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. 2023 Feb 20;15(3):463–469. doi: 10.1016/j.chmed.2022.08.010

Chemical constituents from leaves of Jatropha curcas

Yingjie Wang a, Di Zhou a, Xiaolin Bai b, Qingqi Meng c, Haihui Xie d, Guojiang Wu d, Gang Chen a, Yue Hou c,⁎, Ning Li a,⁎
PMCID: PMC10394345  PMID: 37538861

Abstract

Objective

To investigate the chemical constituents from the leaves of Jatropha curcas and evaluate their inhibition on lipopolysaccharide (LPS)-activated BV-2 microglia cells.

Methods

The n-BuOH extract of the leaves of J. curcas was isolated by macroporous adsorption resin, silica gel, ODS, column chromatography and semi-preparative HPLC. The structures of the compounds were identified by MS, NMR, ECD, and other spectroscopic methods. In addition, anti-neuroinflammatory effects of isolated compounds were evaluated by measuring the production of nitric oxide (NO) in over-activated BV-2 cells.

Results

Seventeen compounds, including (7R,8S)-crataegifin A-4-O-β-D-glucopyranoside (1), (8R,8′R)-arctigenin (2), arctigenin-4′-O-β-D-glucopyranoside (3), (-)-syringaresinol (4), syringaresinol-4′-O-β-D-glucopyranoside (5), (-)-pinoresinol (6), pinoresinol-4′-O-β-D-glucopyranoside (7), buddlenol D (8), (2R,3R)-dihydroquercetin (9), (2S,3S)-epicatechin (10), (2R,3S)-catechin (11), isovitexin (12), naringenin-7-O-β-D-glucopyranoside (13), chamaejasmin (14), neochamaejasmin B (15), isoneochamaejasmin A (16), and tomentin-5-O-β-D-glucopyranoside (17) were isolated and identified. Compounds 2, 4 and 8 significantly inhibited the release of NO in BV-2 microglia activated by LPS, with IC50 values of 18.34, 29.33 and 26.30 μmol/L, respectively.

Conclusion

Compound 1 is a novel compound, and compounds 2, 3, 8, 14–17 are isolated from Jatropha genus for the first time. In addition, the lignans significantly inhibited NO release and the inhibitory activity was decreased after glycosylation.

Keywords: anti-neuroinflammation, flavonoid, Jatropha curcas L., lignans

1. Introduction

Jatropha curcas L. (Euphorbiaceae), also known as ‘Mafengshu’, ‘Xiaotongzi’ in Chinese, is cultivated for the medical purpose and widely spread in tropical regions over the world. Guangxi Herbal Medicine recorded that it was astringent, slightly cold and toxic, and has the effect of dissipating blood stasis and swelling, stanch bleeding, relieving pain, and preventing itching. Previous studies showed that the chemical components from J. curcas were diterpenoids, sesquiterpenes, lignans, and flavonoids (Cavalcante et al., 2020, Zhao et al., 2014). Meanwhile, modern pharmacological activity studies revealed that they exhibited activities of anti-tumor (Zhang et al., 2018), anti-inflammation (Mujumdar & Misar, 2004), anti-oxidation (Li et al, 2014), and anti-bacteria (Othman, Abdullah, Ahmad, Ismail, & Zakari, 2015).

Overactivation of microglia cells induces neuroinflammation, which plays an important role in the development of a variety of neurodegenerative diseases, such as Alzheimer's disease (AD), Parkinson's disease (PD) (Miller and Blanco, 2021, Kwon and Koh, 2020). Therefore, inhibition of over-activated microglia has become a promising therapeutic strategy on neurodegenerative diseases. Previously, we searched for natural inhibitors of microglial activation from Euphorbiaceae herbs and revealed a series of natural lignans (Zhao et al., 2017, Zhou et al., 2020, Bai et al., 2021) of anti-neuroinflammatory effects.

In order to further clarify the pharmacodynamic material basis of J. curcas, the chemical compositions from the leaves of J. curcas were clarified by various spectroscopic analysis, and their anti-neuroinflammatory effects were evaluated by monitoring the production of nitric oxide (NO) in lipopolysaccharide (LPS)-treated BV-2 microglia cells. As a result, seventeen compounds, including (7R,8S)-crataegifin A-4-O-β-D-glucopyranoside (1), (8R,8′R)-arctigenin (2), arctigenin-4′-O-β-D-glucopyranoside (3), (-)-syringaresinol (4), syringaresinol-4′-O-β-D-glucopyranoside (5), (-)-pinoresinol (6), pinoresinol-4′-O-β-D-glucopyranoside (7), buddlenol D (8), (2R,3R)-dihydroquercetin (9), (2S,3S)-epicatechin (10), (2R,3S)-catechin (11), isovitexin (12), naringenin-7-O-β-D-glucopyranoside (13), chamaejasmin (14), neochamaejasmin B (15), isoneochamaejasmin A (16), and tomentin-5-O-β-D-glucopyranoside (17) were isolated and identified (Fig. 1). Among them, compound 1 was an undescribed compound, and compounds 2, 3, 8, 14–17 were isolated from Jatropha genus for the first time. All the identified compounds were evaluated for their inhibitory effects on NO production in LPS-stimulated BV-2 cells. The results indicated that compounds 2, 4 and 8 had significantly inhibition with IC50 values of 18.34, 29.33, and 26.30 μmol/L, respectively. In addition, we found that lignans could significantly inhibit NO release and the inhibitory activity was decreased after glycosylation.

Fig. 1.

