Exploring the Potential of Invasive Species Sargassum muticum: Microwave-Assisted Extraction Optimization and Bioactivity Profiling
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemicals and Solutions
2.2. Algae Sampling and Preparation
2.3. Optimization Procedure
2.3.1. Microwave-Assisted Extraction
2.3.2. Experimental Design and Mathematical Modelling
2.3.3. Response Variables
Extraction Yield
Phytochemical Content
Antioxidant Activity
2.3.4. Statistical Evaluation
2.4. Chemical Characterization by HPLC-ESI-QqQ-MS/MS
2.5. Evaluation of the Biological Properties of the Optimum Extract
2.5.1. Antioxidant Activity (ROS and RNS)
Superoxide Antiradical Activity
Hydrogen Peroxide Scavenging Activity
Hydroxyl Antiradical Scavenging Activity
Nitrogen Oxide Antiradical Scavenging Activity
2.5.2. Antimicrobial Activity Assay
Microorganisms and Cultures
Extract Preparation
Minimal Inhibitory Concentration
2.5.3. Enzyme Inhibition Assays
Cholinesterase Inhibition Assay
Monoamino Oxidase A and B Inhibition Assay
Tyrosinase Inhibition Assay
α-Amilase Inhibition Assay
2.5.4. Antiproliferative Activity
3. Results and Discussion
3.1. Theoretical Response Surface Models and Statistical Verification
3.2. Impact of the Extraction Variables on the Target Responses and Optimal Conditions
3.3. Chemical Characterization by HPLC-ESI-QqQ-MS/MS
3.4. Biological Activities of the Optimum Extract
3.4.1. Scavenging Activity of ROS and RNS
3.4.2. Antimicrobial Activity
3.4.3. Inhibition of Enzymatic Activity
3.4.4. Antiproliferative Activity
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rossi, F.; Incera, M.; Callier, M.; Olabarria, C. Effects of Detrital Non-Native and Native Macroalgae on the Nitrogen and Carbon Cycling in Intertidal Sediments. Mar. Biol. 2011, 158, 2705–2715. [Google Scholar] [CrossRef]
- Pereira, A.G.; Fraga-Corral, M.; Garcia-Oliveira, P.; Lourenço-Lopes, C.; Carpena, M.; Prieto, M.A.; Simal-Gandara, J. The Use of Invasive Algae Species as a Source of Secondary Metabolites and Biological Activities: Spain as Case-Study. Mar. Drugs 2021, 19, 178. [Google Scholar] [CrossRef]
- Tanniou, A.; Vandanjon, L.; Incera, M.; Serrano Leon, E.; Husa, V.; Le Grand, J.; Nicolas, J.L.; Poupart, N.; Kervarec, N.; Engelen, A.; et al. Assessment of the Spatial Variability of Phenolic Contents and Associated Bioactivities in the Invasive Alga Sargassum muticum Sampled along Its European Range from Norway to Portugal. J. Appl. Phycol. 2014, 26, 1215–1230. [Google Scholar] [CrossRef]
- Raoux, A.; Pezy, J.P.; Sporniak, T.; Dauvin, J.C. Does the Invasive Macro-Algae Sargassum muticum (Yendo) Fensholt, 1955 Offer an Appropriate Temporary Habitat for Mobile Fauna Including Non Indigenous Species? Ecol. Indic. 2021, 126, 107624. [Google Scholar] [CrossRef]
- Kraan, S. Sargassum muticum (Yendo) Fensholt in Ireland: An Invasive Species on the Move. J. Appl. Phycol. 2008, 20, 825–832. [Google Scholar] [CrossRef]
- Pinteus, S.; Lemos, M.F.L.; Alves, C.; Neugebauer, A.; Silva, J.; Thomas, O.P.; Botana, L.M.; Gaspar, H.; Pedrosa, R. Marine Invasive Macroalgae: Turning a Real Threat into a Major Opportunity—The Biotechnological Potential of Sargassum muticum and Asparagopsis armata. Algal Res. 2018, 34, 217–234. [Google Scholar] [CrossRef]
- Silva, A.; Cassani, L.; Grosso, C.; Garcia-Oliveira, P.; Morais, S.L.; Echave, J.; Carpena, M.; Xiao, J.; Barroso, M.F.; Simal-Gandara, J.; et al. Recent Advances in Biological Properties of Brown Algae-Derived Compounds for Nutraceutical Applications. Crit. Rev. Food Sci. Nutr. 2024, 64, 1283–1311. [Google Scholar] [CrossRef]
- Pinteus, S.; Lemos, M.F.L.; Silva, J.; Alves, C.; Neugebauer, A.; Freitas, R.; Duarte, A.; Pedrosa, R. An Insight into Sargassum muticum Cytoprotective Mechanisms against Oxidative Stress on a Human Cell in Vitro Model. Mar. Drugs 2017, 15, 353. [Google Scholar] [CrossRef]
- Silva, A.; Silva, S.A.; Carpena, M.; Garcia-Oliveira, P.; Gullón, P.; Barroso, M.F.; Prieto, M.A.; Simal-Gandara, J. Macroalgae as a Source of Valuable Antimicrobial Compounds: Extraction and Applications. Antibiotics 2020, 9, 642. [Google Scholar] [CrossRef]
- Zheng, H.; Du, H.; Ye, E.; Xu, X.; Wang, X.; Jiang, X.; Min, Z.; Zhuang, L.; Li, S.; Guo, L. Optimized Extraction of Polyphenols with Antioxidant and Anti-Biofilm Activities and LC-MS/MS-Based Characterization of Phlorotannins from Sargassum muticum. LWT 2024, 198, 116069. [Google Scholar] [CrossRef]
- Bouzenad, N.; Ammouchi, N.; Chaib, N.; Messaoudi, M.; Bousabaa, W.; Bensouici, C.; Sawicka, B.; Atanassova, M.; Ahmad, S.F.; Zahnit, W. Exploring Bioactive Components and Assessing Antioxidant and Antibacterial Activities in Five Seaweed Extracts from the Northeastern Coast of Algeria. Mar. Drugs 2024, 22, 273. [Google Scholar] [CrossRef]
- Diego-González, L.; Álvarez-Viñas, M.; Simón-Vázquez, R.; Domínguez, H.; Torres, M.; Flórez-Fernández, N. Characterization of the Antiproliferative Activity of Sargassum muticum Low and High Molecular Weight Polysaccharide Fractions. Mar. Drugs 2023, 22, 16. [Google Scholar] [CrossRef]
