylquinic Acid (1). C H O . HR-MS-TOF, m/z 567.411 ([M + Na] ; calcd 567.442).
+
1
2
7 28 12
–
–
+
+
–
ESI-MS, m/z 543 [M – H] , 193 [isoferuloyl – H] . +ESI-MS, m/z: 567 [M + Na] , 545 [M + H] . UV spectrum (ÌåÎÍ,
1
3
ꢈmax, nm): 212 sh, 225, 297, 310. Table 1 lists the PMR and C NMR spectra.
+
1
,5-Di-O-feruloylquinic Acid (2). C H O . HR-MS-TOF, m/z 567.441 ([M + Na] ; calcd. 567.442). -ESI-MS,
2
7 28 12
–
–
+
+
m/z: 543 [M – H] , 193 [feruloyl – H] . +ESI-MS, m/z: 567 [M + Na] , 545 [M + H] . UV spectrum (ÌåÎÍ, ꢈmax, nm): 214
sh, 227, 295, 308. Table 1 lists the PMR and C NMR spectra.
1
3
Alkaline Hydrolysis. The compounds (2 mg) were dissolved in NaOH solution (1 mL, 0.4%) and heated for 30 min
at 50°C. The hydrolysate was neutralized with HCl solution (0.4%) and placed on a Diapak C16M RP-SiO cartridge
2
(
BioKhimMak) that was eluted by H O and EtOH (70%). HPLC analysis of the resulting eluates found quinic acid in the H O
2
2
eluate (t 12.57 min, conditions 2) and ferulic/isoferulic acids in the EtOH eluate (t 10.42/10.96 min, respectively, conditions 3).
R
R
HPLC. Conditions 1: Summit liquid chromatograph (Dionex); LiChrospher RP-18 column (250 ꢇ 10 mm, 10 ꢀm,
Merck); mobile phase H O (A) and MeCN (B); gradient mode (%B) 0–100 min (0–50%); flow rate 2 mL/min; column
2
temperature 30°C, UV detector at 310 nm. Conditions 2: Milikhrom A-02 microcolumn liquid chromatograph (EkoNova);
Rezex ROA-Organic Acid column (2 ꢇ 75 mm, 5 ꢀm, Phenomenex); mobile phase H SO (0.005 M); isocratic mode
2
4
(
0–30 min); flow rate 300 ꢀL/min; column temperature 35°C, detector at 210 nm. Conditions 3: MilikhromA-02 microcolumn
liquid chromatograph (EkoNova); ProntoSIL-120-5-C18 AQ column (2 ꢇ 75 mm, 5 ꢀm, Metrohm AG); mobile phase LiClO4
(
(
0.2 M) in HClO (0.006 M) (A) and MeCN (B); gradient mode (%B) 0–7.6 min (7–22%), 7.6–8.6 min (22–25%), 8.6–12 min
25–27%), 12–17 min (27–100%), 17–20 min (100–7%); flow rate 150 ꢀL/min; column temperature 35°C; UV detector at
4
3
10 nm. Quantitative analysis was performed as described earlier [12].
592

Anti-tyrosinase Activity. The influence of the compounds on monophenolase and diphenolase activity of mushroom
tyrosinase (Sigma, 1715 U/mg) was studied using the microplate method of Kubo et al. [23]. The substrates were L-tyrosine
and L-DOPA (Sigma-Aldrich), respectively. Enzymatic activity was assessed at 475 nm from the extent of dopachrome
formation and expressed as the 50% inhibition of tyrosinase activity (IC , ꢀg/mL). The reference compounds were arbutin
5
0
and kojic acid (Sigma-Aldrich).
ACKNOWLEDGMENT
The work was supported financially by the SB RAS program “Centers of New Medical Technologies.”
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