Fig. 1

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Chemical structures of compounds 1–17.

2. Materials and methods

NMR spectra were tested by Bruker ARX-400 and ARX-600 spectrometer (Bruker Biospin, Rheinstetten, Germany), with TMS as an internal standard. Optical rotations were determined at 20 °C by a MCP200 instrument (Anton Paar, Germany). Bruker micro TOF-Q mass spectrometer (Bruker Biospin, Rheinstetten, Germany) was used to collect HR-ESI-MS data in positive ion and negative ion mode. ECD spectra were measured on a Bio-Logic Science MOS-450 spectrometer (Bio-Logic Science, Japan). IR data was acquired with an IFS 55 Fourier Transform infrared spectrometer (Bruker GMBH, Germany). UV-1800 UV–visible Spectrophotometer (Shimadzu Co., Ltd., Japan). Silica gel (100–200, 200–300 mesh) for chromatography was produced by Qingdao Ocean Chemical Group Co. of China. The macroporous resin (D101) was performed on Cangzhou Baoen Chemical Co., Ltd. (Hebei, China). Preparative HPLC was conducted on a YMC ODS column (5 μm, 20 mm × 250 mm) equipped with a Shimadzu LC-20AR pump system and a Shimadzu ultraviolet/visible (UV/vis, SPD-20A) (Tokyo, Japan). CDCl3, CD3OD, DMSO, and MTT were got from Sigma-Aldrich Company (St. Louis, MO, USA). All the chromatographic and analytical grade reagents were obtained from Tianjin Damao Chemical Company (Tianjin, China).

Leaves of J. curcas L. were collected in Guangdong Province of China in August 2017 and authenticated by Prof. Guojiang Wu and Haihui Xie (South China Botanical Garden, Chinese Academy of Sciences). Plant voucher sample (Number 20171215-L) was reserved in School of Traditional Chinese Materia Medica, Shenyang Pharmaceutical University.

3. Results

3.1. Extraction and isolation

The leaves of J. curcas (9.0 kg) were pulverized and extracted with 95% ethanol for four times (24 h each time) at room temperature, and the solvent was evaporated in vacuo to give a crude extract (1.915 kg). Then, the crude extract was suspended in water and participated with petroleum ether (PE), ethyl acetate (EtOAc), n-butyl alcohol (n-BuOH), respectively. The n-BuOH extract (500.0 g) was first adsorbed by macroporous adsorption resin D101, eluted with 80% ethanol. Then the eluate was subjected to silica gel column chromatography using CH2Cl2/MeOH (100: 0–0: 100) for elution, and eight fractions (Fr. B1–Fr. B8) were obtained. Fr. B1 (1.3 g) was chromatographed on open ODS column eluting by MeOH/H2O (30:70–100:0) and yielded four sub-fractions, and Fr. B1b was further separated by semi-preparative HPLC chromatography (MeOH/H2O 50:50, 3 mL/min) to afford compounds 2 (10.9 mg, tR = 51.0 min), 4 (2.9 mg, tR = 22.4 min), and 6 (8.6 mg, tR = 17.6 min). Fr. B2 (837.2 mg) was purified by ODS and semi-preparative HPLC (MeCN/H2O 25:75, 3 mL/min) to obtained 8 (3.0 mg, tR = 77.2 min). Compounds 14 (3.7 mg, tR = 84.9 min; MeCN/H2O 35:65, 3 mL/min), 15 (5.5 mg, tR = 52.1 min; MeOH/H2O 60:40, 3 mL/min), and 16 (3.1 mg, tR = 30.1 min; MeOH/H2O 60:40, 3 mL/min) were gained from Fr. B3c. Fr. B4 (2.56 g) was first separated on ODS column with MeOH/H2O to get five sub-fractions Fr. B4a–e, and compounds 3 (6.2 mg, tR = 45.1 min), 5 (10.5 mg, tR = 22.8 min), 7 (4.7 mg, tR = 82.4 min) and 9 (5.2 mg, tR = 28.8 min) were obtained by purifying fractions Fr. B4b and 4c by semi-preparative HPLC (MeOH/H2O 40:60, 3 mL/min). Fr. B6 was depurated to provide compounds 10 (21.2 mg, tR = 40.1 min; MeOH/H2O 10:90, 3 mL/min), 11 (6.1 mg, tR = 20.3 min; MeOH/H2O 25:75, 3 mL/min), 12 (2.9 mg, tR = 71.8 min; MeOH/H2O 42:58, 3 mL/min), and 13 (4.8 mg, tR = 36.9 min; MeOH/H2O 42:58, 3 mL/min). Fr. B7 (8.4 g) was further separated and purified by ODS column chromatography, Sephadex LH-20 column chromatography, and semi-preparative HPLC (MeCN/H2O 32:68, 3 mL/min), to acquire compound 1 (12.1 mg, tR = 23.4 min).