- Rodrigues, D.; Costa-Pinto, A.R.; Sousa, S.; Vasconcelos, M.W.; Pintado, M.M.; Pereira, L.; Rocha-Santos, T.; da Costa, J.P.; Silva, A.; Duarte, A.C.; et al. Sargassum muticum and Osmundea pinnatifida Enzymatic Extracts: Chemical, Structural, and Cytotoxic Characterization. Mar. Drugs 2019, 17, 209. [Google Scholar] [CrossRef]
- Dang, T.T.; Bowyer, M.C.; Van Altena, I.A.; Scarlett, C.J. Optimum Conditions of Microwave-Assisted Extraction for Phenolic Compounds and Antioxidant Capacity of the Brown Alga Sargassum Vestitum. Sep. Sci. Technol. 2018, 53, 1711–1723. [Google Scholar] [CrossRef]
- Quitério, E.; Grosso, C.; Ferraz, R.; Delerue-Matos, C.; Soares, C. A Critical Comparison of the Advanced Extraction Techniques Applied to Obtain Health-Promoting Compounds from Seaweeds. Mar. Drugs 2022, 20, 677. [Google Scholar] [CrossRef]
- Grosso, C.; Valentão, P.; Ferreres, F.; Andrade, P.B. Alternative and Efficient Extraction Methods for Marine-Derived Compounds. Mar. Drugs 2015, 13, 3182–3230. [Google Scholar] [CrossRef]
- Yolmeh, M.; Jafari, S.M. Applications of Response Surface Methodology in the Food Industry Processes. Food Bioprocess Technol. 2017, 10, 413–433. [Google Scholar] [CrossRef]
- Liu, Z.; Ren, Z.; Zhang, J.; Chuang, C.-C.; Kandaswamy, E.; Zhou, T.; Zuo, L. Role of ROS and Nutritional Antioxidants in Human Diseases. Front. Physiol. 2018, 9, 477. [Google Scholar] [CrossRef]
- Cassani, L.; Silva, A.; Carpena, M.; Pellegrini, M.C.; García-Pérez, P.; Grosso, C.; Barroso, M.F.; Simal-Gandara, J.; Gómez-Zavaglia, A.; Prieto, M.A. Phytochemical Compounds with Promising Biological Activities from Ascophyllum Nodosum Extracts Using Microwave-Assisted Extraction. Food Chem. 2024, 438, 138037. [Google Scholar] [CrossRef]
- Cassani, L.; Tomadoni, B.; Ponce, A.; Agüero, M.V.; Moreira, M.R. Combined Use of Ultrasound and Vanillin to Improve Quality Parameters and Safety of Strawberry Juice Enriched with Prebiotic Fibers. Food Bioprocess Technol. 2017, 10, 1454–1465. [Google Scholar] [CrossRef]
- Okawa, M.; Kinjo, J.; Nohara, T.; Ono, M. DPPH (1,1-Diphenyl-2-Picrylhydrazyl) Radical Scavenging Activity of Flavonoids Obtained from Some Medicinal Plants. Biol. Pharm. Bull. 2001, 24, 1202–1205. [Google Scholar] [CrossRef] [PubMed]
- Viacava, G.E.; Goyeneche, R.; Goñi, M.G.; Roura, S.I.; Agüero, M.V. Natural Elicitors as Preharvest Treatments to Improve Postharvest Quality of Butterhead Lettuce. Sci. Hortic. 2018, 228, 145–152. [Google Scholar] [CrossRef]
- Lage, M.Á.P.; García, M.A.M.; Álvarez, J.A.V.; Anders, Y.; Curran, T.P. A New Microplate Procedure for Simultaneous Assessment of Lipophilic and Hydrophilic Antioxidants and Pro-Oxidants, Using Crocin and β-Carotene Bleaching Methods in a Single Combined Assay: Tea Extracts as a Case Study. Food Res. Int. 2013, 53, 836–846. [Google Scholar] [CrossRef]
- Oliveira, A.P.; Valentão, P.; Pereira, J.A.; Silva, B.M.; Tavares, F.; Andrade, P.B. Ficus carica L.: Metabolic and Biological Screening. Food Chem. Toxicol. 2009, 47, 2841–2846. [Google Scholar] [CrossRef]
- Gülçin, İ.; Mshvildadze, V.; Gepdiremen, A.; Elias, R. Screening of Antiradical and Antioxidant Activity of Monodesmosides and Crude Extract from Leontice Smirnowii Tuber. Phytomedicine 2006, 13, 343–351. [Google Scholar] [CrossRef] [PubMed]
- Mancini, S.; Nardo, L.; Gregori, M.; Ribeiro, I.; Mantegazza, F.; Delerue-Matos, C.; Masserini, M.; Grosso, C. Functionalized Liposomes and Phytosomes Loading Annona muricata L. Aqueous Extract: Potential Nanoshuttles for Brain-Delivery of Phenolic Compounds. Phytomedicine 2018, 42, 233–244. [Google Scholar] [CrossRef] [PubMed]
- Smirnoff, N.; Cumbes, Q.J. Hydroxyl Radical Scavenging Activity of Compatible Solutes. Phytochemistry 1989, 28, 1057–1060. [Google Scholar] [CrossRef]
- Geng, M.; Ren, M.; Liu, Z.; Shang, X. Free Radical Scavenging Activities of Pigment Extract from Hibiscus syriacus L. Petals In Vitro. Afr. J. Biotechnol. 2012, 11, 429–435. [Google Scholar] [CrossRef]
- Sun, J.; Zhang, X.; Broderick, M.; Fein, H. Measurement of Nitric Oxide Production in Biological Systems by Using Griess Reaction Assay. Sensors 2003, 3, 276–284. [Google Scholar] [CrossRef]
- Soares, C.; Paíga, P.; Marques, M.; Neto, T.; Carvalho, A.P.; Paiva, A.; Simões, P.; Costa, L.; Bernardo, A.; Fernández, N.; et al. Multi-Step Subcritical Water Extracts of Fucus vesiculosus L. and Codium tomentosum Stackhouse: Composition, Health-Benefits and Safety. Processes 2021, 9, 893. [Google Scholar] [CrossRef]
- Paz, M.; Gúllon, P.; Barroso, M.F.; Carvalho, A.P.; Domingues, V.F.; Gomes, A.M.; Becker, H.; Longhinotti, E.; Delerue-Matos, C. Brazilian Fruit Pulps as Functional Foods and Additives: Evaluation of Bioactive Compounds. Food Chem. 2015, 172, 462–468. [Google Scholar] [CrossRef]
- Silva, A.; Rodrigues, C.; Garcia-Oliveira, P.; Lourenço-Lopes, C.; Silva, S.A.; Garcia-Perez, P.; Carvalho, A.P.; Domingues, V.F.; Barroso, M.F.; Delerue-Matos, C.; et al. Screening for Bioactive Properties on Brown Algae from the Northwest Iberian Peninsula. Foods 2021, 10, 1915. [Google Scholar] [CrossRef]
