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Algal Lipids as Modulators of Skin Disease
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This entry is adapted from the peer-reviewed paper 10.3390/metabo12020096

Lipids from algae have been scarcely applied to modulate skin diseases, but they are well known antioxidant and anti-inflammatory agents. They have shown scavenging activities and can modulate redox homeostasis enzymes. They can also downmodulate key inflammatory signaling pathways and transcription factors such as NF-κB, decreasing the expression of pro-inflammatory mediators. Thus, the exploitation of algae lipids as therapeutical agents for the treatment of inflammatory skin diseases is highly attractive.

skin diseases inflammation oxidative stress lipidomics bioactive lipids anti-inflammatory antioxidant macroalgae microalgae

1. Introduction

The skin is considered the largest organ in the human body with important roles for its homeostasis, such as protection against the harmful environment and dehydration [1]. The skin surface protects against pathogens, pollutants, and UV radiation [2][3]. These external stressors can pose a threat to the skin itself, promoting the formation of reactive oxygen species (ROS) that promote a pro-inflammatory response [4], associated with the pathophysiology of skin diseases, such as eczema, atopic dermatitis, psoriasis, vitiligo, and even skin aging or photoaging [5][6]. However, the pathology of skin diseases is not fully understood, and treatments are sometimes ineffective and inappropriate, with a low impact or with significant side effects [7]. Therefore, novel treatments are being sought out to fight the epidemic of skin inflammatory diseases. Synthetic drugs are not as effective as expected, and consumers are increasingly aware of using natural, organic, and environmentally friendly products. These new market trends and consumer preferences are stimulating the search for natural and sustainable ingredients (e.g., extracts of plants, microbes, or algae) to fight skin diseases [8][9]. The demand for natural molecules with beneficial properties for the skin includes the search for alternatives to synthetic molecules with fewer adverse side effects [10].
Algae (microalgae and macroalgae) are photosynthetic organisms considered natural reservoirs of compounds with bioactive properties, such as polysaccharides, vitamins, pigments, and polyunsaturated fatty acids (PUFA) [11]. These molecules are essential for the development of cosmeceuticals and are potential therapeutic agents with applications in skin diseases, including systemic or topical applications [12]. Algae biomass and algae extracts are already used in the treatment of skin diseases, for example, the use of macroalgae in thalassotherapy [13], or the use of algae oils rich in essential omega-6 and omega-3 PUFA (e.g., docosahexaenoic acid, DHA) in skin products [14]. Interest in algae-based products and natural ingredients has increased in the cosmetic and cosmeceutical industries in recent years [15]. Their main application has been as ingredients with hydrating, emollient, emulsifying, and whitening properties. Their use as anti-inflammatory and antioxidant products is also of great interest, but is less explored, and may be important for the management of skin diseases generally associated with periods of exacerbated inflammatory response and chronic inflammation [16].

2. Algae Lipids with Antioxidant Activity

The antioxidant activity of algae occurring lipids has been studied, but is much less explored compared to well-known natural antioxidants such as pigments and phenolic compounds [17][18] (Table 1).
Table 1. Lipid extracts of algae with antioxidant activity tested in chemico and in vitro with potential application on skin diseases. Abbreviations: ABTS—2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid, CAT—catalase, DPPH—2,2-diphenyl-1-picrylhydrazyl, FAME—fatty acyl methyl esters, HO-1—heme oxygenase-1, IL-6—interleukin-6, MAPK—mitogen-activated protein kinase, MMP—metalloproteinase, NHFD—normal human dermal fibroblasts, ROS—reactive oxygen species, SOD—superoxide dismutase, TGF-1—tumor growth factor-1, UVB—ultraviolet B.
Table
Studies Mechanism Assay Identified Lipids Algae Species Ref.
in chemico Free radical scavenging ABTS, DPPH, hydroxyl radical, superoxide anion Polar lipids, neutral lipids, FAME Macroalgae: Bifurcaria bifurcata, Codium tomentosum, Fucus vesiculosus, Gracilaria gracilis Grateloupia turuturu, Palmaria palmata, Porphyra dioica Sargassum muticum, Solieria chordalis, Ulva rigida
Microalgae: Chlorella vulgaris, Chlorococcum amblystomatis, Nannochloropsis oceanica, Phaeodactylum tricornutum, Scenedesmus intermedius Scenedesmus obliquus, Spirulina sp., Tetraselmis chui		 [19][20][21][22]
in vitro Detoxify
intracellular ROS		 Increased the expression of Nrf2 in irradiated HaCat cells
Upregulate target antioxidant enzymes Cu/Zn SOD, CAT, and HO-1		 Crude ethanolic extract Macroalga: Carpomitra costata [23]
Free radical scavenging Superoxide generation on peritoneal leukocytes Sulfoquinovosylacylglycerols Microalgae: Porphyridium cruentum [24]
Inhibition of ROS Photoprotective against UVB in NHDF Crude ethyl acetate extract Microalga: Ettlia sp. YC001 [25]
Enzyme/protein expression Downregulation of expression of MMPs Crude ethanolic extract Microalga: Arthrospira platensis [26]
Enzyme/protein expression Downregulation of expression of MMPs, IL-6 and TGF-1 in human dermal fibroblast
Modulate MAPK in irradiated HaCat cells		 Fucosterol Macroalga: Sargassum fusiforme [27][28]