3.2. Structural identification

Compound 1: a yellow oil with [α]D20- 28.8 (c 0.50, MeOH). Its molecular formula was assigned as C28H36O12 from the HR-ESI-MS at m/z 565.2277 [M + H]+ (calcd. 565.2285). The 1H NMR data (Table 1) of 1 exhibited typical hydrogen signals of ABX coupling system at δH 7.08 (1H, d, J = 8.4 Hz, H-5), 6.99 (1H, d, J = 1.7 Hz, H-2) and 6.86 (1H, dd, J = 8.4, 1.7 Hz, H-6); δH 6.74 (1H, br. s, H-2′) and 6.70 (1H, br. s, H-6′) suggested the presence of a 1,2,4,6-tetrasubstituted benzene rings; δH 4.90 (1H, d, J = 7.4 Hz, H-1″) was an anomeric signal; As well as showed two methoxy signals at δH 3.76 (3H, s, 3-OCH3), 3.78 (3H, s, 3′-OCH3). The 13C NMR spectrum showed the presence of two benzene rings, and further analysis of the NMR data deduced that 1 was a new dihydrobenzofuran neolignan because of the presence of characteristic signals [δC 86.8 (C-7), 65.0 (C-9), 60.1 (C-9′), 49.7 (C-8), 34.7 (C-8′), 31.5 (C-7′); δH 5.44 (1H, d, J = 7.3 Hz, H-7), 3.69 (1H, m, H-8), 4.35 (1H, dd, J = 11.0, 5.7 Hz, H-9a), 4.25 (1H, dd, J = 11.0, 7.4 Hz, H-9b), 2.54 (2H, t, J = 7.6 Hz, H-7′), 1.69 (2H, m, H-8′), 3.41 (2H, overlapped, H-9′)]. According to the HMBC correlations (Fig. 2A) from H-7 to C-1/C-2/C-6/C-8/C-9, H-8 to C-9/C-5′/C-1 proved the existence of oxygen-containing five-membered ring. According to the HMBC correlations from δH 1.98 (3H, s) to δC 170.4 (C-1‴), 20.6 (C-2‴) suggested the presence of an acetyl, and from δH 4.35 (H-9) to 170.4 (C-1‴), speculated that the acetyl group was at C-9. The C-4 was glycosylated according to the correlation of H-1″ to C-4 in HMBC spectrum. In NOESY spectrum, the correlation of δH 3.76 (3-OCH3) with 6.99 (H-2), and 3.78 (3′-OCH3) with 6.74 (H-2′), confirming that two methoxy groups were linked at C-3 and C-3′, respectively. Further, through acid hydrolysis and derivation reaction, the retention times of the hydrolysis derivative product of compound 1 and the monosaccharide standard vertebral product derivative product were compared by HPLC, and it was finally determined that the connected sugar fragment in compound 1 was β-D-glucopyranose (tR = 26.1 min). In addition, the relative configurations of H-7 and H-8 were determined trans based on JH-7,8 = 7.3 Hz (Demont-Caulet et al., 2010, Wang et al., 2010). The absolute configuration was confirmed as 7R,8S by the negative Cotton effect at 270 nm in the ECD spectrum (Fig. 2B; Jiang et al., 2017). So, compound 1 was identified and named (7R,8S)-crataegifin A-4-O-β-D-glucopyranoside.

Table 1.

1H NMR and 13C NMR data of compound 1 in DMSO‑d6.

No. δH (mult., J in Hz) δC No. δH (mult., J in Hz) δC
1 – 134.4 6′ 6.70 (br. s) 116.2
2 6.99 (d, 1.7) 110.4 7′ 2.54 (t, 7.6) 31.5
3 – 149.0 8′ 1.69 (m) 34.7
4 – 146.3 9′ 3.41 (m) 60.1
5 7.08 (d, 8.4) 115.2 1″ 4.90 (d, 7.4) 100.0
6 6.86 (dd, 8.4, 1.7) 118.3 2″ 3.24 (overlapped) 73.2
7 5.44 (d, 7.3) 86.8 3″ 3.25(overlapped) 77.0
8 3.69 (m) 49.7 4″ 3.15 (m) 69.6
9 4.35 (dd, 11.0, 5.7)
4.25 (dd, 11.0, 7.4)		 65.0 5″ 3.26 (overlapped) 76.9
1′ – 135.6 6″ 3.64 (m)
3.43 (overlapped)		 60.6
2′ 6.74 (br. s) 112.8 3-OCH3 3.76 (s) 55.7
3′ – 143.5 3′-OCH3 3.78 (s) 55.7
4′ – 145.5 1‴
2‴		 –
1.98 (s)		 170.4
20.6
5′ – 127.4
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Fig. 2.

Fig. 2

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Key HMBC correlations (red arrow) (A) and experimental ECD spectrum (B) of compound 1.

Compound 2: a yellow powder (MeOH), [α]D20- 30.0 (c 0.50, MeOH). ESI-MS m/z: 395.12 [M + Na]+. 1H NMR (400 MHz, DMSO‑d6), δH 8.79 (1H, br. s, Ar-OH), 6.82 (1H, d, J = 8.0 Hz, H-5′), 6.73 (1H, d, J = 1.7 Hz, H-2), 6.68 (1H, d, J = 8.0 Hz, H-5), 6.63 (1H, d, J = 1.8 Hz, H-2′), 6.59 (1H, dd, J = 8.0, 1.8 Hz, H-6′), 6.57 (1H, dd, J = 8.0, 1.8 Hz, H-6), 4.06 (1H, dd, J = 8.4, 7.1 Hz, H-9), 3.86 (1H, t, J = 8.4 Hz, H-9′), 3.71 (3H, s, –OCH3), 3.70 (3H, s, –OCH3), 3.70 (3H, s, –OCH3), 2.82 (1H, dd, J = 13.2, 5.1 Hz, H-7′a), 2.74 (1H, dd, J = 13.4, 5.1 Hz, H-7′b), 2.69 (1H, m, H-7), 2.67 (1H, dd, J = 13.2, 7.0 Hz, H-8′), 2.47 (1H, m, H-7), 2.46 (1H, m, H-8). 13C NMR (100 MHz, DMSO‑d6): δC 148.6 (C-3), 147.4 (C-3′), 147.3 (C-4), 145.1 (C-4′), 131.3 (C-1), 128.9 (C-1′), 121.6 (C-6′), 120.4 (C-6), 115.3 (C-5′), 113.4 (C-2′), 112.3 (C-2), 111.8 (C-5), 55.5 (–OCH3), 55.4 (–OCH3), 55.3 (–OCH3), 45.7 (C-8′), 40.8 (C-8), 36.9 (C-7), 33.7 (C-7′). Comparing the NMR data of compound 2 with the literature data and according to the JH-8/H-8′ = 7.0 Hz, the relative configurations of H-8 and H-8′ were determined to be trans. The absolute configuration of compound 2 was confirmed as 8R,8′R based on the negative Cotton effect at 233 and 276 nm in the ECD spectrum (Rahman, 1990). So, compound 2 was identified as (8R,8′R)-arctigenin.

