Chemical Structure and Biological Activities of Secondary Metabolites from Salicornia Europaea L

molecules Review Chemical Structure and Biological Activities of Secondary Metabolites from Salicornia europaea L. Sojeong Kim 1, Eun-Young Lee 2, Prima F. Hillman 2, Jaeyoung Ko 3 , Inho Yang 4,* and Sang-Jip Nam 2,* 1 Graduate School of Industrial Pharmaceutical Sciences, Ewha Womans University, Seoul 03760, Korea; [email protected] 2 Department of Chemistry and Nanoscience, Ewha Womans University, Seoul 03760, Korea; [email protected] (E.-Y.L.); primafi[email protected] (P.F.H.) 3 AMOREPACIFIC Research and Development Center, Yongin 17074, Korea; jaeyoungko@amorepacific.com 4 Department of Convergence Study on the Ocean Science and Technology, Korea Maritime and Ocean University, Busan 49112, Korea * Correspondence: [email protected] (I.Y.); [email protected] (S.-J.N.); Tel.: +82-51-410-5398 (I.Y.); +82-23-277-6805 (S.-J.N.) Abstract: Salicornia europaea L. is a halophyte that grows in salt marshes and muddy seashores, which is widely used both as traditional medicine and as an edible vegetable. This salt-tolerant plant is a source of diverse secondary metabolites with several therapeutic properties, including antioxidant, antidiabetic, cytotoxic, anti-inflammatory, and anti-obesity effects. Therefore, this review summarizes the chemical structure and biological activities of secondary metabolites isolated from Salicornia europaea L. Keywords: Salicornia europaea L.; halophyte; phytochemicals; secondary metabolites Citation: Kim, S.; Lee, E.-Y.; Hillman, P.F.; Ko, J.; Yang, I.; Nam, S.-J. Chemical Structure and Biological 1. Introduction Activities of Secondary Metabolites Salicornia europaea L., also known as Salicornia herbacea L., is a halophyte belonging to from Salicornia europaea L. Molecules the Chenopodiaceae subfamily with many common names including glasswort, sea beans, 2021, 26, 2252. https://doi.org/ sea asparagus, and samphire [1]. As implied by its names, this edible plant tolerates up to 10.3390/molecules26082252 3% salinity [2] and grows in salt marshes and muddy seashores in temperate and subtropi- cal regions worldwide, including the western and southern coasts of Korea [3]. In Asia, Academic Editor: Yasuyoshi Miyata S. europaea has been traditionally used as a traditional medicine for constipation, nephropa- thy, hepatitis, diarrhea, obesity, and diabetes, among other disorders [4,5]. Moreover, in Received: 21 March 2021 addition to using S. europaea for glass making, its aerial parts are used in salads, pickles, Accepted: 10 April 2021 Published: 13 April 2021 fermented food, and salt substitutes [6,7]. Therefore, due to the many health benefits of S. europaea, several studies proposed the development of this halophyte as a functional S. europaea Publisher’s Note: MDPI stays neutral food and medicinal plant. Importantly, crude extracts reportedly possess several with regard to jurisdictional claims in therapeutic properties. For instance, the presence of immunomodulatory compounds in published maps and institutional affil- crude extracts was demonstrated via RAW 264.7 macrophage cell line assays [8]. Moreover, iations. the antioxidant activity of S. europaea was measured via the 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging, hydroxyl radical scavenging, and reactive oxygen species (ROS) generation assays [9]. The antihyperglycemic and antihyperlipidemic activities of this plant were also demonstrated in mice fed with a high-fat diet [10] and another study reported that a polysaccharide extract from this plant exhibited anti-inflammatory activity Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. in vitro and in vivo [11]. This article is an open access article In addition to the many studies that have characterized the bioactivity of crude S. eu- distributed under the terms and ropaea extracts or individual fractions, many bioactive secondary metabolites have been iso- conditions of the Creative Commons lated from this plant. Therefore, this review sought to systematically classify the secondary Attribution (CC BY) license (https:// metabolites isolated from S. europaea according to their chemistry and summarize their creativecommons.org/licenses/by/ biological activities. Most of the biological activities of the secondary metabolites discussed 4.0/). herein were taken from separate studies. Many studies generally classify glasswort-like Molecules 2021, 26, 2252. https://doi.org/10.3390/molecules26082252 https://www.mdpi.com/journal/molecules Molecules 2021, 26, 2252 2 of 26 Molecules 2021, 26, 2252 2 of 26 discussed herein were taken from separate studies. Many studies generally classify glasswort-like species as S. europaea due to the difficulties of taxonomic identification of the genusspecies Salicornia. as S. europaea Therefore,due to it theis worth difficulties noting of that taxonomic this manuscript identification is by no of themeans genus a com-Sal- prehensiveicornia. Therefore, review itof is all worth S. europaea noting studies, that this and manuscript instead focuses is by no on means representative a comprehensive examples.review of all S. europaea studies, and instead focuses on representative examples. 