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  • Nutritional and phyto-therapeutic value of the Halophyte Cladium mariscus L. (Pohl.): a special focus on seeds
    Publication . Rodrigues, Maria João; L, Custódio; Mecha, Débora; Zengin, Gokhan; Cziáky, Zoltán; Sotkó, Gyula; Pereira, Catarina Guerreiro
    This work searched for the phyto-therapeutic potential and nutritional value of seeds from the halophyte Cladium mariscus L. (Pohl.), aiming at its use as a source of bioactive ingredients for the food industry. Hence, the nutritional profile, including minerals, of seeds biomass was determined; food-grade samples were prepared, and their phytochemical fingerprinting assessed. Extracts were evaluated for in vitro antioxidant potential, inhibitory capacity towards enzymes related to neuroprotection, diabetes, and hyperpigmentation, and anti-inflammatory properties, along with a toxicological assessment. Sawgrass seeds can be considered a proper nutritional source with a good supply of minerals. All extracts had a high level of total phenolics (65.3–394.4 mg GAE/g DW) and showed a chemically rich and diverse profile of metabolites that have several biological properties described (e.g., antioxidant, anti-inflammatory). Extracts had no significant toxicity (cell viabilities > 80%) and were overall strong antioxidants (particularly at radical scavenging and reducing iron), effective tyrosinase inhibitors (55–71 mg KAE/g DW), showed anti-inflammatory properties (30–60% NO decrease), and had moderate capacity to inhibit enzymes related to neuroprotection (AChE 3.7–4.2, BChE 4.3–6.0 mg GALE/g DW) and diabetes (α-glucosidase 1.0–1.1, α-amylase 0.8–1.1 mmol ACAE/g). Altogether, results suggest that sawgrass seeds have the potential to be exploited as a new food product and are a reservoir of bioactive molecules with prospective applications as ingredients for value-added, functional, and/or preservative food products
  • Chemical profile, antioxidant, antimicrobial, enzyme inhibitory, and cytotoxicity of seven Apiaceae species from Turkey: a comparative study
    Publication . Zengin, Gokhan; Sinan, Kouadio Ibrahime; Ak, Gunes; Mahomoodally, Mohamad Fawzi; Paksoy, Mehmet Yavuz; Picot-Allain, Carene; Glamocilja, Jasmina; Sokovic, Marina; Jeko, Jozsef; Cziaky, Zoltan; Rodrigues, Maria Joao; Pereira, Catarina; Custódio, Luísa
    Several Apiaceae species, used as both food and in complementary and alternative medicine, represents a rich source of potential valuable phytopharmaceuticals which necessitates scientific contemplation. In the present study, the antioxidant, enzyme inhibitory, antimicrobial, and cytotoxic properties of methanol extracts of seven Apiaceae species, (Chaerophyllum macrospermum (Willd. ex Spreng.) Fisch. & C.A.Mey. ex Hohen, Ferula rigidula Fisch. ex DC., Ferula orientalis L., Prangos ferulacea Lindl., Prangos peucedanifolia Fenzl., Ferulago setifolia K. Koch, and Pimpinella anthriscoides Boiss.) were evaluated. Species belonging to the Prangos genus exhibited the highest total phenolic content, namely P. peucedanifolia and P. ferulacea, with values of 47.90 and 44.44 mg gallic acid equivalent/g extract, respectively. P. peucedanifolia also displayed the highest radical scavenging capacity (81.53 and 102.70 mg Trolox equivalent [TE]/g extract for 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid (ABTS), respectively) and reducing power (165.87 and 100.09 mg TE/g extract for cupric reducing antioxidant capacity (CUPRAC) and ferric reducing antioxidant power (FRAP), respectively). C. macrospermum showed the most potent inhibition against Alzheimer's disease related enzymes, namely acetylcholinesterase (4.53 mg galantamine equivalent [GALAE]/g extract) and butyrylcholinesterase (3.22 mg GALAE/g extract). P. ferulacea (131.94 mg kojic acid (KAE) equivalent/g extract) and P. peucedanifolia (4.97 mmol acarbose equivalent (ACAE)/g extract) were potent inhibitors of tyrosinase and a-glucosidase, respectively. In general, studied species were able to reduce cellular viabilities. P. peucedanifolia possessed promising antibacterial potential against Bacillus cereus (Minimum inhibition concentration (MIC): 0.37 mg/mL), L. monocytogenes (MIC: 0.56 mg/mL), P. aeruginosa and Escherichia coli (MIC: 0.27 mg/mL), Salmonella typhimurium and Enterobacter cloacae (MIC: 0.75 mg/mL). F. rigidula showed the highest antifungal effect against Aspergillus ochraceus and Trichoderma viride (MIC: 0.10 mg/mL). The present findings could be the scientific starting point towards the pharmaceutical and/or commercial utilization of these Apiaceae species.