Compound 3: a yellow powder (MeOH), [α]D20- 63.2 (c 0.50, MeOH). ESI-MS m/z: 557.21 [M + Na]+. 1H NMR (600 MHz, DMSO‑d6): δH 6.99 (1H, d, J = 8.0 Hz, H-5′), 6.83 (1H, d, J = 8.0 Hz, H-5), 6.78 (1H, d, J = 1.7 Hz, H-2), 6.68 (1H, overlapped, H-6′), 6.66 (1H, d, J = 1.8 Hz, H-2′), 6.61 (1H, dd, J = 8.0, 1.8 Hz, H-6), 4.84 (1H, d, J = 7.4 Hz, H-1″), 3.72 (3H, s, –OCH3), 3.70 (6H, s, –OCH3). In the 13C NMR (150 MHz, DMSO‑d6) spectrum, compound 3 has a group of carbon signals of β-glucopyranose compared with 2 at δC 100.2 (C-1″), 77.0 (C-5″), 76.9 (C-2″), 73.2 (C-3″), 69.7 (C-4″), 60.6 (C-6″). The above data were consistent with the literature data (Min et al., 2004), compound 3 was confirmed as arctigenin-4′-O-β-D-glucopyranoside.

Compound 4: a white amorphous powder (MeOH), with [α]D20- 47.0 (c 0.10, MeOH). ESI-MS m/z: 441.12 [M + Na]+. 1H NMR (600 MHz, CDCl3): δH 6.58 (4H, s, H-2, 2′, 6, 6′), 4.73 (2H, d, J = 4.0 Hz, H-7, 7′), 4.28 (2H, dd, J = 9.1, 6.9 Hz, H-9a, 9a'), 3.91 (2H, s, H-9b, 9b'), 3.89 (12H, s, –OCH3 × 4), 3.09 (2H, m, H-8, 8′). 13C NMR (150 MHz, CDCl3): δC 147.3 (C-3, 3′, 5, 5′), 134.4 (C-4, 4′), 132.2 (C-1, 1′), 102.8 (C-2, 2′, 6, 6′), 86.2 (C-7, 7′), 72.0 (C-9, 9′), 56.5 (–OCH3), 54.5(C-8, 8′). According to the △δH-9a,H-9b, △δH-9′a,H-9′b = 0.37, determine that relative configuration of H-7/8, H-7′/8′ as trans (Shao, Yang, Feng, Jiang & Zhang, 2018), and compound 4 was identified as (-)-syringaresinol (Wu, Chang, Ko, & Teng, 1995).

Compound 5: a yellow oil (MeOH). [α]D20- 112.7 (c 0.50, MeOH). ESI-MS m/z: 603.20 [M + Na]+. 1H NMR (600 MHz, DMSO‑d6): δH 6.65 (2H, s, H-2, 6), 6.58 (2H, s, H-2′, 6′), 4.67 (1H, d, J = 4.5 Hz, H-7), 4.61 (1H, d, J = 4.5 Hz, H-7′), 4.28 (1H, t-like, H-9a), 4.18 (1H, t-like, H-9′a), 3.79 (2H, dd, J = 6.4, 4.7 Hz, H-8, 8′), 3.78 (2H, m, H-9b, 9b), 3.76 (6H, s, –OCH3 × 2), 3.75 (6H, s, –OCH3 × 2). 13C NMR (150 MHz, DMSO‑d6): δC 152.6 (C-3, 5), 147.9(C-3′, 5′), 137.2 (C-4), 134.8 (C-4′), 133.7 (C-1), 131.3(C-1′), 104.1 (C-2, 6), 103.6(C-2′, 6′), 102.6 (C-1″), 85.3 (C-7), 85.1 (C-7′), 77.2 (C-3″), 76.5 (C-5″), 74.2 (C-2″), 71.3 (C-9, 9′), 69.9 (C-4″), 60.9 (C-6″), 53.7 (C-8), 53.6 (C-8′), 56.4 (–OCH3), 56.0 (–OCH3). The above data were consistent with the literature data (Wu, Chang, Ko, & Teng, 1995), compound 5 was established as (-)-syringaresinol-4′-O-β-D-glucopyranoside.