- Ellman, G.L.; Courtney, K.D.; Andres, V.; Featherstone, R.M. A New and Rapid Colorimetric Determination of Acetylcholinesterase Activity. Biochem. Pharmacol. 1961, 7, 88–95. [Google Scholar] [CrossRef]
- Delerue, T.; Fátima Barroso, M.; Dias-Teixeira, M.; Figueiredo-González, M.; Delerue-Matos, C.; Grosso, C. Interactions between Ginkgo biloba L. and Scutellaria Baicalensis Georgi in Multicomponent Mixtures towards Cholinesterase Inhibition and ROS Scavenging. Food Res. Int. 2021, 140, 109857. [Google Scholar] [CrossRef]
- Weissbach, H.; Smith, T.E.; Daly, J.W.; Witkop, B.; Udenfriend, S. A Rapid Spectrophotometric Assay of Monoamine Oxidase Based on the Rate of Disappearance of Kynuramine. J. Biol. Chem. 1960, 235, 1160–1163. [Google Scholar] [CrossRef]
- Masuda, T.; Yamashita, D.; Takeda, Y.; Yonemori, S. Screening for Tyrosinase Inhibitors among Extracts of Seashore Plants and Identification of Potent Ihibitors from Garcinia subelliptica. Biosci. Biotechnol. Biochem. 2005, 69, 197–201. [Google Scholar] [CrossRef]
- Figueiredo-González, M.; Grosso, C.; Valentão, P.; Andrade, P.B. α-Glucosidase and α-Amylase Inhibitors from Myrcia Spp.: A Stronger Alternative to Acarbose? J. Pharm. Biomed. Anal. 2016, 118, 322–327. [Google Scholar] [CrossRef]
- Roriz, C.L.; Xavier, V.; Heleno, S.A.; Pinela, J.; Dias, M.I.; Calhelha, R.C.; Morales, P.; Ferreira, I.C.F.R.; Barros, L. Chemical and Bioactive Features of Amaranthus caudatus L. Flowers and Optimized Ultrasound-Assisted Extraction of Betalains. Foods 2021, 10, 779. [Google Scholar] [CrossRef]
- Vichai, V.; Kirtikara, K. Sulforhodamine B Colorimetric Assay for Cytotoxicity Screening. Nat. Protoc. 2006, 1, 1112–1116. [Google Scholar] [CrossRef]
- Calhelha, R.C.; Martínez, M.A.; Prieto, M.A.; Ferreira, I.C.F.R. Mathematical Models of Cytotoxic Effects in Endpoint Tumor Cell Line Assays: Critical Assessment of the Application of a Single Parametric Value as a Standard Criterion to Quantify the Dose–Response Effects and New Unexplored Proposal Formats. Analyst 2017, 142, 4124–4141. [Google Scholar] [CrossRef]
- Rumpf, J.; Burger, R.; Schulze, M. Statistical Evaluation of DPPH, ABTS, FRAP, and Folin-Ciocalteu Assays to Assess the Antioxidant Capacity of Lignins. Int. J. Biol. Macromol. 2023, 233, 123470. [Google Scholar] [CrossRef]
- Casas, M.P.; Conde, E.; Domínguez, H.; Moure, A. Ecofriendly Extraction of Bioactive Fractions from Sargassum muticum. Process Biochem. 2019, 79, 166–173. [Google Scholar] [CrossRef]
- Namvar, F.; Mohamad, R.; Baharara, J.; Zafar-Balanejad, S.; Fargahi, F.; Rahman, H.S. Antioxidant, Antiproliferative, and Antiangiogenesis Effects of Polyphenol-Rich Seaweed (Sargassum muticum). BioMed Res. Int. 2013, 2013, 604787. [Google Scholar] [CrossRef]
- Sabeena Farvin, K.H.; Jacobsen, C. Phenolic Compounds and Antioxidant Activities of Selected Species of Seaweeds from Danish Coast. Food Chem. 2013, 138, 1670–1681. [Google Scholar] [CrossRef]
- Rodrigues, D.; Sousa, S.; Silva, A.; Amorim, M.; Pereira, L.; Rocha-Santos, T.A.P.; Gomes, A.M.P.; Duarte, A.C.; Freitas, A.C. Impact of Enzyme- and Ultrasound-Assisted Extraction Methods on Biological Properties of Red, Brown, and Green Seaweeds from the Central West Coast of Portugal. J. Agric. Food Chem. 2015, 63, 3177–3188. [Google Scholar] [CrossRef]
- Erpel, F.; Mateos, R.; Pérez-Jiménez, J.; Pérez-Correa, J.R. Phlorotannins: From Isolation and Structural Characterization, to the Evaluation of Their Antidiabetic and Anticancer Potential. Food Res. Int. 2020, 137, 109589. [Google Scholar] [CrossRef]
- Olate-Gallegos, C.; Barriga, A.; Vergara, C.; Fredes, C.; García, P.; Giménez, B.; Robert, P. Identification of Polyphenols from Chilean Brown Seaweeds Extracts by LC-DAD-ESI-MS/MS. J. Aquat. Food Prod. Technol. 2019, 28, 375–391. [Google Scholar] [CrossRef]
- Isaza Martínez, J.H.; Torres Castañeda, H.G. Preparation and Chromatographic Analysis of Phlorotannins. J. Chromatogr. Sci. 2013, 51, 825–838. [Google Scholar] [CrossRef]
- Agregán, R.; Munekata, P.E.S.; Franco, D.; Dominguez, R.; Carballo, J.; Lorenzo, J.M. Phenolic Compounds from Three Brown Seaweed Species Using LC-DAD–ESI-MS/MS. Food Res. Int. 2017, 99, 979–985. [Google Scholar] [CrossRef]
- Catarino, M.D.; Pires, S.M.G.; Silva, S.; Costa, F.; Braga, S.S.; Pinto, D.C.G.A.; Silva, A.M.S.; Cardoso, S.M. Overview of Phlorotannins’ Constituents in Fucales. Mar. Drugs 2022, 20, 754. [Google Scholar] [CrossRef]
- Zhong, B.; Robinson, N.A.; Warner, R.D.; Barrow, C.J.; Dunshea, F.R.; Suleria, H.A.R. LC-ESI-QTOF-MS/MS Characterization of Seaweed Phenolics and Their Antioxidant Potential. Mar. Drugs 2020, 18, 331. [Google Scholar] [CrossRef]
- Montero, L.; Sánchez-Camargo, A.P.; García-Cañas, V.; Tanniou, A.; Stiger-Pouvreau, V.; Russo, M.; Rastrelli, L.; Cifuentes, A.; Herrero, M.; Ibáñez, E. Anti-Proliferative Activity and Chemical Characterization by Comprehensive Two-Dimensional Liquid Chromatography Coupled to Mass Spectrometry of Phlorotannins from the Brown Macroalga Sargassum muticum Collected on North-Atlantic Coasts. J. Chromatogr. A 2016, 1428, 115–125. [Google Scholar] [CrossRef]
