Microalgal Lipid Extracts: History
View Latest Version
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:
Tiago Alexandre Conde
,
Ioannis Zabetakis
,
Alexandros Tsoupras
,
Isabel Medina
,
Margarida Costa
,
Joana Silva
,
Bruno Neves
,
Pedro Domingues
,
M. Rosário Domingues

Noncommunicable diseases (NCD) and age-associated diseases (AAD) are some of the gravest health concerns worldwide, accounting for up to 70% of total deaths globally. NCD and AAD, such as diabetes, obesity, cardiovascular disease, and cancer, are associated with low-grade chronic inflammation and poor dietary habits. Modulation of the inflammatory status through dietary components is a very appellative approach to fight these diseases and is supported by increasing evidence of natural and dietary components with strong anti-inflammatory activities. The consumption of bioactive lipids has a positive impact on preventing chronic inflammation and consequently NCD and AAD. Thus, new sources of bioactive lipids have been sought out. Microalgae are rich sources of bioactive lipids such as omega-6 and -3 polyunsaturated fatty acids (PUFA) and polar lipids with associated anti-inflammatory activity. PUFAs are enzymatically and non-enzymatically catalyzed to oxylipins and have a significant role in anti and pro-resolving inflammatory responses. Therefore, a large and rapidly growing body of research has been conducted in vivo and in vitro, investigating the potential anti-inflammatory activities of microalgae lipids. The anti-inflammatory potential of microalgae lipids and their possible use to prevent or mitigate chronic inflammation are summarized. 

  • Microalgal Lipid Extracts
  • glycolipids
  • polar lipids
  • inflammation
  • non-communicable diseases
  • cardiovascular diseases

1. Introduction

Noncommunicable diseases (NCD) are disorders that are not transmissible from one person to another (e.g., obesity, diabetes, cancer, autoimmune diseases, cardiovascular diseases, respiratory, and musculoskeletal disorders) and are the result of a multifactorial combination of unhealthy lifestyle habits and genetic predisposition [1]. They are among the leading causes of death, representing around 70% of total global deaths, and are recognized as one of the biggest challenges by the World Health Organization (WHO) and the Food and Agriculture Organization of the United Nations (FAO) [2][3]. One of the leading causes of NCDs is malnutrition, which results from states of obesity, other dietary factors, and undernutrition (e.g., underweight, deficiencies in vitamins, stunting). On the other hand, ageing impacts biological and physiological functions, which promotes and aggravates the development of age-associated diseases (AAD) such as atherosclerosis, hypertension, cardiovascular diseases, Alzheimer’s disease, dementia, arthritis, and osteoporosis [4]. Malnutrition also contributes to the onset of AADs and is often underdiagnosed in elderly patients [5]. Therefore, intervention in dietary habits is a critical approach to tackle these challenges. Another issue associated with unhealthy dietary practices arises from the overexploitation and consequent pollution associated, for example, with current food production, which accounts for 20–35% global greenhouse emissions [3]. A dietary shift to intake small amounts of calories from animal sources and increase the consumption of sustainable, nutrient-rich, and calorically efficient products, such as algae, are recommended by the FAO and WHO to prevent the aggravation of these issues [3].
Most NCDs are associated with low-grade chronic inflammation, characterized by persistently elevated levels of circulating pro-inflammatory cytokines, chemokines, and acute inflammation phase proteins [6]. The persistency of this low-grade chronic inflammation results in cellular, tissue, and organ damage over time, mainly through continuous oxidative stress, which eventually impairs proper body function. Mitigating the inflammatory response can prevent or decrease the severity of NCDs [1]. On the other hand, AADs are associated with the increasing senescence processes associated with ageing, such as telomerase erosion, the oxidative damage of DNA and proteins, mitochondrial dysfunction, oncogene overexpression, or epigenetic factors, that result in stem cell exhaustion, the dysfunction of body systems, and chronic inflammation [7]. To an extent, both NCD and AAD can be prevented by modifying lifestyle-related risk factors, where unhealthy diets play a significant role [8][9]. The modulation of chronic inflammation through diet plays an important role in decreasing the risks and prevalence of NCDs and AADs, as diet can provide components such as omega-3 (ω-3) fatty acids, flavonoids, and vitamins, which can suppress inflammation, decrease oxidative damage, and modulate gene expression [10].
The transition to more sustainable and healthy diets that are capable of preventing the development of NCDs and AADs, requires investment in and development of new food sources and ingredients with high nutritional value and diversity with sustainable production and reduced environmental impact (Figure 1) [3]. Microalgae are a sustainable and highly nutritious alternative that could enrich and contribute to the transition to more environmentally friendly and healthy diets [11][12]. They are a diverse and rich source of nutritional components, such as vitamins (e.g., vitamin B12), carbohydrates, proteins, nucleic acids, lipids (e.g., ω-3 polyunsaturated fatty acids (PUFA), others), and functional components (e.g., chlorophylls, which have antioxidant activity) [13]. Their lipid nutritional value is comparable to that of fish oils, offering an alternative to this commonly used source of ω-3 FA [14][15]. Microalgae are considered a promising source of bioactive components, including bioactive lipids such as ω-3 lipids, essential precursors of anti-inflammatory eicosanoids, and polar lipids [11]. Recent research suggests that marine polar lipids as phospholipids or glycolipids, which are highly concentrated in ω-3 PUFAs, could be more effectively delivered than triglycerides in terms of human health. Polar lipids are more stable and have higher bioavailability than triglycerides [16]. Moreover, as a relevant fact, phospholipids have recently been suggested as an excellent vector of DHA and oxygenated DHA metabolites as protectins, enhancing their in vivo role as inflammation resolvers. Among these, glycolipids (GL) have shown chemotherapeutic potential, anti-proliferative effects, potent inhibition of nitric oxide (NO) release, and anti-inflammatory potential [17]. Only a handful of microalgae species are approved for food consumption; however, the use of microalgae and their lipid extracts as food ingredients are recognized as having the potential to prevent NCDs and AADs and to enrich nutrient-deficient diets.
Ijms 22 09825 g001 550
Figure 1. The relationship and risk of noncommunicable diseases and age-associated diseases are increased by malnutrition originating from poor and unhealthy diets. Malnutrition promotes increased oxidative stress, DNA, cellular and tissue damage, and chronic inflammation. Chronic inflammation is associated with most NCDs and AADs. Bad diets are also associated with the unsustainable exploitation of resources, greenhouse gases (GHG) emissions, and impacts on climate change.
On the other hand, the anti-inflammatory and antioxidant potential of microalgae lipid extracts were intensively studied in the past decade. In this context, this research will address the anti-inflammatory potential of bioactive raw extracts, lipidic fractions, and isolated lipids from microalgae. This information will help valorize and promote microalgal lipids as sustainable and healthy dietary approaches to tackle global malnourishment, NCD, AAD, and environmental degradation.