  • Seasonal variations of the nutritive value and phytotherapeutic potential of Cladium mariscus L. (Pohl.) targeting ruminant’s production
    Publication . Oliveira, Marta; Rodrigues, Maria Joao; Neng, Nuno R.; Nogueira, José Manuel Florêncio; Bessa, Rui J. B.; Custódio, Luísa
    In our endeavor to identify salt-tolerant plants with potential veterinary uses in ruminants' production strategies, we focused on Cladium mariscus L. Pohl (sawgrass), due to its high total phenolic and tannin content, anti-radical properties, and ethnomedicinal uses. Aerial parts were collected along the year in Southern Portugal and evaluated for the nutritional profile and in vitro organic matter digestibility (IVOMD), aiming for its use as feed. Acetone extracts were appraised for total contents in phenolics (TPC), flavonoids (TFC), and tannins (CTC), as well as the chemical composition by HPLC-DAD and in vitro antioxidant and anti-inflammatory properties, targeting its exploitation as phytotherapeutic products. Sawgrass biomass has a limited nutritive value, due to its high neutral detergent fiber (NDF; 596-690 g kg-1 dry matter (DM)) and acid detergent fiber (ADF; 330-418 g kg-1 DM) contents, low crude protein (51.8-87.3 g kg-1 DM) and IVOMD (172-317 g kg-1 organic matter (OM)). Despite differences among seasons, the mineral profile was adequate. The extracts were rich in TPC (88-112 mg g-1), CTC (115-169 mg g-1), and TFC (18.5-20.2 mg g-1), and displayed significant antioxidant capacity, particularly in summer and autumn, whilst no seasonal influence was detected for anti-inflammatory properties (30% reduction of nitric oxide production). Eleven phenolics were quantified: chlorogenic, ferulic, and syringic acids were the most abundant, especially in the autumn sample. Overall, despite the low nutritional interest, sawgrass extracts hold the potential as a source of antioxidant and anti-inflammatory phenolic compounds.
  • Seasonal and geographic dynamics in bioproperties and phytochemical profile of Limonium algarvense Erben
    Publication . Pereira, Catarina Guerreiro; Rodrigues, Maria João; Nawrot-Hadzik, Izabela; Matkowski, Adam; L, Custódio
    This study delved into the influence of ecological and seasonal dynamics on the synthesis of secondary metabolites in the medicinal halophyte Limonium algarvense Erben, commonly known as sea lavender, and examined their antioxidant and anti-inflammatory properties. Aerial parts of sea lavender were systematically collected across winter, spring, summer, and autumn seasons from distinct geographic locations in southern Portugal, specifically “Ria de Alvor” in Portimão and “Ria Formosa” in Tavira. The investigation involved determining the total polyphenolic profile through spectrophotometric methods, establishing the chemical profile via liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry (LC-ESI-QTOF-MS/MS), and evaluating in vitro antioxidant properties using radical and metal-based methods, along with assessing anti-inflammatory capacity through a cell model. Results unveiled varying polyphenol levels and profiles across seasons, with spring and autumn samples exhibiting the highest content, accompanied by the most notable antioxidant and anti-inflammatory capacities. Geographic location emerged as an influential factor, particularly distinguishing plants from “Ria de Alvor”. Seasonal fluctuations were associated with environmental factors, including temperature, which, when excessively high, can impair plant metabolism, but also with the presence of flowers and seeds in spring and autumn samples, which also seems to contribute to elevated polyphenol levels and enhanced bioproperties of these samples. Additionally, genetic factors may be related to differences observed between ecotypes (geographical location). This study underscores sea lavender’s potential as a natural source of antioxidant and anti-inflammatory agents, emphasizing the significance of considering both geographic location and seasonal dynamics in the assessment of phenolic composition and bioactive properties in medicinal plant species.
  • Can macroalgae provide promising anti-tumoral compounds? A closer look at Cystoseira tamariscifolia as a source for antioxidant and anti-hepatocarcinoma compounds
    Publication . Vizetto-Duarte, C; Custódio, Luísa; Acosta, Gerardo; Lago, João H. G.; Morais, Thiago R.; Sousa, Carolina Bruno de; Gangadhar, Katkam N.; Rodrigues, Maria Joao; Pereira, Hugo; Lima, Raquel T.; Vasconcelos, M. Helena; Barreira, Luísa; Rauter, Amélia P.; Albericioi, Fernando; Varela, J.
