A Comparative Study of the Phytochemical Composition, Antioxidant Properties, and In Vitro Anti-Diabetic Efficacy of Different Extracts of Caulerpa prolifera
[en] The Moroccan coastline has been the focus of attention for researchers studying the national algal flora, with the aim of preserving these invaluable natural resources. Since the year 2000, these resources have stimulated great interest in the creation of new drugs, as well as their integration into food supplements and foods. Therefore, this study aims to explore the phytochemistry of a series of extracts derived from Caulerpa prolifera. To ensure better extraction of the various metabolites present, two extraction methods, namely maceration and the Soxhlet method, were employed using solvents of varying polarity (hexane, ethyl acetate, methanol, and water). The chemical composition of the extracts was analyzed using GC-MS for fatty acids and HPLC-DAD for phenolic compounds. Antioxidant activity was evaluated using DPPH and β-carotene bleaching assays, while antidiabetic potential was assessed by in vitro inhibition of α-amylase and α-glucosidase. In addition, Molecular docking models were employed to assess the interaction between the bioactive molecules and the human pancreatic α-amylase and α-glucosidase enzymes. Vanillin, p-coumaric acid, sinapic acid, 7,3′,4′-flavon-3-ol, and kaempferol were the most abundant phenolic compounds. Anti-diabetic and antioxidant effects were highly significant.
Disciplines :
Agriculture & agronomy Chemistry
Author, co-author :
Ouahabi, Safae; Faculty of Medicine and Pharmacy of Oujda, Mohammed First University, Morocco ; Laboratory of Bioresources, Biotechnology, Ethnopharmacology and Health, Faculty of Sciences, Mohammed First University, Oujda, Morocco
Daoudi, Elhouda; Laboratory of Bioresources, Biotechnology, Ethnopharmacology and Health, Faculty of Sciences, Mohammed First University, Oujda, Morocco ; Higher Institute of Nursing Professions and Health Techniques, Oujda, Morocco
Chebaibi, Mohamed; Ministry of Health and Social Protection, Higher Institute of Nursing Professions and Health Techniques, Fez, Morocco ; Biomedical and Translational Research Laboratory, Faculty of Medicine and Pharmacy of Fez, Sidi Mohamed Ben Abdellah University, Fez, Morocco
Mssillou, Ibrahim; National Agency of Medicinal and Aromatic Plants, Principal, Taounate, Morocco
Rahhou, Ilyesse; Higher Institute of Nursing Professions and Health Techniques, Oujda, Morocco
Bnouham, Mohamed; Laboratory of Bioresources, Biotechnology, Ethnopharmacology and Health, Faculty of Sciences, Mohammed First University, Oujda, Morocco
Hammouti, Belkheir; Euromed Research Center, Euromed Polytechnic School, Euromed University of Fes (UEMF), Morocco
Fauconnier, Marie-Laure ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Gotor, Alicia; Institut Polytechnique UniLaSalle, AGHYLE, UniLaSalle, Beauvais, France
Rhazi, Larbi; Institut Polytechnique UniLaSalle, Université d'Artois, Beauvais, France
Ramdani, Mohammed; Laboratory of Applied and Environmental Chemistry (LCAE), Faculty of Sciences, Mohammed First University, Oujda, Morocco
Language :
English
Title :
A Comparative Study of the Phytochemical Composition, Antioxidant Properties, and In Vitro Anti-Diabetic Efficacy of Different Extracts of Caulerpa prolifera