- Elsaman, S.; Elsonbaty, S.M.; Moawed, F.S.M.; Hegazy, M.G.A. Evaluation of Brown Micro-Algae Synergies With Low Dose γ -Radiation Against Chronic Hepatitis Induced by D-Galactosamine in Rats. Dose-Response 2023, 21, 155932582311694. [Google Scholar] [CrossRef]
- Grina, F.; Ullah, Z.; Kaplaner, E.; Moujahid, A.; Eddoha, R.; Nasser, B.; Terzioğlu, P.; Yilmaz, M.A.; Ertaş, A.; Öztürk, M.; et al. In Vitro Enzyme Inhibitory Properties, Antioxidant Activities, and Phytochemical Fingerprints of Five Moroccan Seaweeds. S. Afr. J. Bot. 2020, 128, 152–160. [Google Scholar] [CrossRef]
- Tatsis, E.C.; Boeren, S.; Exarchou, V.; Troganis, A.N.; Vervoort, J.; Gerothanassis, I.P. Identification of the Major Constituents of Hypericum Perforatum by LC/SPE/NMR and/or LC/MS. Phytochemistry 2007, 68, 383–393. [Google Scholar] [CrossRef]
- Ghallab, D.S.; Shawky, E.; Ibrahim, R.S.; Mohyeldin, M.M. Comprehensive Metabolomics Unveil the Discriminatory Metabolites of Some Mediterranean Sea Marine Algae in Relation to Their Cytotoxic Activities. Sci. Rep. 2022, 12, 8094. [Google Scholar] [CrossRef]
- Vallverdú-Queralt, A.; Regueiro, J.; Martínez-Huélamo, M.; Rinaldi Alvarenga, J.F.; Leal, L.N.; Lamuela-Raventos, R.M. A Comprehensive Study on the Phenolic Profile of Widely Used Culinary Herbs and Spices: Rosemary, Thyme, Oregano, Cinnamon, Cumin and Bay. Food Chem. 2014, 154, 299–307. [Google Scholar] [CrossRef]
- Siciliano, T.; De Tommasi, N.; Morelli, I.; Braca, A. Study of Flavonoids of Sechium Edule (Jacq) Swartz (Cucurbitaceae) Different Edible Organs by Liquid Chromatography Photodiode Array Mass Spectrometry. J. Agric. Food Chem. 2004, 52, 6510–6515. [Google Scholar] [CrossRef]
- Gancel, A.-L.; Alter, P.; Dhuique-Mayer, C.; Ruales, J.; Vaillant, F. Identifying Carotenoids and Phenolic Compounds In Naranjilla (Solanum Quitoense Lam. Var. Puyo Hybrid), an Andean Fruit. J. Agric. Food Chem. 2008, 56, 11890–11899. [Google Scholar] [CrossRef]
- Martins, B.T.; Correia da Silva, M.; Pinto, M.; Cidade, H.; Kijjoa, A. Marine Natural Flavonoids: Chemistry and Biological Activities. Nat. Prod. Res. 2019, 33, 3260–3272. [Google Scholar] [CrossRef]
- Rattmann, Y.D.; Mendéz-Sánchez, S.C.; Furian, A.F.; Paludo, K.S.; de Souza, L.M.; Dartora, N.; Oliveira, M.S.; Costa, E.M.d.S.; Miguel, O.G.; Sassaki, G.L.; et al. Standardized Extract of Dicksonia sellowiana Presl. Hook (Dicksoniaceae) Decreases Oxidative Damage in Cultured Endothelial Cells and in Rats. J. Ethnopharmacol. 2011, 133, 999–1007. [Google Scholar] [CrossRef] [PubMed]
- Rajauria, G. Optimization and Validation of Reverse Phase HPLC Method for Qualitative and Quantitative Assessment of Polyphenols in Seaweed. J. Pharm. Biomed. Anal. 2018, 148, 230–237. [Google Scholar] [CrossRef] [PubMed]
- Allwood, J.W.; Evans, H.; Austin, C.; McDougall, G.J. Extraction, Enrichment, and LC-MSn-Based Characterization of Phlorotannins and Related Phenolics from the Brown Seaweed, Ascophyllum Nodosum. Mar. Drugs 2020, 18, 448. [Google Scholar] [CrossRef] [PubMed]
- Vázquez-Rodríguez, B.; Gutiérrez-Uribe, J.A.; Antunes-Ricardo, M.; Santos-Zea, L.; Cruz-Suárez, L.E. Ultrasound-Assisted Extraction of Phlorotannins and Polysaccharides from Silvetia compressa (Phaeophyceae). J. Appl. Phycol. 2020, 32, 1441–1453. [Google Scholar] [CrossRef]
- Li, Y.; Fu, X.; Duan, D.; Liu, X.; Xu, J.; Gao, X. Extraction and Identification of Phlorotannins from the Brown Alga, Sargassum Fusiforme (Harvey) Setchell. Mar. Drugs 2017, 15, 49. [Google Scholar] [CrossRef] [PubMed]
- Lopes, G.; Barbosa, M.; Vallejo, F.; Gil-Izquierdo, Á.; Andrade, P.B.; Valentão, P.; Pereira, D.M.; Ferreres, F. Profiling Phlorotannins from Fucus Spp. of the Northern Portuguese Coastline: Chemical Approach by HPLC-DAD-ESI/MS and UPLC-ESI-QTOF/MS. Algal Res. 2018, 29, 113–120. [Google Scholar] [CrossRef]
- Catarino, M.D.; Silva, A.; Cruz, M.T.; Mateus, N.; Silva, A.M.S.; Cardoso, S.M. Phlorotannins from Fucus Vesiculosus: Modulation of Inflammatory Response by Blocking NF-ΚB Signaling Pathway. Int. J. Mol. Sci. 2020, 21, 6897. [Google Scholar] [CrossRef] [PubMed]
- Wang, T.; Jónsdóttir, R.; Liu, H.; Gu, L.; Kristinsson, H.G.; Raghavan, S.; Ólafsdóttir, G. Antioxidant Capacities of Phlorotannins Extracted from the Brown Algae Fucus Vesiculosus. J. Agric. Food Chem. 2012, 60, 5874–5883. [Google Scholar] [CrossRef] [PubMed]
- Vissers, A.M.; Caligiani, A.; Sforza, S.; Vincken, J.-P.; Gruppen, H. Phlorotannin Composition of Laminaria Digitata. Phytochem. Anal. 2017, 28, 487–495. [Google Scholar] [CrossRef]
- Hermund, D.B.; Plaza, M.; Turner, C.; Jónsdóttir, R.; Kristinsson, H.G.; Jacobsen, C.; Nielsen, K.F. Structure Dependent Antioxidant Capacity of Phlorotannins from Icelandic Fucus Vesiculosus by UHPLC-DAD-ECD-QTOFMS. Food Chem. 2018, 240, 904–909. [Google Scholar] [CrossRef]
- Amarante, S.J.; Catarino, M.D.; Marçal, C.; Silva, A.M.S.; Ferreira, R.; Cardoso, S.M. Microwave-Assisted Extraction of Phlorotannins from Fucus Vesiculosus. Mar. Drugs 2020, 18, 559. [Google Scholar] [CrossRef] [PubMed]
- Zhang, R.; Yuen, A.K.L.; Magnusson, M.; Wright, J.T.; de Nys, R.; Masters, A.F.; Maschmeyer, T. A Comparative Assessment of the Activity and Structure of Phlorotannins from the Brown Seaweed Carpophyllum Flexuosum. Algal Res. 2018, 29, 130–141. [Google Scholar] [CrossRef]