    Marine organisms are a prolific source of drug leads in a variety of therapeutic areas. In the last few years, biomedical, pharmaceutical and nutraceutical industries have shown growing interest in novel compounds from marine organisms, including macroalgae. Cystoseira is a genus of Phaeophyceae (Fucales) macroalgae known to contain bioactive compounds. Organic extracts (hexane, diethyl ether, ethyl acetate and methanol extracts) from three Cystoseira species (C. humilis, C. tamariscifolia and C. usneoides) were evaluated for their total phenolic content, radical scavenging activity against 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2,2'- azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) (ABTS) radicals, and antiproliferative activity against a human hepatocarcinoma cell line (HepG2 cells). C. tamariscifolia had the highest TPC and RSA. The hexane extract of C. tamariscifolia (CTH) had the highest cytotoxic activity (IC50 = 2.31 mu g/mL), and was further tested in four human tumor (cervical adenocarcinoma HeLa; gastric adenocarcinoma AGS; colorectal adenocarcinoma HCT-15; neuroblastoma SH-SY5Y), and two non-tumor (murine bone marrow stroma S17 and human umbilical vein endothelial HUVEC) cell lines in order to determine its selectivity. CTH strongly reduced viability of all tumor cell lines, especially of HepG2 cells. Cytotoxicity was particularly selective for the latter cells with a selectivity index = 12.6 as compared to non-tumor cells. Incubation with CTH led to a 2-fold decrease of HepG2 cell proliferation as shown by the bromodeoxyuridine (BrdU) incorporation assay. CTH-treated HepG2 cells presented also pro-apoptotic features, such as increased Annexin Wpropidium iodide (PI) binding and dose-dependent morphological alterations in DAPI-stained cells. Moreover, it had a noticeable disaggregating effect on 3D multicellular tumor spheroids. Deme boxy cystoketal chromane, a derivative of the meroditerpenoid cystoketal, was identified as the active compound in CTH and was shown to display selective in vitro cYtotoxicitY towards HepG2 cells.
  • Deeper Insights on Alchornea cordifolia (Schumach. & Thonn.) Müll.Arg extracts: chemical profiles, biological abilities, network analysis and molecular docking
    Publication . Sinan, Kouadio Ibrahime; Ak, Gunes; Etienne, Ouattara Katinan; Jekő, József; Cziáky, Zoltán; Gupcsó, Katalin; Rodrigues, Maria Joao; Custódio, Luísa; Mahomoodally, Mohamad Fawzi; Sharmeen, Jugreet B.; Brunetti, Luigi; Leone, Sheila; Recinella, Lucia; Chiavaroli, Annalisa; Orlando, Giustino; Menghini, Luigi; Tacchini, Massimo; Ferrante, Claudio; Zengin, Gokhan
    Alchornea cordifolia (Schumach. & Thonn.) Müll. Arg. is a well-known African medicinal plant traditionally used for various healing purposes. In the present study, methanolic, ethyl acetate and infusion extracts of A. cordifolia leaves were studied for their total phenolic and flavonoid contents and screened for their chemical composition. Moreover, the enzyme (acetyl- and butyryl-cholinesterases, α-amylase, α-glucosidase, and tyrosinase) inhibitory and cytotoxicity activities on HepG2: human hepatocellular carcinoma cells, B16 4A5: murine melanoma cells, and S17: murine bone marrow (normal) cells of extracts were evaluated. Finally, components-targets and docking analyzes were conducted with the aim to unravel the putative mechanisms underlying the observed bio-pharmacological effects. Interestingly, the infusion and methanolic extracts showed significantly higher total phenolic and flavonoid contents compared with the ethyl acetate extract (TPC: 120.38–213.12 mg GAE/g and TFC: 9.66–57.18 mg RE/g). Besides, the methanolic extracts followed by the infusion extracts were revealed to contain a higher number of compounds (84 and 74 compounds, respectively), while only 64 compounds were observed for the ethyl acetate extract. Gallic acid, ellagic acid, shikimic acid, rutin, quercetin, myricetin, vitexin, quercitrin, kaempferol, and naringenin were among the compounds that were commonly identified in all the studied extracts. Additionally, the methanolic and infusion extracts displayed higher antioxidant capacity than ethyl acetate extract in all assays performed. In ABTS and DPPH radical scavenging assays, the methanol extract (500.38 mg TE/g for DPPH and 900.64 mg TE/g for ABTS) exhibited the best ability, followed by the water and ethyl acetate extracts. Furthermore, the extracts exhibited differential enzyme inhibitory profiles. In particular, the methanolic and infusion extracts showed better cytotoxic selectivity activity against human hepatocellular carcinoma cells. Overall, this study demonstrated A cordifolia to be a species worthy of further investigations, given its richness in bioactive phytochemicals and wide potentialities for antioxidants and pharmacological agents.
