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A comprehensive study of pomegranate flowers polyphenols and metabolites in rat biological samples by high-performance liquid chromatography quadrupole time-of-flight mass

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Tiêu đề A Comprehensive Study of Pomegranate Flowers Polyphenols and Metabolites in Rat Biological Samples by High-Performance Liquid Chromatography Quadrupole Time-of-Flight Mass Spectrometry
Tác giả Zainaipuguli Yisimayili, Rahima Abdulla, Qiang Tian, Yangyang Wang, Mingcang Chen, Zhaolin Sun, Zhixiong Li, Fang Liu, Haji Akber Aisa, Chenggang Huang
Trường học University of Chinese Academy of Sciences
Chuyên ngành Pharmacognosy, Natural Product Chemistry, Food Science
Thể loại Research Article
Năm xuất bản 2019
Thành phố Shanghai
Định dạng
Số trang 13
Dung lượng 2,94 MB

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Nội dung

Pomegranate flowers is an ancient medicine that has commonly been used to treat various diseases such as diabetes. However, no reports are available on the metabolic profile of pomegranate flowers in vivo.

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Journal of Chromatography A 1604 (2019) 460472

Contents lists available at ScienceDirect

journal homepage: www.elsevier.com/locate/chroma

Zainaipuguli Yisimayilia, b, c, Rahima Abdullaa, Qiang Tianc, Yangyang Wangb, c,

Mingcang Chenc, Zhaolin Sunc, Zhixiong Lic, Fang Liuc, Haji Akber Aisaa, b, ∗,

Chenggang Huangb, c, ∗

a Key Laboratory of Plant Resources and Chemistry of Arid Zone, Xinjiang Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, Urumqi

830011, China

b University of Chinese Academy of Sciences, Beijing 10 0 049, China

c Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, China

a r t i c l e i n f o

Article history:

Received 21 May 2019

Revised 14 August 2019

Accepted 21 August 2019

Available online 22 August 2019

Keywords:

Punica granatum L flowers

Polyphenols

Ellagitannin

Metabolism

HPLC-Q-TOF-MS 2

a b s t r a c t

flowers extract, including 18 ellagitannins, 14 gallic acid and galloyl derivatives, five anthocyanins and

lites were identified in rat biosamples (urine, feces, plasma and tissues) after orally administered with pomegranate flowers extract This result showed that not all compounds abundant in pomegranate flow- ers extract could be absorbed well in plasma and tissues This finding also suggested a potential correla-

metabolite of ellagitannin compound (corilagin) was firstly identified In addition, this is first report to

rich extracts (or foods) Thus, characterizing its multiple constitution, absorption and metabolic fate of

© 2019 The Authors Published by Elsevier B.V

Pomegranate ( Punica granatum L.) is widely cultivated for its

widely consumed fruit in the regions of Southeast Asia, the

Mediterranean area and USA Notably, pomegranate flowers is an

ancient medicine that has commonly been used to treat vari-

ous diseases such as chronic diarrhea and aphthous stomatitis

In Unani and Ayurvedic medicine, and in some parts of China,

pomegranate flowers have widely been used to treat diabetes

[1–4]

According to previous studies, the health benefits of

pomegranate flowers have been associated with their polyphenol

content, specifically their anthocyanins, flavonoids and tannins

∗ Corresponding authors

E-mail addresses: haji@ms.xjb.ac.cn (H.A Aisa), cghsimm@126.com (C Huang)

content [5,6] Anthocyanins, a type of the flavonoids, are the major pigments responsible for the bright color of pomegranate flowers [5,7] Tannins are one group of natural compounds and the major compounds in pomegranate flowers Besides, the wide range of bioactivities of pomegranate flowers have been associated with the polyphenols isolated from (or present in) pomegranate flowers such as phenolics, ellagitannins and flavonoids as active components based on strategy of screening bioactivity of the isolates with in vitro cell systems evaluation [1,3,5,6,8,9,11] While

it is difficult to make structure-activity correlation conclusion among the phytocompounds in the extract or exploring bioactivity

of the isolates with in vitro cell systems evaluation Because the ingested compounds, at least part of them, reach the circulatory system and specific tissues to exert biological effect as a result

of in vivo process of absorption, distribution, metabolism and excretion [21,25,28] Thus, further studies such as bioavailability and metabolism of these compounds in vivo would be required https://doi.org/10.1016/j.chroma.2019.460472

0021-9673/© 2019 The Authors Published by Elsevier B.V This is an open access article under the CC BY license ( http://creativecommons.org/licenses/by/4.0/ )

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2 Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472

before exploring their some potential activities After oral admin-

istration of pomegranate flowers extract, the phytocompounds

absorbed as native form and their derived metabolites, at least a

portion of them, may be the functional components responsible

for the bioactivities of pomegranate flowers such as antioxidant,

anti-inflammatory, α-glucosidase inhibitory and hepatoprotective

activities [1,5,6,9–11] However, no reports are available on the

metabolic profile of pomegranate flowers in vivo The absence

of scientific evidence for its activities may restrict its further

development including clinical application Thus, characterizing

its multiple constitution, absorption and metabolic fate of these

compounds in vivo is necessary to better analyze the bioactive

components in pomegranate flowers

Therefore, in the present study, using rapid and high sensi-

tive, high-performance liquid chromatography quadrupole time-of-

flight mass spectrometry (HPLC-Q-TOF-MS 2) method, we charac-

terized the phytochemical profile of pomegranate flowers extract

Furthermore, the absorbed compounds and their metabolites in

rat plasma, tissues, urine and feces after oral administration of

pomegranate flowers extract were analyzed comprehensively This

study will provide vital information for finding possible candidates

for the real bioactive compounds in pomegranate flowers and pro-

vide a solid basis for further study of biological properties of the

compounds in pomegranate flowers

2.1 Chemicals and reagents

Reference standards (corilagin, gallic acid, ethyl gallate, el-

lagic acid, brevifolin, brevifolincarboxylic acid, punicalagin, api-

genin, apigenin-7-O-glucoside, kaempferol, luteolin, luteolin-7-

O-glucoside, isoquercetin, urolithin D, urolithin C, urolithin B,

urolithin A) were used to absolutely identified these compounds

in pomegranate flowers and rat biosamples These standards

were purchased from the Chengdu MUST Bio-Technology Co Ltd

(Chengdu, China) Acetonitrile methanol and formic acid were

bought from Thermo Fisher Scientific Co.Ltd (Waltham, Mas-

sachusetts, USA) Milli-Q System (Millipore, Billerica, MA, USA) was

used to prepare purified water for HPLC Other chemicals were

analytical-grade and bought from the Sinopharm Chemical Reagent

Co Ltd (Shanghai, China)

2.2 Instrumentations and investigation conditions

The HPLC-Q-TOF-MS 2 system (Agilent Technologies, Palo Alto,

CA, USA) which consisted of a HPLC system (1260 Series, cou-

pled to an Agilent Q-TOF mass spectrometer equipped with a Dual

Agilent Jet Stream Electrospray Ionization (ESI) sourse (6530 Se-

ries) was used for the identification of components in pomegranate

flowers extract and its metabolites in rat biosamples The chro-

matographic separation for pomegranate flowers extract and bio-

logical samples were accomplished on an ACE Excel 3 Super C18

column (100 × 2.1mm, 3.0 μm), (Advanced Chromatography Tech-

nologies Ltd Aberdeen, Scotland) The HPLC flow rate and column

temperature were set at 0.35 mL/min and at 40 °C, respectively The

optimized mobile phases contain solvent A and solvent B which

were 0.1% formic acid in water and 0.1% formic acid in acetoni-

trile An optimized mobile phase gradient elution was as follows:

0–8.0 min, 3.0% B; 8.0–16.0 min, 3.0–8.0% B; 16.0–32.0 min, 8.0% B;

32.0–54.0 min, 8.0–18.0% B; 54.0–60.0 min, 18.0% B; 60.0–65.0 min,

18.0–50.0% B; 65.0–72.0 min, 50.0–80.0% B; 72.0–76.0 min, 80.0–

95.0% B; 76.0–80.0 min, 95% B; 80.1–85.0 min, 3.0% B In this study,

the mass spectrometric detection for every samples was performed

in both ionization modes The detection parameters for the MS

conditions were as follows: capillary, 40 0 0 V and 350 0 V for pos- itive and negative ionization modes, respectively; nozzle voltage,

500 V; nebulizer, 45 psi; gas temperature and flow rate, 300 °C and 7 L/min; sheath gas temperature and flow rate, 350 °C and

12 L/min; fragmentor, 100 V; collision energy (CE), 15 eV, 30 eV The

m / range of full mass spectra for MS 1 was 10 0–170 0 The m / range was set from 100 to 1200 for MS 2experiments

The HPLC-MS system operation and data analysis were carried out with the Agilent Masshunter Workstation software which con- tain with Data Acquisition (Version B.05.01) software and Qualita- tive Analysis (Version B.06.00) software

2.3 Sample preparation and pretreatment

Dried pomegranate flowers (300 g) were extracted with ethanol /water (7:3, v/v) three times (solid /liquid ratio was 1:15, 1:15, 1:10, respectively) for (12 h, 6 h, 3 h, respectively) at 60 °C The combined extract was concentrated to 1.5 g /mL under vacuum

at 60 °C

2.4 Animal experiment

Sixty male Sprague-Dawly (SD) rats were purchased from Shanghai SLAC Laboratory Animal Co Ltd (Shanghai, China) Before the experiment, all the rats were maintained in house with envi- ronmentally controlled at a 12 h light-dark cycle and at 22 ± 2°C with relative humidity (50 ± 10%) for six days

Before drug administration, all rats were fasted for 10 h and they were free to access water The rats were randomly separated into eleven groups ( n =5 /group) Groups 1–10 were orally ad- ministered with pomegranate flowers extract at a dose of 15 g/kg and used for collecting blood and tissues samples After oral ad- ministration of pomegranate flowers extract, urine and feces (from

0 to 48 h) were collected from the rats in group 10 which were kept separately in metabolic cages The blank biological samples were collected from the rats in group 11 After oral administration

of pomegranate flowers extract, systematic blood (6–8 mL) from aorta abdominal and organs (liver, heart, kidney, spleen, and lung) were collected at 15 min, 0.5 h, 1 h, 2 h, 4 h, 6 h, 8 h, 12 h, 24 h,

48 h (10 time points) The blood biosamples were promptly cen- trifuged (12,0 0 0 rpm, 10 min) The physiological saline water (0.9%) was used to homogenize organs

2.5 Sample preparation

Plasma (200 μL at each time point) and 600 μL acetonitrile were mixed for 5 min and centrifuged (14,0 0 0 rpm, 10 min) The supernatants were separately evaporated to dryness under vac- uum at 40 °C After removal of the solvent of combined residue from ten time points, 200 μL of methanol-water (7:3, v/v) was used to dissolve the residue The tissues homogenate and urine biosamples were treated respectively with the same ways as the plasma Ground feces were mixed with 10 times of methanol (v/w) and extracted in ultrasonic bath for two times (for 30 min) The clear methanol layers were evaporated to dryness under vacuum

at 40 °C Methanol-water (7:3, v/v) used to dissolve the residue was

200 μL After centrifuging (14,000 rpm, 10 min) each sample, 10 μL

of sample was used to analysis by HPLC-Q-TOF-MS 2

In present study, a qualitative analysis of the polyphenols in the pomegranate flowers extract, absorbed compounds and metabo- lites in rats orally administered with pomegranate flowers extract were carried out by using high sensitive HPLC-Q-TOF-MS 2 in both ionization modes

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Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472 3

Fig 1 Base peak chromatogram (BPC) of pomegranate flowers extract: (a) positive ion mode, (b) negative ion mode

3.1 Identification of polyphenols in pomegranate flowers extract

In this study, as shown in Table 1, 67 compounds were

identified in pomegranate flowers extract, including 18 ellagi-

tannins, 14 gallic acid and galloyl derivatives, five anthocyanins

and 18 flavonoids Seven compounds were firstly identified in

pomegranate flowers The peak characterization was performed

based on their retention time (t R), accurate molecular mass (mass

error of less than 5 ppm), major MS/MS fragment ions Further-

more, the experimental data were compared with commercially

available authentic standards for absolutely identification The

base peak chromatograms (positive and negative ion mode) of

pomegranate flowers extract were shown in Fig.1 Analysis of el-

lagitannins, gallic acid and galloyl derivatives were performed in

the negative ion mode because of stronger response in the MS

spectra Both positive and negative ion mode were adopted to

identify anthocyanins and flavonoids

3.1.1 Ellagitannins

Ellagitannins, member of the tannin family, are characterized

as hydrolyzable conjugates containing one or more hexahydrox-

ydiphenoyl (HHDP) group(s) to esterify a sugar, usually glucose

[12] During their MS/MS fragmentation, it can be observed the

typical losses such as galloyl moiety (152 Da), gallic acid (170 Da),

HHDP (302 Da), galloyl-glucose (332 Da), HHDP glucose (482 Da)

and galloyl-HHDP-glucose (634 Da) residues Besides, in the nega-

tive ESI-IT/Q-TOF-MS 2 mode, the characteristic fragment ions ob-

served at m / 300.99 (which is produced after the spontaneous

lactonization of the HHDP unit into ellagic acid) and m / 169.01,

indicate the existence of HHDP group and galloyl group in the

molecule, respectively, based on the fragmentation pattern of el-

lagitannins previously reported in the literatures [12–18]

As shown in Fig 2, peak 25 showed a protonated molecu-

lar ion [M −H]− at m / 633.0730 (0 ppm) with a molecular for-

mula of C 27H 22O 18 In the MS 2 mode, the product ion at m /

463.0544 [M −H −170 Da] −was occurred via the loss of a gallic acid

from the molecular ion The typical fragment ion at m / 300.9995

[M −H−332Da] –, as a base peak, was formed from a galloyl-glucose

moiety loss from the [M −H]− ion The typical fragment ion at m / 169.0130, which was associated with gallic acid, was also observed Peak 25 was absolutely identified as corilagin by comparing with its commercial standard The proposed fragmentation pattern of corilagin was shown in Fig.3

