Canangalias A and B from the stem bark of Cananga latifolia

Phytochemistry Letters 13 (2015) 147–151

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Canangalias A and B from the stem bark of Cananga latifolia Ratchanee Phatchanaa , Yordhathai Thongsrib , Ratree Somwaenga , Kewalin Piboonpola , Chavi Yenjaia,* a Natural Products Research Unit, Department of Chemistry and Center of Excellence for Innovation in Chemistry, Faculty of Science, Khon Kaen University, Khon Kaen 40002, Thailand b Department of Medical Technology, Faculty of Allied Health Science, Naresuan University, Phitsanulok 65000, Thailand

A R T I C L E I N F O

A B S T R A C T

Article history: Received 12 January 2015 Received in revised form 22 April 2015 Accepted 29 May 2015 Available online xxx

Cananga latifolia, a Thai medical plant, is used for the treatment of dizziness and fever. In this study, two new juvenile hormone III analogues, canangalias A and B (1 and 2) and a new phenylpropanoid derivative, 3-(40 -hydroxy-30 -methoxyphenyl)-1-acetoxy-2-propanol (3) were isolated from the stem bark of this plant. In addition, ten known compounds including three juvenile hormone III analogues (4–6), two alkaloids (7–8), two phenylpropanoids (9–10), a neolignan (11), a lignan (12) and catechaldehyde (13) were found. Compounds 4–7 and 12 exhibited antifungal activity against Pythium insidiosum by showing inhibition zone with diameters of 14.0, 24.0, 16.0, 14.0, and 16.1 mm, respectively. ã2015 Phytochemical Society of Europe. Published by Elsevier B.V. All rights reserved.

Keywords: Cananga latifolia Juvenile hormones III Pythium insidiosum Canangalias A and B

1. Introduction Cananga latifolia Finet & Gagnep., in the family Annonaceae, is a deciduous tree distributed in both tropical and subtropical regions. This plant can be found in South-East Asia such as Thailand, Laos, Cambodia, Myanmar, Vietnam and the Malaysian peninsular (Nanakorn, 1998). It can grow up to 20 m and the flower of this plant is fragrant. It has been used in folk medicine for infectious diseases, to treat dizziness and fever (Gyatso, 2000). The stem and bark of this plant had been evaluated for antiplasmodial activity (Hout et al., 2006). Chemical investigation of the stem bark of this plant was reported and abundant juvenile hormones (JH) III analogues found. In addition, the compounds such as cyclohexanol, fatty acid and alkaloid have been found in this plant (Yang et al., 2013). In this study, the purification of the crude EtOAc extract of the stem bark from C. latifolia led to two new JH III analogues and a new phenylpropanoid, together with ten known compounds. In the continuation of our work on antifungal activity against Pythium insidiosum, the chemical constituents from Thai medicinal plants have been evaluated (Sriphana et al., 2013; Sribuhom et al., 2015). Disk diffusion assay was used for testing the activity. Pythiosis is found in tropical and subtropical areas and mostly found in cats, dogs, horses, calves, and humans (De Cock et al., 1987). Antifungal drugs and vaccines are ineffective to this disease due to P. insidiosum is not true fungus (Mendoza, 2005). We

* Corresponding author. Tel.: +66 4320 2222 41x12243; fax: +66 4320 2373. E-mail address: [email protected] (C. Yenjai).

