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Ingol and Ingenol-Type Diterpenes from Euphorbia Trigona Miller with Keratinocyte Inhibitory Activity

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Ingol and Ingenol-Type Diterpenes from Euphorbia Trigona Miller with Keratinocyte Inhibitory Activity plants Article Ingol and Ingenol-Type Diterpenes from Euphorbia trigona Miller with Keratinocyte Inhibitory Activity Reham Hammadi 1, Norbert Kúsz 1 , Csilla Zsuzsanna Dávid 1, Zoltán Behány 2,László Papp 3, Lajos Kemény 2 , Judit Hohmann 1,4,Lóránt Lakatos 2,5,* and Andrea Vasas 1,* 1 Department of Pharmacognosy, Interdisciplinary Excellence Centre, University of Szeged, Eötvös u. 6, 6720 Szeged, Hungary; [email protected] (R.H.); [email protected] (N.K.); [email protected] (C.Z.D.); [email protected] (J.H.) 2 Department of Dermatology and Allergology, University of Szeged, Korányi fasor 6, 6720 Szeged, Hungary; [email protected] (Z.B.); [email protected] (L.K.) 3 Botanical Garden, Eötvös Loránd University, Illés u. 25, 1083 Budapest, Hungary; [email protected] 4 Interdisciplinary Centre of Natural Products, University of Szeged, Eötvös u. 6, 6720 Szeged, Hungary 5 Photo- and Chronobiology Group Eötvös Loránd Research Network (ELKH), Institute of Plant Biology, Biological Research Center Szeged, Temesvári krt. 62, 6726 Szeged, Hungary * Correspondence: [email protected] (L.L.); [email protected] (A.V.); Tel.: +36-62546451 (A.V.) Abstract: Ingenol mebutate, isolated from Euphorbia peplus, is an ingenane-type diterpenoid, primarily used for the topical treatment of actinic keratosis, a premalignant skin condition. The aim of our work was to investigate other Euphorbia species to find structurally similar diterpenes that can be used as alternatives to ingenol mebutate. Pharmacological investigation of Euphorbia candelabrum, Euphorbia Citation: Hammadi, R.; Kúsz, N.; cotinifolia, Euphorbia ramipressa, and Euphorbia trigona revealed the potent keratinocyte (HPV-Ker cell Dávid, C.Z.; Behány, Z.; Papp, L.; line) inhibitory activity of these spurge species. From the methanolic extract of the aerial parts of Kemény, L.; Hohmann, J.; Lakatos, L.; Euphorbia trigona Miller, the most active species, five ingol (1–5) and four ingenane-type diterpenoids Vasas, A. Ingol and Ingenol-Type (6–9) were isolated by various chromatographic separation techniques, including open column Diterpenes from Euphorbia trigona chromatography, vacuum liquid chromatography, thin-layer chromatography, and high-performance Miller with Keratinocyte Inhibitory liquid chromatography. The structures of the compounds were determined by NMR spectroscopic Activity. Plants 2021, 10, 1206. analysis and by comparison of the assignations with the literature data. The cytotoxic activity of https://doi.org/10.3390/ the compounds against keratinocytes was tested in vitro by using ingenol mebutate as a positive plants10061206 control. Among the isolated compounds, two ingenane derivatives (6 and 7) exhibited remarkably stronger cytotoxic activity (IC values 0.39 µM and 0.32 µM, respectively) on keratinocytes than Academic Editor: Salvatore 50 µ Antonino Raccuia ingenol mebutate (IC50 value 0.84 M). These compounds could serve as starting materials for further investigations to find alternatives to Picato® (with active substance ingenol mebutate), which was Received: 26 April 2021 withdrawn from marketing authorization in the European Union. Accepted: 8 June 2021 Published: 14 June 2021 Keywords: Euphorbiaceae; Euphorbia trigona; ingol esters; ingenol diterpenes; keratinocyte; cytotoxi- city; actinic keratosis Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Actinic keratosis (AK) is a skin disorder with erythematous plaques that are frequently found on sun-damaged skin [1]. AK is more likely to occur in men than women and is more prevalent in older adults [2,3]. The main causative agent of AK is excessive Copyright: © 2021 by the authors. UV radiation, which can lead to destructive inflammatory processes, and ultimately to Licensee MDPI, Basel, Switzerland. substantial structural damage to cell DNA and membrane lipids [4]. This article is an open access article AK is considered to be an epidermal dysplasia, in which keratinocytes in the stratum distributed under the terms and basale and stratum spinosum have lost polarity, and appear disordered with pleomorphic conditions of the Creative Commons nuclei. The stratum corneum shows parakeratosis and hyperkeratosis, most probably due Attribution (CC BY) license (https:// to abnormal keratinocyte development [5]. In many AK patients, inflammatory infiltra- creativecommons.org/licenses/by/ tion of lymphocytes and plasma cells in the dermis can also be observed [6]. Although 4.0/). Plants 2021, 10, 1206. https://doi.org/10.3390/plants10061206 https://www.mdpi.com/journal/plants Plants 2021, 10, 1206 2 of 10 spontaneous