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Nghiên cứu thành phần hóa học và khảo sát hoạt tính gây độc tế bào của các hợp chất phân lập từ vỏ cây dà quánh (ceriops decandra)

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L E T T E R - S P E C T R A L A S S I G N M E N TStructure elucidation of two new diterpenes from Vietnamese mangrove Ceriops decandra 1 Department of Bioactive Natural Products, Institu

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L E T T E R - S P E C T R A L A S S I G N M E N T

Structure elucidation of two new diterpenes from

Vietnamese mangrove Ceriops decandra

1 Department of Bioactive Natural Products, Institute of Marine Biochemistry, Vietnam Academy of Science and Technology, Hanoi, Vietnam

2 Melinh Station for Biodiversity, Institute of Ecology and Biological Resourses, Vietnam Academy of Science and Technology, Hanoi, Vietnam

3 Department of Corrosion and Protection of Metals, Institute for Tropical Technology, Vietnam Academy of Science and Technology, Hanoi, Vietnam

4 Department of Chemistry and Catalytic Materials, Institute of Materials Science, Vietnam Academy of Science and Technology, Hanoi, Vietnam

5 Department of Basic Science, University of Fire Fighting and Prevention, Hanoi, Vietnam

6 Faculty of Quality Standards and Reference Substances, Institute of Drug Quality Control Ho Chi Minh city, Ho Chi Minh, Vietnam

Correspondence

Nguyen Van Thanh, Department of Bioactive Natural Products, Institute of Marine Biochemistry, Vietnam Academy of Science and Technology, Hanoi, Vietnam.

Email: thanhcmgu@yahoo.com, nvthanh1977@imbc.vast.vn

Funding information

Vietnam Academy of Science and Technology, Grant/Award Number: T ĐPCCC.04/18-20

1 | I N T R O D U C T I O N

Ceriops decandra (Griff.) W.Theob (Rhizophoraceae), a

true mangrove plant, occur in Africa, Australia, South

Asia, and many countries of Southest Asia [1] The bark

of C decandra is an Indian folk medicine used for the

treatment of diarrhea, amoebiasis, hemorrhage, and

malignant ulcers [2] The leaf extract has been reported

to exhibite antinociceptive activity [3] Previous

phyto-chemical investigations on this plant resulted in the

isola-tion of lupane- and ursane-type triterpenoids from the

leaf [4], beyerane-, pimarane-, kaurane-, and

abietane-type diterpenoids from the roots [1, 5–7], and

abietane-and podocarpane-type diterpenoids from the barks [2,

8] In an ongoing search for bioactive natural products

from mangroves [9, 10], we report here the isolation,

structure elucidation, and cytotoxicity assay of two new

diterpenes, ceridecandrin A (1) and B (2), from

C decandra stem barks Their structures were elucidated

by analysis of HR-QTOF-MS and 1D and 2D NMR

spec-troscopic data It should be noted that compound 1 is the

first example of a 8,15-epoxypimarane-type diterpenoid possessing a 14,16-ether bridge, and compound 2 is the second member of a rare class of 10,19-epoxyrosane-type diterpenoid (Figure 1)

2 | R E S U L T S A N D D I S C U S S I O N Ceridecandrin A (1) was obtained as white, amorphous powder Its molecular formula was determined to be

C20H32O3 on the basis of 13C NMR data (Table 1) and HR-QTOF-MS ion peaks at m/z 321.2416 [M + H]+ (calcd for C20H33O3+, 321.2424), m/z 343.2244 [M + Na]+ (calcd for C20H32O3Na+, 343.2244), and m/z 338.2687 [M + NH4]+(calcd for C20H36O3N+, 338.2690), indicating five index of hydrogen deficiency The 13C NMR and HSQC spectra disclosed 20 carbon signals, corresponding

to four methyls, seven sp3 methylenes (including one oxymethylene at δC 74.2), five sp3 methines (consisting three bearing oxygen atδC70.7, 84.1, and 85.1), and four

sp3quartenary carbons (one oxygenated atδC89.0) The

DOI: 10.1002/mrc.5091

Magn Reson Chem 2020;1–6 wileyonlinelibrary.com/journal/mrc © 2020 John Wiley & Sons, Ltd 1

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presence of five oxygenated carbons and the absence of

any unsaturated carbon, in combination with the

molec-ular formula C20H32O3, suggested that compound 1 was a

pentacyclic diterpenoid with two ether linkages The1H

NMR spectrum exhibited four singlet methyl signals at

δH0.86 (s, H-19),δH0.90 (s, H-20),δH0.91 (s, H-18), and

δH1.06 (s, H-17), three oxygenated methine protons atδH

3.61 (br s, H-14),δ 4.01 (br s, H-15), and δ 4.11 (br s,

F I G U R E 1 Structures of Compounds

1 and 2

T A B L E 1 1

H (500 MHz) and13C NMR (125 MHz) data for 1 (in CDCl 3 ) and 2 (in CD 3 OD)