Snoussi M. Ouchani T. Khouakhi A. Niang-Diop I. Impacts of Sea-Level Rise on the Moroccan Coastal Zone: Quantifying Coastal Erosion and Flooding in the Tangier Bay Geomorphology 2009 107 32 40 10.1016/j.geomorph.2006.07.043
Benhissoune S. Boudouresque C. Verlaque M. A CheckList of Marine Seaweeds of the Mediterranean and Atlantic Coasts of Morocco. I. Chlorophyceae Wille s. l Bot. Mar. 2001 44 171 182 10.1515/BOT.2001.023
Benhissoune S. Boudouresque C. Perret-Boudouresque M. Verlaque M. A Checklist of the Seaweeds of the Mediterranean and Atlantic Coasts of Morocco. III. Rhodophyceae (Excluding Ceramiales) Bot. Mar. 2002 45 391 412 10.1515/BOT.2002.041
Elasri O. Ramdani M. Latrach L. Benyounes H. Mohamed elamin A. Mohammed R. Comparison of Energy Recovery after Anaerobic Digestion of Three Marchica Lagoon Algae (Caulerpa prolifera, Colpomenia sinuosa, Gracilaria bursa-pastoris) Sustain. Mater. Technol. 2017 11 47 52
Wang L. Wang X. Wu H. Liu R. Overview on Biological Activities and Molecular Characteristics of Sulfated Polysaccharides from Marine Green Algae in Recent Years Mar. Drugs 2014 12 4984 5020 10.3390/md12094984
Crockett P.F. Keough M.J. Ecological Niches of Three Abundant Caulerpa Species in Port Phillip Bay, Southeast Australia Aquat. Bot. 2014 119 120 131 10.1016/j.aquabot.2014.08.007
de Senerpont Domis L. Famà P. Bartlett A. Prud’homme van Reine W. Espinosa C. Trono J. Gavino Defining Taxon Boundaries in Members of the Morphologically and Genetically Plastic Genus Caulerpa (Caulerpales, Chlorophyta) J. Phycol. 2003 39 1019 1037 10.1111/j.0022-3646.2003.02-203.x
Fernández-García C. Cortés J. Alvarado J.J. Nivia-Ruiz J. Physical Factors Contributing to the Benthic Dominance of the Alga Caulerpa sertularioides (Caulerpaceae, Chlorophyta) in the Upwelling Bahía Culebra, North Pacific of Costa Rica Rev. Biol. Trop. 2015 60 93 10.15517/rbt.v60i2.19970
Gacia E. Rodríguez-Prieto C. Delgado O. Ballesteros E. Seasonal Light and Temperature Responses of Caulerpa Taxifolia from the Northwestern Mediterranean Aquat. Bot. 1996 53 215 225 10.1016/0304-3770(95)01001-7
Ohba H. Nashima H. Enomoto S. Culture Studies on Caulerpa (Caulerpales, Chlorophyceae) III. Reproduction, Development and Morphological Variation of Laboratory-Cultured, C. racemosa Var peltata. Bot. Mag. 1992 105 589 600 10.1007/BF02489433
Kumari P. Kumar M. Gupta V. Reddy C.R.K. Jha B. Tropical Marine Macroalgae as Potential Sources of Nutritionally Important PUFAs Food Chem. 2010 120 749 757 10.1016/j.foodchem.2009.11.006
Nagappan T. Vairappan C.S. Nutritional and Bioactive Properties of Three Edible Species of Green Algae, Genus Caulerpa (Caulerpaceae) J. Appl. Phycol. 2014 26 1019 1027 10.1007/s10811-013-0147-8
de Gaillande C. Payri C. Remoissenet G. Zubia M. Caulerpa Consumption, Nutritional Value and Farming in the Indo-Pacific Region J. Appl. Phycol. 2017 29 2249 2266 10.1007/s10811-016-0912-6
Paul N.A. Neveux N. Magnusson M. de Nys R. Comparative Production and Nutritional Value of “Sea Grapes”—The Tropical Green Seaweeds Caulerpa lentillifera and C. racemosa J. Appl. Phycol. 2014 26 1833 1844 10.1007/s10811-013-0227-9
