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Applied Sciences applied sciences Review Applications of Sesquiterpene Lactones: A Review of Some Potential Success Cases Laila Moujir 1,*, Oliver Callies 2 , Pedro M. C. Sousa 3, Farukh Sharopov 4 and Ana M. L. Seca 5,6,* 1 Department of Biochemistry, Microbiology, Genetics and Cell Biology, Facultad de Farmacia, Universidad de La Laguna, 38206 San Cristóbal de La Laguna, Spain 2 AbbVie Deutschland GmbH & Co. KG, Knollstrasse, 67061 Ludwigshafen, Germany; [email protected] 3 Faculty of Sciences and Technology, University of Azores, 9500-321 Ponta Delgada, Portugal; sdoffi[email protected] 4 Research Institution “Chinese-Tajik Innovation Center for Natural Products”, Academy of Sciences of the Republic of Tajikistan, Ayni 299/2, Dushanbe 734063, Tajikistan; [email protected] 5 cE3c—Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group & Faculty of Sciences and Technology, University of Azores, Rua Mãe de Deus, 9500-321 Ponta Delgada, Portugal 6 LAQV-REQUIMTE, University of Aveiro, 3810-193 Aveiro, Portugal * Correspondence: [email protected] (L.M.); [email protected] (A.M.L.S.); Tel.: +34-9-22-318513 (L.M.); +351-29-6650174 (A.M.L.S.) Received: 25 March 2020; Accepted: 19 April 2020; Published: 25 April 2020 Abstract: Sesquiterpene lactones, a vast range of terpenoids isolated from Asteraceae species, exhibit a broad spectrum of biological effects and several of them are already commercially available, such as artemisinin. Here the most recent and impactful results of in vivo, preclinical and clinical studies involving a selection of ten sesquiterpene lactones (alantolactone, arglabin, costunolide, cynaropicrin, helenalin, inuviscolide, lactucin, parthenolide, thapsigargin and tomentosin) are presented and discussed, along with some of their derivatives. In the authors’ opinion, these compounds have been neglected compared to others, although they could be of great use in developing important new pharmaceutical products. The selected sesquiterpenes show promising anticancer and anti-inflammatory effects, acting on various targets. Moreover, they exhibit antifungal, anxiolytic, analgesic, and antitrypanosomal activities. Several studies discussed here clearly show the potential that some of them have in combination therapy, as sensitizing agents to facilitate and enhance the action of drugs in clinical use. The derivatives show greater pharmacological value since they have better pharmacokinetics, stability, potency, and/or selectivity. All these natural terpenoids and their derivatives exhibit properties that invite further research by the scientific community. Keywords: Asteraceae; sesquiterpene lactones; alantolactone; arglabin; parthenolide; thapsigargin; in vivo study; anticancer; anti-inflammatory 1. Introduction Traditional or folk medicine relies heavily on the use of compounds-rich plants, like those of the Asteraceae family, of which many such species are commercially available in the form of herbal preparations. These are particularly rich in a wide range of natural terpenoids named sesquiterpene lactones [1] that, in some cases, are considered the active principles of such therapeutic plants [2]. Structurally speaking, sesquiterpene lactones are terpenes that have in common a basic structure of 15 carbons (thus the prefix sesqui-) resulting from biosynthesis involving three isoprene units with a cyclical structure along with a fused α-methylene-γ-lactone ring [3]. Sesquiterpene synthases Appl. Sci. 2020, 10, 3001; doi:10.3390/app10093001 www.mdpi.com/journal/applsci Appl. Sci. 2020, 10, x FOR PEER REVIEW 2 of 33 Appl. Sci. 2020, 10, 3001 2 of 32 15 carbons (thus the prefix sesqui-) resulting from biosynthesis involving three isoprene units with a cyclical structure along with a fused α-methylene-γ-lactone ring [3]. Sesquiterpene synthases catalyze acatalyze common a common biosynthesis biosynthesis route for route sesquiterpene for sesquiterpene lactones, lactones, based based on onthe the cyclization cyclization of of farnesyl farnesyl phosphate resulting resulting from from the 2-C-methyl-D-eryth 2-C-methyl-D-erythritol-4-phosphateritol-4-phosphate (MEP) (MEP) and and mevalonate mevalonate (MVA) (MVA) pathways of of dimethylalyl diphosphate diphosphate and and isopente isopentenylnyl diphosphate diphosphate precursors precursors in in chloroplasts chloroplasts and and cytosol,cytosol, respectively respectively [4]. [4]. However, However, sesquiterpene sesquiterpene lactones lactones have have very very different different chemical structures regardingregarding the the type type and and position position of of the the substituents, substituents, as as well well as as the the size size of of the the non-lactone non-lactone ring ring [5,6]. [5,6]. ForFor this this reason, in in structural terms, sesquiterpene