Peaks 3, 6, 12 and 21 were isomeric compounds All of the peaks had a [M −H] −ion at m / 633.0729 ( −0.63 ppm) with molec- ular formula of C 27H 22O 18 The fragment ion at m / 463.0544 [M −H−170Da] – (loss of a gallic acid), the typical ions at m / 300.9998 and m / 169.0138 were consistent with those of corilagin Thus, peaks 3, 6, 12 and 21 were tentatively identified as galloyl- HHDP-glucose isomers

Peak 10 had a protonated molecular ion [M −H]− at m / 481.0620 ( −1.24ppm) with molecular formula of C 20H 18O 14, and the MS 2 spectrum had fragments at m / 463.0544 [M −H−18Da] and characteristic fragment ion at m / zm / 300.9995 Thus, peak 10 was tentatively identified as HHDP-glucose

Peaks 16, 23, 28, 34 and 35 were isomers All of the peaks had a [M −H]− ion at m / 785.0818 ( −3.18ppm) with molecular formula

of C 34H 26O 22 The fragments at m / 615.0637 [M −H −170 Da] – (loss

of a gallic acid), m / 463.0544 [M −H−170Da-152 Da] – (loss of a gallic acid and a galloyl moiety), the typical ions at m / 300.9998 and m / 169.0138 were observed in the MS 2mode Thus, peaks 16,

23, 28, 34 and 35 were tentatively identified as digalloyl-HHDP- glucoside isomers As an example, the MS/MS spectra and the pro- posed fragmentation pattern of one digalloyl-HHDP-glucoside were shown in Figs.2and 3

As shown in Fig.2, peak 53 had a [M −H]−ion at m / 937.0910 ( −4.58ppm) with molecular formula of C 41H 30O 26 The product ions at m / 767.0748 [M −H −170 Da] – (loss of a gallic acid), m / 615.0683[M −H−170Da −152Da] – (loss of a gallic acid and a gal- loyl moiety), m / 465.0754 [M −H−170Da-302 Da] – (loss of a gallic acid and HHDP moiety), the typical ions at m / 300.9998 and m / 169.0138 were observed in the MS 2 mode Therefore, peak 53 was tentatively identified trigalloyl-HHDP-glucose

Peaks 14, 40 and 46 were isomeric compounds They had a [M −H]− ion at m / 951.0719 ( −2.73ppm) with molecular for-

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4

Table 1

Summary of the mass spectral data of polyphenols identified in pomegranate flower extract by HPLC-Q-TOF-MS/MS

No t R (min)

Molecular

formula Calculated Observed Ion mode Error (ppm) MS/MS fragments Identification

1 1.46 C 13 H 16 O 10 331.0671 331.0668 [M −H] − −0.90 169.0136, 125.0236 Galloyl-glucoside

2 b 2.06 C 7 H 6 O 5 169.0142 169.0140 [M −H] − −1.18 125.0139 Gallic acid

3 2.55 C 27 H 22 O 18 633.0733 633.0729 [M −H] − −0.63 463.0535, 300.9998, 169.0138 Galloyl-HHDP-glucoside

4 2.92 C 20 H 20 O 14 483.0780 483.0782 [M −H] − 0.41 313.0560, 169.0137, 125.0240 Digalloyl- glucoside

5 3.40 C 13 H 16 O 10 331.0671 331.0668 [M −H] − −0.90 169.0136, 125.0236 Galloyl-glucoside

6 4.45 C 27 H 22 O 18 633.0733 633.0729 [M −H] − −0.63 463.0535, 300.9998, 275.0204, 169.0138 Galloyl-HHDP-glucoside

7 5.01 C 13 H 16 O 10 331.0671 331.0668 [M −H] − −0.90 169.0136, 125.0236 Galloyl-glucoside

8 5.96 C 20 H 20 O 14 483.0780 483.0782 [M −H] − 0.41 313.0560, 169.0137, 125.0240 Digalloyl-glucoside

9 9.79 C 21 H 10 O 13 469.0049 469.0028 [M −H] − −4.47 425.0149, 300.9995, 169.0157, 125.0242 Valoneic acid dilactone

10 11.98 C 20 H 18 O 14 481.0624 481.0618 [M −H] − −1.24 463.0510, 300.9995 HHDP-glucoside

11 c 14.60 C 15 H 11 O 7 465.1028 465.1023 [M] + −1.07 303.0486 Delphinidin-3-O-glucoside

12 14.68 C 27 H 22 O 18 633.0733 633.0729 [M −H] − −0.63 463.0535, 300.9998, 275.0204, 169.0138 Galloyl-HHDP-glucoside

13 15.26 C 20 H 20 O 14 483.0780 483.0782 [M −H] − 0.41 313.0560, 169.0137, 125.0240 Digalloyl- glucoside

14 16.93 C 41 H 28 O 27 951.0745 951.0719 [M −H] − −2.73 907.0821, 783.0580, 481.0534, 300.9987 HHDP-valoneoyl-glucoside

15 18.18 C 27 H 31 O 16 611.1612 611.1605 [M] + −1.14 449.1045, 287.0522 Cyaniding-3,5-O-diglucoside

16 18.22 C 34 H 26 O 22 785.0843 785.0818 [M −H] − −3.18 615.0602, 463.0499, 300.9993, 169.0130 Digalloyl-HHDP-glucose

17 b 18.56 C 48 H 28 O 30 1083.0593 1083.0583 [M −H] − −0.92 781.0665, 621.9980, 300.9997 Punicalagin

18 19.74 C 27 H 31 O 15 595.1663 595.1660 [M] + −0.50 433.1133, 271.0606 Pelargonidin-3,5-O-diglucoside

19 19.89 C 20 H 20 O 14 483.0780 483.0782 [M −H] − 0.41 313.0560, 169.0137, 125.0240 Digalloyl-glucoside

20 b 20.19 C 13 H 8 O 8 291.0146 291.0153 [M −H] − 2.40 247.0250, 219.0298, 191.0346 Brevifolincarboxylic acid

21 21.54 C 27 H 22 O 18 633.0733 633.0729 [M −H] − −0.63 463.0535, 300.9998, 275.0204, 169.0138 Galloyl-HHDP-glucoside

22 b , c 24.25 C 9 H 10 O 5 197.0455 197.0451 [M −H] − −2.02 169.0144, 125.0242 Ethyl gallate

23 25.36 C 34 H 26 O 22 785.0843 785.0818 [M −H] − −3.18 615.0602, 463.0499, 300.9993, 169.0130 Digalloyl-HHDP-glucoside

24 26.46 C 34 H 24 O 22 783.0686 783.0685 [M −H] − −0.12 300.9989 Di-HHDP- glucoside

25 b 26.50 C 27 H 22 O 18 633.0733 633.0733 [M −H] − 0 463.0493, 300.9990, 169.0152 Corilagin

26 26.91 C 21 H 21 O 11 449.1078 449.1085 [M] + 1.55 287.0532, 153.0162 Cyanidin 3-O-glucoside

27 27.17 C 21 H 21 O 10 433.1135 433.1133 [M] + −0.46 271.0615 Pelargonidin 3-O-glucoside

28 28.13 C 34 H 26 O 22 785.0843 785.0818 [M −H] − −3.18 615.0602, 463.0499, 300.9993, 169.0130 Digalloyl-HHDP-glucoside