reported herein the chemical constituents from C. latifolia and antifungal activity against P. insidiosum. Juvenile hormones (JHs) are acyclic sesquiterpeniods that are vitally important in several perspectives to all insects. They regulate insect development, reproduction, polyphenism, metamorphosis, diapauses and caste differentiation (Teal et al., 2014). It has been believed that JHs in plants are synthesized against insect herbivorous by preventing the development of insect larvae to insect adults (Chaitanya et al., 2012). The most commonly found JH is JH III, (2E,6E)-10,11-epoxy-3,7,11-trimethyldodeca-2,6-dienoic acid methyl ester which regulates the biological functions of insects (Toong et al., 1988). JH III analogues are harmless to nonarthropods, but selectively effective on insects so they can be used as natural insecticides. JH derivatives have been found in plants such as Cyperus iria and Cyperus aromatics (Bede et al., 1999, 2000) and, recently, C. latifolia (Yang et al., 2013). 2. Results and discussion The EtOAc extract of the stem bark of C. latifolia, collected in Khon Kaen Province in April 2013, was subjected to silica gel column chromatography and further purified by chromatographic methods to obtain 3 new compounds, canangalias A and B (1 and 2) and 3-(40 -hydroxy-30 -methoxyphenyl)-1-acetoxy-2-propanol (3), together with ten known compounds (4–13) (Fig. 1). Ten known compounds were identified as (2E,6E,10R)-10-hydroxy-3,7,11trimethyldodeca-2,6,11-trienoic acid methyl ester (4) (2E,6E,10R)-10,11-dihydroxy-3,7,11-trimethyldodeca-2,6-dienoic

http://dx.doi.org/10.1016/j.phytol.2015.05.025 1874-3900/ ã 2015 Phytochemical Society of Europe. Published by Elsevier B.V. All rights reserved.

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R. Phatchana et al. / Phytochemistry Letters 13 (2015) 147–151

15

O H3CO

1

14

3

2

4

5

6

7

12 10

9

8

11

6

O

13

5

H3CO

OH

3

HO

4'

2

1''

6' 2''

3''

OH

5'

3'

7'

4'

2 1

7

O

O

O

H3CO

OH

3'

1'

2'

O

1

1'

OH O H

OH

4

OCH3 3

O

O

H3CO

OH

H3CO

O

OH

5 O

6

O N

O

OH

O

OH

HO

N

OCH3

9

OCH3

O

O

H

10

OH

CHO

OCH3

H O

OCH3

OCH3 8

7

O HO

OH

OH

H

HO

11

OCH3

O

OH OH

12

13

Fig. 1. The structures of compounds 1–13.

acid methyl ester (5) the major constituent in this plant (Jacobs et al., 1987), (2E,6E,10R)-10,11-epoxy-3,7,11-trimethyldodeca-2,6dienoic acid methyl ester (6) (Rodriguez and Gros, 1990), liriodenine (7) (Li et al., 2009), onychine (8) (Prachayasittikul et al., 2009), 3-(40 -hydroxy-30 -methoxyphenyl)-propane-1,2-diol (9) (Fan and Yue, 2003; Ouyang et al., 2007), 20 ,30 -epoxyeugenol (10), 5-acroleinyl-50 -hydroxy-3-hydroxymethyl-7,30 -dimethoxy2,3-dihydrobenzofuran (11) (Xu and Tan, 2012), pinoresinol (12) (Sriphana et al., 2013), and 3,4-dihydroxybenzaldehyde (13). The structures of all compounds were determined through the analysis of spectroscopic data, 1D- and 2D-NMR, and also MS analysis. It was found that five compounds (1,2, and 4–6) were JH III derivatives and two of them were new derivatives. In addition, a new phenylpropanoid 3 was discovered. Compound 1 was obtained as a colorless oil. It was assigned the molecular formula C16H26O4 as determined from its quasimolecular ion peak at m/z 305.1725 [M + Na]+ (calcd for 305.1729) in the HRESIMS. The 13C NMR and DEPT spectra showed 16 carbon signals (Table 1). The olefinic proton at d 5.65 (H-2) correlated with C-4 and C-15 in the HMBC spectrum (Fig. 2). In this spectrum, the proton at d 3.69 correlated with carbon at d 167.3 which indicated the methyl ester group. The methylene