Position

α 0.85 (1H, overlapped)

31.2 β 1.77 (1H, overlapped)

α 1.69 (1H, overlapped)

α 1.37 (1H, overlapped)

29.8 β 1.95 (1H, dddd, 4.5, 7.0, 14.0, 16.5)

α 1.71 (1H, overlapped)

α 1.17 (1H, ddd, 3.5, 13.5, 13.5)

75.4 3.56 (1H, br d, 4.0)

α 1.42 (1H, overlapped)

β 1.26 (1H, overlapped)

-11 19.3 β 1.75 (1H, dddd, 7.0, 14.0, 14.0, 14.0)

α 1.44 (1H, overlapped)

32.4 α 1.78 (1H, overlapped)

β 1.25 (1H, overlapped)

12 31.2 β 2.00 (1H, dddd, 1.5, 7.0, 14.0)

α 1.59 (1H, overlapped)

33.6 β 1.55 (1H, ddd, 3.5, 13.5, 14.0)

α 1.24 (1H, overlapped)

β 1.23 (1H, overlapped)

16 74.2 α 3.93 (1H, dd, 1.0, 8.0)

β 3.78 (1H, br d, 8.0)

109.3 α 4.93 (1H, dd, 1.0, 17.5)

β 4.87 (1H, overlapped)

α 3.64 (1H, d, 8.5)

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H-7), and a pair of oxymethylene protons atδH3.78 (br d,

J= 8.0 Hz, H-16β)/3.93 (dd, J = 1.0, 8.0 Hz, H-16α)

Careful interpretation of correlations observed in the

COSY and HMBC spectra revealed that the planar

struc-ture of 1 (Figure 2) was similar to that of

8,15R-epoxypimaran-16-ol [7] and ent-8,15R-8,15R-epoxypimaran-16-ol

[11], except for the presence of an additional hydroxyl

group at C-7, and an ether bridge between C-14 and C-16

in 1 Indeed, the HMBC correlation from H-15 (δH4.01)

to C-8 (δC 89.0) established the 8,15-epoxy linkage The

hydroxyl group was located at C-7 due to COSY

cross-peaks of H-5/H-6/H-7, as well as the HMBC correlations

from H-5 (δH 1.28) to C-7 (δC 70.7) The connection of

C-14 and C-16 through an oxygen atom was confirmed by

HMBC correlation from H-14 (δH3.61) to C-16 (δC74.2)

The relative configuration of 1 was determined by the

analysis of coupling constant and NOESY spectrum The

small vicinal coupling constant of H-7 (δH4.11, br s) and

the large vicinal coupling constant of H-3α (δH 1.17,

J= 3.5, 13.5, 13.5 Hz) and H-11β (δH1.75, J = 7.0, 14.0,

14.0, 14.0 Hz) suggested the equatorial orientation of H-7

and the axial orientations of both H-3α and H-11β The

NOESY correlations of H-3α/H3-18, H3-18/H-5,

H-5/H-1α, H-1α/H-2α, H-1α/H-9, H-9/H-11α, H-9/H-12α, H-9/ H-14, H-14/H3-17, H3-20/H-1β, H3-20/H-2β, H3

-20/H-11β, and H-2β/H319 confirmed the structure of pimarane diterpenoid skeleton of 1 [5] andα-configuration of H-14 (Figure 3) The trans-fusion between the B and C rings of pimarane scaffold, together with NOESY cross-peaks of H-16β/H-7 and H-16α/H3-17, indicated that H-15 was β-orientation Thus, structure of 1 was determined as 8,15:14,16-diepoxy-7α-hydroxy-pimarane

Ceridecandrin B (2) was isolated as white, amor-phous powder The molecular formula of 2, C20H32O2, was deduced from the 13C NMR data, and [M + Cl]− ion peaks at m/z 339.2071 and 341.2059 with a ratio of 3:1 (calcd for C20H32O2Cl−, 339.2096, and 341.2067) in the HR-QTOF-MS, corresponding to five index of hydrogen deficiency The 13C NMR and HSQC spectra revealed the presence of 20 carbons, including four nonprotonated carbons (one bearing oxygen at δC

91.2), nine methylenes (one sp2carbon at δC 109.3 and one oxygenated at δC 77.4), four methine (one sp2 car-bon at δC 152.3 and one oxymethine at δC 75.4), and three methyls The presence of two sp2 carbons and three oxygenated carbons, along with the HR-MS data analysis, indicated that 2 was a tetracyclic diterpenoid with an ether bridge The 1H NMR spectrum showed signals for one monosubstituted double bond at δH