Ghosh P. Adhikari U. Ghosal P.K. Pujol C.A. Carlucci M.J. Damonte E.B. Ray B. In Vitro Anti-Herpetic Activity of Sulfated Polysaccharide Fractions from Caulerpa Racemosa Phytochemistry 2004 65 3151 3157 10.1016/j.phytochem.2004.07.025
Hayakawa Y. Hayashi T. Lee J.-B. Srisomporn P. Maeda M. Ozawa T. Sakuragawa N. Inhibition of Thrombin by Sulfated Polysaccharides Isolated from Green Algae Biochim. Biophys. Acta (BBA)-Protein Struct. Mol. Enzymol. 2000 1543 86 94 10.1016/S0167-4838(00)00193-X
Ji H. Shao H. Zhang C. Hong P. Xiong H. Separation of the Polysaccharides in Caulerpa racemosa and Their Chemical Composition and Antitumor Activity J. Appl. Polym. Sci. 2008 110 1435 1440 10.1002/app.28676
Maeda R. Ida T. Ihara H. Sakamoto T. Immunostimulatory Activity of Polysaccharides Isolated from Caulerpa lentillifera on Macrophage Cells Biosci. Biotechnol. Biochem. 2012 76 501 505 10.1271/bbb.110813
Rodrigues J.A.G. Neto É.M. Teixeira L.A.C. de Paula R.C.M. Mourão P.A.d.S. Benevides N.M.B. Structural Features and Inactivation of Coagulation Proteases of a Sulfated Polysaccharidic Fraction from Caulerpa cupressoides Var. Lycopodium (Caulerpaceae, Chlorophyta) Acta Sci. Technol. 2013 35 611 619 10.4025/Actascitechnol.V35i4.16709
Holdt S.L. Kraan S. Bioactive Compounds in Seaweed: Functional Food Applications and Legislation J. Appl. Phycol. 2011 23 543 597 10.1007/s10811-010-9632-5
Doty M.S. Aguilar-Santos G. Caulerpicin, a Toxic Constituent of Caulerpa Nature 1966 211 990 10.1038/211990a0 5968321
Mandlik R.V. Naik S.R. Zine S. Ved H. Doshi G. Antidiabetic Activity of Caulerpa Racemosa: Role of Proinflammatory Mediators, Oxidative Stress, and Other Biomarkers Planta Medica Int. Open 2022 9 e60 e71 10.1055/a-1712-8178
Fajriah S. Rizki I.F. Sinurat E. Characterization and Analysis of the Antidiabetic Activities of Sulphated Polysaccharide Extract from Caulerpa lentillifera Pharmacia 2021 68 869 875 10.3897/pharmacia.68.e73158
Bradshaw P.C. Cytoplasmic and Mitochondrial NADPH-Coupled Redox Systems in the Regulation of Aging Nutrients 2019 11 504 10.3390/nu11030504
Bitwell C. Indra S.S. Luke C. Kakoma M.K. A Review of Modern and Conventional Extraction Techniques and Their Applications for Extracting Phytochemicals from Plants Sci. Afr. 2023 19 e01585 10.1016/j.sciaf.2023.e01585
Alara O.R. Abdurahman N.H. Ukaegbu C.I. Extraction of Phenolic Compounds: A Review Curr. Res. Food Sci. 2021 4 200 214 10.1016/j.crfs.2021.03.011
Do Q.D. Angkawijaya A.E. Tran-Nguyen P.L. Huynh L.H. Soetaredjo F.E. Ismadji S. Ju Y.-H. Effect of Extraction Solvent on Total Phenol Content, Total Flavonoid Content, and Antioxidant Activity of Limnophila aromatica J. Food Drug Anal. 2014 22 296 302 10.1016/j.jfda.2013.11.001
Dhanani T. Shah S. Gajbhiye N.A. Kumar S. Effect of Extraction Methods on Yield, Phytochemical Constituents and Antioxidant Activity of Withania somnifera Arab. J. Chem. 2017 10 S1193 S1199 10.1016/j.arabjc.2013.02.015
Guo H. Yao J. Sun Z. Duan D. Effects of Salinity and Nutrients on the Growth and Chlorophyll Fluorescence of Caulerpa lentillifera Chin. J. Ocean. Limnol. 2015 33 410 418 10.1007/s00343-015-4105-y
Jung K.A. Lim S.-R. Kim Y. Park J.M. Potentials of Macroalgae as Feedstocks for Biorefinery Bioresour. Technol. 2013 135 182 190 10.1016/j.biortech.2012.10.025