Compound 6: a white needle crystal (MeOH), m.p. 119–120 °C, [α]D20- 42.6 (c 0.50, MeOH). ESI-MS m/z: 381.14 [M + Na]+. 1H NMR (600 MHz, CD3OD) δH 6.94 (2H, br. s, H-2, 2′), 6.80 (2H, d, J = 8.1 Hz, H-6, 6′), 6.76 (2H, d, J = 8.1 Hz, H-5, 5′), 4.70 (2H, d, J = 3.7 Hz, H-7, 7′), 4.22 (2H, m, H-9a, 9′a), 3.85 (6H, s, –OCH3 × 2), 3.82 (2H, d, J = 2.7 Hz, H-9b, 9′b), 3.13 (2H, m, H-8, 8′). 13C NMR (150 MHz, CD3OD): δC 149.1 (C-4, 4′), 147.3 (C-3, 3′), 133.8 (C-1, 1′), 120.0 (C-6, 6′), 116.1 (C-5, 5′), 110.9 (C-2, 2′), 87.6 (C-7, 7′), 72.6 (C-9, 9′), 56.4 (–OCH3), 55.4 (C-8, 8′). According to the △δH-9a, H-9b, △δH-9′a, H-9′b = 0.40, determine that relative configuration of H-7/8, H-7′/8′ as trans, and compound 6 was identified as (-)-pinoresinol (Li, Zhai, Tang & Duan, 2010).

Compound 7: a white amorphous powder (MeOH), [α]D20- 37.4 (c 0.50, MeOH). ESI-MS m/z: 543.06 [M + Na]+. 1H NMR (600 MHz, DMSO‑d6): 7.04 (1H, dd, J = 8.5, 2.0 Hz, H-5), 6.95 (1H, d, J = 1.7 Hz, H-2), 6.89 (1H, d, J = 1.7 Hz, H-5′), 6.85 (1H, dd, J = 8.2, 1.9 Hz, H-6), 6.75 (1H, dd, J = 8.2, 1.7 Hz, H-2′), 6.72 (1H, d, J = 8.1 Hz, H-6′), 4.89 (1H, d, J = 7.4 Hz, H-1″), 4.68 (1H, d, J = 4.0 Hz, H-7), 4.60 (1H, d, J = 4.0 Hz, H-7′), 4.12 (2H, m, H-9a, 9′a), 3.76 (6H, s, –OCH3 × 2), 3.04 (1H, m). 13C NMR (150 MHz, DMSO‑d6): δC 148.9 (C-4′), 147.5 (C-4), 145.9 (C-3), 145.8 (C-3′), 135.2 (C-1), 132.2 (C-1′), 118.6 (C-6, 6′), 110.1 (C-2), 115.1 (C-5, 5′) 110.4 (C-2′), 100.2 (C-1″), 85.1 (C-7), 84.8 (C-7′), 77.0 (C-2″), 76.8 (C-4″), 73.2 (C-5″), 70.9 (C-9), 70.8 (C-9′), 69.7 (C-3″), 60.6(C-6″), 55.7 (–OCH3), 55.6 (–OCH3), 53.7 (C-8′), 53.6 (C-8). The above data were consistent with the literature data (Su, Wu, & Shen, 2008), 7 was established as pinoresinol-4′-O-β-D-glucopyranoside.

Compound 8: a yellow oil (MeOH), ESI-MS m/z: 667.23 [M + Na]+. 1H NMR (600 MHz, DMSO‑d6): δH 6.66 (2H, d, J = 1.2 Hz, H-2, 6), 6.63 (2H, s, H-2′, 6′), 6.60 (2H, s, H-2″, 6″), 4.88 (1H, d, J = 5.1 Hz, –OH), 4.83 (1H, t, J = 4.9 Hz, H-7″), 4.65 (1H, d, J = 4.0 Hz, H-7′), 4.62 (1H, d, J = 4.0 Hz, H-7), 4.18 (2H, m, H-9a, 9′a), 4.04 (1H, m, H-8″), 3.79 (1H, m, H-9′b), 3.75 (12H, s, –OCH3 × 4), 3.71 (6H, s, –OCH3 × 2), 3.62 (1H, t, J = 5.7 Hz, H-9″a), 3.23 (1H, m, H-9″b), 3.05 (1H, m, H-8, 8′). 13C NMR (150 MHz, DMSO‑d6): δC 152.5 (C-3, 5), 147.9 (C-3′, 5′), 147.3 (C-3″, 5″), 137.0 (C-1), 135.3 (C-4), 134.8 (C-4′), 134.2 (C-4″), 132.1 (C-1′), 131.5 (C-1″), 104.1 (C-2, 6), 103.6 (C-2′, 6′), 103.2 (C-2″, 6″), 86.9 (C-8″), 85.3 (C-7), 85.1 (C-7′), 71.5 (C-7″), 71.3 (C-9), 71.1 (C-9′), 60.2 (C-9″), 53.6 (C-8), 53.8 (C-8′), 56.0 (–OCH3), 55.8 (–OCH3). According to the △δH-9a, H-9b, △δH-9′a, H-9′b = 0.39, determine that relative configuration of H-7/8, H-7′/8′ as trans. Compared with data in literature, compound 8 was identified as buddlenol D (Li et al., 2010, Xiong et al., 2011).

