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Wound Healing Activity and Phytochemical Screening of Purified Fractions of Sempervivum Tectorum L. Leaves on HCT 116

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Wound Healing Activity and Phytochemical Screening of Purified Fractions of Sempervivum Tectorum L. Leaves on HCT 116 Received: 31 January 2019 Revised: 12 March 2019 Accepted: 17 April 2019 DOI: 10.1002/pca.2844 SPECIAL ISSUE ARTICLE Wound healing activity and phytochemical screening of purified fractions of Sempervivum tectorum L. leaves on HCT 116 Fabio Cattaneo1 | Simona De Marino2 | Melania Parisi1 | Carmen Festa2 | Martina Castaldo1 | Claudia Finamore3 | Francesca Duraturo1 | Cristiana Zollo1 | Rosario Ammendola1 | Franco Zollo2 | Maria Iorizzi3 1 Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi Abstract di Napoli Federico II, Naples, Italy Introduction: Sempervivum tectorum L. (Crassulaceae), is a succulent perennial plant 2 Dipartimento di Farmacia, Università degli widespread in Mediterranean countries and commonly used in traditional medicine Studi di Napoli “Federico II”, Naples, Italy 3 Dipartimento di Bioscienze e Territorio, for ear inflammation, ulcers and skin rashes as a refrigerant and astringent. Università degli Studi del Molise, Pesche, Objective: To demonstrate the therapeutic effects of the plant, various fractions (Isernia), Italy were purified and characterised. The potential wound healing activity, proliferation Correspondence rate and intracellular signalling cascades were investigated by using human epithelial Maria Iorizzi, Dipartimento di Bioscienze e Territorio, Università degli Studi del Molise, colorectal carcinoma (HCT 116) cells. Contrada Fonte Lappone, I–86090 Pesche Methodology: An extraction method without organic solvents was applied for the (Isernia), Italy. Email: [email protected] first time. The purification was carried out by droplet counter current chromatogra- phy (DCCC) coupled with high‐performance liquid chromatography (HPLC) and electrospray ionisation mass spectrometry (ESI‐MS) data. By nuclear magnetic reso- nance (NMR) [1H, 13C and two‐dimensional (2D) experiments] pure components were identified. Wound healing and cell proliferation assays were utilised to determine the role of the isolated S. tectorum (SVT) fraction on cellular migration and proliferation. The signalling pathways elicited from the SVT fractions, were analysed by Western blot analysis. Results: In this study two rare natural components were identified, namely mono- saccharide sedoheptulose and polyalcohol 2‐C‐methyl‐D‐erythritol, along with known organic acids and flavonoids. The fractions with high level of sedoheptulose enhance the proliferation and the cellular migration of epithelial HCT 116 cells. The intracellular signalling cascades elicited from the purified fractions induce the c‐Src‐mediated transactivation of EGFR and the activation of the STAT3 pathway which, in turn, are crucially involved in the cellular proliferation and migration. Conclusions: Our study demonstrates the efficacy of purified fractions of S. tectorum L. in enhancing cellular proliferation and migration, suggesting their potential role as topical therapeutic treatments for wound healing. KEYWORDS 2‐C‐Methyl‐D‐erythritol, NMR spectroscopy, sedoheptulose, Sempervivum tectorum L., wound healing activity Phytochemical Analysis. 2019;1–11. wileyonlinelibrary.com/journal/pca © 2019 John Wiley & Sons, Ltd. 1 2 CATTANEO ET AL. 1 | INTRODUCTION a method developed in our group. Herein we analyse the effects on cellular migration and proliferation as well as the putative intracellular Herbs and plants have been used in traditional medicine for hundreds of signalling cascades triggered by treatment with S. tectorum in human years for therapeutic purposes since whole herbs contain complex mix- epithelial colorectal carcinoma (HCT 116) cells. tures of organic components that can work together to produce a ben- eficial effect. In recent years there has been growing tendency to use herbal preparations and a renewed interest of chemists in the identifica- 2 | EXPERIMENTAL tion of natural compounds for pharmaceutical or cosmetic applications.1 Sempervivum tectorum L. known as houseleek, is a wild‐growing 2.1 | Plant material succulent perennial plant with thick leaf rosettes, belonging to the family of Crassulaceae, widespread in arid climates such as the Medi- Selected rosettes of wild growing S. tectorum L. (Crassulaceae) were terranean countries from Spain to Asia Minor. The genus Sempervivum collected at Colli al Volturno, a mountainous area of Isernia (central comprises approximately 50 species frequently employed in traditional Italy) in June 2016 and identified by Dr Paola Fortini. A voucher spec- medicine in Serbia, Bosnia and Turkey to cure common ailments, par- imen was deposited (SVT‐129‐2016) at the Herbarium of the ticularly earache,2 ear inflammations and dermatophyte