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Discovery and Application of Macroalgae-Derived Natural Products

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A special issue of Marine Drugs (ISSN 1660-3397).

Deadline for manuscript submissions: closed (30 April 2019) | Viewed by 84173

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Prof. Dr. Artur M. S. Silva

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Guest Editor

LAQV-REQUIMTE, Department of Chemistry, University of Aveiro, 3810-193 Aveiro, Portugal
Interests: organic chemistry; green synthetic organic chemistry; synthesis of heterocyclic compounds; natural products; NMR techniques; synthesis of new compounds with biocidal and antioxidant activities
Special Issues, Collections and Topics in MDPI journals

Dr. Marta Correia-da-Silva

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1. Laboratório de Química Orgânica e Farmacêutica, Departamento de Ciências, Químicas, Faculdade de Farmácia, Universidade do Porto, Rua Jorge Viterbo Ferreira 228, 4050-313 Porto, Portugal
2. CIIMAR | Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Novo Edifício do Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos, s/n, 4450-208 Matosinhos, Portugal
Interests: medicinal chemistry; synthesis of sulfated and glycosylated small-molecule mimetics of heparin; discovery of biological activities for persulfated versus partially sulfated small molecules; antifouling studies of partially sulfated small molecules; antithrombotic studies of persulfated small molecules; structure–activity and structure–property relationship studies of bioactive small molecules
Special Issues, Collections and Topics in MDPI journals

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Dear Colleagues,

Macroalgae is a term used for seaweeds and other benthic marine algae that are generally visible to the naked eye. They include members of four different phyla, namely, Rhodophyta (red), Ochrophyta (brown), Chlorophyta (green), and Cyanobacteria (dark blue), and are represented by at least 30,000 species worldwide supplying oxygen to the biosphere, food for marine organisms and man, and fertilizers for agriculture.

Macroalgae produce structurally unique natural compounds, and several examples of lead compounds have emerged from marine algae, such as antiviral and immunostimulants, anticoagulant and antithrombotic, antioxidant and anti-aging, etc. Therefore, the exploitation of natural compounds isolated from macroalgae or of macroalgae-inspired synthetic compounds offers excellent opportunities for the agriculture, pharmaceutical, and cosmeceutical industries.

As Guest Editors of this Special Issue of Marine Drugs, we invite you to provide research and review articles describing the isolation of new bioactive compounds from macroalgae as well as the achievement of macroalgae-inspired synthetic compounds, their conservation and innovative applications.

Prof. Dr. Artur M. S. Silva
Prof. Dr. Marta Correia da Silva
Guest Editors

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Marine Drugs is an international peer-reviewed open access monthly journal published by MDPI.

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Keywords

Macroalgae
Secondary metabolites
Isolation of bioactive compounds
Biological activities
Marine drugs
Biotechnology
Synthesis of macroalgae-derived compounds

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Published Papers (12 papers)

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Research

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20 pages, 3479 KiB

Open AccessArticle

Screening of Chaetomorpha linum Lipidic Extract as a New Potential Source of Bioactive Compounds

by Loredana Stabili, Maria Immacolata Acquaviva, Federica Angilè, Rosa Anna Cavallo, Ester Cecere, Laura Del Coco, Francesco Paolo Fanizzi, Carmela Gerardi, Marcella Narracci and Antonella Petrocelli

Mar. Drugs 2019, 17(6), 313; https://doi.org/10.3390/md17060313 - 28 May 2019

Cited by 38 | Viewed by 6379

Abstract

Recent studies have shown that marine algae represent a great source of natural compounds with several properties. The lipidic extract of the seaweed Chaetomorpha linum (Chlorophyta, Cladophorales), one of the dominant species in the Mar Piccolo of Taranto (Mediterranean, Ionian Sea), revealed an antibacterial activity against Vibrio ordalii and Vibrio vulnificus, common pathogens in aquaculture, suggesting its potential employment to control fish and shellfish diseases due to vibriosis and to reduce the public health hazards related to antibiotic use in aquaculture. This extract showed also an antioxidant activity, corresponding to 170.960 ± 16. mmol Trolox equivalent/g (oxygen radical absorbance capacity assay—ORAC) and to 30.554 ± 2.30 mmol Trolox equivalent/g (Trolox equivalent antioxidant capacity assay—TEAC). The chemical characterization of the extract, performed by 1D and 2D NMR spectroscopy, highlighted the presence of free, saturated (SAFAs), unsaturated (UFAs) and polyunsaturated (PUFAs) fatty acids. The high content of ω-6 and ω-3 PUFAs confirmed also by gas chromatography indicates the potentiality of this algal species in the production of fortified food. The antibacterial activity seems related to the presence of linolenic acid present at high density, while the antioxidant activity could be likely ascribable to molecules such as carotenoids and chlorophylls (characterized also by thin-layer chromatography), known for this property. The presence of polyhydroxybutyrate, a biopolymer with potentiality in the field of biodegradable bioplastics was also detected. The exploitation of C. linum for a future biotechnological application is also encouraged by the results from a first attempt of cultivating this species in an integrated multi-trophic aquaculture (IMTA) system. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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10 pages, 2713 KiB

