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Phytochemistry and Pharmacology of Genus Ephedra ZHANG Ben-Mei1∆, WANG Zhi-Bin1∆, XIN Ping1, WANG Qiu-Hong2, BU He1, KUANG Hai-Xue1*

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Phytochemistry and Pharmacology of Genus Ephedra ZHANG Ben-Mei1∆, WANG Zhi-Bin1∆, XIN Ping1, WANG Qiu-Hong2, BU He1, KUANG Hai-Xue1* Chinese Journal of Natural Chinese Journal of Natural Medicines 2018, 16(11): 08110828 Medicines doi: 10.3724/SP.J.1009.2018.00811 Phytochemistry and pharmacology of genus Ephedra ZHANG Ben-Mei1∆, WANG Zhi-Bin1∆, XIN Ping1, WANG Qiu-Hong2, BU He1, KUANG Hai-Xue1* 1 Key Laboratory of Chinese Materia Medica (Ministry of Education), Heilongjiang University of Chinese Medicine, Harbin 150040, China; 2 Department of Natural Medicinal Chemistry, College of Pharmacy, Guangdong Pharmaceutical University, Guangzhou 510000, China Available online 20 Nov., 2018 [ABSTRACT] The genus Ephedra of the Ephedraceae family contains more than 60 species of nonflowering seed plants distributed throughout Asia, America, Europe, and North Africa. These Ephedra species have medicinal, ecological, and economic value. This review aims to summarize the chemical constituents and pharmacological activities of the Ephedra species to unveil opportunities for future research. Comprehensive information on the Ephedra species was collected by electronic search (e.g., GoogleScholar, Pubmed, SciFinder, and Web of Science) and phytochemical books. The chemical compounds isolated from the Ephedra species include alka- loids, flavonoids, tannins, polysaccharides, and others. The in vitro and in vivo pharmacological studies on the crude extracts, fractions and few isolated compounds of Ephedra species showed anti-inflammatory, anticancer, antibacterial, antioxidant, hepatoprotective, anti-obesity, antiviral, and diuretic activities. After chemical and pharmacological profiling, current research is focused on the antibac- terial and antifungal effects of the phenolic acid compounds, the immunosuppressive activity of the polysaccharides, and the antitumor activity of flavonoids. [KEY WORDS] Ephedra; Phytochemistry; Pharmacology [CLC Number] R284.1, R965 [Document code] A [Article ID] 2095-6975(2018)11-0811-18 Introduction used to treat cold, bronchial asthma, cough, fever, flu, head- ache, edema and allergies. E. sinica has become a natural Ephedra is a genus of non-flowering seed plants belong- product source of ephedrine, pseudoephedrine, and other com- [1] ing to the Ephedraceae family , which includes approxi- pounds [3]. In addition, in some western countries, Ephedra mately 67 species, mainly in the desert areas of Asia, America, sinica has been used as a dietary supplement [4]. It can also be Europe and North Africa. Among these species, 15 ones and used to lose weight by increasing sweating and basal metabo- four varieties can be found in China. Ephedra sinica is a lism and by stimulating the central nervous system [5]. More- member of genus Ephedra and is the primary species that has over, it has also been combined with cardiovascular drugs to been used in China for more than 5000 years [2]. treat cardiovascular diseases [6]. Many reports about the side Ephedrae Herba is defined as the stem of Ephedra sinica effects of E. sinica have emerged, especially in western coun- Stapf, Ephedra intermedia Schrenket C. A. Meyer, or Ephedra tries. A number of side effects of over-the-counter drugs con- equisetina Bunge (Ephedraceae) in the Chinese Pharma- taining ephedrine have been reported, such as myocardial copoeia 15th edition. Dried E. sinica stems are traditionally infarction, arrhythmia, epilepsy, loss of consciousness, and death [7]. In 2004, the FDA announced the prohibition of die- [Received on] 28-Dec.-2017 tary supplements containing E. sinica [8]. With the restriction [Research funding] The study was supported by the Major State on the use of E. sinica and its related preparations in the US, Basic Research Development Program (973 Program) of China ( No. other countries have also joined the ban, which has led to 2013CB531800). difficulties in the use and development of ephedra drugs. To [*Corresponding author] Tel: 86-451-87267188, Fax: 86-451-8726- 7188, E-mail: hxkuang@ yahoo.com resolve this problem, novel pharmacological effects of △These authors contributed equally to this work. ephedra should be investigated. In addition to ephedrine al- These authors have no conflict of interest to declare. kaloids, there are other substances in ephedra, such as poly- – 811 – ZHANG Ben-Mei, et al. / Chin J Nat Med, 2018, 16(11): 811828 saccharides, flavonoids (30–71), tannins (72–118), and mis- more than 145 compounds have been isolated and identified cellaneous compounds (119–145). These substances have from the genus Ephedra, including alkaloids, flavonoids, anti-inflammatory, anticancer, antibacterial, antioxidant, and tannins, and polysaccharides. The compounds isolated from hepatoprotective activities. We