Literature Reviewing Strategy

This revision was performed using the platform Web of Science. The keywords used were a combination of “microalgae”, with “anti-inflammatory”, “immunomodulatory”, and immunomodulation. The inclusion criteria were the use of microalgae organic extracts or the use of microalgae isolated lipid classes and species that have been reported to have anti-inflammatory/pro-resolving effects. Out of 138 results, only 32 met the proposed criteria. The excluded works referred to the use of aqueous extracts. Other banned works involved evaluating the anti-inflammatory activity of pigments or other non-lipidic-based molecules that did not fit the purpose of this research.
The included works were analyzed and were categorized by considering the microalga phylum (Figure 2A) and the type of lipid extracts or fractions that were used (Figure 2B). Microalgae from the phylum Chlorophyta were the most studied regarding anti-inflammatory activity. Most of the studies used crude lipid extracts in the anti-inflammatory activity assays [18][19][20]. In contrast, others used lipid fractions in specific classes of lipids, such as glycolipids, phospholipids, or others (Figure 2B) [21][22]. Among these, the ones that used glycolipids from microalgae enriched fractions were the most studied [23][24][25].
Ijms 22 09825 g002 550
Figure 2. (A) Microalgae of different phyla were used in the assays to evaluate the anti-inflammatory activity of lipids. (B) Type of lipid extracts from microalgae used to assay the anti-inflammatory activity.