2. Oleanane Oleanane Triterpenoid Triterpenoid Saponins Triterpenoid saponins saponins are are abundant abundant in in plants plants and and possess possess a variety a variety of biological of biological activities,activities, including including antifungal, antifungal, antiviral, antiviral, antiox antioxidant,idant, antiglycation, antiglycation, and and anticancer anticancer proper- prop- tieserties [12–15]. [12–15 More]. More than than twenty twenty oleanane-t oleanane-typeype triterpenoid triterpenoid saponins, saponins, including including 30-noro- 30- leananenoroleanane triterpenoid triterpenoid saponins, saponins, have haveso far so been far beenisolated isolated from from S. europaeaS. europaea (Figure(Figure 1). 1). Figure 1. ChemicalChemical structures of oleanane tr triterpenoiditerpenoid saponins isolated from Salicornia europaea ((1–21).). InIn 2012, aa newnew 30-noroleanane 30-noroleanane triterpenoid triterpenoid saponin, saponin, 3b -hydroxy-23-oxo-30-noroleana-3β-hydroxy-23-oxo-30-noroleana-12,20(29)-diene-28-oic12,20(29)-diene-28-oic acid acid 3-O- b3--DO-glucuronopyranosyl-28--β-D-glucuronopyranosyl-28-O-b-OD--glucopyranosideβ-D-glucopyranoside (1), (and1), and three three known known triterpenoid triterpenoid saponins saponins (2–4 )(2 were–4) were also isolatedalso isolated from from an n-BuOH an n-BuOH fraction frac- of tionan S. of europaea an S. europaeaextract[ 5extract]. The known[5]. The compounds known compounds were identified were as identified 30-norhederagenin as 30-norheder- 3-O-b-D- ageninglucuronopyranosyl-28- 3-O-β-D-glucuronopyranosyl-28-O-b-D-glucopyranosideO-β-D (-glucopyranoside2), gypsogenin 3-O -(b2-),D -glucuronopyranosidegypsogenin 3-O-β-D- glucuronopyranoside(3), and gypsogenin 3- O(3-),b -andD-glucuronopyranosyl-28- gypsogenin 3-O-β-D-glucuronopyranosyl-28-O-b-D-glucopyranosideO (-4β).-D The-gluco- an- tioxidant activities of compounds 1–4 have been evaluated by measuring their 1,1-diphenyl- pyranoside (4). The antioxidant activities of compounds 1–4 have− been evaluated by meas- uring2-picryl-hydrazyl their 1,1-diphenyl-2-picryl-hydrazyl (DPPH) radical and peroxynitrite (DPPH) (ONOOradical and) scavenging peroxynitrite activities. (ONOO All−) scavengingfour compounds activities. were All found four tocompounds be potent were scavengers found to for be both potent authentic scavengers peroxynitrite for both authenticand peroxynitrite peroxynitrite produced and peroxynitrite by morpholinosydnonimine produced by morpholinosydnonimine (SIN-1) (IC50 between <<1 (SIN-1) and 21.9 µM). Notably, compound 2 had the lowest IC50 values (<<1 µM) for both authentic (IC50 between <<1 and 21.9 μM). Notably, compound 2 had the lowest IC50 values (<<1 μM) ONOO− and ONOO− produced by SIN-1, but displayed no significant DPPH radical scavenging activity. Compound 1 also possesses a potent antifungal activity against Col- letotrichum gloeosporioides [16]. Compound 1 has been previously isolated from Salicornia Molecules 2021, 26, 2252 3 of 26 bigelovii. Compound 3 has been isolated from the flowering plant Gypsophila pacifica and exhibited promising hepatoprotective activity [17]. This triterpenoid saponin has also been isolated from fruits of Acanthopanax senticosus and showed pancreatic lipase inhibitory activity (Table1)[18]. In the same year, Yin et al. reported the isolation and structural elucidation of 3b,29- dihydroxyolean-12-en-28-oic acid 28-O-b-D-glucopyranosyl ester (5), a new oleanane triterpenoid saponin, along with four previously identified compounds: oleanolic acid 28-O-b- D-glucopyranoside (6), chikusetsusaponin IVa methyl ester (7), calenduloside E (8), and calenduloside E 60-methyl ester (9)[19]. The plant sample in question was collected in Jiangsu Province, China, along the Yellow Sea shore. Although the biological activity of 5 has not yet been described, the bioactivities of compounds 6–9 have been studied extensively. Compound 6, isolated from Drypetes paxii reportedly exhibits antibacterial activity [20], and an isolate from the plant Aralia cordata has been reported to possess anti-inflammatory effects [21]. A synthesized version of compound 6 also displayed potent α-glucosidase and α-amylase inhibitory activities [22]. The reported biological effects of compound 7 include anticancer [23–25], antifungal [16], and anti-inflammatory [26] activities. Compound 8 exhibited potent spermicidal [27] and anticancer

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