The pathophysiology of inflammatory skin diseases is associated with unregulated elevated levels of ROS and the activity of enzymes and proteins involved in the regulation of oxidative stress [29]. In cells, mitochondria metabolize oxygen, producing ROS. During the oxidative phosphorylation in mitochondria, oxygen is converted to O2•−, which can be transformed in H2O2 by superoxide dismutase, and then to water by glutathione peroxidase (GPX) or peroxiredoxin III (PRX III) radical [30]. Under normal conditions, the mitochondria ROS production is balanced by the production of a variety of antioxidants. However, oxidative stress occurs when there is an imbalance between ROS and antioxidants production. An imbalance in ROS production leads to redox signaling from cellular organelles, causing mitochondrial damage and dysfunction in several conditions [31]. However, the application of algae lipids to prevent mitochondrial dysfunction and modulate the oxidative status is little understood and requires in-depth study to understand the mechanisms underlying this potential antioxidant role. The use of crude extracts from algae may reduce ROS levels induced by UVB and impair the expression of MMPs and thymine dimers formation due to UVB exposure in skin cells [26]. These studies were performed using complex crude extracts rich in lipids and not with isolated lipids or fractions. This hinders the understanding of the mechanisms of action of algal lipids as antioxidants, and more work is needed to determine the potential protective role of algal lipids in skin diseases. A better understanding of this antioxidant action is needed, for example, there is a lack of knowledge about the impact of specific lipid classes or lipid molecules in the enzymes and proteins involved in the regulation of oxidative stress, such as metalloproteinases, HO-1, catalase, or superoxide dismutase.