sesquiterpene lactones lactones are are organized organized into into several several subclasses: subclasses: eudesmanolideeudesmanolide (a (a 6/6 6/6 bicyclic structure), guaianolide and and pseudoguaianolide (both (both 5/7 5/7 bicyclic compounds),compounds), germacranolide germacranolide (with (with a a 10-membered 10-membered ri ring)ng) and and xanthanolide (containing (containing a a non-cyclic carboncarbon chain chain and and a a seven-membered seven-membered ring) [7,8] [7,8] (Figure 1 1).). FigureFigure 1. BasicBasic chemical chemical structure structure of of each of the sesquiterpenesesquiterpene lactone subclasses:subclasses: eudesmanolide, eudesmanolide, guaianolide,guaianolide, pseudoguai pseudoguaianolide,anolide, germacranolide, and xanthanolide. SomeSome of thesethese subclassessubclasses have have compounds compounds that that exhibit exhibit a wide a wide range range of biological of biological activities. activities. These Theserange fromrange antitumor from antitumor [9] to anti-inflammatory, [9] to anti-inflammatory, including antimalarial, including antimicrobial,antimalarial, antioxidantantimicrobial, [10], antioxidantneuroprotective [10], [neuroprotective11], hepatoprotective, [11], hepatoprot and immune-stimulantective, and immune-stimulant properties [12,13 properties]. Regarding [12,13]. the Regardingstructure/activity the structure/activity relationship of relationship these compounds, of these it appearscompounds, that theit appearsα-methylene- that theγ -lactoneα-methylene- nucleusγ- lactonehas a crucial nucleus role has in almosta crucial all role their in observed almost all biological their observed effects, suchbiological as cytotoxic, effects, antitrypanosomal,such as cytotoxic, antitrypanosomal,and anti-inflammatory and actions anti-inflammatory [12,14]. Other actions specific structural[12,14]. Other moieties specific of sesquiterpene structural lactonemoieties seem of sesquiterpeneto influence their lactone activity. seem For to example,influence the their presence activity of. For electrophilic example, sites the presence associated of with electrophilic medium /siteshigh associatedlipophilicity with increase medium/high antimycobacterial lipophilicity activity, increase while antimycobacterial a double bond activity, exo to while the cyclopentenone a double bond exoring to seems the cyclopentenone to favor anti-inflammatory ring seems to favor activity anti [-inflammatory7,8,14]. The interaction activity [7,8,14]. of the Theα,β interaction-unsaturated of thecyclopentenone α,β-unsaturated nucleus cyclopentenone with the target nucleus depends with largelythe target on depends the geometry largely of on the the molecule, geometry which of the is molecule,also a factor which that is influences also a factor the that level influences of activity the exhibited level of activity by sesquiterpene exhibited by lactones sesquiterpene [7,15]. Moreover, lactones [7,15].the number Moreover, of alkylating the number groups of in thealkylating structure grou of sesquiterpeneps in the structure lactones of contributes sesquiterpene to the lactones level of contributesactivity they to display, the level two of groupsactivity being they thedisplay, optimal two number groups [ 7being,15]. The the structureoptimal /numberactivity relationship[7,15]. The structure/activityspecific to each sesquiterpene relationship lactonespecific presentedto each sesquiterpene in this review lactone will be presented discussed in in this detail review throughout will be discussedSection2. Scientific in detail evidencethroughout shows Section an action 2. Scientific mechanism evidence common shows to sesquiterpene an action mechanism lactones. The common structural to sesquiterpeneelements α-methylene- lactones.γ -lactoneThe structural and α,β -unsaturatedelements α-methylene- cyclopentenoneγ-lactone act as and alkylating α,β-unsaturated groups on cyclopentenoneproteins found in act cells as through alkylating Michael groups addition, on pr especiallyoteins found their in thiol cells groups. through They Michael thereby addition, affect cell especiallyfunctionality, their i.e., thiol gene groups. regulation, They protein thereby synthesis, affect cell and functionality, cell metabolism i.e., [15 gene–17]. regulation, protein synthesis,In recent and years, cell metabolism the scientific [15–17]. community has already shown an oustanding growth of interest in the sesquiterpeneIn recent years, lactones, the largely scientific due community to the success has of already artemisinin—one shown an ofoustanding the best known—and growth of interest the broad in thespectrum sesquiterpene of activities lactones, exhibited largely by thisdue compound’sto the success chemical of artemisinin—one family [18–20 ].of
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