2. Microalgae Lipids: Structural Diversity and Functionality

The microalgae lipidome includes two main groups of lipids: neutral lipids (fatty acids, TAG, and sterols) and polar lipids (sphingolipids, phospholipids (PL), glycolipids (GL), and betaine lipids (BL)). Polar lipids can develop several biological functions, acting as the structural components of cell membranes, which constitute lipoproteins, energy reserves, and signaling molecules [26].
Microalgae are rich in polar lipids, constituting 41–92% of total lipids, while neutral lipids constitute 5–51%. The lipidomic profile of several microalgae species have been studied, and significant polar lipids, represented in Figure 3, that have been identified include species from several classes of phospholipids, such as phosphatidic acid (PA), phosphatidylserine (PS), phosphatidylethanolamine (PE), phosphatidylinositol (PI), phosphatidylcholine (PC), phosphatidylglycerol (PG); glycolipids, such as digalactosyldiacylglycerol (DGDG), sulfoquinovosylmonoacylglycerol (SQDG), monogalactosyldiacylglycerol (MGDG); and betaines lipids, such as diacylglyceroltrimethylhomoserine (DGTS), diacylglyceryl hydroxymethyl-N,N,N-trimethyl-β-alanine (DGTA), and diacylglyceryl carboxyhydroxy methyl-choline (DGCC), as represented in Figure 3. Some of the polar lipid species described here were reported as being biologically active [27][28][29][30][31][32][33].
Ijms 22 09825 g003 550
Figure 3. Main classes of polar lipids found in microalgae: glycerophospholipids (or phospholipids), glycoglycerolipids (or glycolipids), and betaine lipids.
Polar lipids and neutral lipids are the leading FA carriers, which are the most studied lipids in microalgae. [34][35][36][37][38]. Microalgae FAs are typically 12 to 22 carbons long with up to 6 unsaturations; however, short-chain FA and oxidized PUFAs have been reported [39][40]. FAs such as the omega-6 and arachidonic acid (ARA) and the ω-3 FAs, such as α-linolenic acid (ALA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA), are usually associated with the nutritional value and bioactive properties from algae. They are precursors of pro- and anti-inflammatory eicosanoids, respectively, and contribute to the balance of both omega-6 and ω-3 FA, which are important for the normal functioning of the immune system [41][42][43].
Polar lipids have been described as potent bioactive compounds [44][45], and therefore, the interest in understanding their bioactive mechanisms and the extent of their bioactive potential have increased. Several studies have pointed to PL and GL, especially those esterified with ω-3 PUFAs, as possessing antioxidant, anti-inflammatory, anti-obesity, anti-tumor, anti-viral and anti-bacterial activity [16][17][46][47]. The bioactivities observed for these lipids hold exciting potential for natural sources prospection and can pose an alternative to the current sources of these lipids (e.g., fish oils). Fish oil is a commercially available ingredient and nutritional supplement rich in ω-3 PUFAs [3][48][49]. Still, microalgae are considered a sustainable alternative to fish oils and as a source of healthy and bioactive ω-3 PUFAs.
Anti-inflammatory activity was one of the main biological activities reported for microalgae lipid extracts [17]. Moreover, some microalgae polar lipids have been reported to have anti-inflammatory activity [17][22][50]. The following section will discuss the anti-inflammatory activity observed for microalgae lipid extracts and fractionated lipids. These studies evaluated pro-inflammatory markers, and some tried to understand a possible relationship between the selected microalgae species, extracts, and fractions and their immunomodulatory activity. Distinct parameters such as the induction or attenuation of cytokine production, the gene expression of inflammatory markers, and the activation or inhibition of signaling pathways were approached.

3. The Anti-Inflammatory Potential of Microalgal Lipid Extracts

The anti-inflammatory properties of bioactive lipids were evaluated using crude extracts from several microalgae, namely Chlorella vulgaris, Chlorella ovalis, Nannochloropsis oculata, Nannochloropsis granulata, Nannochloropsis oceanica, Phaeoductylum tricornutum, Amphidinium carterae; the diatoms Odontella mobiliensis, Pseudonitzschia pseudodelicatissima, Coscinodiscus actinocyclus, and Alexandrium minutum; and the mutant microalgae species Tetraselmis sp. (IMP3 and CTP4) or cyanobacteria Arthrospira maxima [19][32][33][50][51][52][53][54][55]. Different solvents and solvent systems were used to extract the lipids, making an accurate comparison of the results difficult. In these studies, the anti-inflammatory potential was accessed through the evaluation of the release/production of inflammatory mediators, such as the tumor necrosis factor α (TNF-α) and interleukin-6 (IL-6), prostaglandin E2 (PGE2) and NO, and the expression of the key enzymes, such as cyclooxygenase-2 (COX-2) and iNOS.
Very few studies were performed in animal models [23][24][56][57]. The reduction of croton-induced oedema in mice and neutrophils concentration in the wound region of zebrafish was observed when treated with lipids from microalgae [23][24]. Other studies observed the response of pro-inflammatory markers, namely cytokines, to microalgae extracted lipids in inflammatory disease models of induced colitis in rats and diabetic mice [56][57]. The lack of studies performed in animal models of disease hampers elucidation of the complete impact of lipids in the complex network of inflammation.