29 b , c 28.54 C 12 H 8 O 6 247.0248 247.0244 [M −H] − −1.61 219.0305, 191.0348 Brevifolin

30 30.30 C 21 H 10 O 13 469.0049 469.0028 [M −H] − −4.47 425.0149, 300.9995, 169.0157, 125.0242 Valoneic acid dilactone

31 31.29 C 27 H 24 O 18 635.0890 635.0881 [M −H] − −1.42 465.0677, 313.0568, 169.0124 Trigalloyl- glucoside

32 c 33.29 C 14 H 10 O 8 305.0303 305.0300 [M −H] − −0.98 273.0061, 245.0082, 217.0141 Methyl brevifolincarboxylate

( continued on next page )

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Table 1 ( continued )

No t R (min) Molecular

formula

Calculated Observed Ion mode Error (ppm) MS/MS fragments Identification

33 c 33.89 C 33 H 28 O 22 775.0999 775.0937 [M −H] − −7.99 757.0854, 465.0680, 300.9992, 169.0139 Ellagitannin

34 34.59 C 34 H 26 O 22 785.0843 785.0818 [M −H] − −3.18 615.0602, 463.0499, 300.9990, 169.0130 Digalloyl-HHDP-glucoside

35 37.70 C 34 H 26 O 22 785.0843 785.0818 [M −H] − −3.18 615.0602, 463.0499, 300.9990, 169.0130 Digalloyl-HHDP-glucoside

36 42.12 C 21 H 10 O 13 469.0049 469.0028 [M −H] − −4.47 425.0149, 300.9995, 169.0157, 125.0242 Valoneic acid dilactone

37 a 43.25 C 27 H 30 O 16 611.1607 /609.1461 611.1605 [M + H] + /[M −H] − −1.14 449.1045, 287.0522, 153.0159 Luteolin-O-diglucoside

38 43.54 C 27 H 24 O 18 635.0890 635.0881 [M −H] − −1.42 465.0677, 313.0568, 169.0124 Trigalloyll-glucoside

39 a , c 44.15 C 27 H 30 O 15 595.1657 /593.1512 595.1660 [M + H] + /[M −H] − −0.50 433.1133, 271.0606, 153.0179 Apigenin-O-diglucoside

40 45.10 C 41 H 28 O 27 951.0745 951.0719 [M −H] − −2.73 907.0821, 783.0580, 481.0534, 300.9987 HHDP-valoneoyl-glucoside

41 c 46.55 C 15 H 12 O 8 319.0459 319.0459 [M −H] − 0 273.0036, 245.0085, 217.0141 Ethyl brevifolincarboxylate

42 b 46.98 C 14 H 6 O 8 300.9990 300.9998 [M −H] − 2.65 283.9967, 257.0083, 229.0139, 201.0181 Ellagic acid

43 47.04 C 41 H 28 O 27 951.0745 951.0734 [M −H] − −1.15 933.0629, 613.0448, 463.0492, 300.9994, Galloyl-HHDP-DHHDP-hexoside

44 47.33 C 27 H 30 O 16 611.1607/609.1461 611.1605 [M + H] + /[M −H] − −1.14 449.1045, 287.0522, 153.0159 Luteolin-O-diglucoside

45 48.36 C 34 H 28 O 22 787.0999 787.0972 [M −H] − −3.43 617.0745, 465.0659, 313.0582, 169.0147 Tetragalloyl-glucoside

46 49.02 C 41 H 28 O 27 951.0745 951.0719 [M −H] − −2.73 907.0821, 783.0580, 481.0534, 300.9987 HHDP-valoneoyl-glucoside

47 a , b , c 49.52 C 21 H 20 O 12 465.1028 /463.0882 465.1021 [M + H] + /[M −H] − −1.50 303.0484, 153.0152 Isoquercetin

48 a , b 50.23 C 21 H 20 O 11 449.1078 /447.0993 449.1085 [M + H] + /[M −H] − 1.55 287.0573, 153.0187 Luteolin 7-O-glucoside

49 52.32 C 34 H 28 O 22 787.0999 787.0972 [M −H] − −3.43 617.0745, 465.0659, 313.0582, 169.0147 Tetragalloyl-glucoside

50 a 53.16 C 21 H 20 O 11 449.1078 /447.0993 449.1085 [M + H] + /[M −H] − 1.55 287.0573, 153.0187 Luteolin −7-O-glucoside isomer

51 a 54.51 C 21 H 20 O 12 465.1028 465.1021 [M + H] + /[M −H] − −1.50 303.0499, 153.0178 Tricetin 4  -O- β-glucoside

52 a, b 55.90 C 21 H 20 O 10 433.1129 /431.0984 433.1128 [M + H] + /[M −H] − −0.23 271.0612 Apigenin-7-O-glucoside

53 56.28 C 41 H 30 O 26 937.0953 937.0910 [M −H] − −4.58 767.0682, 615.0477, 465.0674, 300.9999, 169.0148 Trigalloyl-HHDP-glucose

54 57.53 C 27 H 20 O 17 615.0628 615.0621 [M −H] − −1.13 445.0438, 300.9999, 169.0132 Galloyl-ellagic acid glucoside

55 a 58.18 C 21 H 20 O 11 449.1078 /447.0993 449.1085 [M + H] + /[M −H] − 1.55 287.0569, 153.0196 Kaempferol-O-glucoside

56 58.69 C 41 H 32 O 26 939.1109 939.1061 [M −H] − −5.11 769.0873, 617.0752, 465.0647, 313.0547, 169.0130 Pentagalloyl-glucoside

57 a 60.73 C 21 H 20 O 11 449.1078 /447.0993 449.1085 [M + H] + /[M −H] − 1.55 287.0569, 153.0196 Kaempferol-O-glucoside

58 a 61.86 C 21 H 20 O 12 465.1028 465.1021 [M + H] + /[M −H] − −1.50 303.0499, 153.0178 Tricetin-4  -O- β-glucoside isomer

59 a 62.72 C 15 H 10 O 7 303.0499 303.0503 [M + H] + /[M −H] − 1.31 153.0193 Tricetin

60 a 63.76 C 21 H 20 O 10 433.1129 /431.0984 433.1128 [M + H] + /[M −H] − −0.23 271.0612 Apigenin-7-O-glucoside isomer

61 64.02 C 43 H 34 O 28 997.1164 997.1138 [M −H] − −2.60 953.1216, 783.0990, 633.0715, 481.0912, 300.9994,

169.0149

Punictannin A

62 a 65.13 C 21 H 20 O 12 465.1028 /463.0882 465.1021 [M + H] + /[M −H] − −1.50 303.0484, 153.0152 Quercetin

63 65.66 C 43 H 34 O 28 997.1164 997.1138 [M −H] − −2.60 953.1216, 783.0990, 633.0715, 481.0912, 300.9994,

64 a , b 65.70 C 15 H 10 O 6 287.0550 /285.0405 287.0554 [M + H] + /[M −H] − 1.39 153.0178 Luteolin

65 a , b 67.07 C 15 H 10 O 5 271.0601 /269.0455 271.0603 [M + H] + /[M −H] − 0.73 153.0173 Apigenin

66 a , b 67.25 C 15 H 10 O 6 287.0550 /285.0405 287.0555 [M + H] + /[M −H] − 1.74 153.0175 Kaempferol