Ortiz J. Romero N. Robert P. Araya J. Lopez-Hernández J. Bozzo C. Navarrete E. Osorio A. Rios A. Dietary Fiber, Amino Acid, Fatty Acid and Tocopherol Contents of the Edible Seaweeds Ulva Lactuca and Durvillaea antarctica Food Chem. 2006 99 98 104 10.1016/j.foodchem.2005.07.027
Qudus B. Aroyehun A. Abdul Razak S. Palaniveloo K. Nagappan T. Suraiza Nabila Rahmah N. Wee Jin G. Chellappan D.K. Chellian J. Kunnath A.P. Bioprospecting Cultivated Tropical Green Algae, Caulerpa Racemosa (Forsskal) J. Agardh: A Perspective on Nutritional Properties, Antioxidative Capacity and Anti-Diabetic Potential Foods 2020 9 1313 10.3390/foods9091313 32961907
Bano S. Perveen S. Ahmad V.U. Bano N. Shameel M. Chemical Constituents of Endarachne binghamiae (Scytosiphonales, Phaeophyta) from the Karachi Coast Bot. Mar. 1987 30 371 372 10.1515/botm.1987.30.5.371
Bano S. Hayee A. Ahmad V.U. Shaikh W. Usmanghani K. Shameel M. Marine Natural Products. Part VII. Steroids from a Red Alga Asparagopsis sandfordiana Pol. J. Chem. 1988 62 905 906
Wood B.J.B. Fatty Acids and Lipids in Algae Microbial Lipids Academic Press New York, NY, USA 1988 807 867
Hertog M.G.L. Feskens E.J.M. Kromhout D. Hertog M.G.L. Hollman P.C.H. Hertog M.G.L. Katan M.B. Dietary Antioxidant Flavonoids and Risk of Coronary Heart Disease: The Zutphen Elderly Study Lancet 1993 342 1007 1011 10.1016/0140-6736(93)92876-U
Manach C. Mazur A. Scalbert A. Polyphenols and Prevention of Cardiovascular Diseases Curr. Opin. Lipidol. 2005 16 77 84 10.1097/00041433-200502000-00013
van Dam R.M. Hu F.B. Coffee Consumption and Risk of Type 2 Diabetes: A Systematic Review JAMA 2005 294 97 10.1001/jama.294.1.97
Panche A.N. Diwan A.D. Chandra S.R. Flavonoids: An Overview J. Nutr. Sci. 2016 5 e47 10.1017/jns.2016.41
Ferdous U.T. Balia Yusof Z.N. Insight into Potential Anticancer Activity of Algal Flavonoids: Current Status and Challenges Molecules 2021 26 6844 10.3390/molecules26226844
Duthie G. Morrice P. Antioxidant Capacity of Flavonoids in Hepatic Microsomes Is Not Reflected by Antioxidant Effects In Vivo Oxidative Med. Cell. Longev. 2012 2012 1 6 10.1155/2012/165127 22919437
Tungmunnithum D. Thongboonyou A. Pholboon A. Yangsabai A. Flavonoids and Other Phenolic Compounds from Medicinal Plants for Pharmaceutical and Medical Aspects: An Overview Medicines 2018 5 93 10.3390/medicines5030093 30149600
Fernández-Agulló A. Pereira E. Freire M.S. Valentão P. Andrade P.B. González-Álvarez J. Pereira J.A. Influence of Solvent on the Antioxidant and Antimicrobial Properties of Walnut (Juglans regia L.) Green Husk Extracts Ind. Crops Prod. 2013 42 126 132 10.1016/j.indcrop.2012.05.021
Tundis R. Loizzo M.R. Menichini F. Natural Products as α-Amylase and α-Glucosidase Inhibitors and Their Hypoglycaemic Potential in the Treatment of Diabetes: An Update Mini Rev. Med. Chem. 2010 10 315 331 10.2174/138955710791331007
Hameed I. Masoodi S.R. Mir S.A. Nabi M. Ghazanfar K. Ganai B.A. Type 2 Diabetes Mellitus: From a Metabolic Disorder to an Inflammatory Condition World J. Diabetes 2015 6 598 10.4239/wjd.v6.i4.598
Arayne M. Sultana N. Mirza A. MH Z. Siddiqui F. In Vitro Hypoglycemic Activity of Methanolic Extracts of Some Indigenous Plants Pak. J. Pharm. Sci. 2007 20 268 273
Daoudi N.E. Bouziane O. Bouhrim M. Bnouham M. Natural Aldose Reductase Inhibitors for Treatment and Prevention of Diabetic Cataract: A Review Herba Pol. 2022 68 35 58 10.2478/hepo-2022-0002