3.1. In Vitro Evaluation of Microalgal Lipids Impact in Key Pro-Inflammatory Enzymes

The evaluation of COX-2 and iNOS activity and expression are the most common parameters measured in screenings for anti-inflammatory potential, both generally and for microalgal extracts. COX-2 is an enzyme induced by pro-inflammatory mediators that converts arachidonic acid to prostaglandins. The modulation of its activity and expression provides information regarding the production of pro-inflammatory prostaglandins with a critical role in the initial onset of inflammation [58]. COX-2 inhibition was reported in studies using lipid extracts from Gloeothece sp., Chlorella vulgaris grown under auto- and heterotrophic conditions, Chlorococcum amblystomatis and lipid extracts enriched in ω-3 PUFAs from Tetraselmis sp. mutant strains (IMP3 and CTP4), Skeletonema sp., and Nitzschia palea [19][53][59][60][61]. These studies evaluated the inhibitory COX-2 activity of the crude lipids with a commercial assay in chemico. The evaluation of the capacity of lipid extracts to modulate COX-2 activity was also performed in in vitro cells studies, using lipid extracts from Chlorella vulgaris, Chloromonas reticulata, Micractinium sp., Nannochloropsis oculata, Nitzschia palea, and Phaeodactylum tricornutum. The results showed COX-2 inhibition and the downregulation of COX-2 protein levels in Raw264.7 cells [20][52][60][62][63][64][65].
On the other hand, assessing iNOS activity and expression provides information regarding the production of NO, a key molecule for induction and inflammation maintenance. The most common strategy to assess the impact of the tested lipid extracts on iNOS activity relies on evaluating their effects on LPS-triggered NO production by Raw 264.7 macrophages. For instance, Amphidinium carterae, Chlorella sp., Chloromonas reticulata, Micractinium sp., Nannochloropsis oculata, Nitzschia palea, and Phaeoductylum tricornutum lipid extracts were shown to reduce NO levels and iNOS expression induced by LPS in Raw264.7 cells [20][51][52][60][62][63][64][65][66]. Moreover, MGDG and DGDG [67], two classes of glycolipids, and DGTS [22], one of the betaine lipids, extracted from Nannochloropsis granulata, revealed intense NO inhibitory activity in Raw264.7 macrophages. Finally, rats supplemented with Nannochloropsis oculata extracted glycolipid-rich oil revealed a significant reduction of NO production through the downregulation of iNOS [68].
Abu-Serie et al. [63] reported that extracts from Chlorella vulgaris reduced NF-κB expression together with iNOS and COX-2 in an in vitro model of lipopolysaccharide-stimulated white blood cells. The NF-κB signaling pathway plays a central role in inflammation by regulating the transcription of pro-inflammatory genes such as COX-2, iNOS, and multiple pro-inflammatory cytokines [69]. Therefore, the decreased expression of COX-2 and iNOS caused by microalgae lipid extracts could result from the downregulation of this particular pathway, opening new target possibilities that require further study.

3.2. In Vitro Evaluation of Microalgae Lipids Impact in Pro-Inflammatory Cytokines

Another essential step to determine the anti-inflammatory potential of microalgae lipid extracts is evaluating the production/release of pro-inflammatory cytokines, such as TNF-α, IL-1β, and IL-6, in activated immune cells. Pro-inflammatory cytokines are predominantly produced by activated immune cells (e.g., macrophages, monocytes, lymphocytes) and play an essential role in pro-inflammatory reactions [70]. Their inhibition results in the attenuation of the inflammatory response, posing a decisive step towards inflammation resolution. The assessment of TNF-α, IL-1β, and IL-6 levels in cell lines (Raw264.7 and THP-1 macrophages) reported for lipid extracts from Nitzschia palea, Chlorella vulgaris, Tetraselmis suecica, Micractinium sp., Aurantiochytrium mangrovei, Phaeodactylum tricornutum, Chloromona reticulata, and Spirulina maxima showed the capacity to downregulate their production [20][60][62][63][64][65][66][71]. When compared to the use of crude extracts to evaluate the downregulatory effect of microalgae lipids on pro-inflammatory cytokines, the studies using isolated lipid classes and species are reduced. Oxylipins resulting from the enzymatical oxidation of PUFAs, isolated from Chlamydomonas debaryana and Nannochloropsis gaditana, and LPC(16:0), isolated from Cylindrotheca Closterium, showed the capacity to downregulate LPS-triggered TNF-α production in THP-1 macrophages [72][73]. The induction of IL-6 in LPS-activated Raw264.7 cells was decreased with free and esterified DGLA from a mutant strain of the microalga Lobosphaera incisa P127 [74]. Another study observed a reduction in TNF-α, IL-6, and IL-1β expression in peritoneal blood mononuclear cells (PBMC) treated with ergosterol and 7-dehydroporiferasterol isolated from the microalga Dunaliella tertiolecta [75]. This mix of phytosterols from the microalga Dunaliella tertiolecta raised anti-inflammatory cytokine IL-10 levels, strengthening the anti-inflammatory potential. Ávila-Román et al. described newly isolated oxylipins from Chlamydomonas debaryana derived from 16:4 and 18:4 fatty acids and used them as diet supplementation in a 2,4,6-trinitrobenzenesulfonic acid (TNBS)-induced colitis animal model, observing a downregulation of TNF-α. The most active oxylipin was a C-16 hydroxy acid [72].