proton (H-5) showed correlation with C-7 (d 134.8) in the HMBC experiment. The 1H and 13C NMR spectra are similar to those of compound 5 except the hydroxy group at C-10 was replaced by a carbonyl group (dC 214.0). The triplet signals at d 2.29 and 2.62 (J = 7.6 Hz) were assigned as H-8 and H-9, respectively. In the HMBC spectrum, H-8 correlated with C-6, C-7, C-10 and C-14. The methyl group at H-12 and H-13 showed the same signals at d 1.38 and correlated with C-10 and C-11 in the HMBC experiment. Thus, this compound was determined as (2E,6E)-11-hydroxy-3,7,11-trimethyldodeca-10-one-2,6-dienoic acid methyl ester which was named canangalia A. Compound 2 was obtained as a colorless oil. It was assigned the molecular formula C16H26O5 as determined from its quasimolecular ion peak at m/z 321.1675 [M + Na]+ (calcd for 321.1678) in the HRESIMS. The 13C NMR and DEPT spectra showed 16 carbon signals. The 1H and 13C NMR spectra showed a methyl ester group at dH/dC 3.69/51.0 which correlated with a carbonyl carbon (dC 167.4) indicating the methyl ester moiety (Table 1). The olefinic proton at dH 5.73 correlated with a carbon at dC 115.2 in the HMQC spectrum. This proton showed long-range correlations with C-4 (d 34.8) and C-6 (d 19.2) in the HMBC experiment (Fig. 2). Two singlet signals at d 4.84 and 4.76 were assigned as exocyclic olefinic

R. Phatchana et al. / Phytochemistry Letters 13 (2015) 147–151

149

Table 1 1 H and 13C NMR (400 MHz) spectral data of compounds 1-3 Position

1

2 a

dC type

dH (J in ppm)

3

dC type

a

dH (J in ppm)

1

167.3 C

2 3

115.6 CH 159.8 C

5.65, s

115.2 CH 160.5 C

5.73, s

4 5 6 7 8 9 10 11 12 13 14 15 10 20 30 40

40.8 CH2 26.0 CH2 124.0 CH 134.8 C 33.5 CH2 34.5 CH2 214.0 C 76.3 C 26.6 CH3 26.6 CH3 16.3 CH3 18.9 CH3

2.16, m 2.16, m 5.10, br s

34.8 CH2 31.9 CH2 19.2 CH3

2.39, br t (8.5) 2.07, t (8.5) 2.19, s

5

167.4 C

dH (J in ppm)

67.9 CH2

4.17, m 4.01, m 4.04, m 2.77, dd (13.6, 4.8) 2.70, dd (13.6, 7.2)

71.0 CH 39.8 CH2

2.29, t (7.6) 2.62, t (7.6)

1.38, s 1.38, s 1.62, s 2.16, s 107.1 C 146.1 C 26.8 CH2

0

81.3 CH 106.8 CH2

100 200 300 OCH3 OH COCH3 COCH3

21.8 CH3 81.1 C 29.6 CH3 51.0 CH3

51.0 CH3

3.69, s

129.0 C 112.0 CH 146.8 C 144.7 C

2.74, m 2.25, m 1.95, m 1.83, dd (14.4, 7.6) 4.01, d (3.7) 4.84, s 4.76, s 1.44, s

26.8 CH2

60 70

a

dC typea

1.32, s 3.69, s

6.73, s

114.7CH

6.86, d (7.8)

122.2CH

6.71, d (7.8)

56.1 CH3

3.88, s 5.56, s 2.11, s

21.0 CH3 171.3 C

Multiplicities were deduced from DEPT and HMQC experiments.

protons at H-70, which were correlated with a carbon at d 106.8 in the HMQC spectrum. These protons showed correlations with carbons at C-20 (d 107.1) and C-40 (d 26.8) in the HMBC spectrum. It should be noted that the chemical shift at d 107.1 displayed the characteristic of a hemi-ketal group. The 1H–1H COSY spectrum showed the correlations in the aliphatic region, representing H-4/ H-5 and H-40 /H-50 /H-60 . The doublet signal at d 4.01 (J = 3.7 Hz) was assigned as H-60 and connected to the carbon at d 81.3 in the HMQC spectrum. Two methyl protons at H-100 (dH/dC 1.44/21.8) and H-300 (dH/dC 1.32/29.6) showed long range correlations with C-60 and C-