67 a 67.31 C 17 H 14 O 7 331.0812 /329.0667 331.0813 [M + H] + /[M −H] − 0.30 315.0496, 299.0549, 270.0516, 133.1010 Tricin

a Error (ppm) and fragment ions taken from the positive ion mode (in case detected in both modes)

b Confirmed by using reference standard

c Firstly identified compounds in pomegranate flower

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6 Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472

Fig 2 The MS/MS spectra of typical ellagitannins and galloyl derivatives in pomegranate flowers

Fig 3 Proposed fragmentation pattern of typical ellagitannins and galloyl derivatives in pomegranate flowers

mula of C 41H 28O 27 These compounds had major fragment ions

at m / 907.0821[M −H−44Da] – (loss of a CO 2), m / 783.0580, m /

481.0534, m / 300.9987 in their MS 2 mode Therefore, peaks 14,

40 and 46 were tentatively identified as HHDP-valoneoyl-glucoside

isomers

3.1.2 Gallic acid and galloyl derivatives

Peak 2 had a [M −H]− ion at m / 169.0140 ( −1.18ppm) with

molecular formula of C 7H 6O 5 The product ion at m / 125.0239

[M −H −44 Da] − was generated via the elimination of CO 2 unit

from the molecular ion Peak 22 showed a [M −H]− ion at m /

197.0451 ( −2.02ppm) with molecular formula of C 9H 10O 5 and the

MS 2 spectrum had fragment ions at m / 169.0144 [M −H −28 Da] –

(loss of a C H moiety) and m / 125.0242 [M −H−28Da-44 Da] –

(loss of a C 2H 4 and a CO 2 moieties) Peaks 2 and 22 were abso- lutely identified as gallic acid and ethyl gallate by comparing with their reference standards, respectively

Peaks 1, 5 and 7 displayed molecular ion [M −H]− at m / 331.0 6 68 ( −0.90 ppm) with molecular formula of C 13H 16O 10 The fragment ion at m / 169.0136 [M −H−162Da] – (loss of a glucose moiety), and m / 125.0236 [M −H−162Da-44 Da] – were correlated

to gallic acid on the basis of the MS/MS spectra data Thus, peaks

1, 5 and 7 were tentatively identified as galloyl-glucose isomers Peaks 4, 8, 13 and 19 were isomeric compounds All of them showed a [M −H] − ion at m / 483.0782 (0.41 ppm) with molec- ular formula of C 20H 20O 14 The fragment ion at m / 313.0560 [M −H−170Da] – (loss of a gallic acid), the characteristic ions at

m / 169.0137 and ion at m / 125.0240 were observed in the MS 2

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Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472 7 mode Therefore, peaks 4, 8, 13 and 19 were tentatively identified

as digalloyl-glucose isomers

Peaks 31 and 38 exhibited a [M −H]− ion at m / 635.0881

( −1.42ppm) with molecular formula of C 27H 24O 18 The fragment

ions at m / 465.0689 [M −H −170 Da] – (loss of a gallic acid), m /

313.0575 [M −H−170Da-152 Da] – (loss of a gallic acid and a galloyl

moiety), typical fragment ion at m / 169.0127 and fragment ion at

m / 125.0254 were observed in the MS 2mode Therefore, Peaks 31

and 38 were tentatively identified as trigalloyl-glucoside isomers

As an example, the MS/MS spectra of one trigalloyl-glucoside was

shown in Fig.2

Peaks 45 and 49 had a [M −H]− ion at m / 787.0972

( −3.43ppm) with molecular formula of C 34H 28O 22 The MS 2 spec-

tra of these two peaks exhibited fragments at m / 617.0772

[M −H−170Da] –(loss of a gallic acid), m / 465.0654 [M −H−170Da-

152 Da] – (loss of a gallic acid and a galloyl moiety), m /

313.0531[M −H−170Da-152 Da-152 Da] – (loss of a gallic acid and

two galloyl moieties), the typical ion at m / 169.0138 There-

fore, peaks 45 and 49 were tentatively identified as tetragalloyl-

glucopyranoside As an example, the MS/MS spectra and proposed

fragmentation pattern of one tetragalloyl-glucopyranoside were

shown in Figs.2and 3

As shown in Fig.2, peak 56 exhibited deprotonated molecular

ion [M −H] − at m / 939.1061 ( −5.11 ppm) with molecular formula

of C 41H 32O 26 The fragments at m / 769.0873 [M −H−170Da] –, m /

617.0772 [M −H−170Da-152 Da] –, m / 465.0654 [M −H−170Da-

152 Da-152 Da] –, m / 313.0531[M −H −170 Da-152 Da-152 Da-

152 Da] –, the typical fragment ion at m / 169.0138 and fragment

ion at m / 125.01 were observed in MS 2 experiment Therefore,

peak 56 was tentatively identified as pentagalloyl-glucoside

According to the mass fragmentation patterns of galloyl deriva-

tives and ellagitannins, it is suggested that if galloyl derivatives or

ellagitannins have one or more galloyl group(s) to esterify a sugar

(usually glucose), molecular ion firstly remove one molecule gal-

lic acid (C 7H 6O 5, 170 Da), and then continuously lose one or more

galloyl group(s) (C 7H 4O 4, 152 Da) in the mass fragmentation pro-

cess The typical losses during their fragmentation are a gallic acid

(170 Da) and a galloyl moiety (152 Da)

3.1.3 Others

Peak 42 had a precursor ion [M −H]− ion at m / 300.9998

(2.65 ppm) with molecular formula of C 14H 6O 8 The product ions

at m / 283.9963 and m / 257.0092 were yielded by the loss of

H 2O (18 Da) unit and CO 2 (44 Da) unit from the [M −H]− ion, re-

spectively Furthermore, the fragments at m / 229.0133 and m /

201.0182 were also observed Thus, peak 42 was absolutely iden-

tified as ellagic acid by comparing with its commercial standard

Peak 29 exhibited a protonated molecular ion [M −H]− at m /

247.0244 ( −1.61 ppm) with molecular formula of C 12H 8O 6 The

fragment ions at m / 219.0305 and m / 191.0348 were occurred

via the removal of CO unit and continuing removal of CO unit from

the molecular ion, respectively Peak 20 had molecular ion [M −H] −

at m / 291.01 (2.40 ppm) with the molecular formula of C 13H 8O 8

The fragment ion m / 247.02 was generated by the loss of CO 2

unit from the molecular ion The fragment ions at m / 219.02 and

m / 191.03 were consistent with those of compound 29 Peaks 29

and 20 and were absolutely identified as brevifolin and brevifolin-

carboxylic acid by comparing with their commercial standards, re-

spectively

Peak 32 had a [M −H]− ion at m / 305.0300 ( −0.98ppm) with

molecular formula of C 14H 10O 8 The fragment ions at m / 273.0061,

m / 245.0082, m / 217.0141were observed in the MS 2 mode Peak

41 displayed [M −H]− ion at m / 319.01 ( −1.31ppm) with molec-

ular formula of C 15H 12O 8 In the MS/MS spectrum, the fragment

ions at m / 273.0036, m / 245.0152 and m / 217.0167 were gener-

ated by the removal of C H O unit and continuing removal of CO

(28 Da) and two CO (28 Da) unit from the molecular ion, respec- tively Moreover, the fragmentation patterns of peaks 32 and 41 were in agreement with fragmentation patterns reported in the lit- erature [13] Peaks 32 and 41 were tantetively identified as methyl brevifolincarboxylate and ethyl brevifolincarboxylate

