Pharmacological and Antioxidant Activities of Rhus Coriaria L. (Sumac)

antioxidants Review Pharmacological and Antioxidant Activities of Rhus coriaria L. (Sumac) Halima Alsamri 1, Khawlah Athamneh 1,2, Gianfranco Pintus 3,4 , Ali H. Eid 5,6 and Rabah Iratni 1,* 1 Department of Biology, College of Science, United Arab Emirates University, Al-Ain 15551, UAE; [email protected] (H.A.); [email protected] (K.A.) 2 Department of Chemistry, College of Arts and Sciences, Khalifa University, Abu Dhabi 127788, UAE 3 Department of Medical Laboratory Sciences, College of Health Sciences, University of Sharjah, Sharjah 27272, UAE; [email protected] 4 Department of Biomedical Sciences, University of Sassari, Viale San Pietro 43, 07100 Sassari, Italy 5 Department of Basic Medical Sciences, College of Medicine, QU Health, Qatar University, Doha 2713, Qatar; [email protected] 6 Biomedical and Pharmaceutical Research Unit, QU Health, Qatar University, Doha 2713, Qatar * Correspondence: [email protected]; Tel.: +971-3-713-6526; Fax: +971-3-7134-927 Abstract: Rhus coriaria L. (Anacardiaceae), commonly known as sumac, is a commonly used spice, condiment, and flavoring agent, especially in the Mediterranean region. Owing to its bountiful beneficial values, sumac has been used in traditional medicine for the management and treatment of many ailments including hemorrhoids, wound healing, diarrhea, ulcer, and eye inflammation. This plant is rich in various classes of phytochemicals including flavonoids, tannins, polyphenolic compounds, organic acids, and many others. By virtue of its bioactive, Rhus coriaria possesses power- ful antioxidant capacities that have ameliorative and therapeutic benefits for many common diseases including cardiovascular disease, diabetes, and cancer. This review describes the phytochemical properties of R. coriaria and then focuses on the potent antioxidant capacities of sumac. We then dissect the cellular and molecular mechanisms of sumac’s action in modulating many pathophysio- logical instigators. We show how accumulating evidence supports the antibacterial, antinociceptive, antidiabetic, cardioprotective, neuroprotective, and anticancer effects of this plant, especially that Citation: Alsamri, H.; Athamneh, K.; toxicity studies show that sumac is very safe to consume by humans and has little toxicity. Taken Pintus, G.; Eid, A.H.; Iratni, R. together, the findings we summarize here support the utilization of this plant as an attractive target Pharmacological and Antioxidant for drug discovery. Activities of Rhus coriaria L. (Sumac). Antioxidants 2021, 10, 73. https:// Keywords: Rhus coriaria; phytochemical; antioxidant; anticancer; antimicrobial doi.org/10.3390/antiox10010073 Received: 22 November 2020 Accepted: 5 January 2021 Published: 8 January 2021 1. Introduction Rhus coriaria L., commonly known as sumac, is a Mediterranean plant that belongs Publisher’s Note: MDPI stays neu- to the Anacardiaceae family and is traditionally used as a spice and flavoring agent [1]. tral with regard to jurisdictional clai- It grows as a shrub with a height range of 3–4 m and has pinnate leaves arranged in pairs ms in published maps and institutio- of 6 or 8 small leaflets, with a cluster of white flowers at terminal inflorescences (Figure1A). nal affiliations. The fruits are spherical and become reddish drupe when ripe (Figure1B) [ 2]. Dried fruits, reduced to a dark red powder, with an acidic and astringent taste is often used as spice in several Mediterranean and Middle Eastern countries such as Lebanon, Syria, Jordan, Turkey, and Iran [3]. For example, powdered sumac is often directly added to salad or Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. offered along with minced meat to add lemony taste. In some countries like Lebanon and This article is an open access article Syria, powdered sumac is sometimes used in the composition of zaatar, a mixture of herbs distributed under the terms and con- and spices in infusion or as a replacement for capers and red pepper. At the industrial level, ditions of the Creative Commons At- Sumac leaves and bark, which contain large amounts of tannins, were used for centuries in tribution (CC BY) license (https:// tanning fine leather [4]. In addition to its use as a culinary herb and tanning agent, Rhus creativecommons.org/licenses/by/ coriaria has been used in Middle Eastern and South Asian countries, for thousands of years, 4.0/). as a traditional medicine for the treatment of several diseases including cancer [5–7]. Sumac Antioxidants 2021, 10, 73. https://doi.org/10.3390/antiox10010073 https://www.mdpi.com/journal/antioxidants Antioxidants 2021, 10, x FOR PEER REVIEW 2 of 28 Antioxidants 2021, 10, 73 agent, Rhus coriaria has been used in Middle Eastern and South Asian countries, for thou-2 of 27 sands of years, as a