Baynes J.W. Thorpe S.R. Role of Oxidative Stress in Diabetic Complications: A New Perspective on an Old Paradigm Diabetes 1999 48 1 9 10.2337/diabetes.48.1.1
Dalli M. Daoudi N.E. Abrigach F. Azizi S. Bnouham M. Kim B. Gseyra N. In Vitro α-Amylase and Hemoglobin Glycation Inhibitory Potential of Nigella Sativa Essential Oil, and Molecular Docking Studies of Its Principal Components Front. Pharmacol. 2022 13 1036129 10.3389/fphar.2022.1036129
Nainu F. Frediansyah A. Mamada S.S. Permana A.D. Salampe M. Chandran D. Emran T.B. Simal-Gandara J. Natural Products Targeting Inflammation-Related Metabolic Disorders: A Comprehensive Review Heliyon 2023 9 e16919 10.1016/j.heliyon.2023.e16919
Oboh G. Ogunsuyi O.B. Ogunbadejo M.D. Adefegha S.A. Influence of Gallic Acid on α-Amylase and α-Glucosidase Inhibitory Properties of Acarbose J. Food Drug Anal. 2016 24 627 634 10.1016/j.jfda.2016.03.003 28911570
Ouahabi S. Loukili E.H. Daoudi N.E. Chebaibi M. Ramdani M. Rahhou I. Bnouham M. Fauconnier M.-L. Hammouti B. Rhazi L. et al. Study of the Phytochemical Composition, Antioxidant Properties, and In Vitro Anti-Diabetic Efficacy of Gracilaria Bursa-Pastoris Extracts Mar. Drugs 2023 21 372 10.3390/md21070372 37504903
Hayat J. Akodad M. Moumen A. Baghour M. Skalli A. Ezrari S. Belmalha S. Phytochemical Screening, Polyphenols, Flavonoids and Tannin Content, Antioxidant Activities and FTIR Characterization of Marrubium vulgare L. from 2 Different Localities of Northeast of Morocco Heliyon 2020 6 e05609 10.1016/j.heliyon.2020.e05609 33305038
Muniyandi K. George E. Sathyanarayanan S. George B.P. Abrahamse H. Thamburaj S. Thangaraj P. Phenolics, Tannins, Flavonoids and Anthocyanins Contents Influenced Antioxidant and Anticancer Activities of Rubus Fruits from Western Ghats, India Food Sci. Hum. Wellness 2019 8 73 81 10.1016/j.fshw.2019.03.005
Belkacemi L. Belalia M. Djendara A. Bouhadda Y. Antioxidant and Antibacterial Activities and Identification of Bioactive Compounds of Various Extracts of Caulerpa Racemosa from Algerian Coast Asian Pac. J. Trop. Biomed. 2020 10 87 10.4103/2221-1691.275423
Cotas J. Leandro A. Monteiro P. Pacheco D. Figueirinha A. Gonçalves A.M.M. da Silva G.J. Pereira L. Seaweed Phenolics: From Extraction to Applications Mar. Drugs 2020 18 384 10.3390/md18080384
Daoudi N.E. Bouhrim M. Ouassou H. Legssyer A. Mekhfi H. Ziyyat A. Aziz M. Bnouham M. Inhibitory Effect of Roasted/ Unroasted Argania Spinosa Seeds Oil on α- Glucosidase, α-Amylase and Intestinal Glucose Absorption Activities S. Afr. J. Bot. 2020 135 413 420 10.1016/j.sajb.2020.09.020
Lakshmanasenthil S. Vinoth Kumar T. Geetharamani D. Shanthi Priya S. α-Amylase and α-Glucosidase InhibitoryActivity of Tetradecanoic Acid (TDA) from Sargassum wightii with Relevance to Type 2 Diabetes Mellitus J. Biol. Act. Prod. Nat. 2018 8 180 191 10.1080/22311866.2018.1474803
Salazar M.O. Osella M.I. Arcusin D.E.J. Lescano L.E. Furlan R.L.E. New α-Glucosidase Inhibitors from a Chemically Engineered Essential Oil of Origanum vulgare L. Ind. Crops Prod. 2020 156 112855 10.1016/j.indcrop.2020.112855
Wuttke A. Idevall-Hagren O. Tengholm A. P2Y 1 Receptor-dependent Diacylglycerol Signaling Microdomains in β Cells Promote Insulin Secretion FASEB J. 2013 27 1610 1620 10.1096/fj.12-221499