Compound 9: a yellow powder (MeOH) with [α]D20- 5.6 (c 0.50, MeOH). ESI-MS m/z: 303.03 [M−H]-. 1H NMR (600 MHz, DMSO‑d6) δH 11.92 (1H, br s, 5-OH), 6.87 (1H, d, J = 1.2 Hz, H-2′), 6.74 (2H, overlapped, H-5′, 6′), 5.87 (1H, d, J = 1.7 Hz, H-6), 5.82 (1H, d, J = 1.7 Hz, H-8), 4.96 (1H, d, J = 11.2 Hz, H-2), 4.48 (1H, d, J = 11.2 Hz, H-3). 13C NMR (150 MHz, DMSO‑d6): δC 197.6 (C-4), 167.3 (C-7), 163.3 (C-9), 162.5 (C-5), 145.8 (C-4′), 144.9 (C-3′), 128.1 (C-1′), 119.4 (C-6′), 115.4 (C-2′), 115.1 (C-5′), 100.3 (C-10), 96.1 (C-6), 95.1 (C-8), 83.0 (C-2), 71.5 (C-3). According to the JH-2, H-3 = 11.2 Hz, the relative configurations of H-2/H-3 were determined trans. The absolute configuration of compound 9 was confirmed as 2R,3R based on the positive Cotton effect at 300–340 nm in the ECD spectrum (Liu, Shi, Li, Wang, & Zhang, 2011). So, compound 2 was identified as (2R,3R)-dihydroquercetin.

Compound 10: a yellow powder (MeOH) with [α]D20- 10.2 (c 0.50, MeOH). ESI-MS m/z: 579.25 [2 M−H]-. 1H NMR (600 MHz, DMSO‑d6): δH 9.02 (4H, br s, Ar-OH), 6.71 (1H, br s, H-2′), 6.67 (1H, d, J = 7.6 Hz, H-5′), 6.58 (1H, d, J = 7.6 Hz, H-6′), 5.88 (1H, d, J = 1.8 Hz, H-8), 5.68 (1H, d, J = 1.8 Hz, H-6), 4.47 (1H, d, J = 7.4 Hz, H-2), 3.80 (1H, m, H-3), 2.65 (1H, dd, J = 16.0, 8.0 Hz, H-4a), 2.34 (1H, dd, J = 16.0, 5.2 Hz, H-4b). 13C NMR (150 MHz, DMSO‑d6): δC 156.5 (C-7), 156.2 (C-5), 155.4 (C-9), 145.0 (C-4′), 145.0 (C-3′), 130.5 (C-1′), 118.3 (C-6′), 115.1 (C-2′), 114.6 (C-5′), 99.0 (C-10), 95.1 (C-6), 93.8 (C-8), 81.0 (C-2), 66.3 (C-3), 27.9 (C-4). According to the positive Cotton effect at 240 and 280 nm, compound 10 was identified as (2S,3S)-epicatechin (Liu, Shi, Li, Wang, & Zhang, 2011).

Compound 11: a yellow powder (MeOH) with [α]D20+ 43.2 (c 0.50, MeOH). ESI-MS m/z: 288.94 [M−H]-. 1H NMR (600 MHz, DMSO‑d6): δH 6.88 (1H, d, J = 1.4 Hz, H-2′), 6.66 (1H, d, J = 8.1 Hz, H-5′), 6.58 (1H, dd, J = 8.1, 1.6 Hz, H-6′), 5.89 (1H, d, J = 2.2 Hz, H-8), 5.71 (1H, d, J = 2.2 Hz, H-6), 4.73 (1H, br. s, H-2), 4.00 (1H, m, H-3), 2.67 (1H, dd, J = 16.4, 4.6 Hz, H-4a), 2.34 (1H, dd, J = 16.4, 3.6 Hz, H-4b). 13C NMR (150 MHz, DMSO‑d6): δC 156.5 (C-7), 156.2 (C-5), 155.8 (C-9), 144.5 (C-4′), 144.5 (C-3′), 130.6 (C-1′), 117.9 (C-6′), 114.9 (C-2′), 114.8 (C-5′), 98.5 (C-10), 95.1 (C-6), 94.1 (C-8), 78.1 (C-2), 64.9 (C-3), 27.9 (C-4). According to the positive Cotton effect at 240 nm and the negative Cotton effect at 280 nm, compound 11 was identified as (2R,3S)-catechin (Nechepurenko et al., 2008).

Compound 12: a yellow powder (MeOH). ESI-MS m/z: 431.11 [M−H]-. 1H NMR (600 MHz, DMSO‑d6): δH 13.54 (1H, br. s, 5-OH), 7.90 (2H, d, J = 8.8 Hz, H-2′, 6′), 6.91 (2H, d, J = 8.8 Hz, H-3′, 5′), 6.73 (1H, s, H-3), 6.43 (1H, s, H-8), 4.58 (1H, d, J = 9.8 Hz, H-1″), 4.06 (1H, t-like, H-2″), 3.68 (1H, d, J = 10.9 Hz, H-6″a), 3.42 (1H, dd, J = 10.9, 4.1 Hz, H-6″b), 3.20 (1H, overlapped, H-3″), 3.16 (1H, overlapped, H-5″), 3.13 (1H, overlapped, H-4″). 13C NMR (150 MHz, DMSO‑d6): δC 181.7 (C-4), 163.2 (C-2/7), 161.3 (C-4′), 160.7 (C-5), 156.4 (C-9), 128.4 (C-2′, 6′), 121.1 (C-1′), 116.0 (C-3′, 5′), 109.0 (C-6), 102.6 (C-3/10), 93.9 (C-8), 81.5 (C-5″), 79.0 (C-3″), 73.2 (C-1″), 70.6 (C-4″), 70.2 (C-2″), 61.5 (C-6″). The above data were consistent with the literature data, compound 12 was established as isovitexin (Hosoya, Yun, & Kunugi, 2005).