traditional medicine for the treatment of several diseases including cancer [5–7]. Sumac fruits were used in folks medicine to treat several illnesses that in- cludefruits liver were disease used in [8], folks diarrhea medicine [8–10], to treat urinary several system illnesses issues that [8], includeand ulcers liver [11]. disease In addi- [8], tion,diarrhea the powdered [8–10], urinary fruits system were also issues used [8], to and stimulate ulcers [perspiration11]. In addition, and the reduce powdered cholesterol fruits [10].were The also many used totherapeutic stimulate perspirationeffects of Rhus and coriaria reduce could cholesterol be attributed [10]. The to many its various therapeutic bio- logicaleffects properties of Rhus coriaria such ascould antioxidant, be attributed anti-inflammatory, to its various hypoglycemic, biological properties hypolipidemic such as activitiesantioxidant, [2]. anti-inflammatory,As of today, over 200 hypoglycemic, phytochemicals hypolipidemic were isolated activities from Rhus [2]. coriaria As of today, and theseover 200include phytochemicals organic acids, were phenolic isolated acids, from phenolicRhus coriaria compoundsand these conjugated include organic with malic acids, acidphenolic derivatives, acids, phenolic flavonoids, compounds isoflavonoids, conjugated hydrolysable with malic tannins, acid derivatives, anthocyanins, flavonoids, terpenoids,isoflavonoids, and other hydrolysable compounds tannins, such as anthocyanins, butein, iridoid, terpenoids, and coumarin and other derivatives. compounds This such re- viewas butein, aims iridoid,to provide and a coumarincomprehensive derivatives. overview This of review the phytochemical aims to provide and a comprehensivepharmacolog- icaloverview studies of published the phytochemical on Rhus coriaria and pharmacological. studies published on Rhus coriaria. FigureFigure 1. 1. ((AA)) RhusRhus coriaria coriaria plantplant and and ( (BB)) RhusRhus coriaria coriaria fruit.fruit. 2. General Composition and Minerals and Vitamins Contents of Rhus coriaria 2. General Composition and Minerals and Vitamins Contents of Rhus coriaria The overall composition of the dried sumac fruit is mainly composed of moisture (6– The overall composition of the dried sumac fruit is mainly composed of moisture 11.8%), essential oil content (1.0%), protein (2.3–2.6%), fiber (14.6–22.15%), ash (1.5– (6–11.8%), essential oil content (1.0%), protein (2.3–2.6%), fiber (14.6–22.15%), ash (1.5–2.66%), 2.66%),and water-soluble and water-soluble extract extract (63.8%) (63.8%) and fatty and oil fatty (17.4%) oil (17.4%) [12]. The [12]. mineral The mineral composition composi- of tionsumac of sumac fruits, determinedfruits, determined usinginductively using induct coupledively coupled plasma plasma atomic atomic emission emission spectrometer spectrometer(ICP-AES), (ICP-AES), showed thatshowed K, Ca, that Mg, K, Ca, P, Fe, Mg, Na, P, Zn, Fe, Mn,Na, Cu,Zn, Mn, and AlCu, are and the Al predominant are the pre- dominantelements [elements13–15]. It [13–15]. is worth It mentioningis worth mentioning that mineral that contentsmineral contents were found were to found be affected to be affectedby environmental by environmental factors and factors the geographic and the geog locationsraphic where locations sumac where fruits sumac were collected fruits were [16]. collectedAs for the [16]. vitamin As for content, the vitamin sumac fruitcontent, contained sumac thiamine, fruit contained riboflavin, thiamine, pyridoxine, riboflavin, cyanocobal- pyr- idoxine,amin, nicotinamide, cyanocobalamin, biotin, nicotinamide, and ascorbic acidbiotin, [16 ].and ascorbic acid [16]. 3.3. Phytochemical Phytochemical Constituents Constituents of of RhusRhus coriaria coriaria ExtractExtract RhusRhus coriaria coriaria isis rather rather rich rich in in many many phytochemical phytochemical compounds. compounds. One One of ofthe the earliest earli- studiesest studies carried carried out in out 1896 in 1896identified identified myricetin myricetin and gallic and gallicacid as acid components as components of the ofleave the extractleave extract [14]. Since [14]. then, Since many then, other many components other components were identified were identified in different in different parts of parts su- macof sumac (Table (Table 1). More1). recently, More recently, a most a comprehensive most comprehensive study investigating study investigating the phytochemi- the phy- caltochemical composition composition of the fruit of theextract fruit identified extract identified 211 phytoconstituents 211 phytoconstituents including including tannins, (iso)flavonoids,tannins, (iso)flavonoids, terpenoids, terpenoids, anthocyanins, anthocyanins, and many and others. many Importantly, others. Importantly, 180 of the

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