3.1.4 Anthocyanins

Anthocyanins are naturally occurring plant pigments with unique chromatographic behavior Anthocyanins carry an inher- ent positive charge and can easily donate protons to free radicals ([M] +) under ( +) ESI condition [19]

Peak 11 had a positively charged molecular ion [M] + at m / 465.1023 ( −1.07ppm) with molecular formula of C 15H 11O 7, and MS/MS fragment ions at m / 303.0486 [M −162Da] +, which this characteristic matched with the loss of glucose (162 Da) and sug- gested that the aglycone was delphinidin Thus, peak 11 was ten- tatively identified as delphinidin-3-O-glucoside

Peak 15 had a positively charged molecular ion [M] + at

m / 611.1605 with molecular formula of C 27H 31O 16, yielding by fragment ions at m / 449.1045 [M −162Da] + and m / 287.0522 [M −162Da-162 Da] +, which suggested that the aglycone was cyanidin Thus, peak 15 was tentatively identified as cyanidin-3, 5- O-diglucoside

Peak 18 had a positively charged molecular ion [M] + at m / 595.1660 ( −0.50 ppm) with molecular formula of C 27H 31O 15 In

MS 2 mode, the fragment ions at m / 433.1132 [M −162Da] + and

m / 271.0600 [M −162Da-162 Da] +were observed, which suggested that the aglycone was pelargonidin Thus, peak 18 was tentatively identified as pelargonidin-3, 5-diglucoside

Peak 26 had a positively charged molecular ion [M] + at m / 449.1085 with molecular formula of C 21H 21O 11, yielding by frag- ment ion at m / 287.0532 [M −162 Da] +, which suggested that the aglycone was cyanidin Thus, peak 26 was tentatively identified as cyanidin-3-O-glucoside

Peak 27 had a positively charged molecular ion [M] + at m / 433.1133 ( −0.46ppm) with molecular formula of C 21H 21O 10, yield- ing by fragment ion m / 271.0600 [M −162Da] + by the loss of a glucose moiety, which suggested that the aglycone was pelargoni- din Thus, peak 27 was tentatively identified as pelargonidin-3- glucoside

3.1.5 Flavonoids

Peaks 64 displayed the molecular ion [M + H] +/[M −H] − at m / 287.0554 / 285.0409 with molecular formula of C 15H 10O 6, and main MS/MS fragment ion at m / 153.0178 Peaks 65 exhib- ited precursor ion [M + H] +/[M −H] − at m / 271.0603 /269.0455 (0.73 ppm) with molecular formula of C 15H 10O 5, and main MS/MS fragment ion at m / 153.0173 Peaks 66 showed the molecular ion [M + H] +/[M −H] − at m / 287.0555 / 285.0407 with molecular for- mula of C 15H 10O 6, and main MS/MS fragment ion at m / 153.0175 Peaks 64, 65 and 66 were absolutely identified as luteolin, apigenin and kaempferol by compariing with their authentic standards, re- spectively

Peaks 48 showed the molecular ion [M +H] +/[M −H]− at m / 449.1085 / 447.0993 with molecular formula of C 21H 20O 11 In the positive MS 2 mode, the fragment ion at m / 287.0573 (match- ing with the aglycone of luteolin) appeared after neutral loss of

a glucose (162 Da) moiety from the molecular ion Peaks 52 had [M + H] +/[M −H] − at m / 433.1139 / 431.0984 with molecular for- mula of C 21H 20O 10 The positive MS 2 spectrum showed the main product ion at m / 271.0612 after neutral loss of a glucose (162 Da) moiety from the molecular ion Thus, peaks 48 and 52 were absolutely identified as luteolin-7-O-glucoside and apigenin-7-O- glucoside by comparing with their authentic standards

Peaks 47 was detected in both ionization modes with molecu- lar ion [M +H] +/[M −H]−at m / 465.1028/463.0882 with molecular

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8 Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472

Fig 4 Extracted ion chromatogram, the MS/MS spectra and chemical structures (from left to right) of pelargonidin 3-O-glucoside (detected only in positive ion mode) and

apigenin-7-O-glucoside (detected in both positive and negative ion mode)

formula of C 21H 20O 12 The main fragment ion at m / 303.0484 was

observed in the MS 2mode after the loss of a glucose (162 Da) moi-

ety from the molecular ion Peaks 47 was absolutely identified as

isoquercetin by comparing with its commercial standard

It is worth to note that several flavonol glycosides and an-

thocyanin glycosides compounds have the same molecular ions

and mass fragmentation patterns in ESI ( +) positive ionization

mode ([M] + of anthocyanins and [M + H] + of flavonol glycosides

are the same), occurring as mono- or di-glucosides For example,

when the aglycone parts of two different species are quercetin

and delphnidin or pelargonidin and apigenin or kaempferol /lu-

teolin and cyanidin As a representative example, Fig 4 showed

that pelargonidin 3-glucoside and apigenin-7-O-glucoside share

the same molecular ion, same fragmentation behavior and same

major fragment ions in their positive MS/MS spectrum However,

these isomeric structures in the positive ion mode could not be

distinguished based on the MS 1 and MS 2 data Thus, the similar

fragmentation patterns between these two different species com-

plicate accurate structural elucidation and remain challenging For

the accurate identification, the three strategies below were taken

into account First, both positive and negative ionization mode

were used to determine the molecular weight The identification of

the flavones were carried out based on the observation of the pro-

tonated and deprotonated molecules ([M + H] + and [M −H] − ions),

which have also been described by other authors using IT /Q-TOF

[16,17,21] Anthocyanins carry an inherent positive charge and can

easily donate protons to free radicals ([M] +) under ( +) ESI condi-

tion Thus, most reported LC/MS studies of anthocyanins were also

performed in the positive ion mode because of maximum sensitiv-

ity [19–24] Anthocyanins do not ionize at all because of the ab-

sence of a free hydroxyl group in the negative ion mode, and de-

protonated molecular ion ([M–H] –) for anthocyanins could not be

detected because of the neutralization of the charge [19] Thus, the

unique molecular ion [M–2H] – in negative ion mode analysis may

provide additional information for identification of anthocyanins

compounds, but [M–2H] – of anthocyanins and [M–H] – of flavonol glycosides are also the same Only a limited number of LC/MS stud- ies of anthocyanins were carried out with the molecular ion [M– 2H] – in negative ion mode, but the full scan MS 1 spectrum from negative ionization mode was complex [22–24]