Open AccessArticle

Efficient Extraction of Carotenoids from Sargassum muticum Using Aqueous Solutions of Tween 20

by Flávia A. Vieira and Sónia P. M. Ventura

Mar. Drugs 2019, 17(5), 310; https://doi.org/10.3390/md17050310 - 25 May 2019

Cited by 10 | Viewed by 3983

Abstract

The replacement of synthetic compounds by natural products witnesses an increasing demand from the pharmaceutical, cosmetic, food and nutraceutical industries. Included in the set of natural raw materials that are poorly explored are the macroalgae. Despite the detailed characterization and identification of most relevant biomolecules that are present in the main macroalgae species, there remains a lack of efficient and economically viable processes available to meet the needs of the markets. In this work, an efficient and single-step process, based on aqueous solutions of Tween 20, to recover carotenoids from Sargassum muticum, an invasive brown macroalgae species present in the Portuguese coast, is proposed and optimized allowing an extraction yield of 2.78 ± 0.4 mg_carotenoids.g_{dried mass}⁻¹, which is shown to increase the extraction efficiency by 38% when compared with traditional methods. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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21 pages, 3562 KiB

Open AccessArticle

Anticoagulant and Antithrombotic Properties in Vitro and in Vivo of a Novel Sulfated Polysaccharide from Marine Green Alga Monostroma nitidum

by Sujian Cao, Xiaoxi He, Ling Qin, Meijia He, Yajing Yang, Zhichun Liu and Wenjun Mao

Mar. Drugs 2019, 17(4), 247; https://doi.org/10.3390/md17040247 - 25 Apr 2019

Cited by 54 | Viewed by 5081

Abstract

Sulfated polysaccharides from marine algae have high potential as promising candidates for marine drug development. In this study, a homogeneous sulfated polysaccharide from the marine green alga Monostroma nitidum, designated MS-1, was isolated using water extraction and anion-exchange and size-exclusion chromatography. Results of chemical and spectroscopic analyses showed that MS-1 mainly consisted of →3)-α-l-Rhap-(1→ and →2)-α-l-Rhap-(1→ residues, with additional branches consisting of 4-linked β-d-xylose, 4-/6-linked d-glucose, terminal β-d-glucuronic acid, and 3-/2-linked α-l-rhamnose. Sulfate ester groups substituted mainly at C-2/C-4 of →3)-α-l-Rhap-(1→ and C-4 of →2)-α-l-Rhap-(1→ residues, slightly at C-2 of terminal β-d-glucuronic residues. MS-1 exhibited strong anticoagulant activity in vitro and in vivo as evaluated by the activated partial thromboplastin time and thrombin time assays, and significantly decreased platelet aggregation. The anticoagulant activity mechanism of MS-1 was mainly attributed to strong potentiation thrombin by heparin cofactor-II, and it also hastened thrombin and coagulation factor Xa inhibitions by potentiating antithrombin-III. MS-1 possessed markedly thrombolytic activity evaluated by plasminogen activator inhibitior-1, fibrin degradation products, and D-dimer levels using rats plasma, and recanalization rate by FeCl₃-induced carotid artery thrombosis in mice. MS-1 exhibited strong antithrombotic activity in vitro and in vivo evaluated by the wet weighs and lengths of thrombus, and thrombus occlusion time by electrically-induced carotid artery thrombosis in rats. These results suggested that MS-1 could be a promising marine drug for prevention and therapy of thromboembolic disease. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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40 pages, 3017 KiB