- Chouh, A.; Nouadri, T.; Catarino, M.D.; Silva, A.M.S.; Cardoso, S.M. Phlorotannins of the Brown Algae Sargassum Vulgare from the Mediterranean Sea Coast. Antioxidants 2022, 11, 1055. [Google Scholar] [CrossRef] [PubMed]
- Treml, J.; Šmejkal, K. Flavonoids as Potent Scavengers of Hydroxyl Radicals. Compr. Rev. Food Sci. Food Saf. 2016, 15, 720–738. [Google Scholar] [CrossRef] [PubMed]
- Balboa, E.M.; Conde, E.; Moure, A.; Falqué, E.; Domínguez, H. In Vitro Antioxidant Properties of Crude Extracts and Compounds from Brown Algae. Food Chem. 2013, 138, 1764–1785. [Google Scholar] [CrossRef] [PubMed]
- Miyasaka, N.; Hirata, Y. Nitric Oxide and Inflammatory Arthritides. Life Sci. 1997, 61, 2073–2081. [Google Scholar] [CrossRef]
- Kalinowska, M.; Gołębiewska, E.; Świderski, G.; Męczyńska-Wielgosz, S.; Lewandowska, H.; Pietryczuk, A.; Cudowski, A.; Astel, A.; Świsłocka, R.; Samsonowicz, M.; et al. Plant-Derived and Dietary Hydroxybenzoic Acids—A Comprehensive Study of Structural, Anti-/Pro-Oxidant, Lipophilic, Antimicrobial, and Cytotoxic Activity in MDA-MB-231 and MCF-7 Cell Lines. Nutrients 2021, 13, 3107. [Google Scholar] [CrossRef]
- Phang, S.J.; Teh, H.X.; Looi, M.L.; Arumugam, B.; Fauzi, M.B.; Kuppusamy, U.R. Phlorotannins from Brown Algae: A Review on Their Antioxidant Mechanisms and Applications in Oxidative Stress-Mediated Diseases. J. Appl. Phycol. 2023, 35, 867–892. [Google Scholar] [CrossRef]
- Yang, E.-J.; Ham, Y.M.; Lee, W.J.; Lee, N.H.; Hyun, C.-G. Anti-Inflammatory Effects of Apo-9′-Fucoxanthinone from the Brown Alga, Sargassum muticum. DARU J. Pharm. Sci. 2013, 21, 62. [Google Scholar] [CrossRef] [PubMed]
- Pérez, M.J.; Falqué, E.; Domínguez, H. Antimicrobial Action of Compounds from Marine Seaweed. Mar. Drugs 2016, 14, 52. [Google Scholar] [CrossRef]
- Moorthi, P.V. Antimicrobial Properties of Marine Seaweed, Sargassum muticum against Human Pathogens. J. Coast. Life Med. 2015, 3, 122–125. [Google Scholar] [CrossRef]
- Puspita, M.; Déniel, M.; Widowati, I.; Radjasa, O.K.; Douzenel, P.; Marty, C.; Vandanjon, L.; Bedoux, G.; Bourgougnon, N. Total Phenolic Content and Biological Activities of Enzymatic Extracts from Sargassum muticum (Yendo) Fensholt. J. Appl. Phycol. 2017, 29, 2521–2537. [Google Scholar] [CrossRef] [PubMed]
- Feigin, V.L.; Nichols, E.; Alam, T.; Bannick, M.S.; Beghi, E.; Blake, N.; Culpepper, W.J.; Dorsey, E.R.; Elbaz, A.; Ellenbogen, R.G.; et al. Global, Regional, and National Burden of Neurological Disorders, 1990–2016: A Systematic Analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019, 18, 459–480. [Google Scholar] [CrossRef] [PubMed]
- Gelenberg, A.J. The Prevalence and Impact of Depression. J. Clin. Psychiatry 2010, 71, e06. [Google Scholar] [CrossRef] [PubMed]
- Pinteus, S.; Lemos, M.F.L.; Alves, C.; Silva, J.; Pedrosa, R. The Marine Invasive Seaweeds Asparagopsis armata and Sargassum muticum as Targets for Greener Antifouling Solutions. Sci. Total Environ. 2021, 750, 141372. [Google Scholar] [CrossRef] [PubMed]
- Nagatsu, T.; Nakashima, A.; Watanabe, H.; Ito, S.; Wakamatsu, K. Neuromelanin in Parkinson’s Disease: Tyrosine Hydroxylase and Tyrosinase. Int. J. Mol. Sci. 2022, 23, 4176. [Google Scholar] [CrossRef]
- Hasegawa, T. Tyrosinase-Expressing Neuronal Cell Line as in Vitro Model of Parkinson’s Disease. Int. J. Mol. Sci. 2010, 11, 1082–1089. [Google Scholar] [CrossRef]
- Barbosa, M.; Fernandes, F.; Carlos, M.J.; Valentão, P.; Andrade, P.B. Adding Value to Marine Invaders by Exploring the Potential of Sargassum muticum (Yendo) Fensholt Phlorotannin Extract on Targets Underlying Metabolic Changes in Diabetes. Algal Res. 2021, 59, 102455. [Google Scholar] [CrossRef]
Experimental Design | Response | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Coded Value | Natural Value | ||||||||||
X1 | X2 | X3 | X1: t | X2: P | X3: S | Y | TPC | DPPH | ABTS | BCM | |
min | Bar | % | mg/g dw | mg PGE/g dw | nM R•/g dw | nM R•/g dw | µM βC/g dw | ||||
1 | −1 | −1 | −1 | 7.5 | 5.6 | 20.3 | 408.113 | 52.949 | 32.613 | 30.013 | 0.077 |
2 | −1 | −1 | 1 | 7.5 | 5.6 | 79.7 | 284.507 | 35.267 | 22.206 | 43.618 | 0.019 |
3 | −1 | 1 | −1 | 7.5 | 16.4 | 20.3 | 516.582 | 73.520 | 40.914 | 34.242 | 0.076 |
4 | −1 | 1 | 1 | 7.5 | 16.4 | 79.7 | 329.433 | 39.579 | 24.805 | 50.334 | 0.025 |
5 | 1 | −1 | −1 | 20.5 | 5.6 | 20.3 | 447.439 | 54.063 | 29.799 | 26.433 | 0.103 |
6 | 1 | −1 | 1 | 20.5 | 5.6 | 79.7 | 319.175 | 39.136 | 24.985 | 48.838 | 0.037 |
7 | 1 | 1 | −1 | 20.5 | 16.4 | 20.3 | 477.789 | 72.839 | 36.781 | 31.324 | 0.050 |
8 | 1 | 1 | 1 | 20.5 | 16.4 | 79.7 | 327.477 | 40.152 | 14.969 | 43.802 | 0.015 |
9 | 1.68 | 0 | 0 | 25 | 11 | 50 | 422.345 | 43.478 | 23.240 | 90.862 | 0.028 |
10 | −1.68 | 0 | 0 | 3 | 11 | 50 | 339.210 | 47.617 | 23.277 | 88.618 | 0.062 |
11 | 0 | −1.68 | 0 | 14 | 2 | 50 | 283.555 | 31.099 | 16.772 | 37.657 | 0.039 |
12 | 0 | 1.68 | 0 | 14 | 20 | 50 | 416.642 | 39.453 | 20.731 | 46.387 | 0.035 |
13 | 0 | 0 | −1.68 | 14 | 11 | 0 | 412.876 | 27.954 | 13.193 | 21.225 | 0.095 |