infections.3,4 Dipartimento di Bioscienze e Territorio, University of Molise (Pesche, Among botanicals, S. tectorum leaves, fresh juice and bruised leaves Isernia). The rosettes were immediately analysed. from S. tectorum, are used in folk medicine in Europe almost exclu- sively for external purposes such as for the treatment of warts, ulcers, 2.2 | General experimental procedures skin rashes and corns, as a refrigerant and astringent.5 In Italy the juice and leaves have been applied for insect bites while the beaten aerial Electrospray ionisation mass spectrometry (ESI‐MS) experiments were part placed on the brow has been reported to reduce the severity of performed on an Applied Biosystem API 2000 triple‐quadrupole mass headaches.6 It has also been found that a S. tectorum extract has spectrometer. Optical rotations were determined on a Jasko P‐2000 lipid‐lowering activities in rats,7 significant antinociceptive activities5 polarimeter. Nuclear magnetic resonance (NMR) spectra were and liver protecting with membrane stabilising effects.8 Antioxidant obtained on a Varian Inova 500 NMR spectrometer (1H at 500 MHz activities have been evidenced in vitro9-12 and in vivo13 and have been and 13C at 125 MHz) equipped with a Sun hardware, δ (ppm), J in attributed to the presence of the plant's phenolic compounds. Drink- Hz, using a solvent signal for the calibration (13CD OD at δ 49.0 ing tea prepared from the leaves is recommended in folk medicine 3 C and residual CD HOD at δ = 3.31). The spectra in D O (deuterated for ulcer treatment.14 Several papers have reported the polyphenol 2 H 2 water) contained TSP‐d [3‐(trimethylsilyl)propionic‐2,2,3,3‐d acid composition5,15 and the flavonoid content of S. tectorum from differ- 4 4 sodium salt] as the internal standard. The heteronuclear single‐ ent geographical areas.16 quantum coherence (HSQC) spectra were optimised for an average Sempervivum tectorum as a succulent plant, has a crassulacean acid 1J of 140 Hz; the gradient‐enhanced heteronuclear multiple bond metabolism (CAM), and presents a typical ecophysiological adaptation CH correlation (HMBC) experiments were optimised for a 3J of 8 Hz. to arid conditions due to an efficient water conservation strategy and CH Droplet counter current chromatography (DCCC) fractionation was a specialised photosynthetic mode with a carbon dioxide (CO2) con- performed on a DCC‐A apparatus (Tokyo Rikakikai Co., Tokyo, Japan) centrating mechanism. During the night, carbon dioxide is fixed and equipped with 250 glass‐columns. Sephadex LH‐20 (4 cm × 80 cm; is stored in cell vacuoles in the form of malate. Throughout the follow- 25–100 μm) (Sigma‐Aldrich Chemie GmbH, Steinheim, Germany). ing day, malate is released from the vacuoles and CO2, produced by High‐performance liquid chromatography (HPLC) was performed the malate decarboxylation can enter the Calvin cycle and can be used using a Waters 510 pump equipped with a Rheodyne 7125 injector as a substrate for Rubisco to provide sugars and other carbohydrates and a Waters 401 differential refractometer as the detector on a Luna to the plant. The physiological homeostasis of CAM plants under C column (5 μm, 250 mm × 4.6 mm i.d.) (Phenomenex, Torrance, CA, long‐term drought is due to a significant starch conservation and an 18 USA); Eurospher 100–5NH (250 mm × 4.6 mm i.d.) (Vertex Plus, adaptation of the equilibrium of carbohydrate balances.17 2 Knauer, Berlin, Germany). A number of homeopathic products containing houseleek are marketed in the United Kingdom and the United States (Homeopathic Medicine Boiron; Washington Homeopathic Products) while others 2.3 | Extraction and isolation are used as cosmetics (Ilcsi Natural Cosmetics, Hungary) or in cosmetic formulations.18 Eight fresh rosettes (492 g) of S. tectorum (SVT) were cleaned, washed Although several pharmacological activities have been reported for and homogenated at room temperature without any solvent. The the S. tectorum leaves, a complete characterisation of the extracts is homogenate was then centrifuged to give a supernatant and a precip- still not available, and previous analyses have highlighted only the itate. The supernatant was freeze‐dried to give 4.07 g of lyophilised polyphenolic components. extract (ST1), while the precipitate was extracted overnight with The present study is focused on the determination of the phyto- methanol (MeOH) (500 mL) at room temperature and provided chemical profile by applying an extraction any organic solvents using 5.10 g of MeOH extract (ST2). CATTANEO ET AL. 3 Then, 2.00 g of the ST1 extract was submitted to DCCC with to give kaempferol‐3‐O‐rhamnosyl‐glucoside‐7‐O‐rhamnoside (9.2 mg) n‐BuOH–Me2CO–H2O (3:1:5) in the descending mode (the upper and kaempferol‐3,7‐di‐O‐rhamnoside (2.2 mg). phase was the stationary phase) to give six main fractions (A–F, see Table 1). The obtained fractions were monitored by TLC on silica
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