200 in the HMBC spectrum. In addition, both of them also correlated to each other. The relative stereochemistry of this compound is shown in Fig. 2. The NOESY experiment showed the correlation between H-70 (d 4.84) and H-5 which indicated the cofacial of these two groups (Fig 2). The a-equatorial orientation of H-60 was determined from the small coupling constant (d 4.01, d, J = 3.7 Hz). It was indicated that isopropanol group located at the b-axial orientation. From all data, this compound was determined as (2E)-3-methyl-5-[-60 -(200 -hydroxypropan-200 -yl)-30 -methenyl-

O O

O

H3CO

OH

OH

HO

O

O 3

1

O H3CO

OH O

2

OH

OH

OH

H3CO O

O NOESY

H H

2

Fig. 2. The HMBC and NOESY correlations of compounds 1–3.

H

J 5',6' = 3.7 Hz

150

R. Phatchana et al. / Phytochemistry Letters 13 (2015) 147–151

20 -hydroxy-20 -tetrahydropyran-20 -yl]-pent-2-enoic acid methyl ester which was named canangalia B. Compound 3 was obtained as a colorless oil. It was assigned the molecular formula C12H16O5 as determined from its quasimolecular ion peak at m/z 263.0893 [M + Na]+ (calcd for 263.0895) in the HRESIMS. The IR spectrum showed an absorption band of a hydroxy group at 3414 cm1 and carbonyl group at 1720 cm1. Three aromatic protons at d 6.86 (d, J = 7.8 Hz), d 6.71 (d, J = 7.8) and d 6.73 (s) were assigned as H-50 , H-60 and H-20 , respectively (Table 1). The methoxy proton at dH/dC 3.88/ 56.1 showed a correlation with carbon at d 146.8 (C-30 ) while a phenolic proton correlated with a carbon at d 144.7 (C-40 ). The proton H-50 displayed correlations with C-10 (d 129.0) and C-30 (d 146.8) in the HMBC experiment. The 13C and DEPT spectra showed two methylene carbons at d 39.8 and 67.9 which were assigned to C-3 and C-1, respectively. Two doublet of doublet signals at d 2.77 (J = 13.6, 4.8 Hz, H-3a) and d 2.70 (J = 13.6, 7.2 Hz, H-3b) correlated with carbons at d 67.9 (C-1), d 71.0 (C-2), d 129.0 (C-10 ), d 112.0 (C-20 ) and d 122.2 (C-60 ) in the HMBC experiment (Fig. 2). The multiplet signals at d 4.17 and 4.01 were assigned as H-1a and H-1b, respectively, which connected to the same carbon at d 67.9 in the HMQC spectrum. These protons showed correlations with the carbonyl carbon at d 171.3. The methyl group at dH/dC 2.11/ 21.0 displayed long range correlation with carbonyl carbon, indicating an acetoxy group. After basic hydrolysis, compound 9 was obtained. Then the stereochemistry of this compound was assigned as S. Thus, compound 3 was determined as 3-(40 -hydroxy30 -methoxyphenyl)-1-acetoxy-2-propanol. In conclusion, the extraction and purification of the crude EtOAc extract of the stem bark from C. latifolia led to two new JH III analogues named canangalias A and B (1 and 2) and a new phenylpropanoid derivative 3, together with ten known compounds. It was found that compounds 4–7 and 12 showed antifungal activity against P. insidiosum with diameters of 14.0, 24.0, 16.0, 14.0, and 16.1 mm, respectively (Table 2). In addition, this plant contained abundant of juvenile hormones III analogues. 3. Experimental 3.1. General experimental procedures Melting points were determined on a SANYO Gallenkamp (UK) melting point apparatus and are uncorrected. UV spectra were measured on an Agilent 8453 UV–vis spectrophotometer (Germany). IR spectra were recorded as KBr disks or thin films, using Perkin Elmer Spectrum One FT-IR spectrophotometer (UK). The NMR spectra were recorded on a Varian Mercury plus spectrometer (UK) operating at 400 MHz (1H) and at 100 MHz (13C). Mass spectra were determined on a Micromass Q-TOF 2 hybrid quadrupole time-of-flight (Q-TOF) mass spectrometer with a Z-spray ES source (Micromass, Manchester, UK). Optical rotation was obtained using a JASCO DIP-1000 digital polarimeter. Thin layer chromatography (TLC) was carried out on MERCK silica gel 60 F254 TLC aluminium sheet. Column chromatography was Table 2 Antifungal activity of compounds against P. insidiosum. Compound