In this study, the molecular ion [M–2H] –for anthocyanins was not detected in the extracted ion chromatogram (EIC) when ex- tracting this specific mass from the negative full-scan MS 1dataset, which there was no mixed peak with the similar retention time when compared with the positive ion mode Thus, for the iden- tification of anthocyanins, the positive ion mode was used for their identification and the negative ionization mode was used for verification in this study This characteristic is especially use- ful for distinguishing anthocyanin glycosides from flavonol glyco- sides with the same ‘quasi’-molecular ions (M + = [M + H] + and [M–2H] – = [M–H] –) that co-exist in some plants It becomes very simple to distinguish between two different species if neg- ative ionization mode is employed Thus, it is easy to distin- guish rapidly between pelargonidin 3-glucoside and apigenin-7-O- glucoside when comparing the full scan MS spectrum in the neg- ative ionization mode Secondly, anthocyanins compounds have a characteristic elution order in reversed phase liquid chromatogra- phy (RP-LC), which elute before the flavonol glycosides [25] The retention times of the pelargonidin 3-O-glucoside (27.11 min) and apigenin-7-O-glucoside (55.90 min) on a reverse phase C18 col- umn differed by 28.8 min, which indicate that peak 27 (pelargoni- din 3-O-glucoside) must be an anthocyanin with much higher po- larity Thirdly, apigenin-7-O-glucoside were further confirmed by comparing with the fragmentation pattern and chromatographic retention time of its authentic standard Besides, according the studies previously reported, a photodiode array detector (DAD) to measure UV/Vis molecular absorbance was used to differentiate these two different species since anthocyanins have a typical λmax

at ∼330 nm and between 440 and 540 nm [5,18,20,23] The ab- sorbance maxima for flavonol glycosides were at 250 and 370 nm

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Z Yisimayili, R Abdulla and Q Tian et al / Journal of Chromatography A 1604 (2019) 460472 9 [21,24] These strategies are significantly vital considering that MS

and MS/MS date obtained under ESI conditions do not allow iden-

tification of isomeric structures for distinguishing anthocyanin gly-

cosides from flavonol glycosides

3.2 Identification and analysis of absorbed compounds and their

metabolites in rat biosamples

How to find new candidates as bioactive compounds from

medicinal herbs with a higher probability for research and devel-

opment in drug discovery remain challenging and controversial

A common strategy for identifying the active constituents from

medicinal herbs in the field of separation science is to screen

bioactivity of the isolates with in vitro cell systems evaluation, al-

though there has been a steadily rise in animal and human stud-

ies [3,5,6,8,9,11] However, sometimes the biological effects of the

screened compounds do not live up to in vivo study Because the

ingested compounds, at least part of them, reach the circulatory

system and specific tissues to exert biological effect as a result

of in vivo process of absorption, distribution, metabolism and ex-

cretion It is known that the absorbed compounds could be fur-

ther metabolized by various drug-metabolizing enzymes in vivo

[21,25,28] For example, the previous studies reported the isolation

of phenolics from pomegranate flowers such as punicatannins A

and B, 1, 6-di-O-galloyl- β-D-glucose and 3, 4, 6-tri-O-galloyl- β-D-

glucose Furthermore, they evaluated the abilities of these isolates

to inhibit α-glucosidase inhibitory activities in vitro for seeking the

bioactive antidiabetic compounds from pomegranate flowers [6,11]

Thus, we were interested in absorption, distribution and metabolic

fate of the compounds after oral administration of pomegranate

flowers extract in vivo , especially those isolates

In the present study, according to accurate mass and fragmen-

tation pattern generated by the HPLC-Q-TOF-MS 2, 22 absorbed

compounds and their 35 metabolites were absolutely or tenta-

tively identified in rat biosamples after oral administration of

pomegranate flowers extract The workflow of metabolite iden-

tification take three steps, firstly, the probable metabolites were

postulated based on the metabolism rules of compounds Sec-

ondly, the molecular ion [M + H] +/[M] + or [M −H] − for proba-

ble metabolites were extracted from the full-scan MS 1 dataset of

dosed rat biological samples Thirdly, the peaks detected in the

EIC were further analyzed by the QTOF-MS/MS dataset of dosed

rat biological samples Among them, 15 absorbed compounds and

metabolites were further confirmed with their authentic stan-

dards Among the metabolites, most of them were found in urine

(19 absorbed compounds and 31 metabolites), feces (21 absorbed

compounds and 25 metabolites) and plasma (15 absorbed com-

pounds and 17 metabolites) samples, only a few of them were

found in tissues, respectively ( Table 2) Ellagitannins were abun-

dant in pomegranate flowers extract (18 ellagitannins), but only

corilagin was detected in plasma and tissues Galloyl derivates

were also abundant in pomegranate flowers extract (14 galloyl

derivates), but none of them was detected in plasma and tis-

sues Our results indicate that ellagitannins and galloyl derivates

were not well absorbed in plasma and tissues It is worth to note

that the isolates (punicatannins A and B, 1, 6-di-O-galloyl- β-D-

glucose and 3, 4, 6-tri-O-galloyl- β-D-glucose) were not found in

plasma or tissues after oral administration of pomegranate flow-

ers extract This our in vivo finding have not totally supported

the in vitro findings that these isolates were bioactive antidiabetic

compounds present in pomegranate flower According to previ-

ous studies, after normal consumption of ellagitannins-rich foods

or extracts, ellagitannins are rarely detected in plasma due to

their low bioavailability Ellagitannins are metabolized by the in-

testinal flora to produce ellagic acid and urolithins metabolites

[27–30]

Moreover, most of metabolism studies of ellagitannins were mainly focused on ellagic acid, which is one of the main hydrolysates of ellagitannins, and urolithins and their derived metabiolites in plasma, urine and feces in recent years [26–28] Remarkably, in the present study, ellagitannin corilagin and nine phase II conjugate metabolites of corilagin were firstly identified

in plasma and tissues after oral administration of pomegranate flowers extract As shown in Fig 5, metabolite C5 (retention time = 11.96 min) had a molecular ion [M −H]− at m / 809.1056 (C 28H 29O 26−, 0.24 ppm), which was 176 Da higher than that of co- rilagin (O5), suggesting that C5 was glucuronide conjugate metabo- lite The fragment ion at m / 633.0676, as a base peak, was pro- duced by natural loss of a glucuronic acid (176 Da) from the [M −H] − ion Besides, the fragment ion at m / 463.0532, the typ- ical fragment ions at m / 300.9958 and m / 169.0138 were also consistent with those of corilagin Thus, C5 was identified as glu- curonidation of corilagin This is a first report to identify mono- glucuronide conjugated metabolite of ellagitannin compound in vivo Metabolites C1 and C2 had molecular ion [M −H]− at m / 713.0298 (C 27H 21O 21S −, −0.56ppm), which was 80 Da (SO 3) higher than that of corilagin Thus, C1 and C2 were identified as sulfa- tion metabolites of corilagin Metabolite C3 had a molecular ion [M −H]−at m / 647.0894 (C 28H 23O 18−, 0.61 ppm), which was 14 Da (CH 2) higher than that of corilagin Therefore, C3 was identified

as methylation metabolite of corilagin Metabolite C4 had a molec- ular ion [M −H]− at m / 661.1048 (C 29H 25O 18−, 0.30 ppm), which was 28 Da (2 CH 2) higher than that of corilagin Therefore, C4 was identified as Di-methylation metabolite of corilagin Metabolites C6 and C7 had molecular ion [M −H]− at m / 823.1208 (C