3. Algae Lipids with Anti-Inflammatory Activity

The lipids of macro- and microalgae have been studied for their anti-inflammatory and immunomodulatory activity. Most of the studies tested crude lipid extracts or fractions of lipid classes of algae and were mainly performed in chemico and in vitro (Table 2). They mainly measured the impact of lipids on the levels of inflammatory effector molecules such as prostaglandins and nitric oxide (NO), cytokines such as TNF-α, IL-6, and IL-1β, and on the activation of inflammatory signaling pathways (NF-κB) or cyclooxygenase-2 (COX-2) activity. Few studies have evaluated in vivo models measuring the effect of lipids on skin cells, such as epidermal cells.
Table 2. Lipid extracts of algae with anti-inflammatory activity tested in chemico, in vitro and in vivo with a potential application on skin diseases. Abbreviation: COX-2—cyclooxygenase-2, DGDG—digalactosyldiacylglycerol, DGLA—dihomo-γ-linolenic acid, DGTS—diacylglyceryltrimethylhomoserine, DNFB—2,4-dinitrofluorobenzene, IL-6—interleukin-6, MGDG—monogalactosyldiacylglycerol, MGMG—monogalactosylmonoacylglycerol, MGTS—monoacylglyceryltrimethylhomoserine, MMHDA—methoxylated fatty acids, NF-κB—nuclear factor kappa-light-chain-enhancer of activated B cells, NO—nitric oxide, PBMC—peripheral blood mononuclear cell, PC- phosphatidylcholine, PG—phosphatidylglycerol, PGE2—prostaglandin E2, PLA2—phospholipase A2, SQDG—sulfoquinovosyldiacylglycerol, TLR—Toll-like receptor, TNBS—2,4,6-trinitrobenzene sulfonic acid, TNF-α—tumor necrosis factor-α, TPA—12-O-tetradecanoylphorbol-13-acetate.
Table
Studies Action Model Identified Lipids Algae Species Ref.
In chemico COX-2 inhibition COX-2 kit assay Polar lipids Macroalgae: Codium tomentosum, Fucus vesiculosus Gracilaria gracilis, Palmaria palmata, Porphyra dioica, Ulva rigida,
Microalgae: Chlorella vulgaris, Chlorococcum amblystomatis, Gloeothece sp., Skeletonema sp., Tetraselmis sp. mutants		 [19][32][33][34][35]
In vitro NO inhibition Raw 264.7 Polar and non-polar lipids;
PC, PG, DGDG, DGTS, MGDG, MGMG, SQDG classes;
Free and ethyl esterified DGLA		 Macroalgae: Chondrus crispus, Lobophora sp.Palmaria palmata,
Microalgae: Chlorella sorokiniana Lobosphaera incisa, Nannochloropsis granulata, Tetraselmis chui,		 [36][37][38][39][40][41][42][43]
Decrease in PGE2 Downregulation of COX-2 Raw 264.7;
White blood cells;
Epidermal cells		 Crude ethanolic extracts;
lipid extracts rich in PC; free and ethyl esterified DGLA		 Macroalgae: Laminaria ochroleuca
Microalgae: Chlorella vulgaris, Chloromonas reticulata, Lobosphaera incisa Micractinium sp., Phaeodactylum tricornutum,		 [41][44][45][46][47][48]
Downregulation of mRNA expression of pro-inflammatory cytokines
Downregulation of cytokines levels: TNF-α, IL-6, IL-1α, and IL-1β		 THP-1;
PBMC;
Epidermal cells;
HaCaT cells		 Crude ethanolic extracts; lipid extracts;
lipid extracts rich in MGDG, DGDG and SQDG;
Lipid extracts rich in PC; LPC(16:0);
oxylipins;
ergosterol and 7-dehydroporiferasterol;
free and ethyl esterified DGLA		 Macroalgae: Chondrus crispus, Laminaria ochroleuca, Palmaria palmata, Porphyra dioica, Prasiola japonica
Microalgae: Aurantiochytrium mangrovei, Chlamydomonas debaryana, Chlorella vulgaris, Chloromonas reticulata, Cylindrotheca closterium, Dunaliella tertiolecta, Micratinium sp., Nannochloropsis gaditana, Nitzschia palea, Phaeodactylum tricornutum, Lobosphaera incisa Spirulina maxima, Pavlova lutheri, Tetraselmis suecica,		 [23][41][44][45][46][47][49][50][51][52][53][54][55][56][48][57][58]
Inhibition of pro-inflammatory signaling pathways mediated by TLR and NF-κB THP-1 Lipid extracts rich in MGDG, DGDG, and SQDG Macroalgae: Chondrus crispus, Palmaria palmata, Porphyra dioica
Microalgae: Pavlova lutheri		 [49]
In vivo Attenuation of ear oedema PLA2 kit assay;
Mice with ear oedema;
DNFB-induced in naive C57BL/6 mice		 MMHDA;
Lipid extracts rich in PC;
MGDG, DGDG, and SQDG fractions		 Macroalgae: Ishige okamurae, Laminaria ochroleuca
Microalgae: ETS-05 cyanobacterium.		 [48][59][60]
Neutrophil gathering in the wound region Wounded zebrafish model Glycolipids rich in γ-linolenic acid Microlagae: Spirulina platensis [61]
Inhibition of pro-inflammatory cytokines production: TNF-α, IL-6, IL-8, IFN- γ, IL-1β, IL-17 db/db and CD1 mice model of diabetes mellitus;
TNBS-induced colitis rats;
BALB/c mice skin; TPA-induced hyperplasia murine model		 Crude ethanolic extract; omega-3 fatty acids;
oxylipins;
MGDG cream		 Macroalgae: Sargassum cristaefolium
Microalgae: Chlamydomonas debaryana, Isochrysis galbana		 [62][63][64][65]
Downregulation of iNOS and COX-2, and decrease in NO and PGE2 production TNBS-induced colitis rat;
BALB/c mice skin; TPA-induced hyperplasia murine model		 Crude ethanolic extract; oxylipins; MGDG cream Macroalgae: Sargassum cristaefolium
Microalgae: Chlamydomonas debaryana, Isochrysis galbana		 [63][64][65]

It was demonstrated that methoxylated fatty acids (MMHDA) isolated from macroalga Ishige okamurae [60] and MGDG, DGDG, and SQDG fractions from microalga ETS-05 cyanobacterium [59] presented anti-inflammatory activity by reducing ear oedema (swelling) in a mouse model. The anti-inflammatory action of MMHDA has been associated with the inhibition of phospholipase A2 (PLA2), the enzyme responsible for the hydrolysis of the sn-2 position of membrane glycerophospholipids to liberate arachidonic acid (AA). The reduction in neutrophils was observed in the wound region of a zebrafish model when glycolipids rich in γ-linolenic acid from the microalga Spirulina platensis were used [61]. Extracts with omega-3 FA isolated from microalgae promoted the reduction of CD4+ T cells production of the pro-inflammatory mediators IFN-γ, TNF-α, and IL-4 and increased the secretion of IL-17A, IL-14, and TGF-β in a db/db and CD1 mouse model of diabetes Mellitus [62]. Downregulation of TNF-α was also observed, as well as decreased expression of iNOS and COX-2, when 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced colitis rats were supplemented with oxylipins extracted from Chlamydomonas debaryana [63].