Stalikas C.D. Extraction, Separation, and Detection Methods for Phenolic Acids and Flavonoids J. Sep. Sci. 2007 30 3268 3295 10.1002/jssc.200700261 18069740
Azwanida N. A Review on the Extraction Methods Use in Medicinal Plants, Principle, Strength and Limitation Med. Aromat. Plants 2015 4 196 10.4172/2167-0412.1000196
Dai J. Mumper R.J. Plant Phenolics: Extraction, Analysis and Their Antioxidant and Anticancer Properties Molecules 2010 15 7313 7352 10.3390/molecules15107313 20966876
Taibi M. Loukili E.H. Elbouzidi A. Baraich A. Haddou M. Bellaouchi R. Saalaoui E. Asehraou A. Addi M. Bourhia M. et al. Exploring the Pharmacological Potential of the Chemically Characterized Essential Oil from Clinopodium nepeta Subsp. Ascendens: A Combined In Vitro and In Silico Analysis Moroc. J. Chem. 2024 12 997 1021 10.48317/IMIST.PRSM/MORJCHEM-V12I3.47197
Loukili E.H. Abrigach F. Bouhrim M. Bnouham M. Fauconnier M. Ramdani M. Chemical Composition and Physicochemical Analysis of Opuntia dillenii Extracts Grown in Morocco J. Chem. 2021 2021 8858929 10.1155/2021/8858929
Brand-Williams W. Cuvelier M.E. Berset C. Use of a Free Radical Method to Evaluate Antioxidant Activity LWT-Food Sci. Technol. 1995 28 25 30 10.1016/S0023-6438(95)80008-5
Bekkouch O. Harnafi M. Touiss I. Khatib S. Harnafi H. Alem C. Amrani S. In Vitro Antioxidant and In Vivo Lipid-Lowering Properties of Zingiber officinale Crude Aqueous Extract and Methanolic Fraction: A Follow-Up Study Evid.-Based Complement. Altern. Med. 2019 2019 9734390 10.1155/2019/9734390
Hbika A. Daoudi N.E. Bouyanzer A. Bouhrim M. Mohti H. Loukili E.H. Mechchate H. Al-Salahi R. Nasr F.A. Bnouham M. et al. Artemisia Absinthium L. Aqueous and Ethyl Acetate Extracts: Antioxidant Effect and Potential Activity In Vitro and In Vivo against Pancreatic α-Amylase and Intestinal α-Glucosidase Pharmaceutics 2022 14 481 10.3390/pharmaceutics14030481
Lafraxo S. El Moussaoui A. A Bin Jardan Y. El Barnossi A. Chebaibi M. Baammi S. Ait Akka A. Chebbac K. Akhazzane M. Chelouati T. et al. GC-MS Profiling, In Vitro Antioxidant, Antimicrobial, and In Silico NADPH Oxidase Inhibition Studies of Essential Oil of Juniperus thurifera Bark Evid.-Based Complement. Altern. Med. 2022 2022 6305672 10.1155/2022/6305672
Herrera-Calderon O. Chacaltana-Ramos L.J. Huayanca-Gutiérrez I.C. Algarni M.A. Alqarni M. Batiha G.E.-S. Chemical Constituents, In Vitro Antioxidant Activity and In Silico Study on NADPH Oxidase of Allium sativum L. (Garlic) Essential Oil Antioxidants 2021 10 1844 10.3390/antiox10111844
El Abdali Y. Mahraz A.M. Beniaich G. Mssillou I. Chebaibi M. Bin Jardan Y.A. Lahkimi A. Nafidi H.-A. Aboul-Soud M.A.M. Bourhia M. et al. Essential Oils of Origanum compactum Benth: Chemical Characterization, in Vitro, in Silico, Antioxidant, and Antibacterial Activities Open Chem. 2023 21 20220282 10.1515/chem-2022-0282
Amrati F.E.-Z. Elmadbouh O.H.M. Chebaibi M. Soufi B. Conte R. Slighoua M. Saleh A. Al Kamaly O. Drioiche A. Zair T. et al. Evaluation of the Toxicity of Caralluma europaea (C.E) Extracts and Their Effects on Apoptosis and Chemoresistance in Pancreatic Cancer Cells J. Biomol. Struct. Dyn. 2023 41 8517 8534 10.1080/07391102.2022.2135595