34H 31O 24−,

−0.36ppm), which was 176 Da (a glucuronic acid) and 14 Da (CH 2) higher than that of corilagin Therefore, C6 and C7 were iden- tified as glucuronidation and methylation metabolites of corila- gin Metabolite C8 had a molecular ion [M −H]− at m / 837.1364 (C 35H 33O 24−, −0.67 ppm), which was176 Da (a glucuronic acid) and 28 Da (2 CH 2) higher than that of corilagin Therefore, C8 was identified as glucuronidation and di-methylation metabolite of co- rilagin The fragmentation patterns of metabolites C1–C4 and C6– C8 were similar to that those of metabolites previously reported for corilagin ( Fig 5) [29] Furthermore, the binding sites of phase

II conjugate metabolites (C1–C9) of corilagin were determined by combining with our previous study [29] The nine phase II con- jugate metabolites of corilagin are the methylation, glucuronida- tion and sulfation conjugated metabolites This finding raises the possibility that phase II conjugate metabolites of ellagitannin co- rilagin may function as biological antioxidant, anti-inflammatory,

α-glucosidase inhibitory and hepatoprotective activities after oral administration of pomegranate flowers extract

Besides, 17 metabolites of ellagic acid including urolithins and their derived metabolites were identified in this study Ellagic acid and gallic acid were identified in plasma and tissues Not only el- lagic acid and gallic acid are two main compounds in pomegranate flowers, as shown in Fig 6, but also two main the hydrolyzed metabolite of ellagitannins in rats after oral administration of pomegranate flowers extract This may illustrate the wide distri- bution of ellagic acid and gallic acid in rat biosamples Metabolites urolithin D, urolithin C, urolithin A and urolithin B were identi- fied in plasma and some tissues and further confirmed with their standards Besides, sulfation, methylation, glucuronidation metabo- lites of urolithins were found in plasma but not much in differ- ent organs, some of which have been identified in previous studies [30] The fragmentation patterns of them were consistent with pre- vious study [30] Flavonoids were also abundant in pomegranate flowers extract (18 flavonoids), and most of them was detected

in plasma and tissues The free and mainly glucuronide conju- gated flavonoids were identified in plasma and liver The flavonoids glucuronide metabolites showed typical loss of a 176 Da (a glu-

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Table 2

Summary of the mass spectral data and distribution of absorbed compounds and metabolites detected in the rat biological samples orally administrated with pomegranate flower extract

NO t (min) R Biotransformation Formula (neutral) [M −H]

fragments Error (ppm) U F P L S K H Lg Calculated Observed

O1 2.02 Gallic acid C 7 H 6 O 5 169.0142 169.0141 125.0241 −0.59 + + + + + + + – G1 8.45 Methylation of gallic acid C 8 H 8 O 5 183.0299 183.0297 168.0061, 124.0165 −1.09 + + + – – – – – G2 11.24 Methylation of gallic acid C 8 H 8 O 5 183.0299 183.0297 168.0067, 124.0165 −1.09 + + + – – – – – G3 3.32 Di-methylation of gallic acid C 8 H 8 O 5 197.0455 197.0452 169.0126, 125.0245 −1.52 + – – – – – – – O2 5.90 Digalloyl-glucoside C 20 H 20 O 14 483.0780 483.0773 313.0567, 169.0139, 125.0248 −1.44 – + – – – – – – O3 14.60 Galloyl-HHDP-glucoside C 27 H 22 O 18 633.0733 633.0726 463.0514, 300.9992, 169.0144 −1.10 + – – – – – – – O4 21.50 Galloyl-HHDP-glucoside C 27 H 22 O 18 633.0733 633.0726 463.0519, 300.9993, 169.0140 −1.10 + + – – – – – – O5 a 26.46 Corilagin C 27 H 22 O 18 633.0733 633.0733 463.0524, 300.9991, 169.0136 0 + + + + + + + – C1 8.04 Sulfation of corilagin C 27 H 22 O 21 S 713.0302 713.0298 633.0713, 463.0522, 300.9993, 169.0144 −0.56 + + – – – – – – C2 24.84 Sulfation of corilagin C 27 H 22 O 21 S 713.0302 713.0298 633.0713, 463.0522, 300.9993, 169.0144 0.56 + + – – – – – – C3 43.56 Methylation of corilagin C 28 H 24 O 18 647.0890 647.0894 463.0490, 300.9990 0.61 + + + + – – – – C4 53.47 Di-methylation of corilagin C 29 H 26 O 18 661.1046 661.1048 477.0641, 315.0149, 169.0138 0.30 + + + – – – – – C5 b 20.18 Glucuronidation of corilagin C 28 H 30 O 26 809.1054 809.1056 633.0676,463.0532, 300.9958 0.24 + – + – – – – – C6 22.66 Glucuronidation and methylation of corilagin C 34 H 32 O 24 823.1211 823.1208 647.0860, 463.0538, 300.9991 −0.36 + + + + – + + – C7 44.91 Glucuronidation and methylation of corilagin C 34 H 32 O 24 823.1211 823.1208 647.0860, 463.0538, 300.9991 −0.36 + + + + – + + – C8 5.03 Glucuronidation and di-methylation of corilagin C 35 H 34 O 24 837.1367 837.1364 661.1035, 477.0670, 315.0153 −0.67 + – + + – + – – C9 33.19 Di-glucuronidation of corilagin C 39 H 38 O 30 985.1375 985.1386 633.0781, 300.9973 −0.35 + – – – – – – – O6 a 46.95 Ellagic acid C 14 H 6 O 8 300.9990 300.9994 283.9972, 257.0091, 229.0137, 201.0192 1.32 + + + + + + + + E1 8.81 Sulfation of ellagic acid C 14 H 6 O 11 S 380.9558 380.9555 300.9992, 229.0169 −0.78 + + – + – – – – E2 9.56 Glycosylation of ellagic acid C 20 H 16 O 13 463.0518 463.0522 300.9995, 201.0220 0.86 + + – – – – – + E3 56.36 Methylation of ellagic acid C 15 H 8 O 8 315.0146 315.0140 299.9910 −1.90 + – + + + – – – E4 55.35 Methylation and sulfation of ellagic acid C 15 H 8 O 11 S 394.9715 394.9718 315.0146, 299.9905 0.75 + + + + – – – – E5 57.38 Methylation and sulfation of ellagic acid C 15 H 8 O 11 S 394.9715 394.9718 315.0146, 299.9905 0.75 + + – + – – – + E6 46.43 Glucuronidation and methylation of ellagic acid C 21 H 16 O 14 491.0467 491.0463 315.0146, 299.9908, 201.0213 −0.81 + + – + – – – + E7 50.68 Glucuronidation and di-methylation of ellagic acid C 22 H 18 O 14 505.0624 505.0621 329.0308, 314.0066, 299.9909, 201.0234 −0.59 + + – – – – – – E8 47.78 Methylation and glycosylation of ellagic acid C 21 H 18 O 13 477.0675 477.0679 315.0146, 299.9903, 201.0202 0.83 + + + + + – + – E9 a 36.16 Urolithin D C 13 H 8 O 6 259.0248 259.0245 241.0152, 231.0299 −1.15 + + + – – – – – E10 27.51 Sulfation and di-methylation of Urolithin D C 15 H 12 O 9 S 367.0129 367.0129 287.0575, 259.0604 0 + + + – – + – –

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