Concentration (mg/ml) Inhibition zone (mm) Interpretationa

4 5 6 7 12 Terbinafine

16 78 43 13 76 100

a

Interpretation; A: active, IA: inactive.

14.0 24.0 16.0 14.0 16.1 –

A A A A A IA

done with silica gel 0.063–0.200 mm or less than 0.063 mm. Preparative layer chromatography (PLC) was carried out on glass supported silica gel plates using silica gel 60 PF254 for preparative layer chromatography. All solvents were routinely distilled prior to use. 3.2. Plant material The stem bark of C. latifolia was collected in April 2013 from Phuwieng District, Khon Kaen Province, Thailand. The plant was identified by Dr. Pranom Chantaranothai, Faculty of Science, Khon Kaen University. A botanically identified voucher specimen (KKU012013) was deposited at the herbarium of the Department of Chemistry, Faculty of Science, Khon Kaen University, Thailand. 3.3. Extraction and isolation Air-dried stem bark (4.7 kg) of C. latifolia was ground into powder and then extracted successively at room temperature with hexanes (3  15 L), EtOAc (3  10 L) and MeOH (3  10 L). The filtrated samples were combined, and the solvents were evaporated in vacuo to yield crude hexanes (40 g), EtOAc (103 g) and MeOH (154 g), respectively. The crude EtOAc extract was subjected to silica gel flash column chromatography (FCC) and subsequently eluted with a gradient system of three solvent systems (hexanes, EtOAc and MeOH) by gradually increasing the polarity of the elution solvents system. On the basis of their thin layer chromatography (TLC) characteristics, the fractions which contained the same major compounds were combined to give eight fractions, F1–F8. Fraction F3 was purified by silica gel FCC and eluted with a gradient of 20% EtOAc:hexanes to give five subfractions, F3.1–F3.5. Subfractions F3.2 and F3.3 were further purified by silica gel FCC using 20% EtOAc:hexanes as eluent to give 1 (7.8 mg, 0.0001%) and 6 (20.5 mg, 0.0004%), respectively. Further purification of F3.4 with gel filtration (Sephadex LH-20) and eluting with MeOH afforded 7 (7.9 mg, 0.00017%). Fraction F4 was purified by silica gel FCC and eluted with a gradient of 20% EtOAc:hexanes to give five subfractions, F4.1–F4.5. Subfraction F4.2 was further purified by silica gel FCC using 20% EtOAc:hexanes as eluent to give 5 (2.5 g, 0.0532%) and 8 (4.5 mg, 0.0001%). Subfraction F4.4 was purified on silica gel FCC and eluted with a gradient of EtOAc:hexanes to give five subfractions, F4.4.1–F4.4.5. Subfraction F4.4.2 was subjected on a column of Sephadex LH-20, using MeOH as eluent and then by PLC (40% EtOAc:hexanes) to give 2 (9.2 mg, 0.0002%). Subfraction F4.4.4 was purified by PLC and 40% EtOAc:hexanes was used as developing solvent to afford 4 (10.3 mg, 0.00022%). Fraction F5 was separated by silica gel FCC and eluted with a gradient of EtOAc: hexanes and then PLC (10% MeOH:CH2Cl2) yielding 10 (4.3 mg, 0.00009%). Fraction F6 was purified by silica gel FCC and eluted with a gradient of EtOAc:hexanes to give four subfractions, F6.1– F6.4. Subfraction F6.2 was purified on silica gel FCC and eluted with a gradient of MeOH:CH2Cl2 to give 3 (8.5 mg, 0.00018%) and 13 (0.5, 0.01%). Further purification of F6.3 by PLC using 10% MeOH:CH2Cl2 as developing solvent gave 12 (4.7 mg, 0.0001%). Fraction F7 was purified by silica gel FCC and eluted with a gradient of MeOH: CH2Cl2 to give 11 (25.6 mg, 0.00054%). Purification of F8 by silica gel FCC and elution with a gradient of 5% MeOH:CH2Cl2 and then PLC (10% MeOH:CH2Cl2) gave 9 (33.4 mg, 0.0007%). 3.4. Spectroscopic data of compounds Canangalia A (1) Colorless oil; UV (CHCl3) lmax (log e) 203 (4.25) nm; IR (neat) nmax 3486, 2948, 1713, 1648, 1436, 1224, 1148 cm1; 1H NMR (CDCl3, 400 MHz) and 13C NMR (CDCl3, 100 MHz) spectroscopic data, see Table 1; HRESIMS m/z 305.1725 [M + Na]+ (calcd for C16H26O4 + Na 305.1729).