conducted a systematic review each species are documented in Tables 1–6. Their chemical of the literature to summarize the currently reported chemical structures are shown in Figs. 1–5. constituents and pharmacological activities of Ephedra. Alkaloids Alkaloids are the main components of this genus. Historical and Botanical Characterization of Ephedra Twenty-nine alkaloids, 1–29, were isolated from this genus. E. sinica is one of the original species of the Ephedraceae Structural characteristics of these compounds are listed as family that was recorded in the Chinese Pharmacopoeia as follows: (1) the amphetamine-type alkaloids (6–18) are the “Ma Huang”. As a stimulant and an anti-asthmatic, E. sinica main active ingredients of E. sinica, including amphetamine has a long medicinal history for the treatment of cold, fever, alkaloids of three stereoisomers (6–11). In addition, com- headache, rhinobyon and other symptoms [9]. In the ancient pound 12, structurally similar to ephedrine, is an anti-in- Han Dynasty, E. sinica was recorded as a stimulant and anti- flammatory compound isolated from Ephedra sinica and be- tussive agent. During the time of the Roman Empire, E. sinica longs to the oxazolone derivatives. Compounds 13 and 14 was well known until it was eventually dropped from medie- may also belong to the oxazolidine alkaloid of the structure. val European literature [10]. However, in the beginning of the Compounds 15 and 16, structurally similar to pseudoephed- 20th century, Ephedra sinica emerged as a weight loss and rine and ephedrine, are trace alkaloids in E. sinica. Compound performance enhancement drug and gradually attracted inter- 18 is a new amphetamine-type alkaloid, which is isolated est. However, products containing Ephedra were banned in from the ethanol extract from the E. sinica stem. (2) Ephedri- the US in 2004 after several years of high-profile reports of nes isolated from the E. sinica root are mainly macrocyclic adverse events [11]. spermine alkaloids (1–4) and an imidazole alkaloid (5). (3) In E. sinica plants are perennial herbs standing, more than recent years, five new quinoline alkaloids have been isolated one meter tall, with thin stems, no leaves, and a strong smell from other species of Ephedra (19–23). These quinoline al- of pine and astringency [12]. Furthermore, E. sinica is a kaloids have a carboxyl group on the C-2 position and have drought-tolerant shrub distributed in both temperate and sub- oxygen-containing substitutions on the benzene ring (20, tropical arid environments in the northern hemisphere and 22–23). Generally, these substitutions are methoxyl and hy- South America [13]. droxyl groups. (4) A pyrrolidine alkaloid (24) is isolated from Progress in Phytochemical Studies on the Genus the seeds of E. foeminea and E. foliata. (5) Other alkaloids (25–29) have been isolated from other species of Ephedra. Ephedra The plant sources, names and structures of these alkaloid Until now, phytochemical studies have revealed that compounds are shown in Table 1 and Fig. 1. Table 1 Alkaloids different species of the genus Ephedra (the structures of main compounds are illustrated in Fig. 1) Classification Chemical name Plant source Ref. Macrocyclic spermine alkaloids Ephedradine A (1) E. sinica (root) [26] Ephedradine B (2) E. sinica (root) [27] Ephedradine C (3) E. sinica (root) [27] Ephedradine D (4) E. sinica (root) [28] Imidazole alkaloid Feruloylhistamine (5) E. sinica (root) [29] Amphetamine-type alkaloids D(–)-Ephedrine (6) E. Sinica, E. nebrodensis, E. major [30-32] L(+)-Pseudoephedrine (7) E. sinica, E. nebrodensis [31, 33] D(–)Norephedrine (8) E. sinica, E. nebrodensis [31, 33] L(+)-Noreseudoephedrine (9) E. sinica [31, 33] D(–)Methylephedrine (10) E. sinica, E. nebrodensis [31, 33] L(+)-Methylpseudoephedrine (11) E. sinica, E. nebrodensis [31, 33] Ephedroxane (12) E. sinica [34-35] 3, 4-Dimethyl-5-pheyloxazolidine (13) E. sinica [17, 35] 2, 3, 4-Trimethyl-5-phenyloxazolidine (14) E. sinica [17, 35] O-benzoyl-L(+)-pseudoephedrine (15) E. sinica [35-36] O-benzoyl-D(–)-ephedrine (16) E. sinica [35-36] Hordenine (17) E. aphylla [35, 37] (S)-N-((1R, 2S)-1-hydroxy-1-phenylpropan-2-yl)-5- E. sinica [35, 38] oxopyrrolidine-2-carboxamide (18) – 812 – ZHANG Ben-Mei, et al. / Chin J Nat Med, 2018, 16(11): 811828 Continued Classification Chemicla name Plant source Ref. Quinoline alkaloids Transtorine (19) E. transitoria [39] 6-Methoxykynurenic acid (20) E. pachyclada ssp. sinaica [40] Kynurenic acid (21) E. pachyclada ssp. sinaica [40] 6-Hydroxykynurenic acids (22) E. foeminea ssp. foliata [40] Ephedralone (23) E. Alata, E. aphylla [41-42] Pyrrolidine alkaloid cis-3, 4-Methanoproline (24) E. foeminea ssp. foliate (seed) [43] Other alkaloids Maokonine (25) E. sinica (root) [44] (±)-1-Phenyl-2-imido-1-propanol (26) E. sinica [45] Tetramethylpyrazine (27) E. sinica [46] N-methybenzlamine (28) E. sinica [47] (2S, 3S, 4S)-2-(carboxycyclopropyl)glycine
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