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Isolation and Identification of Alkaloids from Macleaya Microcarpa by UHPLC–Q-TOF-MS and Their Cytotoxic Activity in Vitro, An

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Isolation and Identification of Alkaloids from Macleaya Microcarpa by UHPLC–Q-TOF-MS and Their Cytotoxic Activity in Vitro, An Sai et al. BMC Chemistry (2020) 14:5 https://doi.org/10.1186/s13065-020-0660-1 BMC Chemistry RESEARCH ARTICLE Open Access Isolation and identifcation of alkaloids from Macleaya microcarpa by UHPLC– Q-TOF-MS and their cytotoxic activity in vitro, antiangiogenic activity in vivo Chunmei Sai1,2, Jian’an Wang1, Binjie Li3, Lin Ding1, Huiyun Wang1, Qibao Wang1, Huiming Hua3, Fangpeng Zhang2 and Qiang Ren1* Abstract Background: Extensive bioactivities of alkaloids from the genus Macleaya (Macleaya cordata (Willd.) R. Br. and Macleaya microcarpa (Maxim.) Fedde) have been widely reported, as well as more and more concerned from the sci- entifc communities. However, systematic research on the phytochemical information of M. microcarpa is incomplete. The aim of this study was to rapidly and conveniently qualitative analyze alkaloids from M. microcarpa by ultra-perfor- mance liquid chromatography/quadrupole-time-of-fght mass spectrometry (UHPLC–Q-TOF-MS) using accurate mass weight and characteristic fragment ions, furthermore separate and identify the main alkaloids, test antitumor activity in vitro and antiangiogenic activity in vivo. Results: A total of 14 alkaloids from fruits of M. microcarpa were identifed by UHPLC–Q-TOF-MS, including 5 pro- topines, 2 benzophenanthridines, 1 dimer, 1 dihydrobenzophenanthridines and 5 unknown structure compounds. Two major alkaloids were isolated by various column chromatographic methods. Their structures were determined by NMR data and related literatures. The two major alkaloids were evaluated for intro cytotoxic activities against HL-60, MCF-7, A-549, and in vivo antiangiogenic activity using transgenic zebrafsh. Conclusions: Current qualitative method based on UHPLC–Q-TOF-MS technique provided a scientifc basis for isola- tion, structural identifcation, and in vitro or in vivo pharmacological further study of alkaloids from M. microcarpa in the future. Keywords: Macleaya microcarpa, Alkaloids, Isolation and identifcation, UHPLC–Q-TOF-MS, Biological activity Introduction very extensive application value and great exploitation Te genus Macleaya contains two species, Macleaya cor- foreground as well as pesticide, veterinary drug, medici- data (Willd.) R. Br. and Macleaya microcarpa (Maxim.) nal ones in North America, Europe, China, which are Fedde, which mainly distributed in Japan, South and directly associated with the multifarious alkaloids and Northwest China, on slopes of grass or thickets at alti- their signifcant biological activities. A variety of alka- tudes of 450–1600 m [1]. Tey are well-known for their loids from M. cordata, such as sanguinarine, cheler- ythrine, protopine, allocryptopine, and others, exhibit *Correspondence: [email protected] anti-microbial, anti-infammatory, insecticidal, analgesic, 1 College of Pharmacy, Jining Medical University, Rizhao 276826, anticancer activity, have irreplaceable pharmacological Shandong, China Full list of author information is available at the end of the article © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo- main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Sai et al. BMC Chemistry (2020) 14:5 Page 2 of 11 efects [2–4]. However, systematic researches on the phy- (n-BuOH), to aford PE, CH2Cl2, n-BuOH and aqueous tochemical composition of M. microcarpa are few. extracts (For further separation and purifcation). UHPLC–Q-TOF-MS is widely used in qualitative com- Te crude ethanol extracts (200 mg) was dissolved with positions. Te method can provide high resolution and 5 mL methanol by sonication at 200 W for 15 min. Te accuracy data, as well as abundant structural informa- solution was fltered with a 0.22 µm and then analyzed by tion such as high-resolution second-stage mass fragment UHPLC–Q-TOF-MS. ions [5, 6]. Tis study aimed to rapidly and conveniently characterize alkaloids from M. microcarpa by UHPLC– UPLC–Q‑TOF‑MS analysis Q-TOF-MS using accurate mass weight and characteris- Agilent 1290 series Rapid Resolution LC system was tic fragment ions, furthermore separate and identify the coupled with Agilent 6530 Accurate-Mass quadru- main alkaloids by chromatographic and spectral tech- pole time of fight (Q-TOF) mass spectrometer (Agilent niques, test antitumor activity in vitro using the trypan Technologies, CA, USA) equipped with an electrospray blue method and MTT method reported previously ionization (ESI) interface. Te chromatographic separa- [7], and antiangiogenic activity in vivo using transgenic tion of analyzed crude ethanol extracts was performed zebrafsh [8]. on TOSOH TSK gel ODS-100V (4.6 × 150 mm, 3.0 µm) column (Tosoh Bioscience, Japan). Te column tempera- Materials and methods ture was maintained at 35 °C. Te injection volume was Plant materials 5 μL. Te mobile phase consisted of 0.05% formic acid Te fruits of Macleaya microcarpa (Maxim.) Fedde were (v/v) (A) and acetonitrile (ACN) (B). Te gradient pro- collected from Xiaguan Town, Neixiang County, Nan- gram was applied as follows: 0–5 min at 30% B; 5–20 min yang, Henan Province, China, in September 2017. (Notes: at 30–54% B; 20–23 min at 54–70% B; 23–40 min at It was not a protective plant and was allowed to be col- 70–80% B; 40–50 min at 80–90% B; 50–52 min at 90–30% lected). It was identifed by Prof. Jian’an Wang (College of B; 52–60 min at 30% B. Te fow rate was adjusted to Pharmacy, Jining Medical University, Shandong, China). 1.0 mL/min. Te outlet of UHPLC was split (1:4) and Te voucher sample (XGBLH-20170918) was deposited introduced into the ESI source. in pharmaceutical experimental center, College of Phar- Te MS conditions were set as follows: drying gas at macy, Jining Medical University, Rizhao, China. a fow rate of 10 L/min; drying gas temperature, 350 °C; pressure of nebulizer gas pressure, 45 psig; capillary volt- age ( ) 3000 V positive and negative ion modes and the Chemicals and reagents ± mass range from m/z 100 to 1200 Da. Te MS/MS spec- Chromatographic grade acetonitrile was purchased from tra were acquired with auto MS/MS mode at the acquisi- Honeywell, Burdick & Jackson. LC/MS-grade acetonitrile tion rate of 2 spectra/s. was purchased from Mallinckrodt Baker, Inc. (Phillips- Te calculation of the elemental composition was burg, NJ, USA). Chromatographic grade formic acid was acquired with Mass Hunter Workstation Software (Qual- purchased from TEDIA, Inc (Fairfeld, USA). Deionized itative Analysis Version B.06.00) (Agilent Technologies, water was purifed by Millipore purifcation system (Mil- CA, USA). lipore, MA, USA). Column chromatography (CC) was performed with silica gel (100–200 and 200–300 mesh, Isolation of two major alkaloids Shanghai Taitan Chemical Co. Ltd., Shanghai, China) and Te dichloromethane extract (365 g) was fractioned mci gel CHP20/P120 (Mitsubishi chemical corporation, using silica gel column chromatography (CC) and eluted Japan) and Sephadex LH-20 (GE Healthcare, Sweden). with petroleum ether (60–90 °C)–ethyl acetate (100:5, TLC analysis was carried out with glass plate precoated 100:10, 100:20, 100:50, 1:1 and 0:100, v/v) to yield six silica gel (HSGF254, Yantai Jiangyou Silicone Develop- fractions (Fr.A–Fr.F). Fr E was subjected to Sephadex ment Co. Ltd., Qingdao, China). LH-20 eluting with CH2Cl2–MeOH (1:1), and further recrystallization to yield compounds 2 (prtopine, 40 mg). Sample preparation Te precipitate during extraction of dichlorometh- Te air-dried and crushed fruits of M. microcarpa ane was separated by mci gel CHP20P CC eluting with (15.0 kg) were extracted with 95% EtOH (18 L) under MeOH–H2O (85:15) to aford compound 7 (cheleryth- cold maceration 3 times, each time for 7 days, respec- rine, 30 mg). tively. Te combined extracts were concentrated in vacuo to yield crude ethanol extracts, which was suspended NMR spectral analysis 1 13 in H2O, successively partitioned with Petroleum ether H and C NMR spectra were acquired with Bruker (PE), Methylene chloride (CH2Cl2) and N-butyl alcohol AV-600 NMR spectrometer (Billerica, MA, USA) using Sai et al. BMC Chemistry (2020) 14:5 Page 3 of 11 Fig. 1 The high resolution mass spectra and secondary mass spectra for 9 known compounds Sai et al. BMC Chemistry (2020) 14:5 Page 4 of 11 Fig. 2 The high resolution mass spectra and secondary mass spectra for 5 unknown compounds solvent signals (CDCl3: δH 7.26/δC 77.16, CD3OD: δH HL-60, and MTT assay against MCF-7 and A-549 [10, 3.31/δC 49.00), with tetramethylsilane (TMS) as an inter- 11]. nal standard. In the trypan blue method, cells in logarithmic growth 4 were seeded at 5 × 10 cells/mL in 24-well microplates, Cytotoxic activity test in vitro 2 mL/well, and incubated with various concentrations of Te method of cytotoxic activity test in vitro had based the compounds at 37 °C for 72 h. 50 μL suspension was on our previously published work [9]. HL-60 (human taken from each well, and 50 μL 0.4% trypan blue was leukaemia cell lines), MCF-7 (human breast cancer cell added to mix well, and observed under an optical micro- lines), A-549 (human lung adenocarcinoma cell lines), scope within 3 min.
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