Research Progress on the Efficacy and Chemical Components of Medicinal Taxillus chinensis (DC.) Dans

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  Abstract Taxillus chinensis (DC.) Danser is a traditional Chinese medicine, which has the effects of nourishing the liver and kidney and strengthening the bones and muscles. Its properties and efficacy were recorded in many ancient Chinese herbal medicine books and modern books. In addition, other parasitic plants of the Loranthaceae family also have the effects of promoting blood circulation, checking diarrhea, and resisting tumor to treat various diseases. This paper reviewed recent scholars’ research on the efficacy and chemical composition of medicinal Loranthaceae plants, and expounded the similarities and differences between T. chinensis and other medicinal Loranthaceae plants.
  Key words Taxillus chinensis (DC.) Danser; Importance; Chemical composition; Efficacy
  
  Received: July 27, 2020  Accepted: September 30, 2020
  Supported by Subproject of Guangxi Key Laboratory of Zhuang and Yao Medicines (GXZYZZ2020A-03); Collaborative Innovation Center for Zhuang and Yao Medicines (GJKY[2013]20); Guangxi Key Laboratory of Zhuang and Yao Medicines (GJKZ[2014]32); Guangxi Zhuang Medicine Quality Standard (Volume 3) Quality Evaluation and Standard Research Project (GXZC2014-G3-1577-YLZB-B-3).
  Yuan LIANG (1996-), male, P. R. China, master, devoted to research about quality control of traditional Chinese medicine.
  * Corresponding author. E-mail: 136067251@qq.com.
   Taxillus chinensis (DC.) Danser (Sangjisheng) is a commonly used Chinese medicine in China, as well as a common medicinal material used in the Loranthaceae family. It was first recorded in Shen Nong’s Materia Medica, and in many herbal works such as Classified Materia Medica, Xinxiu Bencao (Newly-revised Materia Medica), Compendium of Materia Medica, Bencaojing Kaozhu and Chinese Materia Medica after that. The 1977 edition of Chinese Pharmacopoeia included it as dry stems and branches with leaves of Loranthus parasiticus (L.) Merr.[1], and its Latin name was changed in the 1985 edition to T. chinensis (DC.) Danser[2], which is also used in the 2015 edition of Chinese Pharmacopoeia[3], and the botanical name in Flora of China is Taxillus chinensis (DC.) Danser (Guangjisheng). Compendium of Materia Medica recorded that "T. chinensis is bitter in taste, neutral in nature and non-toxic. It mainly treats lumbago, strong back carbuncle in children, and has the effects of smoothing the skin, strengthening teeth, promoting growth of beard and eyebrows, and preventing miscarriage". Modern studies have found that it has the effects of dispelling rheumatism, invigorating the liver and kidney, strengthening muscles and bones, and preventing miscarriage, and is used for treating rheumatic arthritis, waist and knee weakness, muscle and bone weakness, metrorrhagia, bleeding during pregnancy, threatened abortion, dizziness and so on.   Vhcum coloratum (Komar.) Nakai (Hujisheng) is also a commonly used traditional Chinese medicine in the Loranthaceae family. It was included in the 1977 edition of Chinese Pharmacopoeia as the dry stems and branches with leaves of V. coloratum (Komar.) Nakai[1], which also has the effects of dispelling wind-damp, nourishing liver and kidney, strengthening muscles and bones, and preventing miscarriage. In addition to T. chinensis and V. coloratum included in Chinese Pharmacopoeia, many ancient and modern Chinese herbal medicine works described the source, traits, meridian tropisms, and efficacy of medicinal parasitic plants. However, there is no specific description of other parasitic plants in Chinese Pharmacopoeia from the 1977 edition to the 2015 edition.
  Loranthaceae plants belong to the semi-parasitic plant. They have leaves and stems, and their nutrients coming from the host’s supply and photosynthesis make them grow rapidly[4]. China has a wide range of plant resources in the Loranthaceae family. There are many varieties under natural distribution, such as T. chinensis, V. coloratum, and Scurrula parasitica L., which have a long history of medicinal use and high medicinal value. Current research has found that T. chinensis also has the effect of scavenging oxygen free radicals to delay aging[5-6]. Meanwhile, T. chinensis and other parasitic plants are often referred to as parasitic tea. They are used as raw materials for making tea in China, Africa, Germany and other parts of Europe, and have been found to have certain blood pressure towering[7-8], anti-oxidation, and blood lipid-lowering effects[9]. T. chinensis is commonly used to treat tumors and other diseases in Indonesia and other regions[10-11].