This entry is adapted from the peer-reviewed paper 10.3390/ijms22189825

References

  1. Budreviciute, A.; Damiati, S.; Sabir, D.K.; Onder, K.; Schuller-Goetzburg, P.; Plakys, G.; Katileviciute, A.; Khoja, S.; Kodzius, R. Management and Prevention Strategies for Non-communicable Diseases (NCDs) and Their Risk Factors. Front. Public Health 2020, 8, 1–11.
  2. GBD 2016 Causes of Death Collaborators. Global, regional, and national age-sex specifc mortality for 264 causes of death, 1980–2016: A systematic analysis for the Global Burden of Disease Study. Lancet 2017, 390, 1151–1210.
  3. FAO; WHO. Sustainable and Healthy Diets: Guiding Principles; FAO: Rome, Italy, 2019.
  4. Jaul, E.; Barron, J. Age-Related Diseases and Clinical and Public Health Implications for the 85 Years Old and Over Population. Front. Public Health 2017, 5, 335.
  5. Amarya, S.; Singh, K.; Sabharwal, M. Changes during aging and their association with malnutrition. J. Clin. Gerontol. Geriatr. 2015, 6, 78–84.
  6. Phillips, C.M.; Chen, L.-W.; Heude, B.; Bernard, J.Y.; Harvey, N.C.; Duijts, L.; Mensink-Bout, S.M.; Polanska, K.; Mancano, G.; Suderman, M.; et al. Dietary Inflammatory Index and Non-Communicable Disease Risk: A Narrative Review. Nutrients 2019, 11, 1873.
  7. McHugh, D.; Gil, J. Senescence and aging: Causes, consequences, and therapeutic avenues. J. Cell Biol. 2017, 217, 65–77.
  8. Everitt, A.V.; Hilmer, S.N.; Brand-Miller, J.C.; Jamieson, H.A.; Truswell, A.S.; Sharma, A.P.; Mason, R.S.; Morris, B.J.; Le Couteur, D.G. Dietary approaches that delay age-related diseases. Clin. Interv. Aging 2006, 1, 11–31.
  9. Margină, D.; Ungurianu, A.; Purdel, C.; Tsoukalas, D.; Sarandi, E.; Thanasoula, M.; Tekos, F.; Mesnage, R.; Kouretas, D.; Tsatsakis, A. Chronic Inflammation in the Context of Everyday Life: Dietary Changes as Mitigating Factors. Int. J. Environ. Res. Public Health 2020, 17, 4135.
  10. Hardman, W.E. Diet components can suppress inflammation and reduce cancer risk. Nutr. Res. Pract. 2014, 8, 233–240.
  11. Khan, M.I.; Shin, J.H.; Kim, J.D. The promising future of microalgae: Current status, challenges, and optimization of a sustainable and renewable industry for biofuels, feed, and other products. Microb. Cell Fact. 2018, 17, 1–21.
  12. Ravindran, B.; Gupta, S.K.; Cho, W.M.; Kim, J.K.; Lee, S.R.; Jeong, K.H.; Lee, D.J.; Choi, H.C. Microalgae potential and multiple roles-current progress and future prospects-an overview. Sustainability 2016, 8, 1215.
  13. Kay, R.A.; Barton, L.L. Microalgae as food and supplement. Crit. Rev. Food Sci. Nutr. 1991, 30, 555–573.
  14. Krupanidhi, S.; Sanjeevi, C.B. Omega-3 Fatty Acids for Nutrition and Medicine: Considering Microalgae Oil as a Vegetarian Source of EPA and DHA. Curr. Diabetes Rev. 2007, 3, 198–203.
  15. Sharma, J.; Sarmah, P.; Bishnoi, N.R. Market Perspective of EPA and DHA Production from Microalgae. In Nutraceutical Fatty Acids from Oleaginous Microalgae; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2020; pp. 281–297.
  16. Lordan, R.; Redfern, S.; Tsoupras, A.; Zabetakis, I. Inflammation and cardiovascular disease: Are marine phospholipids the answer? Food Funct. 2020, 11, 2861–2885.