Open AccessArticle

Biomolecular Composition and Revenue Explained by Interactions between Extrinsic Factors and Endogenous Rhythms of Saccharina latissima

by Xueqian Zhang and Marianne Thomsen

Mar. Drugs 2019, 17(2), 107; https://doi.org/10.3390/md17020107 - 10 Feb 2019

Cited by 33 | Viewed by 8873

Abstract

This review provides a systematic overview of the spatial and temporal variations in the content of biomolecular constituents of Saccharina latissima on the basis of 34 currently available scientific studies containing primary measurements. We demonstrate the potential revenue of seaweed production and biorefinery systems by compiling a product portfolio of high-value extract products. An investigation into the endogenous rhythms and extrinsic factors that impact the biomolecular composition of S. latissima is presented, and key performance factors for optimizing seaweed production are identified. Besides the provisioning ecosystem service, we highlight the contribution of green-engineered seaweed production systems to the mitigation of the ongoing and historical anthropogenic disturbances of the climate balance and nutrient flows. We conclude that there are risks of mismanagement, and we stress the importance and necessity of creating an adaptive ecosystem-based management framework within a triple-helix partnership for balancing the utilization of ecosystem services and long-term resilience of aquatic environment. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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11 pages, 956 KiB

Open AccessArticle

Glycerolipid Composition of the Red Macroalga Agarophyton Chilensis and Comparison to the Closely Related Agarophyton Vermiculophyllum Producing Different Types of Eicosanoids

by Masaki Honda, Takashi Ishimaru, Yutaka Itabashi and Mikhail Vyssotski

Mar. Drugs 2019, 17(2), 96; https://doi.org/10.3390/md17020096 - 2 Feb 2019

Cited by 6 | Viewed by 4037

Abstract

The red macroalga Agarophyton chilensis is a well-known producer of eicosanoids such as hydroxyeicosatetraenoic acids, but the alga produces almost no prostaglandins, unlike the closely related A. vermiculophyllum. This indicates that the related two algae would have different enzyme systems or substrate composition. To carry out more in-depth discussions on the metabolic pathway of eicosanoids between the two algae, we investigated the characteristics of glycerolipids, which are the substrates of eicosanoids production, of A. chilensis and compared them to the reported values of A. vermiculophyllum. In A. chilensis, monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), sulfoquinovosyldiacylglycerol (SQDG), and phosphatidylcholine (PC) were the major lipid classes and accounted for 44.4% of the total lipid extract. The predominant fatty acids were arachidonic acid (20:4n-6), an eicosanoids precursor, and palmitic acid (16:0). The 20:4n-6 content was extremely high in MGDG and PC (>70%), and the 16:0 content was extremely high in DGDG and SQDG (>40%). A chiral-phase HPLC analysis showed that fatty acids were esterified at the sn-1 and sn-2 positions of those lipids. The glycerolipid molecular species were determined by reversed-phase HPLC–ESI–MS analysis. The main glycerolipid molecular species were 20:4n-6/20:4n-6 (sn-1/sn-2) for MGDG (63.8%) and PC (48.2%), 20:4n-6/16:0 for DGDG (71.1%) and SQDG (29.4%). These lipid characteristics of A. chilensis were almost the same as those of A. vermiculophyllum. Hence, the differences of the eicosanoids producing ability between the two algae would not be due to the difference of substrate composition but the difference of enzyme system. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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17 pages, 1097 KiB

Open AccessArticle

Effect of Oven-Drying on the Recovery of Valuable Compounds from Ulva rigida, Gracilaria sp. and Fucus vesiculosus

by Andreia F.R. Silva, Helena Abreu, Artur M.S. Silva and Susana M. Cardoso

Mar. Drugs 2019, 17(2), 90; https://doi.org/10.3390/md17020090 - 1 Feb 2019

Cited by 58 | Viewed by 5666

Abstract

The effect of oven-drying at 25, 40 and 60 °C was evaluated on three macroalgae of relevance in Europe, namely Ulva rigida, Gracilaria sp. and Fucus vesiculosus, with respect to quality aspects, including their potential to be exploited as a source of valuable compounds. Notably, as compared to freeze-drying, oven-drying at 25 °C promoted the extraction of chlorophylls and carotenoids from U. rigida, as well as those of phycoerythrin and chlorophyll a from Gracilaria sp., while 40 °C favored the recovery of fucoxanthin and pheophytin a from F. vesiculosus. On the other hand, the use of oven-drying had a negative impact on the extraction of phenolic compounds from this alga, also diminishing the antioxidant activity of the resulting extracts. Instead, the impact of oven-drying of raw material on the recovery of specific polysaccharides differed among the macroalgae. While the amounts of ulvans and fucoidans obtained from macroalgae dried at higher temperatures tended to be superior, the recovery of agar was not affected with the drying temperatures applied to Gracilaria sp. The overall results showed that oven-drying might serve as a good alternative to stabilize Ulva rigida, Gracilaria sp. and Fucus vesiculosus, especially if extraction of pigments and polysaccharides is aimed, thought the appropriate temperature applied must be adapted for each macroalgae. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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13 pages, 1323 KiB