5.82 (dd, J = 10.5, 17.5 Hz, H-15), δH 4.87

(H-16β)/4.93 (dd, J = 1.0, 17.5 Hz, H-16α), one oxymethine group at δH 3.56 (br d, J = 4.0 Hz, H-3), one oxymethylene group at δH 3.64 (d, J = 8.5 Hz,

H-19α)/3.68 (d, J = 8.5 Hz, H-19β), and three singlet methyls at δH 0.96 (s, H-20), δH 0.97 (s, H-18), and δH

1.02 (s, H-17) Detailed analysis of COSY and HMBC correlations (Figure 2) revealed that the planar struc-ture of 2 was closely related to that of euphomianol A [12], a rosane-type diterpenoid with a 10,19-oxygen bridge, except for the absence of a hydroxy group at C-5 in 2 This was confirmed by the COSY cross-peaks

of H-5/H2-6/ H2-7/H-8/H2-14 and the HMBC correla-tions from H2-19 (δH 3.64/3.68) to C-3 (δC 75.4), C-4 (δC 49.0), C-5 (δC 45.6), C-10 (δC 91.2), and C-18 (δC

16.1)

According to the coupling constant values between H-3 and H-2β (J = 4.5 Hz), between H-2β and H-1α (J = 14.0 Hz), and between H-12β and H-11α (J = 13.5 Hz), H-3 was assigned as equatorial orientation, and both H-2β and H-12β were in axial orientation The NOESY correlations of H-3/H-2β, 19α,

H-2β/H-1β, H-19β/H-6β, H-6β/H3-20, and H3-20/H-12β revealed that these protons were cofacial and they were in β-configuration (Figure 3) By contrast, NOE cross-peaks

of H-1α/H-5, H-5/H-6α, H-5/H-8, H-8/H3-17, and H3-17/ H-12α demonstrated that these protons were α-oriented

F I G U R E 2 Key COSY ( ) and HMBC correlations

( ) of 1 and 2

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Therefore, the structure of 2 was identified as

10,19-epoxy-3α-hydroxy-rosane

Compounds 1 and 2 were evaluated for cytotoxicity

against three cancer cell lines: SK-LU-1, HepG2, and

MCF7 Ellipticine was used as a positive control The

results showed that both compounds exhibited weak

cytotoxicity against three cell lines with IC50 values in

the range of 20.02 to 60.28μg/mL (Table 2)

3 | M A T E R I A L S A N D M E T H O D 3.1 | General

Optical rotations were measured using a JASCO

P-2000 polarimeter (JASCO, Oklahoma, OK, US) The HR-QTOF-MS were recorded on an Agilent 6530 Accurate-Mass Q-TOF LC/MS system (CA, USA) Col-umn chromatography (CC) was performed on silica gel (Kieselgel 60, 70–230 mesh and 230–400 mesh, Merck, Darmstadt, Germany) and YMC*GEL resins (ODS-A,

12 nm S-150μm, YMC Co., Ltd.) Analytical thin layer chromatography (TLC) systems were performed on pre-coated silica gel 60 F254 (1.05554.0001, Merck) and

RP-18 F254S plates (1.15685.0001, Merck), and the isolated compounds were visualized by spraying with 10%

H2SO4 in water and then heating for 1.5–2 min All procedures were carried out with solvents purchased from commercial sources that were used without fur-ther purification

F I G U R E 3 Key NOESY correlations ( ) of 1 and 2

T A B L E 2 Cytotoxicity of Compounds 1 and 2

Compound

IC 50 ( μg/mL)

1 58.36 ± 5.83 60.28 ± 2.77 44.17 ± 3.23

2 22.10 ± 2.65 27.53 ± 1.53 20.02 ± 1.55

Ellipticinea 0.41 ± 0.05 0.47 ± 0.03 0.35 ± 0.04

a Positive control substance.