  17. Da Costa, E.; Silva, J.; Mendonça, S.H.; Abreu, M.H.; Domingues, M.R.R.; Mendonça, S.H.; Abreu, M.H.; Domingues, M.R.R. Lipidomic approaches towards deciphering glycolipids from microalgae as a reservoir of bioactive lipids. Mar. Drugs 2016, 14, 101.
  18. Batista, A.P.; Niccolai, A.; Bursic, I.; Sousa, I.; Raymundo, A.; Rodolfi, L.; Biondi, N.; Tredici, M.R. Microalgae as Functional Ingredients in Savory Food Products: Application to Wheat Crackers. Foods 2019, 8, 611.
  19. Couto, D.; Melo, T.; Conde, T.A.; Costa, M.; Silva, J.; Domingues, M.R.M.; Domingues, P. Chemoplasticity of the polar lipid profile of the microalgae Chlorella vulgaris grown under heterotrophic and autotrophic conditions. Algal Res. 2021, 53, 102128.
  20. Suh, S.-S.; Hong, J.-M.; Kim, E.J.; Jung, S.W.; Kim, S.-M.; Kim, J.E.; Kim, I.-C.; Kim, S. Anti-inflammation and Anti-Cancer Activity of Ethanol Extract of Antarctic Freshwater Microalga, Micractinium sp. Int. J. Med. Sci. 2018, 15, 929–936.
  21. Bergé, J.P.; Debiton, E.; Dumay, J.; Durand, P.; Barthomeuf, C. In Vitro Anti-inflammatory and Anti-proliferative Activity of Sulfolipids from the Red Alga Porphyridium cruentum. J. Agric. Food Chem. 2002, 50, 6227–6232.
  22. Banskota, A.H.; Stefanova, R.; Sperker, S.; McGinn, P.J. New diacylglyceryltrimethylhomoserines from the marine microalga Nannochloropsis granulata and their nitric oxide inhibitory activity. Environ. Boil. Fishes 2013, 25, 1513–1521.
  23. Yang, X.; Li, Y.; Li, Y.; Ye, D.; Yuan, L.; Sun, Y.; Han, D.; Hu, Q. Solid Matrix-Supported Supercritical CO2 Enhances Extraction of γ-Linolenic Acid from the Cyanobacterium Arthrospira (Spirulina) platensis and Bioactivity Evaluation of the Molecule in Zebrafish. Mar. Drugs 2019, 17, 203.
  24. Bruno, A.; Rossi, C.; Marcolongo, G.; Di Lena, A.; Venzo, A.; Berrie, C.P.; Corda, D. Selective in vivo anti-inflammatory action of the galactolipid monogalactosyldiacylglycerol. Eur. J. Pharmacol. 2005, 524, 159–168.
  25. Banskota, A.H.; Gallant, P.; Stefanova, R.; Melanson, R.; O’Leary, S.J.B. Monogalactosyldiacylglycerols, potent nitric oxide inhibitors from the marine microalga Tetraselmis chui. Nat. Prod. Res. 2013, 27, 1084–1090.
  26. Fahy, E.; Subramaniam, S.; Brown, H.A.; Glass, C.K.; Merrill, A.H.; Murphy, R.C.; Raetz, C.R.H.; Russell, D.W.; Seyama, Y.; Shaw, W.; et al. A comprehensive classification system for lipids. J. Lipid Res. 2005, 46, 839–862.
  27. Yao, L.; Gerde, J.A.; Lee, S.-L.; Wang, T.; Harrata, K.A. Microalgae Lipid Characterization. J. Agric. Food Chem. 2015, 63, 1773–1787.
  28. Liu, P.; Corilo, Y.; Marshall, A.G. Polar Lipid Composition of Biodiesel Algae Candidates Nannochloropsis oculata and Haematococcus pluvialis from Nano Liquid Chromatography Coupled with Negative Electrospray Ionization 14.5 T Fourier Transform Ion Cyclotron Resonance Mass Spectrometry. Energy Fuels 2016, 30, 8270–8276.
  29. Yang, M.; Meng, Y.; Chu, Y.; Fan, Y.; Cao, X.; Xue, S.; Chi, Z. Triacylglycerol accumulates exclusively outside the chloroplast in short-term nitrogen-deprived Chlamydomonas reinhardtii. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2018, 1863, 1478–1487.
  30. White, D.A.; Rooks, P.A.; Kimmance, S.; Tait, K.; Jones, M.; Tarran, G.A.; Cook, C.; Llewellyn, C.A. Modulation of Polar Lipid Profiles in Chlorella sp. in Response to Nutrient Limitation. Metabolites 2019, 9, 39.