14 | 0 | 0 | 1.68 | 14 | 11 | 100 | 90.659 | 14.862 | 13.383 | 26.439 | 0.108 |
15 | −1.68 | −1.68 | −1.68 | 3 | 2 | 0 | 326.108 | 14.007 | 6.283 | 14.382 | 0.049 |
16 | −1.68 | −1.68 | 1.68 | 3 | 2 | 100 | 45.433 | 9.453 | 4.951 | 11.464 | 0.002 |
17 | −1.68 | 1.68 | −1.68 | 3 | 20 | 0 | 408.116 | 26.199 | 11.739 | 40.126 | 0.035 |
18 | −1.68 | 1.68 | 1.68 | 3 | 20 | 100 | 92.315 | 14.401 | 11.175 | 19.584 | 0.007 |
19 | 1.68 | −1.68 | −1.68 | 25 | 2 | 0 | 411.209 | 15.708 | 3.755 | 21.712 | 0.033 |
20 | 1.68 | −1.68 | 1.68 | 25 | 2 | 100 | 64.104 | 2.232 | 3.506 | 6.091 | 0.010 |
21 | 1.68 | 1.68 | −1.68 | 25 | 20 | 0 | 434.463 | 27.583 | 14.425 | 25.247 | 0.036 |
22 | 1.68 | 1.68 | 1.68 | 25 | 20 | 100 | 111.355 | 6.944 | 10.739 | 22.927 | 0.004 |
23 | 0 | 0 | 0 | 14 | 11 | 50 | 342.489 | 45.218 | 51.749 | 51.096 | 0.063 |
24 | 0 | 0 | 0 | 14 | 11 | 50 | 359.681 | 42.236 | 62.114 | 52.667 | 0.077 |
25 | 0 | 0 | 0 | 14 | 11 | 50 | 381.981 | 33.916 | 53.071 | 39.287 | 0.051 |
26 | 0 | 0 | 0 | 14 | 11 | 50 | 407.065 | 41.149 | 58.712 | 66.833 | 0.084 |
27 | 0 | 0 | 0 | 14 | 11 | 50 | 393.724 | 38.906 | 61.215 | 49.374 | 0.070 |
28 | 0 | 0 | 0 | 14 | 11 | 50 | 364.892 | 37.272 | 65.683 | 65.124 | 0.062 |
Coefficients | Parametric Responses to the cccd | |||||
---|---|---|---|---|---|---|
Extract | Phytochemical | Antioxidant Activity | ||||
Yield | TPC | DPPH• | ABTS•+ | BCM | ||
(A) Fitting Coefficients Obtained | ||||||
Intercept | b0 | 379.21 ± 17.58 | 41.62 ± 3.90 | 58.92 ± 3.62 | 53.86 ± 5.0 | 0.070 ± 0.005 |
Linear effect | b1 | ns | ns | ns | ns | ns |
b2 | 20.70 ± 8.51 | 3.18 ± 1.89 | 1.77 ± 1.47 | ns | −0.013 ± 0.010 | |
b3 | −62.28 ± 28.54 | −17.12 ± 6.34 | ns | 13.66 ± 6.8 | −0.037 ± 0.010 | |
Quadratic effect | b11 | 14.13 ± 13.70 | 5.24 ± 3.04 | −10.72 ± 2.39 | 10.26 ± 3.3 | −0.011 ± 0.004 |
b22 | ns | ns | −12.31 ± 2.39 | −6.61 ± 3.3 | −0.014 ± 0.004 | |
b33 | −31.48 ± 13.70 | −3.30 ± 3.04 | −14.25 ± 2.39 | −13.05 ± 3.3 | 0.009 ± 0.004 | |
Cubiceffect | b111 | ns | ns | ns | ns | ns |
b222 | ns | ns | ns | ns | 0.004 ± 0.004 | |
b333 | −11.38 ± 11.23 | 4.72 ± 2.49 | ns | −5.59 ± 2.7 | 0.011 ± 0.004 | |
Interactive effect | b12 | ns | ns | ns | ns | ns |
b13 | ns | ns | ns | ns | ns | |
b23 | ns | ns | ns | ns | ns | |
b123 | ns | ns | ns | ns | ns | |
b1122 | ns | ns | ns | ns | ns | |
b1133 | ns | ns | ns | ns | ns | |
b2233 | ns | ns | ns | ns | ns | |
b112233 | −4.07 ± 2.22 | −1.42 ± 0.49 | 2.43 ± 0.49 | ns | ns | |
R2 | 0.9298 | 0.8140 | 0.9042 | 0.8289 | 0.8487 | |
(B) Optimal Conditions And Response Values Obtained | ||||||
Optimum conditions | X1: t (min) | 14.00 ± 1.87 | 3.00 ± 0.87 | 14.00 ± 1.87 | 3.00 ± 0.87 | 14.00 ± 1.87 |
X2: P (bar) | 20.00 ± 2.24 | 20.00 ± 2.24 | 11.38 ± 1.69 | 11.00 ± 1.66 | 8.90 ± 1.49 | |
X3: S (%) | 0.00 ± 0.00 | 35.88 ± 3.0 | 50.00 ± 3.54 | 61.72 ± 3.93 | 8.70 ± 1.47 | |
mg/g dw | mg/g dw | nM R•/g dw | nM R•/g dw | µM βC/g dw | ||
Response | 483.87 ± 35.26 | 66.10 ± 13.03 | 58.98 ± 17.30 | 85.88 ± 20.70 | 0.112 ± 0.043 | |
Experimental | 469.4 ± 8.86 | 44.28 ± 1.95 | 50.15 ± 2.84 | 83.20 ± 11.57 | 0.101 ± 0.096 |
ID | Ref | Pol | Formula | MW (Da) | Prec. (m/z) | Product (m/z) | Col. Energy (V) | RFL (V) | Compound | Class | Subclass | mg/g E |
---|---|---|---|---|---|---|---|---|---|---|---|---|
C1 | [51] | [M − H]− | C16H16O6 | 304.095 | 302.72 | 92.883, 94.8 | 17.54, 17.43 | 111 | 3-O-Methylcatechin | Flavonoids | Flavanols | 0.029 |
C2 | [51] | [M − H]− | C15H14O7 | 306.074 | 322.877 | 138.967, 240.883 | 27.39, 18.41 | 109 | Gallocatechin | Flavonoids | Flavanols | <LOQ |
C3 | [53,54] | [M − H]+ | C16H14O6 | 302.079 | 303.636 | 90.967, 262.967 | 27.44, 5.3 | 117 | Hesperetin | Flavonoids | Flavanones | 0.642 |
C4 | [55,56] | [M − H]− | C21H22O11 | 450.116 | 448.576 | 94.8, 300.717 | 28.35, 9.14 | 104 | Taxifolin-O-rhamnoside | Flavonoids | Flavanonols | 0.010 |
C5 | [49] | [M − H]+ | C16H12O5 | 284.068 | 306.358 | 90.967, 91.967 | 28.3, 28.71 | 97 | Acacetin | Flavonoids | Flavones | <LOQ |
C6 | [47,57] | [M − H]− | C21H20O10 | 432.106 | 448.659 | 266.8, 300.717 | 10.11, 9.2 | 86 | Apigenin-7-glucoside | Flavonoids | Flavones | 0.021 |
C7 | [49] | [M − H]− | C16H12O6 | 300.063 | 298.689 | 92.917, 224.667 | 18, 9 | 105 | Hispidulin | Flavonoids | Flavones | 0.070 |
C8 | [47] | [M − H]+ | C21H20O11 | 448.101 | 470.64 | 112.8, 336.717 | 26.58, 10.56 | 108 | Luteolin-O-hexoside | Flavonoids | Flavones | 0.125 |
C9 | [58] | [M − H]+ | C27H30O16 | 610.153 | 610.544 | 112.8, 246.717 | 36.69, 25.62 | 147 | Luteolin-7-O-rutinoside | Flavonoids | Flavones | 0.063 |
C10 | [51] | [M − H]− | C27H30O14 | 578.164 | 576.706 | 352.55, 394.717 | 18.85, 8.39 | 93 | Rhoifolin | Flavonoids | Flavones | <LOQ |
C11 | [51] | [M − H]− | C17H14O7 | 330.074 | 346.794 | 138.667, 272.833 | 15, 9 | 68 | 3,7-Dimethylquercetin | Flavonoids | Flavonols | 0.007 |
C12 | [59,60] | [M − H]+ | C22H22O12 | 478.111 | 478.668 | 112.8, 114.8 | 24.46, 23.45 | 143 | Isorhamnetin 3-O-glucoside | Flavonoids | Flavonols | 0.090 |
C13 | [47,61] | [M − H]+ | C21H20O11 | 448.101 | 470.64 | 112.8, 114.8 | 26.63, 26.84 | 109 | Kaempferol-3-O-glucoside | Flavonoids | Flavonols | 0.125 |