Compound 13: a yellow powder (MeOH). ESI-MS m/z: 457.06 [M + Na]+. 1H NMR (600 MHz, DMSO‑d6): δH 7.33 (2H, d, J = 8.5 Hz, H-2′, 6′), 6.80 (2H, d, J = 8.5 Hz, H-3′, 5′), 6.15 (1H, br. s, H-8), 6.13 (1H, br. s, H-6), 5.50 (1H, m, H-2), 4.98/4.96 (1H, d, J = 7.7 Hz, H-1″), 3.38 (1H, overlapped, H-3a), 2.74 (1H, dt, J = 17.0, 3.0 Hz, H-3b). 13C NMR (150 MHz, DMSO‑d6): δC 197.3 (C-4), 163.1 (C-9), 165.3/165.2* (C-7), 163.0/162.8* (C-5), 157.8 (C-4′), 129.0 (C-1′), 128.5/128.6* (C-2′, 6′), 115.2 (C-3′, 5′), 103.2 (C-10), 99.6/99.4* (C-1″), 96.5 (C-6), 95.4 (C-8), 78.7 (C-2), 42.1/42.0* (C-3). The above data were consistent with the literature data, compound 13 was established as naringenin-7-O-β-D-glucopyranoside (Maltese, Erkelens, van der Kooy, Choi, & Verpoorte, 2009).

Compound 14: a brown powder (MeOH) with [α]D20 0 (c 0.50, MeOH). ESI-MS m/z: 541.20 [M−H]-. 1H NMR (600 MHz, DMSO‑d6): δH 12.08 (1H, s, 5-OH), 6.80 (4H, d, J = 8.3 Hz, H-2′, 2‴, 6′, 6‴), 6.70 (4H, d, J = 8.3 Hz, H-3′, 3‴, 5′, 5‴), 5.64 (2H, d, J = 11.6 Hz, H-2, 2″), 5.44 (2H, s, H-8, 8″), 5.37 (2H, s, H-6, 6″), 2.56 (2H, J = 11.6 Hz, H-3, 3″). 13C NMR (150 MHz, DMSO‑d6): δC 196.1 (C-4, 4″), 167.4 (C-7, 7″), 163.6 (C-5, 5″), 161.9 (C-9, 9″), 158.0 (C-4′, 4‴), 129.1 (C-2′, 2‴, 6′, 6‴), 127.4 (C-1′, 1‴), 115.2 (C-3′, 3‴, 5′, 5‴), 98.8 (C-10, 10″'), 97.8 (C-6, 6″), 97.0 (C-8, 8″), 82.6 (C-2, 2″), 48.5 (C-3, 3″). The relative configurations of H-2/H-3, H-2″/H-3″, and H-3/H-3″ were confirmed as cis through the chemical shift and coupling constant of H-2/H-2″/H-3/H-3″ (Xu et al., 2012). The absolute configuration of compound 14 was confirmed as 2S,3R,2″R,3″S based on the positive Cotton effect at 270–290, 310–330 nm in the ECD spectrum (Li, Khalid, & Zhu, 2018). According to the above data, identified 14 as chamacjasin.

Compound 15: a brown powder (MeOH) with [α]D20- 102.6 (c 0.50, MeOH). ESI-MS m/z: 541.20 [M−H]-. 1H NMR (600 MHz, CD3OD): δH 7.15 (2H, d, J = 8.4 Hz, H- 2‴, 6‴), 6.93 (2H, d, J = 8.4 Hz, H-2′, 6′), 6.79 (2H, d, J = 8.4 Hz, H-3′, 5′), 6.65 (2H, d, J = 8.4 Hz, H-3‴, 5‴), 5.98 (1H, br. s, H-8), 5.87 (1H, d, J = 1.8 Hz, H-8″), 5.78 (1H, d, J = 2.4 Hz, H-6″), 5.75 (1H, d, J = 2.4 Hz, H-6), 5.54 (1H, d, J = 4.8 Hz, H-2), 5.14 (1H, d, J = 9.0 Hz, H-2″), 3.27 (1H, dd, J = 3.6, 9.0 Hz, H-3″), 3.14 (1H, br. s, H-3). 13C NMR (150 MHz, CD3OD): δC 198.5 (C-4″), 196.2 (C-4), 168.5 (C-7′'), 168.4 (C-7), 165.4 (C-5″), 165.1 (C-5), 163.3 (C-8a), 158.9 (C-4‴), 158.6 (C-4′), 158.1 (C-8a″), 130.8 (C-1‴), 130.2 (C-2‴, 6‴), 128.7 (C-1′), 128.5 (C-2′, 6′), 116.4 (C-3‴, 5‴), 116.1 (C-3′, 5′), 105.0 (C-4a″), 103.8 (C-4a), 97.2 (C-6″), 97.1 (C-6), 96.4 (C-8′'″), 96.0 (C-8), 81.54 (C-2), 83.2 (C-2″), 50.7 (C-3), 49.6 (C-3″). According to the JH-2 = 4.8 Hz, JH = 9.0 Hz, JH-3′' = 3.6, 9.0 Hz, the relative configurations of H-2/H-3, H-2″/H-3″, H-3/H-3″ were determined cis, trans, cis, respectively. The absolute configuration of compound 15 was confirmed as 2S,3S,2″S,3″R based on the negative Cotton effect at 270–290 nm and the positive Cotton effect at 310–330 nm in the ECD spectrum (Li, Khalid, Zhu, & Zhang, 2018). Compared NMR data with the data in literature, and compound 15 was identified as neochamacjasin B (Wang et al., 2014).