  31. Řezanka, T.; Podojil, M. Preparative separation of algal polar lipids and of individual molecular species by high-performance liquid chromatography and their identification by gas chromatography—Mass spectrometry. J. Chromatogr. A 1989, 463, 397–408.
  32. Koukouraki, P.; Tsoupras, A.; Sotiroudis, G.; Demopoulos, C.A.; Sotiroudis, T.G. Antithrombotic properties of Spirulina extracts against platelet-activating factor and thrombin. Food Biosci. 2020, 37, 100686.
  33. Shiels, K.; Tsoupras, A.; Lordan, R.; Nasopoulou, C.; Zabetakis, I.; Murray, P.; Saha, S.K. Bioactive Lipids of Marine Microalga Chlorococcum sp. SABC 012504 with Anti-Inflammatory and Anti-thrombotic Activities. Mar. Drugs 2021, 19, 28.
  34. Katiyar, R.; Arora, A. Health promoting functional lipids from microalgae pool: A review. Algal Res. 2020, 46, 101800.
  35. Adarme-Vega, T.C.; Lim, D.K.Y.; Timmins, M.; Vernen, F.; Felicitas, V.; Schenk, P.M. Microalgal biofactories: A promising approach towards sustainable omega-3 fatty acid production. Microb. Cell Factories 2012, 11, 96.
  36. Maltsev, Y.; Maltseva, K. Fatty Acids of Microalgae: Diversity and Applications. In Reviews in Environmental Science and Biotechnology; Springer: Dordrecht, The Netherlands, 2021; Volume 20, pp. 515–547.
  37. Shen, P.-L.; Wang, H.-T.; Pan, Y.-F.; Meng, Y.-Y.; Wu, P.-C.; Xue, S. Identification of Characteristic Fatty Acids to Quantify Triacylglycerols in Microalgae. Front. Plant Sci. 2016, 7, 162.
  38. Ramesh Kumar, B.; Deviram, G.; Mathimani, T.; Duc, P.A.; Pugazhendhi, A. Microalgae as rich source of polyunsaturated fatty acids. Biocatal. Agric. Biotechnol. 2019, 17, 583–588.
  39. Rettner, J.; Werner, M.; Meyer, N.; Werz, O.; Pohnert, G. Survey of the C20 and C22 oxylipin family in marine diatoms. Tetrahedron Lett. 2018, 59, 828–831.
  40. Challagulla, V.; Nayar, S.; Walsh, K.; Fabbro, L. Advances in techniques for assessment of microalgal lipids. Crit. Rev. Biotechnol. 2017, 37, 566–578.
  41. Mankad, D.; Dupuis, A.; Smile, S.; Roberts, W.; Brian, J.; Lui, T.; Genore, L.; Zaghloul, D.; Iaboni, A.; Marcon, P.M.; et al. A randomized, placebo controlled trial of omega-3 fatty acids in the treatment of young children with autism. Mol. Autism 2015, 6, 18.
  42. Barros, R.; Moreira, A.; Fonseca, J.; Delgado, L.; Castel-Branco, M.G.; Haahtela, T.; Lopes, C.; Moreira, P. Dietary intake of α-linolenic acid and low ratio of n-6:n-3 PUFA are associated with decreased exhaled NO and improved asthma control. Br. J. Nutr. 2011, 106, 441–450.
  43. Rennie, K.L.; Hughes, J.; Lang, R.; Jebb, S.A. Nutritional management of rheumatoid arthritis: A review of the evidence. J. Hum. Nutr. Diet. 2003, 16, 97–109.
  44. Zheng, L.; Fleith, M.; Giuffrida, F.; O’Neill, B.V.; Schneider, N. Dietary Polar Lipids and Cognitive Development: A Narrative Review. Adv. Nutr. 2019, 10, 1163–1176.
  45. Rey, F.; Lopes, D.; Maciel, E.; Monteiro, J.P.; Skjermo, J.; Funderud, J.; Raposo, D.; Domingues, P.; Calado, R.; Domingues, M.R. Polar lipid profile of Saccharina latissima, a functional food from the sea. Algal Res. 2019, 39, 101473.