Open AccessArticle

Analysis of the Transcriptome of the Red Seaweed Grateloupia imbricata with Emphasis on Reproductive Potential

by Pilar Garcia-Jimenez, Carlos Llorens, Francisco J. Roig and Rafael R. Robaina

Mar. Drugs 2018, 16(12), 490; https://doi.org/10.3390/md16120490 - 7 Dec 2018

Cited by 13 | Viewed by 4139

Abstract

Grateloupia imbricata is an intertidal marine seaweed and candidate model organism for both industry and academic research, owing to its ability to produce raw materials such as carrageenan. Here we report on the transcriptome of G. imbricata with the aim of providing new insights into the metabolic pathways and other functional pathways related to the reproduction of Grateloupia species. Next-generation sequencing was carried out with subsequent de novo assembly and annotation using state-of-the-art bioinformatic protocols. The results show the presence of transcripts required for the uptake of glycerol, which is a specific carbon source for in vitro culture of G. imbricata and nucleotide sequences that are involved in polyamine-based biosynthesis, polyamine degradation, and metabolism of jasmonates and ethylene. Polyamines, ethylene and methyl jasmonate are plant growth regulators that elicit the development and maturation of cystocarps and the release of spores from seaweeds. Our results will inform studies of the mechanisms that control polysaccharide accumulation, cystocarp formation and spore release. Moreover, our transcriptome information clarifies aspects of red seaweed carposporogenesis with potential benefits for enhancing reproduction. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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13 pages, 2763 KiB

Open AccessArticle

Structure and Bioactivity Screening of a Low Molecular Weight Ulvan from the Green Alga Ulothrix flacca

by Peipei Li, Songsong Wen, Kunlai Sun, Yuqin Zhao and Yin Chen

Mar. Drugs 2018, 16(8), 281; https://doi.org/10.3390/md16080281 - 15 Aug 2018

Cited by 21 | Viewed by 5702

Abstract

A water-soluble low molecular–weight polysaccharide named UP2-1 was isolated and purified from the marine green algae Ulothrix flacca using ion-exchange and size-exclusion chromatography. Composition and characteristics analyses showed that UP2-1 was a sulfated glucuronorhamnan consisting of rhamnose and glucuronic acid in a ratio of 2:1 with 21% sulfate content and a molecular weight of 5.0 kDa. Structural properties were determined using desulfation and methylation analyses combined with infrared spectrum (IR), gas chromatography-mass spectrometer (GC-MS) and nuclear magnetic resonance (NMR). The results showed that UP2-1 was a type of ulvan composed of alternate 4-linked-α-L-rhamnose residues (→4)-α-L-Rha(1→) and 4-linked-β-D-glucouronoc acid residues. The sulfate groups were mainly present in the O-3 position of →4)-α-L-Rha(1→. Most (70%) of the rhamnose was sulfated. UP2-1 also had a small amount of →4)-α-L-Rha(1→ branch at the O-2 position of the →4)-α-L-Rha(1→. UP2-1 exhibited significant anticoagulant and immunomodulating activity in vitro. This study demonstrated that the green algae Ulothrix flacca, which is used as a food and traditional marine herb in China, could also be considered as a source of bioactive ulvan. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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Review

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19 pages, 2083 KiB

Open AccessFeature PaperReview

Isolation and Potential Biological Applications of Haloaryl Secondary Metabolites from Macroalgae

by Ana Jesus, Marta Correia-da-Silva, Carlos Afonso, Madalena Pinto and Honorina Cidade

Mar. Drugs 2019, 17(2), 73; https://doi.org/10.3390/md17020073 - 22 Jan 2019

Cited by 38 | Viewed by 5785

Abstract

Macroalgae have been reported as an important source of halogenated aromatic secondary metabolites, being the majority of these derivatives isolated from red algae. Halophenols and haloindoles are the most common haloaryl secondary metabolites isolated from these marine organisms. Nevertheless, some halogenated aromatic sesquiterpenes and naphthalene derivatives have also been isolated. Most of these secondary metabolites showed interesting biological activities, such as antitumor, antimicrobial, antidiabetic, and antioxidant. This review describes in a systematic way the distribution and natural occurrence of halogenated aromatic secondary metabolites from extracts of red, brown, and green algae, as well as biological activities reported for these compounds. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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27 pages, 3163 KiB