In model studies on skin diseases, the protective effect of the ethanolic extract of Sargassum cristaefolium against ultraviolet-irradiated skin keratinocytes and BALB/c mice skin has been demonstrated [64]. The inhibition of ROS production and suppression of the apoptotic process in irradiated cells, such as the decrease of caspases, downregulation of COX-2, IL-1β, IL-8, IL-6, TNF-α, and INF-γ, and down-modulation of NF-κB signaling, were some of the reported mechanisms of action. L. ochroleuca lipid extract have been shown to reduce ear oedema, in a murine model of skin inflammation induced by the chemical sensitizer 2,4-dinitro-fluorobenzene applied to the ear of naive C57BL/6 mice [48]. A cream containing MGDG extracted from the microalga Isochrysis galbana has been reported to have beneficial effects in the treatment of a 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced hyperplasia murine model [65]. Pre-treatment of these mice with this MGDG cream reduced skin oedema and epidermal thickness. In addition, the pro-inflammatory cytokines TNF-α, IL-1β, IL-6, and IL-17 produced in epidermal tissue were downregulated and the expression of COX-2 was inhibited. The results of this study were very promising as they involved a model of skin disease and isolated algal lipids and showed a strong anti-inflammatory effect as well as an improved skin condition. Such results highlight algal lipids as promising pharmacological strategies for the therapy of inflammatory skin pathologies.
Algal lipids have shown anti-inflammatory potential as modulators of signaling pathways and mediators, known as the main hallmarks of inflammation, such as COX-2 and iNOS, but also the modulation of the production of cytokines (TNF-α, IL-6, IL-1β, and IFN-γ), as described in Figure 1. Indeed, as mentioned in Section 2, inflammatory skin diseases are characterized by systemic inflammation [66] with the infiltration of immune cells, such as neutrophils. Algal lipids such as glycolipids rich in γ-linolenic acid from the microalga S. platensis have been reported to reduce neutrophil infiltration in a wound region model of zebrafish [61]. Neutrophils are the main producers of ROS capable of activating transcription factors, such as NF-κB, responsible for the regulation of genes involved in inflammation [67]. Interestingly, the use of extracts in immune and skin cell lines reduced this pro-inflammatory pathway [49][50][59]
Metabolites 12 00096 g001 550
Figure 1. Algae lipids can target mediators responsible for the onset and progression of skin inflammatory diseases.

4. Concluding Remarks

Algal lipids have been shown to be effective in countering the pathophysiological processes responsible for the onset and progression of inflammatory skin diseases, such as oxidative stress and inflammation. Algal lipids have shown antioxidant activity through ROS scavenging and the modulation of important enzymes involved in the regulation of the redox state, showing the ability to attenuate the pro-oxidative state in these diseases. These extracts also contributed for the modulation of the inflammatory response at several levels, such as the modulation of signaling pathways and transcription factors such as NF-κB and MAPKs, conditioning the activation of immune cells and the production of inflammatory mediators. This modulation was demonstrated in vitro and in vivo, in different animal models of inflammatory diseases. The most studied and highlighted species were polar lipids with anti-inflammatory activity, belonging to glycolipids and phospholipids, namely MGDG, DGDG, and SQDG, and PC classes, respectively. Less reported classes included PG and DGTS species, sterols, and free and esterified FA, which also showed potential as anti-inflammatory agents. This synergistic action holds great promise for the application of algal lipids in the management of acute and chronic inflammatory skin diseases. However, the application of algal lipids in these skin diseases is an underexplored area, with few studies focusing on an integrated system, which needs to be explored in the near future.
More studies that unveil the action of lipids in models of inflammatory skin diseases (in vitro and in vivo) are needed to understand the modulating capacity of algal lipids, to fight against these diseases, such as atopic dermatitis or psoriasis. Other challenges are the lack of structural characterization of bioactive lipids, and to unveil the synergistic effect of all components of lipid extracts, as well as to reveal the structure–bioactivity relationship. These results could highlight algal lipids as therapeutic alternatives for skin diseases. The current therapeutic approaches for skin inflammatory diseases are not quite effective, are uncomfortable, and can have undesired effects, and some are expensive and not available to most patients. Algae lipids are natural antioxidant and anti-inflammatory agents that can counteract changes observed in skin inflammatory diseases, promote a return to homeostasis, and treat these conditions. They can be used as topical agents, which is preferable in the cosmeceutical industry, and are cheap to produce, extending their use to poorer countries and patients with low incomes. If these promises hold true, algal lipids could feature in the road map for the development of new pharmaceuticals and cosmeceuticals, as a treatment for skin diseases for topical or systemic administration.

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Diana Lopes
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