  • From threat to opportunity: Harnessing the invasive Carpobrotus edulis (L.) N.E.Br for nutritional and phytotherapeutic valorization amid seasonal and spatial variability
    Publication . Pereira, Catarina Guerreiro; Neng, Nuno R.; Custódio, Luísa
    Carpobrotus edulis (L.) N.E.Br. (Hottentot-fig) is a problematic invasive species found in coastal areas worldwide. Mechanical removal is a common control method, leaving the removed biomass available as a possible source of natural phytochemicals with prospective commercial applications. While the Hottentot-fig’s vegetative organs have been studied previously, this work establishes for the first time a seasonal and spatial comparative analysis of its nutritional, chemical, and bioactivity profiles (in three locations over four seasons). Proximate and mineral contents were assessed, along with its phenolic composition and in vitro antioxidant and anti-inflammatory properties. Hottentot-fig’s biomass offered a good supply of nutrients, mainly carbohydrates, proteins, and minerals, with a tendency for higher concentrations of the most relevant minerals and proteins in autumn and winter, and in plants from sites A (Ria de Alvor lagoon) and B (Ancão beach). The extracts were rich in polyphenolics, with higher levels in spring and summer, especially for luteolin7-O-glucoside and salicylic and coumaric acids. The extracts were also effective antioxidants, with stronger radical scavenging activities in spring and summer, along with anti-inflammatory properties. Our results suggest that the usually discarded plant material of this invasive halophyte could be valuable as a source of natural products with potential biotechnological applications in the food and nutraceutical industries.
  • Chemical profiling and biological evaluation of Nepeta baytopii extracts and essential oil: An endemic plant from Turkey
    Publication . Zengin, Gokhan; Mahomoodally, Mohamad Fawzi; Aktumsek, Abdurrahman; Jekő, József; Cziáky, Zoltán; Rodrigues, Maria João; Custódio, Luísa; Polat, Rıdvan; Cakilcioglu, Ugur; Ayna, Adnan; Gallo, Monica; Montesano, Domenico; Picot-Allain, Carene
    Nepeta baytopii is a poorly studied, endemic Nepeta species (Lamiaceae) of Turkey. For the first time, the biological activities (antioxidant, enzyme inhibition, and cytotoxicity properties) of the hexane, ethyl acetate, methanol, water/methanol, and water extracts and essential oil prepared from N. baytopii aerial parts were assessed. Hydro-methanol (41.25 mg gallic acid equivalent (GAE)/g) and water extracts (50.30 mg GAE/g), respectively showed the highest radical scavenging (94.40 and 129.22 mg Trolox equivalent (TE)/g, for 2,2-diphenyl-1-picrylhydrazyl radical and 2,2-azinobis (3-ethylbenzothiazoline-6-sulfonic acid radical scavenging assays) and reducing (229.37 and 129.55 mg TE/g, for ferric-reducing antioxidant power and cupric-reducing antioxidant capacity assays) capacities in vitro. An interestingly high inhibition was observed for ethyl acetate extract against butyrylcholinesterase (10.85 mg galantamine equivalent/g). The methanol extract showed high cytotoxicity (31.7%) against HepG2 cells. Caryophyllene oxide was identified in high concentrations in the essential oil (39.3%). Luteolin and apigenin and their derivatives were identified from the methanol and water extracts. The results obtained from this study highlighted that the abundance of highly bioactive compounds from Nepeta baytopii ensures the multiple biological activities of the tested extracts, and this suggests a potential use in the pharmaceutical and nutraceutical fields, and therefore should be investigated further.