  Documentary Records
  T. chinensis and other medicinal parasitic plants are spread and reproduced by birds eating T. chinensis fruits and attaching the seeds to the branches through bird excrement. Unlike other parasitic plants, when encountering an environment with appropriate temperature and humidity, T. chinensis can quickly develop and grow[12]. For example, Compendium of Materia Medica[13] described "Many trees have thereon parasitic plants, which have similar stems and leaves. Birds eat their fruit and dung on the trees, and the seeds grow into plants in contact with air”. In this way, T. chinensis grows on many trees (such as mulberry, pine, maple, Phellodendron sinii, etc.). Classified Materia Medica[14] recorded that “T. chinensis can grow on Quercus dentata Thunb., beech, willow, Salix sinopurpurea, maple, etc., but only that on mulberry is suitable for use. However, it is very difficult to distinguish, and doctors dare not use it unless they collect it themselves. Or the stems can be broken to observe their color, deep-yellow ones with sticky juice are regarded as true”. The ancients noticed that the effects of parasitic plants on different hosts are different, and believed that only those on mulberry are available.   In the long-term medicinal use and observation of Loranthaceae plants, the ancients discovered that the Loranthaceae plants have different traits and appearances on trees. Bencaojing Kaozhu[15] described that “the case, which looks like ephedra and is called Songyelan, is a Loranthaceae plant”. Zhongling said “The parasitic plants in the West have leaves like Elaeagnus leaves and yellow and ripe autumn fruits like raspberries, and are quite different from those born on the hackberry in the East”. Modern research has found that there are many parasitic plants in the Loranthaceae family, some of which are commonly used as medicinal products, such as T. chinensis, Scurrula parasitica L., V. coloratum, Tolypanthus maclurei (Merr.) Danser, etc. For example, Chinese Materia Medica[16], Guangxi Yaoyongzhiwu Minglu (Guangxi Medicinal Plant List)[17] published in 1986 included and described the nature, flavor and efficacy of many different parasitic medicinal materials of the Loranthaceae family, as shown in Table 1.
  Chinese Materia Medica recorded 21 parasitic plants in 9 genera under the Loranthaceae family (Dendrophthoe, Helixanthera, Korthalsella, Loranthus, Macrosolen, Scurrula, Taxillus, Tolypanthus, Viscum), which are different in nature, meridian tropism and efficacy. Most parasitic drugs are bitter in taste and neutral in nature, and have the effects of dispelling wind-damp and nourishing liver and kidney. However, there are differences in the efficacy of some parasitic plants. For example, in addition to dispelling wind-damp and nourishing liver and kidney, Korthalsella japonica, Macrosolen cochinchinensis and Scurrula parasitica also have the effect of activating blood and relieving pain; Dendrophthoe pentandra and Helixanthera parasitica have the effect of curing dysentery; Viscum album L. subsp. meridianum has the effect of promoting lactation; and T. thibetensis has the effects of clearing away the lung-heat and promoting urination that other parasitic plants do not have. Meanwhile, the differences in the efficacy of V. ovalifolium and T. chinensis were also described in Shengcao Yaoxing Beiyao[18]. In the folk, V. ovalifolium is mostly used to treat joint disadvantages caused by wind, cold and dampness, and relieve cough, while T. chinensis is mostly used to treat weakened muscles and bones, waist and knee pain caused by liver and kidney deficiency and blood deficiency. It shows that the effects of different parasitic plants are not exactly the same, and there are different effects and applications for parasitic plants.   Chemical Components
  According to literature reports, parasitic medicinal materials such as T. chinensis are rich in flavonoids, alkaloids, terpenoids, organic acids, polysaccharides, proteins and other compounds. Modern studies have shown that flavonoids can enhance the body’s ability to resist self-oxidation and scavenge free radicals[19], and can effectively reduce blood lipids and cholesterol, relax blood vessels and improve blood vessel permeability. Most alkaloids have the effects of anti-bacterial and anti-inflammatory effects. The terpenoids can dispelling wind, expelling parasites, and reliving pain. The organic acids, polysaccharides and proteins can participate in the body’s metabolism, immunity and other activities to resist aging and improve blood circulation[19]. These components are closely related to the efficacy of parasitic plants. The research on parasitic plants under the Loranthaceae family has been carried out around these chemical components (see Table 2 for the results). However, because of the characteristics of parasitic plants, the influences of host plants on the quality of T. chinensis medicinal material cannot be completely ignored, and the results should be treated dialectically.