C14 | [47] | [M − H]− | C27H30O16 | 610.153 | 626.457 | 285, 552.583 | 25, 13 | 102 | Kaempferol-O-hesoxide | Flavonoids | Flavonols | <LOQ |
C15 | [47,57] | [M − H]− | C27H30O15 | 594.158 | 628.428 | 446.633, 554.633 | 11.07, 12.68 | 98 | Kaempferol-O-rutinoside | Flavonoids | Flavonols | 0.009 |
C16 | [62] | [M − H]− | C15H10O8 | 318.038 | 316.997 | 151, 179 | 24, 19 | 161 | Myrecetin | Flavonoids | Flavonols | 0.007 |
C17 | [47] | [M − H]− | C21H19O12 | 463.088 | 462.63 | 271, 300.167 | 43, 27 | 119 | Quercetin-O-glucoside | Flavonoids | Flavonols | <LOQ |
C18 | [47,61] | [M − H]− | C24H22O15 | 550.096 | 566.899 | 251.25, 354.917 | 37, 15 | 119 | Quercetin-3-O-malonylglucoside | Flavonoids | Flavonols | <LOQ |
C19 | [47] | [M − H]− | C27H30O16 | 610.153 | 609.113 | 271.083, 300.33 | 59, 37 | 291 | Quercetin-O-rutinoside | Flavonoids | Flavonols | <LOQ |
C20 | [51] | [M − H]− | C22H20O11 | 460.101 | 494.37 | 270.8, 344.8 | 19.3, 11.12 | 113 | Glycitein-7-O-glucuronide | Flavonoids | Isoflavone | <LOQ |
C21 | [51] | [M − H]− | C17H16O5 | 300.1 | 316.736 | 92.883, 94.8 | 16.32, 16.27 | 88 | Sativanone | Flavonoids | Isoflavone | <LOQ |
C22 | [51] | [M − H]− | C7H6O2 | 122.037 | 156.889 | 70.967, 96.883 | 16.63, 12.99 | 79 | p-Hydroxybenzaldehyde | Other | HBD | 0.018 |
C23 | [51] | [M − H]− | C10H8O4 | 192.042 | 190.918 | 86.917, 110.917 | 17, 12 | 48 | Scopoletin | Other | HC | 0.077 |
C24 | [51] | [M − H]− | C20H26O4 | 330.183 | 328.893 | 271, 293, 271, 293 | 14, 12, 14, 12 | 72 | Carnosol | Other | Other | <LOQ |
C25 | [51] | [M − H]− | C13H16O8 | 300.085 | 316.721 | 92.8, 94.8 | 16.27, 16.52 | 90 | 4-Hydroxybenzoic acid glucoside | Phenolic acids | HBA | 0.258 |
C26 | [62] | [M − H]− | C7H6O5 | 170.022 | 168.981 | 79.24, 125.083 | 24, 15 | 121 | Gallic acid | Phenolic acids | HBA | 0.038 |
C27 | [63] | [M − H]− | C7H6O6S | 217.989 | 217.031 | 88.967, 181.05 | 20.11, 9.4 | 62 | Hydroxybenzoic acid sulphate | Phenolic acids | HBA | 21.861 |
C28 | [51] | [M − H]− | C8H8O7S | 247.999 | 247.042 | 88.967, 211.05 | 22, 10.81 | 150 | Vanillic acid 4-sulfate | Phenolic acids | HBA | 0.047 |
C29 | [51] | [M − H]− | C16H18O9 | 354.095 | 353.055 | 111, 172.917 | 22, 12 | 83 | Chlorogenic acid | Phenolic acids | HCA | <LOQ |
C30 | [64] | [M − H]− | C7H12O6 | 192.063 | 191.023 | 86.917, 110.917 | 17, 12 | 76 | Quinic acid | Phenolic acids | HCA | 0.110 |
C31 | [51] | [M − H]− | C11H12O5 | 224.068 | 222.944 | 164.883, 204.717 | 13.09, 13.49 | 150 | Sinapic acid | Phenolic acids | HCA | <LOQ |
C32 | [65] | [M − H]+ | C12H10O7 | 266.043 | 266.592 | 112.833, 114.833 | 9, 8 | 84 | Bifuhalol | Tannins | HT | 3.121 |
C33 | [66] | [M − H]− | C24H18O12 | 498.08 | 496.706 | 92.833, 240.833 | 32, 18 | 75 | Bisfucophlorethol | Tannins | HT | 0.047 |
C34 | [65] | [M − H]− | C36H22O18 | 742.081 | 758.834 | 626.583, 684.75 | 14, 15 | 113 | Dieckol | Tannins | HT | 0.013 |
C35 | [50,65] | [M − H]+ | C12H10O6 | 250.048 | 251.097 | 82.833, 205.083 | 33, 16 | 65 | Difucol | Tannins | HT | 7.555 |
C36 | [47] | [M − H]− | C20H20O14 | 484.085 | 482.545 | 332.717, 334.717 | 10.11, 10.71 | 119 | Digalloylglucose | Tannins | HT | 0.039 |
C37 | [49] | [M − H]− | C24H18O13 | 514.075 | 548.594 | 338.8, 474.633 | 19.86, 11.87 | 90 | Deshydroxetrafuhalol | Tannins | HT | <LOQ |
C38 | [49] | [M − H]− | C42H30O23 | 902.118 | 900.411 | 616.633, 632.383 | 21.68, 30.48 | 147 | Dihydroxiheptafuhalol | Tannins | HT | <LOQ |
C39 | [52] | [M − H]+ | C36H26O19 | 762.107 | 784.646 | 183.967, 602.633 | 29.97, 8.44 | 154 | Dihydroxyhexafuhalol | Tannins | HT | 0.075 |
C40 | [52] | [M − H]+ | C54H38O28 | 1134.155 | 1156.444 | 974.383, 1065.383 | 10.66, 652 | 179 | Dihydroxynonafuhalol | Tannins | HT | 0.088 |
C41 | [52] | [M − H]− | C48H34O25 | 1010.139 | 1008.432 | 528.05, 972.55 | 39.27, 15.11 | 299 | Dihydroxyoctafuhalol | Tannins | HT | 0.013 |
C42 | [52] | [M − H]+ | C30H22O16 | 638.091 | 638.398 | 112.8, 456.717 | 38.72, 10.31 | 133 | Dihydroxypentafuhalol | Tannins | HT | 0.041 |
C43 | [52] | [M − H]− | C60H42O31 | 1258.171 | 1275.057 | 1184.3 | 5.61 | 165 | Deshydroydecafuhalol | Tannins | HT | 0.034 |
C44 | [65] | [M − H]+ | C18H10O9 | 370.032 | 370.582 | 112.8, 114.717 | 16.78, 18.65 | 94 | Dioxinodehydroeckol | Tannins | HT | 0.360 |
C45 | [67] | [M − H]− | C24H16O13 | 512.059 | 510.602 | 210.8, 284.8 | 24.87, 17.89 | 97 | Diphlorethohydroxycarmalol | Tannins | HT | 0.037 |
C46 | [65] | [M − H]+ | C18H12O9 | 372.048 | 371.348 | 112.917, 118.833 | 15, 5 | 104 | Eckol | Tannins | HT | 0.070 |
C47 | [66] | [M − H]− | C24H18O12 | 498.08 | 496.623 | 287.083, 348.667 | 18, 9 | 103 | Fucodiphlorethol | Tannins | HT | 0.024 |
C48 | [68] | [M − H]− | C18H10O9 | 370.032 | 368.825 | 110.883, 186.8 | 20.72, 10.56 | 70 | Phloroethol | Tannins | HT | 0.328 |
C49 | [66] | [M − H]− | C18H14O9 | 374.064 | 372.774 | 224.75, 298.17 | 14, 9 | 93 | Fucophlorethol | Tannins | HT | <LOQ |
C50 | [69] | [M − H]− | C60H42O30 | 1242.176 | 1241.302 | 877.383, 968.383 | 24, 16 | 174 | Fucophlorethol decamer | Tannins | HT | <LOQ |