R. Phatchana et al. / Phytochemistry Letters 13 (2015) 147–151

Canangalia B (2) Colorless oil; [a]23D + 81.5 (c 0.1, CHCl3); UV (CHCl3) lmax (log e) 218 (4.21) nm; IR (neat) nmax 3473, 2946, 1718, 1649, 1437, 1224, 1150 cm1; 1H NMR (CDCl3, 400 MHz) and 13C NMR (CDCl3, 100 MHz) spectroscopic data, see Table 1; HRESIMS m/z 321.1675 [M + Na]+ (calcd for C16H26O5 + Na 321.1678). 3-(40 -hydroxy-30 -methoxyphenyl)-1-acetoxy-2-propanol (3) Colorless oil; [a]23D  24.5 (c 0.1, CHCl3); UV (CHCl3) lmax (log e) 203 (3.95), 282 (2.93) nm; IR (neat) nmax 3414, 2939, 1720, 1515, 1234, 1033, 816, 797 cm1; 1H NMR (CDCl3, 400 MHz) and 13C NMR (CDCl3, 100 MHz) spectroscopic data, see Table 1; HRESIMS m/z 263.0893 [M + Na]+ (calcd for C12H16O5 + Na 263.0895). 3.5. Antifungal activity; disk diffusion assay All purified compounds were dissolved in CH2Cl2 to final volumes of 100 ml. Then 20 ml of the tested compounds was impregnated on sterilized discs (6.0 mm) (Whatman, England) and placed on the Sabouraud Dextrose Agar (SDA) plate (Oxoid, UK) which had been inoculated with an agar block of P. insidiosum (11 cm). Plates were kept at room temperature for 2 h in the laminar flow cabinet, then inverted and incubated at 25  C for 3, 6 and 9 days. Terbinafine (20 mg/100 ml; 20 ml/disk) (Sigma– Aldrich, USA) and a disk with CH2Cl2 only were used as control discs. Inhibition of the mycelial growth of P. insidiosum compared with the control was observed and reported as positive antifungal activity. Acknowledgments We thank Rajamangala University of Technology Isan Khon Kaen Campus for financial support to R.P. The Center of Excellence for Innovation in Chemistry (PERCH-CIC), Office of the Higher Education Commission, Ministry of Education are gratefully acknowledged. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. phytol.2015.05.025.

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