Compound 16: a brown powder (MeOH) with [α]D20 0 (c 0.50, MeOH). ESI-MS m/z: 541.20 [M−H]-. 1H NMR (600 MHz, DMSO‑d6): δH 7.00 (4H, d, J = 8.4 Hz, H-2′, 2‴, 6′, 6‴), 6.79 (4H, d, J = 8.4 Hz, H-3′, 3‴, 5′, 5‴), 5.89 (2H, d, J = 1.8 Hz, H-8, 8″), 5.75 (2H, d, J = 1.8 Hz, H-6, 6″), 4.77 (2H, br. s, H-2, 2″), 3.70 (2H, br. s, H-3, 3″). 13C NMR (150 MHz, DMSO‑d6): δC 194.8 (C-4, 4″), 167.2 (C-7, 7″), 163.5 (C-5, 5″), 162.5 (C-9, 9″), 158.4 (C-4′, 4‴), 129.5 (C-2′, 2‴, 6′, 6‴), 126.7 (C-1′, 1‴), 115.5 (C-3′, 3‴, 5′, 5‴), 101.0 (C-10, 10″), 96.3 (C-6, 6″), 95.1 (C-8, 8″), 80.6 (C-2, 2″), 47.2 (C-3, 3″). The relative configurations of H-2/H-3, H-2″/H-3″ were confirmed as cis, cis by the coupling constant of H-2, H-2″, and H-3/H-3″ was confirmed as trans through the chemical shift of H-2/H-2″/H-3/H-3″ (Feng, Pei, Zhang, Hua, & Wang, 2004). Compared NMR data and specific rotation of 16 with the data in literature, and identified compound 16 as isoneochamaejasmin A.

Compound 17: a yellow powder (MeOH). ESI-MS m/z: 429.16 [M + HCOOH-H]-. 1H NMR (600 MHz, DMSO‑d6): δH 8.19 (1H, d, J = 9.7 Hz, H-4), 6.94 (1H, s, H-8), 6.27 (1H, d, J = 9.7 Hz, H-3), 3.90 (3H, s, –OCH3), 3.77 (3H, s, –OCH3). 13C NMR (150 MHz, DMSO‑d6): δC 160.3 (C-2), 156.8 (C-7), 150.9 (C-9), 145.7 (C-5), 140.3 (C-4), 137.9 (C-6), 112.0 (C-3), 107.6 (C-10), 104.1 (C-1′), 96.7 (C-8), 77.4 (C-3′), 76.3 (C-5′), 74.7 (C-2′), 69.7(C-4′), 60.9 (C-6′), 60.8 (–OCH3), 55.6 (–OCH3). According to above data, compound 17 was confirmed as tomentin-5-O-β-D-glucopyranside (Hammoda et al., 2008).

3.3. Inhibitory effects on LPS-stimulated BV-2 microglial cell over-activation

Neuroinflammation is a protective physiological response to injury or disease in the central nervous system, which is manifested by over-activation of microglia and the release of a large number of cytotoxic factors, causing damage to neurons, which is considered to be closely related to the pathogenesis of neurodegenerative diseases (Miller and Blanco, 2021, Kwon and Koh, 2020). Here, the Griess assay was used to detect the effect of the compounds on the release of NO by LPS-induced BV-2 microglia, and cell viability was assessed using the MTT assay (Zhao et al., 2017). As a result, compounds 2, 4 and 8 showed significant inhibitory activity [IC50 values of (18.34 ± 2.29), (29.33 ± 1.15), (26.30 ± 2.61) μmol/L, respectively], which was superior to the positive drug minocycline [IC50 value of (39.36 ± 3.12) μmol/L]; Compounds 6, 10, and 14 showed weak inhibitory activity [IC50 values were (59.20 ± 2.98), (58.01 ± 3.34), (85.54 ± 2.80) and (52.01 ± 2.51) μmol/L, respectively], as shown in Fig. 3. In addition, compounds 1, 3, 5, 7, 11, 12, 13 and 17 showed no significant inhibitory activitives (IC50 > 100 μmol/L), and compounds 9 and 15 showed significant cytotoxicity at the active concentration.

Fig. 3.

Fig. 3

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Anti-neuroinflammatory activities of isolated compounds on LPS-induced NO production in BV-2 cells (mean ± SE, n = 3). ###P < 0.001 vs control group, ***P < 0.001 vs LPS group.

4. Conclusion

The phytochemical investigation of n-BuOH extract from the leaves of J. curcas resulted in the discovery of eight lignans, eight flavonoids and one coumarin compound were isolated and identified. Among them, an undescribed compound, and compounds 2, 3, 8, 14–17 were isolated from Jatropha genus for the first time. Moreover, their anti-neuroinflammatory effects were evaluated by monitoring the production of nitric oxide in over-activated BV-2 cells. Compounds 2, 4 and 8 displayed significant effects, better than positive control (minocycline), while compounds 6, 10, and 14 had weak inhibitory activity. In addition, we found that lignans significantly inhibited NO release and the inhibitory activity was decreased after glycosylation. In conclusion, this study provided a basic theoretical basis for the study of chemical constituents of J. curcas, and also provided a basis for its further development and utilization.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was financially supported by National Natural Science Foundation of China (No. 81872768, U1903122), Shenyang Young Scientific and Technological Innovators Program (No. RC200408), Doctoral Scientific Research Foundation of Liaoning Province (No. 2020-BS-129).

Contributor Information

Yue Hou, Email: houyue@mail.neu.edu.cn.

Ning Li, Email: liningsypharm@163.com.

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