  Flavonoids and glycosides
  Flavonoid compounds[19] refer to a class of compounds with the basic structure of 2-phenylchromone. They are often bonded with sugars to form various glycosides, which are widely found in various plants in nature, playing an important role in growth, maturation, reproduction, sterilization and other aspects. Meanwhile, they are the basis of the efficacy of some Chinese medicines. Modern research believes that the efficacy of T. chinensis and V. coloratum is based on many flavonoids in the plants for nourishing the liver, kidney and strengthening the bones and muscles[20]. Therefore, the relevant research on the flavonoids of these parasitic plant is abundant. Current research has found that they contain flavonoids such as avicularin, rutin, quercitrin, quercetin and a small amount of catechol[21].
  Macrosolen cochinchinensis (Lour.) Van Tiegh. is a plant in Macrosolen of Loranthaceae, which often called M. cochinchinensis in the folk, which has the effects of clearing heat, relieving cough and lowering blood pressure. Its flavonoids are similar to T. chinensis, and it also contain quercitrin, quercetin, gallic acid, orientin and other ingredients[22]. In recent years, some scholars have also discovered through thin layer and high performance liquid chromatography studies that M. cochinchinensis contains flavonoids such as astilbin, rutin and orientin[23-25].   H. parasitica Lour. is a plant of the genus Helixanthera of the Loranthaceae family. It was recorded in Guangxi Medicinal Plants List[17] as Wubanjisheng and to contain quercetin, gallic acid and other ingredients[26]. Qin et al.[27] compared T. chinensis, M. cochinchinensis, and H. parasitica, and determined the contents of total flavonoids in the three plants. It was found that H. parasitica on the same host had the highest content. Meanwhile, the investigation on the three parasitic plants collected in different seasons found that the total flavonoid content of M. cochinchinensis and H. parasitica were the most obvious with seasonal changes, and the total flavonoid content of T. chinensis mainly concentrated in the three months of February, August and October.
  Yang et al.[28] found that V. liquidambaricolum Hayata contains flavonoids such as chrysin, eriodictyol, and liquidambar viscum, as well as trans-cinnamic acid and oleanolic acid.
  
   Scholars studied the anti-HIV activity of V. album L. var. meridianum in vitro. They extracted the plant and discovered that it contains 3′,4′-dimethoxy taxifolin, 3,5,7,4′-tetrahydroxy-3′-methoxyflavanone, eriodictyol, naringenin, homoeriodictyol, homoeriodictyol-7-O-β-D-glucopyranoside, 5,4′-dihydroxyflavanone-7-O-β-D-glucopyranoside, quercetin-3-O-α-L-rhamnoside, and 5,7-dihydroxychromone. They also found that V. album L. var. meridianum also contains (+)-pinoresinol, 1,7-bis(4-hydroxyphenyl)-3-heptanol and acer lignin[29].
  In addition, some scholars have discovered that T. levinei (Merr.) H. S. Kiu contains protocatechuic acid, isoquercitrin, quercetin 3-O-(6″-galloyl)-β-D-glucopyranoside, and quercetin 3-O-β-D-glucuronide[30-31], and T. thibetensis (Lecomte) Danser contains flavonoids such as quercitrin, avicularin and quercetin[32].
  Scurrula parasitica L.[33-34] have been studied for related chemical components from an early stage, and found to contain quercitrin, quercetin, rutin[35] and other flavonoids, and it also contains lipids and polysaccharides. The flavonoids contained in the S. parasitica are similar to those in T. chinensis in composition, and the two have close maximum absorption wavelengths under ultraviolet absorption[36]. Li et al.[37] used ethanol extraction and ultraviolet spectrophotometry to determine the flavonoid contents of T. chinensis and S. parasitica on a variety of trees (mulberry, chestnut rree, oleander, etc.). They found that the contents of total flavonoids contained in T. chinensis and S. parasitica on the same host were quite different, and the total flavonoids contained in the two parasitic plants differ by more than 20 mg/g, and were the highest in leaves. Modern research has found that V. ovalifolium Wall. et DC. contains different main components from T. chinensis[38]. V. ovalifolium contains more triterpene saponins, and when using ultraviolet spectrophotometry to determine the total flavonoid contents of T. chinensis and V. ovalifolium on grapefruit trees, it was found that the total flavonoid contents of T. chinensis and V. ovalifolium were, respectively, 8.47% and 2.98%, which were quite different and had a ratio of approximately 2.84∶1[39].   Modern research has also extracted rhamnazin-3-O-β-D-apiose (1→2)-O-β-D-glucoside [40], 4′-dihydroxy-5,3′-dimethoxydihydroflavone, 5,7,3′,4′-tetraoxydihydroflavone, naringenin-7-O-β-D-glucoside, naringenin, and pinocembrin[41-42], and 4′-o-acetyl quercitrin  was extracted from S. ferruginea Danser[43].