regression of AK is very common (>50%) [7], the condition must be taken seriously, since it can develop into malignant lesions, such as squamous cell carcinoma (SCC), the second most common form of skin cancer, and basal cell carcinoma (BCC). These conditions predominantly affect light-skinned populations [6]. Treatment options for AK include destructive therapies (e.g., surgery, cryotherapy, dermabrasion, and photodynamic therapy (PDT)), topical medications (e.g., topical fluorouracil, imiquimod, ingenol mebu- tate, and diclofenac), and field ablation treatments (chemical peels and laser resurfacing) [8]. Self-directed treatments are preferred by patients, but are time-consuming, as they need to be applied for weeks or months before producing clinical results. Although many options are available, the search for new and more effective agents of AK is in progress. Ingenol mebutate (Picato®) is the active ingredient of the sap of Euphorbia peplus [9,10], a plant that has long been used in Australian folk medicine for the treatment of skin cancers. It is offered with a short treatment schedule (2–3 days), providing an effective and sustained clearance of AK lesions with a predictable onset and short duration of local skin responses [11]. Ingenol mebutate acts on keratinocytes in two different ways: (1) induces the cell death of aberrant keratinocytes, and (2) induces a lesion-directed immune response that is mediated, at least partially, by the enzyme family protein kinase C (PKC) [11]. The ingenol-mebutate-induced cell death is mediated through the PKCδ/mitogen-activated protein kinase (MEK)/extracellular signal-regulated kinase (ERK) pathway. PKCδ is a key mediator in cell differentiation and the inhibition of proliferation in various tissues. Ingenol mebutate directly binds to PKCδ and leads to its phosphorylation, which activates MEK/ERK signaling, resulting in decreased viability and cell proliferation [12]. The topical application of ingenol mebutate causes rapid cell death via necrosis. Subsequently, the concentration of TNF-α and IL-8 promptly increases, which leads to the recruitment and infiltration of neutrophils into the inflamed region, followed by the activation of an apoptotic cell death [13]. Unfortunately, Picato is no longer authorized in the EU, as the European Medicinal Agency has concluded that the medicine may increase the risk of skin cancer and that its risks outweigh its benefits. Searching for new analogues of ingenol mebutate with a higher potency and a more favorable side effect spectrum seems to be a rational aim of phytochemical researchers. Most of the plants belonging to the genus Euphorbia (family Euphorbiaceae) contain a milky irritant latex and accumulate different types of diterpenoid esters, characteristic of the family [14,15]. In recent decades, numerous pharmacological investigations into Euphor- biaceae plants focused on the authentication of their traditional use in cancerous conditions and confirmed the efficacy of various diterpenes as promising antitumor agents [15,16]. However, no publication can be found in the literature about the keratinocyte inhibitory activity of the Euphorbia species. In a continuation of our work dealing with the isolation of biologically active diter- penoids, different extracts, prepared from E. candelabrum Trémaux ex Kotschy, E. cotinifolia (L.) Millsp., E. ramipressa Croisat, and E. trigona Mill., were tested for their keratinocyte inhibitory activities. E. candelabrum and E. cotinifolia were reported to contain ingenol derivatives [17]. Although E. ramipressa was not investigated from the phytochemical and pharmacological perspectives, as it belongs to the same section (Euphorbia sect. Eu- phorbia) as E. candelabrum and other ingenol derivative-containing species (e.g., E. nivulia, E. antiquorum, E. kamerunica), it is worthy of investigation [18]. Based on the results of the pharmacological assay, E. trigona Mill. was chosen for further examination. E. trigona is native to Central Africa, where it is commonly planted around villages as a ceremonial plant [19]. In Japan and the United States, it is cultivated as an indoor ornamental plant [20]. In the traditional medicinal use of E. trigona, usually, some drops of the latex are added to palm wine for the treatment of severe cases of constipation or epileptic attacks. It is also used as an arrow and fish poison [19]. The plant is also well recognised in India, as it has been used in Ayurveda to combat infections (e.g., in the urinary tract) and to alleviate the symptoms inflammation [21]. Plants 2021, 10, 1206 3 of 10 Previous studies have revealed the presence of ingol and ingenol esters in the latex of E. trigona that are responsible for its strong skin-irritating and pesticidal properties [20]; while lectins, another important class of phytoconstituents
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