  • Deciphering the chemical constituents of phlomis monocephala extracts using UHPLC-HRMS and their antioxidant, neuroprotective, antidiabetic and toxic potentials
    Publication . Zheleva-Dimitrova, Dimitrina; Zengin, Gokhan; Bouyahya, Abdelhakim; Ahmed, Shakeel; Guerreiro Pereira, Catarina Alexandra; Sharifi-Rad, Majid; Custódio, Luísa
    In the current study, five different extracts ( n -hexane, ethyl acetate, dichloromethane, ethanol, and water) of Phlomis monocephala were analyzed for the first time by ultra -high-performance liquid chromatography -high resolution mass spectrometry (UHPLC-HRMS) to identify their phenolic compounds. The extracts were also evaluated for their non -enzyme antioxidant activities using a variety of methods, including DPPH and, ABTS center dot+ scavenging activities, reduction of ferric (Fe 3 + ), and cupric ions (Cu 2 + ), metal chelating (MCA) activities, and phosphomolybdenum (PBD). Additionally, the extracts were assessed for their in vitro enzyme inhibition potential (acetylcholinesterase (AChE)/butyrylcholinesterase (BChE), alpha-amylase, alpha-glucosidase, and tyrosinase). Furthermore, cell viability was evaluated on HepG2 (human hepatocellular carcinoma), S17 cells (murine bone marrow stromal) and RAW (murine macrophages). UHPLC-HRMS allowed for the identification of 115 compounds from different chemical groups including flavonoids, iridoid glycosides, phenylethanoid glycosides and others. Most of the extracts had strong antioxidant potential and were rich in phenolic compounds. Ethanol and water extracts appear as the most promising antioxidant extracts providing the highest values followed by ethyl acetate by all the methodologies employed in this study. Furthermore, all the extracts, except the aqueous extract, inhibited all the enzymes significantly. Surprisingly, the aqueous extract did not show a prominent inhibition (low or no inhibition) against these enzymes. Hexane, ethyl acetate, and dichloromethane exhibited extremely significant cytotoxic effects against all cell lines at a higher concentration. The HepG2 cells demonstrated lower sensitivity to the extracts than RAW and S17 cells. In conclusion, P. monocephala can be considered as a valuable ingredient for the production of functional applications including nutraceuticals.
  • Decoding chemical profiles and biological activities of aerial parts and roots of Eryngium thorifolium Boiss by HPLC-MS/MS, GC-MS and in vitro chemical assays
    Publication . Gokhan Zengin; Sakina Yagi; Omayma A. Eldahshan; Abdel Nasser Singab; Selami Selvi; Rodrigues, Maria João; Custódio, Luísa; Stefano Dall’Acqua; Sathish Kumar M Ponnaiya; Shaza H. Aly
    Eryngium species are widely distributed and primarily utilised for medicinal and culinary purposes. This study aimed to evaluate the chemical composition, antioxidant, enzyme inhibition, and cytotoxic properties of various extracts from the aerial parts and roots of E. thorifolium Boiss. The chemical composition of ethyl acetate, methanol, and water extracts was analysed using High-Performance Liquid Chromatography-Electrospray Ionization Tandem Mass Spectrometry (HPLC-ESI-MS/MS), while the hexane ones were examined using Gas Chromatography-Mass Spectrometry (GC-MS) analysis. The most predominant class of secondary metabolites identified were fatty acid amides and flavonoids as hexose conjugates. Extracts from the aerial parts exhibited the highest antioxidant activity, with the methanol and water extracts showing the best anti- 2,2-diphenyl-1-picrylhydrazyl (DPPH) (21.9 mg trolox equivalent (TE)/g) and anti- 2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) (89.26 mg TE/g) activities. Enzyme inhibition tests revealed that the hexane extract from the roots had the highest anti-acetylcholinesterase activity (2.49 mg galantamine equivalent (GALAE)/g). Additionally, both the hexane and ethyl acetate extracts from the aerial parts demonstrated the highest antibutyrylcholinesterase activity (3.13 and 3.71 mg GALAE/g, p ≥ 0.05). At a concentration of 100 μg/mL, all extracts from the roots and aerial parts, except the water one, displayed potent cytotoxicity against the human embryonic (HEK 293) and murine macrophages (RAW 264.7) cell lines, with cellular viability ranging from 1.66 to 2.62% compared to the control (0.5% DMSO) (89.2 and 95.1%, respectively). Through network pharmacology and molecular docking, the phytochemicals of E. thorifolium show significant potential as natural compounds targeting key proteins involved in cancer progression, including Bcl-2, c-KIT, PI3K, and AKT. Their binding affinities and predicted interactions highlight their possible therapeutic applications in managing various cancers. These findings suggested E. thorifolium is a promising source of phytochemicals targeting specific oxidative stresslinked diseases, including cancer, diabetes and neurodegenerative disorders.