C51 | [70] | [M − H]− | C42H30O21 | 870.128 | 869.421 | 589, 792.833, 794.5 | 25, 17, 14 | 127 | Fucophlorethol heptamer | Tannins | HT | <LOQ |
C52 | [70] | [M − H]− | C36H26O18 | 746.112 | 744.405 | 596.25, 670.5 | 19, 12 | 119 | Fucophlorethol hexamer | Tannins | HT | <LOQ |
C53 | [69] | [M − H]− | C54H38O27 | 1118.16 | 1153.262 | 971.467, 1135.55 | 12.08, 9.35 | 149 | Fucophlorethol nonamer | Tannins | HT | 0.038 |
C54 | [69] | [M − H]− | C48H34O24 | 994.144 | 992.437 | 810.467, 901.467 | 10.51, 7.68 | 142 | Fucophlorethol octamer | Tannins | HT | 0.059 |
C55 | [66] | [M − H]− | C36H26O18 | 746.112 | 744.405 | 460.55, 670.55 | 23.55, 12.99 | 113 | Fucotetraphlorethol | Tannins | HT | 0.026 |
C56 | [70] | [M − H]− | C30H22O15 | 622.096 | 656.365 | 506.633, 582.55 | 14.25, 12.63 | 99 | Fucotriphlorethol | Tannins | HT | 0.087 |
C57 | [71] | [M − H]− | C42H30O21 | 870.128 | 904.397 | 550.55, 624.633 | 31.99, 22.19 | 127 | Heptafucol | Tannins | HT | <LOQ |
C58 | [65] | [M − H]− | C42H30O24 | 918.113 | 952.382 | 672.133, 878.383 | 51, 17.84 | 256 | Heptafuhalol | Tannins | HT | 0.020 |
C59 | [52] | [M − H]+ | C36H26O21 | 794.097 | 832.443 | 773.55, 814.467 | 26.08, 5.3 | 148 | Hexafuhalol | Tannins | HT | <LOQ |
C60 | [47] | [M − H]+ | C42H30O25 | 934.108 | 934.415 | 722.883, 752.467 | 23.55, 12.13 | 151 | HHDP-galloylglucose | Tannins | HT | 0.177 |
C61 | [66] | [M − H]− | C24H14O12 | 494.049 | 492.591 | 344.717, 418.717 | 11.22, 10.71 | 113 | Hydroxyfucofuroeckol | Tannins | HT | 0.045 |
C62 | [52] | [M − H]+ | C42H30O25 | 934.108 | 934.415 | 752.467, 850.467 | 11.42, 16.78 | 152 | Hydroxyheptafuhalol | Tannins | HT | 0.182 |
C63 | [49] | [M − H]− | C36H26O22 | 810.092 | 808.384 | 658.55, 676.55 | 13.34 | 116 | Hydroxyhexafuhalol | Tannins | HT | <LOQ |
C64 | [49] | [M − H]− | C30H22O18 | 670.081 | 668.54 | 486.6, 520.6, 594.6 | 10.16, 14.1, 13.8 | 103 | Hydroxypentafuhalol | Tannins | HT | 0.059 |
C65 | [71] | [M − H]− | C24H18O15 | 546.065 | 580.501 | 300.8, 506.633 | 13.14, 12.03 | 99 | Hydroxytetrafuhalol | Tannins | HT | 0.061 |
C66 | [52] | [M − H]− | C48H34O28 | 1058.124 | 1056.749 | 844.717 | 14.65 | 153 | Octafuhalol | Tannins | HT | <LOQ |
C67 | [71] | [M − H]− | C30H22O17 | 654.086 | 652.545 | 262.717, 470.633 | 29.72, 9.95 | 101 | Pentafuhalol | Tannins | HT | <LOQ |
C68 | [47] | [M − H]+ | C24H16O12 | 496.064 | 496.614 | 112.917, 114.833 | 23, 22 | 133 | Phloroeckol | Tannins | HT | 0.244 |
C69 | [51] | [M − H]+ | C6H6O3 | 126.032 | 126.081 | 56.083, 98 | 21, 12 | 78 | Phloroglucinol | Tannins | HT | 0.053 |
C70 | [72] | [M − H]− | C24H18O14 | 530.07 | 528.612 | 394.667, 454.667 | 10, 11 | 110 | Tetrafuhalol | Tannins | HT | 0.009 |
C71 | [69] | [M − H]− | C18H14O9 | 374.064 | 372.69 | 93224.833 | 23, 15 | 93 | Trifucol | Tannins | HT | 0.139 |
C72 | [52] | [M − H]− | C18H14O10 | 390.059 | 388.768 | 206.8333, 14.75 | 9, 10 | 68 | Trifuhalol | Tannins | HT | 0.040 |
C73 | [65] | [M − H]− | C30H20O17 | 652.07 | 650.613 | 318.717, 468.633 | 19.1, 9.75 | 101 | Trifuhalolhydroxycarmalol | Tannins | HT | <LOQ |
C74 | [51] | [M − H]− | C13H8O4 | 228.042 | 244.929 | 94.8, 96.717 | 6.47, 6.01 | 63 | Urolithin A | Tannins | HT | 0.071 |
Optimized Extract | Positive Control | |
---|---|---|
A: Antioxidant Activity (IC50, µg/mL) | ||
IC50 (µg/mL) | Ascorbic acid | |
•NO | 100.1 | 446 |
O2−• | 57.72 | 160 |
H2O2 | 227.9 | 51 |
OH•− | 989.5 | 183 |
B: Health promoting enzymes (IC50, µg/mL) | ||
tyrosinase | 238.7 | Kojic acid = 2.00 |
α-amylase | 31.60 | Acarbose = 300 |
C: Cytotoxicity (GI50, µg/mL) | ||
Ellipticine | ||
A549 (lung adenocarcinoma) | 132.7 | <0.78 |
HepG2 (hepatocellular carcinoma) | 34.49 | 0.85 ± 0.046 |
AGS (gastric adenocarcinoma) | 40.19 | <0.78 |
Vero | 144.8 | <0.78 |
D: Antimicrobial activity (mm; mg/mL) | ||
Inhibition zone (mm) | MIC (mg/mL) | |
Escherichia coli | - | >8 |
Staphylococcus epidermidis | - | >8 |
Bacillus cereus | - | >8 |
Staphylococcus aureus | 9.42 ± 1.04 | 8 |
Salmonella enteritidis | - | 8 |
Pseudomonas aeruginosa | >8 |
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Silva, A.; Cassani, L.; Carpena, M.; Lourenço-Lopes, C.; Grosso, C.; Chamorro, F.; García-Pérez, P.; Carvalho, A.; Domingues, V.F.; Barroso, M.F.; et al. Exploring the Potential of Invasive Species Sargassum muticum: Microwave-Assisted Extraction Optimization and Bioactivity Profiling. Mar. Drugs 2024, 22, 352. https://doi.org/10.3390/md22080352
Silva A, Cassani L, Carpena M, Lourenço-Lopes C, Grosso C, Chamorro F, García-Pérez P, Carvalho A, Domingues VF, Barroso MF, et al. Exploring the Potential of Invasive Species Sargassum muticum: Microwave-Assisted Extraction Optimization and Bioactivity Profiling. Marine Drugs. 2024; 22(8):352. https://doi.org/10.3390/md22080352
Chicago/Turabian StyleSilva, Aurora, Lucia Cassani, Maria Carpena, Catarina Lourenço-Lopes, Clara Grosso, Franklin Chamorro, Pascual García-Pérez, Ana Carvalho, Valentina F. Domingues, M. Fátima Barroso, and et al. 2024. "Exploring the Potential of Invasive Species Sargassum muticum: Microwave-Assisted Extraction Optimization and Bioactivity Profiling" Marine Drugs 22, no. 8: 352. https://doi.org/10.3390/md22080352