  Terpenoids
  Both oleanolic acid and ursolic acid belong to pentacyclic triterpenoids[19], which have certain anti-inflammatory effects. In addition, oleanolic acid has diuretic, heart-strengthening and anti-arrhythmic effects, while ursolic acid is often used as a broad-spectrum antibacterial agent to treat acute hepatitis and other diseases.
  Zhu et al.[44] used ethanol extraction and HPLC methods to analyze T. chinensis and V. ovalifolium on different trees (persimmon, loquat, and pomegranate), and used methanol, acetonitrile and 0.05% ammonium acetate solution to carry out elution separation test. It was found that on the same host, oleanolic acid and ursolic acid were not detected in T. chinensis, but oleanolic acid was detected in V. ovalifolium. In addition, V. ovalifolium also contains lupeol acetate, β-sitosterol, lupeol palmitate and other chemical components[45]. Studies on S. parasitica found that it contains 3β,15α-dihydroxy-lupin-20(29)-ene, 3-epi ursolic acid, and lupin-20(29)- ene-3-O-α-D-glucoside and other triterpenoids[46]. V. coloratum also contains β-amyranol, β-sitosterol, β-acety-lamyranol, lupeol, betulinic acid, daucosterol, β-amyrin plamitate, amyrandiol, and eleutheroside E and other ingredients[47-48]. Liu et al.[29] found through research that V. album L. var. meridianum also contains lupeol, betulinic acid, betulinol, oleanolic acid and daucossterol. There are also triterpenoids such as lupeol in M. cochinchinensis[49].
  Cardiac glycosides
  Cardiac glycosides are a class of drugs that selectively act on the heart and strengthen myocardial contractility. Clinically, it is mainly used to treat cardiac insufficiency. Improper use of cardiac glycosides can cause headaches, dizziness, ventricular premature beats, ventricular tachycardia, atrioventricular block and other side effects. Therefore, medicinal materials containing cardiac glycosides should be used carefully. The 2015 edition of Chinese Pharmacopoeia points out that no cardiac glycoside compounds should be detected in T. chinensis medicinal materials[3]. Chai et al.[50] used UPLC-Q-TOF-MS/MS (ultra performance liquid chromatography-time-of-flight mass spectrometry) to analyze the cardiac glycosides in the S. parasitica grown on oleander and found the parasitic plant contained a variety of cardiac glycosides. Meanwhile, compared with the cardiotonic effect of T. chinensis grown on the same host[51], it was found that the cardiotonic effect of S. parasitica was significantly stronger than that of T. chinensis, so when using S. parasitica as a medicine, attention should be paid to the influence of its host on the plant. In the follow-up, it is necessary to further study the components and efficacy of cardiac glycosides in S. parasitica with oleander as the host to determine its toxicological mechanism and whether there is a certain potential for efficacy.   Alkaloids
  Alkaloids are a type of nitrogen-containing alkaline organic compounds. Although the content of alkaloids in plants is small, they are closely related to humans. It has long been recognized that some plants or crude extracts containing alkaloids can treat diseases or be used as poison[19]. Su et al.[52] used methanol-hydrochloric acid ultrasound and RP-HPLC technology with water: acetonitrile:phosphoric acid:triethylamine salt as a mobile phase for elution and separation to determine the berberine hydrochloride content in T. chinensis on P. sinii. It was found that the content of berberine hydrochloride in T. chinensis collected in Guangxi area was as high as 7.58 mg/g.
  Lignans
  Lignans are a type of natural compounds formed by polymerization of two molecules of phenylpropanoid derivatives. They have the function of scavenging free radicals in the body and resisting oxidation. Wang et al.[53] studied V. coloratum in many places and found that the parasitic plant contained lignan type syringaresinol. Among the collected materials, V. coloratum from Dongsheng in Shandong had the highest content of 348.0 mg/L, and that collected in Tangshan had the lowest content of 17.4 mg/L. Liu et al.[29] found that V. album L. var. meridianum also contains lignans such as (-)-syringaresinol and caruilignan D.