Open AccessReview

Seaweed Secondary Metabolites In Vitro and In Vivo Anticancer Activity

by Djenisa H. A. Rocha, Ana M. L. Seca and Diana C. G. A. Pinto

Mar. Drugs 2018, 16(11), 410; https://doi.org/10.3390/md16110410 - 26 Oct 2018

Cited by 77 | Viewed by 10368

Abstract

Isolation, finding or discovery of novel anticancer agents is very important for cancer treatment, and seaweeds are one of the largest producers of chemically active metabolites with valuable cytotoxic properties, and therefore can be used as new chemotherapeutic agents or source of inspiration to develop new ones. Identification of the more potent and selective anticancer components isolated from brown, green and red seaweeds, as well as studies of their mode of action is very attractive and constitute a small but relevant progress for pharmacological applications. Several researchers have carried out in vitro and in vivo studies in various cell lines and have disclosed the active metabolites among the terpenoids, including carotenoids, polyphenols and alkaloids that can be found in seaweeds. In this review the type of metabolites and their cytotoxic or antiproliferative effects will be discussed additionally their mode of action, structure-activity relationship and selectivity will also be revealed. The diterpene dictyolactone, the sterol cholest-5-en-3β,7α-diol and the halogenated monoterpene halomon are among the reported compounds, the ones that present sub-micromolar cytotoxicity. Additionally, one dimeric sesquiterpene of the cyclolaurane-type, three bromophenols and one halogenated monoterpene should be emphasized because they exhibit half maximal inhibitory concentration (IC₅₀) values between 1–5 µM against several cell lines. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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34 pages, 1280 KiB

Open AccessFeature PaperReview

Phycochemical Constituents and Biological Activities of Fucus spp.

by Marcelo D. Catarino, Artur M. S. Silva and Susana M. Cardoso

Mar. Drugs 2018, 16(8), 249; https://doi.org/10.3390/md16080249 - 27 Jul 2018

Cited by 145 | Viewed by 12752

Abstract

Seaweeds are known to be a good supply of key nutrients including carbohydrates, protein, minerals, polyunsaturated lipids, as well as several other health-promoting compounds capable of acting on a wide spectrum of disorders and/or diseases. While these marine macroalgae are deeply rooted in the East Asian culture and dietary habits, their major application in Western countries has been in the phycocolloid industry. This scenario has however been gradually changing, since seaweed consumption is becoming more common worldwide. Among the numerous edible seaweeds, members of the genus Fucus have a high nutritional value and are considered good sources of dietary fibers and minerals, especially iodine. Additionally, their wealth of bioactive compounds such as fucoidan, phlorotannins, fucoxanthin and others make them strong candidates for multiple therapeutic applications (e.g., antioxidant, anti-inflammatory, anti-tumor, anti-obesity, anti-coagulant, anti-diabetes and others). This review presents an overview of the nutritional and phytochemical composition of Fucus spp., and their claimed biological activities, as well as the beneficial effects associated to their consumption. Furthermore, the use of Fucus seaweeds and/or their components as functional ingredients for formulation of novel and enhanced foods is also discussed. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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18 pages, 3998 KiB

Open AccessReview

Overview on the Antihypertensive and Anti-Obesity Effects of Secondary Metabolites from Seaweeds

by Ana M. L. Seca and Diana C. G. A. Pinto

Mar. Drugs 2018, 16(7), 237; https://doi.org/10.3390/md16070237 - 14 Jul 2018

Cited by 77 | Viewed by 9960

Abstract

Hypertension and obesity are two significant factors that contribute to the onset and exacerbation of a cascade of mechanisms including activation of the sympathetic and renin-angiotensin systems, oxidative stress, release of inflammatory mediators, increase of adipogenesis and thus promotion of systemic dysfunction that leads to clinical manifestations of cardiovascular diseases. Seaweeds, in addition to their use as food, are now unanimously acknowledged as an invaluable source of new natural products that may hold noteworthy leads for future drug discovery and development, including in the prevention and/or treatment of the cardiovascular risk factors. Several compounds including peptides, phlorotannins, polysaccharides, carotenoids, and sterols, isolated from brown, red and green macroalgae exhibit significant anti-hypertensive and anti-obesity properties. This review will provide a comprehensive overview of the recent advances on bioactive pure compounds isolated from different seaweed sources focusing on their potential use as drugs to treat or prevent hypertension and obesity. On the other hand, although it is obvious that macroalgae represent promising sources of antihypertensive and anti-obesity compounds, it is also clear that further efforts are required to fully understand their cellular mechanisms of action, to establish structure-inhibition relationships and mainly to evaluate them in pre-clinical and clinical trials. Full article

(This article belongs to the Special Issue Discovery and Application of Macroalgae-Derived Natural Products)

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