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3.2 | NMR spectra

NMR spectra were recorded on a Bruker Ascend

500/Avance III HD spectrometer at temperature of

303 K Compounds 1 and 2 were dissolved in CDCl3and

CD3OD, respectively, and transferred into 5-mm NMR

tubes 1H and13C chemical shifts (δ) were referenced to

tetramethylsilane (TMS) at 0.00 ppm Coupling constants

(J) were expressed in Hertz (Hz) The 1H NMR

experi-ments were carried out with spectrometer frequency

(SF) = 500.20 MHz, spectral width in Hz

(SWH) = 10,000 Hz, acquisition time (AQ) = 3.2768 s,

number of scans (NS) = 16, relaxation delay (D1) = 1.0 s,

90 pulse width (P1) = 10.00 μs, Fourier transform size

(SI) = 65,536, and line broadening (LB) = 0.3 Hz The

13

C NMR spectrum was acquired with SF = 125.77 MHz,

SWH = 31,250 Hz, AQ = 1.048 s, NS = 1,536, D1 = 2.0 s,

P1 = 10.00 μs, SI = 32,768, and LB = 1.0 Hz The 2D

NMR spectra were recorded using Bruker library pulse

sequence condition as follows: for HSQC, NS = 4,

D1 = 2.0 s, SWH = 6009.615 Hz, time domain data points

(TD) = 2048, AQ = 0.1704 s; for HMBC, NS = 16,

SWH = 3012.048 Hz, AQ = 0.3399 s, D1 = 1.3 s,

TD = 2048; for COSY, SWH = 3067.485 Hz, TD = 2048,

NS = 2, AQ = 0.3338 s, D1 = 1.8 s; and for NOESY,

SWH = 2994.012 Hz, TD = 2048, NS = 8, AQ = 0.3420 s,

D1 = 1.8 s

3.3 | Plant material

The stem barks of C decandra were collected from Ca

Mau province, Vietnam, in July 2018 and identified by

Dr Nguyen The Cuong A voucher specimen

(PCCC-01-CD) was deposited in the Department of Bioactive

Natural Products, Institute of Marine Biochemistry,

Viet-nam Academy of Science and Technology (VAST)

3.4 | Extraction and isolation

The air-dried, powdered stem barks of C decandra

(9 kg) were extracted with EtOAc three times at room

temperature in ultrasonic bath The crude residue

(100 g) was separated on a silica gel CC and eluted

with n-hexane/EtOAc mixtures of increasing polarity

(100:0 ! 0/100) to obtained 12 fractions, E1–E12

Fraction E5 was divided into eight fractions, E5A–

E5H, by a silica gel CC (n-hexane/EtOAc, 15/1)

Frac-tion E5H was subjected to a silica gel CC

(n-hexane/EtOAc, 2.5/1) to give three fractions, E5H1–

E5H3 Fraction E5H1 was further chromatographed on

a silica gel CC (n-hexane/acetone, 2/1) to yield two

fractions, E5H1A and E5H1B Fraction E5H1B was separated on a silica gel CC (CH2Cl2/EtOAc, 4/1), followed by a silica gel CC (n-hexane/acetone, 10/1) to obtained three fractions, E5H1B1–E5H1B3 Fraction E5H1B1 was purified by a silica gel CC (n-hexane/acetone, 10/1) to yield Compound 1 (1.7 mg) Compound 2 (1.3 mg) was purified by YMC CC (MeOH/H2O, 6/1) from fraction E5H1B2

3.5 | Physical and spectroscopic data Ceridecandrin A (1): white, amorphous powder, α25

D

+52.8 (c 0.8, MeOH); 1H NMR (CDCl3, 500 MHz) and

13

C NMR (CDCl3, 125 MHz) spectral data, see Table 1; HR-QTOF-MS: m/z 321.2416 [M + H]+ (calcd for

C20H33O3+, 321.2424), m/z 343.2244 [M + Na]+(calcd for

C20H32O3Na+, 343.2244), and m/z 338.2687 [M + NH4]+ (calcd for C20H36O3N+, 338.2690)

Ceridecandrin B (2): white, amorphous powder, α25

D

+60.7 (c 0.4, MeOH); 1H NMR (CD3OD, 500 MHz) and

13

C NMR (CD3OD, 125 MHz) spectral data, see Table 1; HR-QTOF-MS: m/z 339.2071, and 341.2059 [M + Cl]− (calcd for C20H32O2Cl−, 339.2096, and 341.2067)

3.6 | Cytotoxicity assays The cytotoxicity assays for ceridecandrin A (1) and B (2) were performed using the SRB method [13] as a reviously reported protocol [14]

The raw NMR data files of the spectra including the relevant fid(s) are given in the Supporting Information

A C K N O W L E D G E M E N T S This research was supported by the Vietnam Academy

of Science and Technology (project code:

TĐPCCC.04/18-20) We thank Dr Dang Vu Luong, Institute of Chemistry, VAST, for NMR measurement and Prof Do Thi Thao, Institute of Biotechnology, VAST, for cytotoxicity assays

P E E R R E V I E W The peer review history for this article is available at https://publons.com/publon/10.1002/mrc.5091

O R C I D Nguyen Van Thanh https://orcid.org/0000-0002-5473-5999

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S U P P O R T I N G I N F O R M A T I O N Additional supporting information may be found online

in the Supporting Information section at the end of this article

How to cite this article: Van Thanh N, Linh KTP, Binh PT, et al Structure elucidation of two new diterpenes from Vietnamese mangrove Ceriops decandra Magn Reson Chem 2020;1–6 https://doi.org/10.1002/mrc.5091

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