  Others
  In addition, the research on the medicinal plants of T. chinensis has also found many chemical components with clear structure, which can promote human health (such as anti-tumor) or help to explore the characteristics of parasitic plants.
  Qin et al.[54] studied the total vitamin C contained in H. parasitica, M. cochinchinensis, and T. chinensis (the hosts of which were peach trees and oleander trees) by ultraviolet spectrophotometry and 2,4-dinitrophenylhydrazine method, and found that the three parasitic medicinal materials were rich in vitamin C and there were also differences in the vitamin C content between the three parasitic plants. Zhang et al.[55] used UPLC/MS/MS with acetonitrile-formic acid water as a mobile phase combined with electrospray ionization mass spectrometry in positive mode to detect V. coloratum, and found that V. coloratum contains the antitumor compound 1,7-bis (4-hydroxyphenyl) -1,4-heptadien-3-one. Through the research on the component, it was found that the host had no obvious influence on the component but there was a certain connection with the place of origin as the level of the component was different between different places of origin. Their study can provide important reference for the development of V. coloratum in the field of anti-tumor. V. coloratum also contains meso-inositol, syringin-O-β-D-api (1→2) glucoside, 2,3-butanediol monoglucoside, syringin, caffeic acid, palmitic acid, ferulic acid, succinic acid, protocatechuic acid, tetracosanoic acid to octacosanoic acid and other ingredients[47-48].   Related scholars have also studied M. cochinchinensis and found that it contains 3,3-di-o-methyl ellagic, ellagic acid cycloeucalyptol, epichlorohydrin, (23Z) -9,19- cycloart-23-ene-3α,25-diol, friedelin, 1-dotriacontanol, β-sitosterol, dotriacontanoic acid and other ingredients[25,49].
  Liu et al.[46] obtained 7β-hydroxy-hop-22(29)-en-3β-palmitate, uvaol and 3β-hydroxy-hop-22(29)-en, and  stigmasterol-3-O-β-D-glycopyranoside through the study of S. parasitica. Wang et al.[56] conducted microwave digestion of T. chinensis and V. coloratum, and used flame atomic absorption spectrometry to detect mineral elements. It was found that the mineral elements contained in the two parasitic plants were at an overall high level, such as K, Mg, Ca and Zn.
   Through the above-mentioned research, it can be found that most of the plants in the Loranthaceae family contain flavonoids such as rutin, quercetin and its glycosides and terpenoids such as oleanolic acid and lupeol, as well as other components such as alkanol and carboxylic acid. However, as the research progressed, it was found that the components contained in the parasitic plants were different from each other. For example, studies have found that most parasitic plants contain oleanolic acid, while T. chinensis does not detect to contain this component; V. ovalifolium has a higher level of terpenoids compared with other parasitic plants; V. album L. var. meridianum also contain eriodictyol and homoeriodictyol; V. coloratum contains palmitic acid, protocatechuic acid, succinic acid, ferulic acid, caffeic acid, and rhamnazine and its glycosides; and V. liquidambaricolum contains liquidambar viscum, trans-cinnamic acid and other components. That is to say, the chemical components contained in different parasitic plants are not the same. Due to the similarities and differences in the chemical components contained in different parasitic plants, there may be similarities and differences in the efficacy of different parasitic plants. The above-mentioned parasitic plants (T. chinensis, V. coloratum, S. parasitica, V. album L. var. meridianum (V. album), M. cochinchinensis) were described in Chinese Materia Medica as having a certain effect of dispelling wind-damp and nourishing liver and kidney, but V. album L. var. meridianum also has the effect of promoting lactation in addition to dispelling wind-damp. In addition to the above-mentioned parasitic plants, there are still many medicinal plants in the Loranthaceae family, but for many parasitic plants, few studies have been conducted on their chemical composition. H. parasitica, T. levinei and T. thibetensis are only studied to contain flavonoids, and there have been no reports on further excavation of other components.   [30] LI LQ, LI MR, ZHU AJ. Studies on the chemical constituents of Taxillus levinei (Merr.) H.S.KIU.[J]. China Journal of Chinese Materia Medica,1996(1):34-35, 63-64. (in Chinese)
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  Editor: Yingzhi GUANG  Proofreader: Xinxiu ZHU
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