  46. Schneider, H.; Braun, A.; Füllekrug, J.; Stremmel, W.; Ehehalt, R. Lipid Based Therapy for Ulcerative Colitis—Modulation of Intestinal Mucus Membrane Phospholipids as a Tool to Influence Inflammation. Int. J. Mol. Sci. 2010, 11, 4149–4164.
  47. Tsoupras, A.; Lordan, R.; Zabetakis, I. Inflammation, not Cholesterol, Is a Cause of Chronic Disease. Nutrients 2018, 10, 604.
  48. European Commission. The EU Blue Economy Report 2020; European Commission: Brussels, Belgium, 2020.
  49. Draaisma, R.B.; Wijffels, R.H.; Slegers, P.; Brentner, L.B.; Roy, A.; Barbosa, M. Food commodities from microalgae. Curr. Opin. Biotechnol. 2013, 24, 169–177.
  50. Samarakoon, K.; Ko, J.-Y.; Shah, M.R.; Lee, J.-H.; Kang, M.-C.; Kwon, O.-N.; Lee, J.-B.; Jeon, Y.-J. In vitro studies of anti-inflammatory and anticancer activities of organic solvent extracts from cultured marine microalgae. ALGAE 2013, 28, 111–119.
  51. Sanjeewa, K.K.A.; Fernando, I.P.S.; Samarakoon, K.W.; Lakmal, H.H.C.; Kim, E.A.; Kwon, O.N.; Dilshara, M.G.; Lee, J.B.; Jeon, Y.J. Anti-inflammatory and anti-cancer activities of sterol rich fraction of cultured marine microalga nannochloropsis oculata. ALGAE 2016, 31, 277–287.
  52. Cardoso, C.; Pereira, H.; Franca, J.; Matos, J.; Monteiro, I.; Pousão-Ferreira, P.; Gomes, A.; Barreira, L.; Varela, J.; Neng, N.; et al. Lipid composition and some bioactivities of 3 newly isolated microalgae (Tetraselmis sp. IMP3, Tetraselmis sp. CTP4, and Skeletonema sp.). Aquac. Int. 2019, 28, 711–727.
  53. Lauritano, C.; Andersen, J.H.; Hansen, E.; Albrigtsen, M.; Escalera, L.; Esposito, F.; Helland, K.; Hanssen, K.Ø.; Romano, G.; Ianora, A. Bioactivity Screening of Microalgae for Antioxidant, Anti-Inflammatory, Anticancer, Anti-Diabetes, and Antibacterial Activities. Front. Mar. Sci. 2016, 3, 1–18.
  54. Banskota, A.H.; Sperker, S.; Stefanova, R.; McGinn, P.J.; O’Leary, S.J.B. Antioxidant properties and lipid composition of selected microalgae. Environ. Boil. Fishes 2018, 31, 309–318.
  55. Banskota, A.H.; Stefanova, R.; Sperker, S.; Melanson, R.; Osborne, J.A.; O’Leary, S.J.B. Five new galactolipids from the freshwater microalga Porphyridium aerugineum and their nitric oxide inhibitory activity. Environ. Boil. Fishes 2013, 25, 951–960.
  56. Ávila-Román, J.; Talero, E.; Alcaide, A.; De Los Reyes, C.; Zubía, E.; García-Mauriño, S.; Motilva, V. Preventive effect of the microalga Chlamydomonas debaryana on the acute phase of experimental colitis in rats. Br. J. Nutr. 2014, 112, 1055–1064.
  57. Gutiérrez-Pliego, L.E.; Martinez-Carrillo, B.E.; Resendiz-Albor, A.A.; Arciniega-Martínez, I.M.; Escoto-Herrera, J.A.; Rosales-Gómez, C.A.; Valdes-Ramos, R. Effect of Supplementation with n-3 Fatty Acids Extracted from Microalgae on Inflammation Biomarkers from Two Different Strains of Mice. J. Lipids 2018, 2018, 1–10.
  58. Wang, D.; DuBois, R.N. The role of COX-2 in intestinal inflammation and colorectal cancer. Oncogene 2009, 29, 781–788.
  59. Da Costa, E.; Amaro, H.M.; Melo, T.; Guedes, A.C.; Domingues, M.R. Screening for polar lipids, antioxidant, and anti-inflammatory activities of Gloeothece sp. lipid extracts pursuing new phytochemicals from cyanobacteria. J. Appl. Phycol. 2020, 32, 3015–3030.
  60. Lakshmegowda, S.B.; Rajesh, S.K.; Kandikattu, H.K.; Nallamuthu, I.; Khanum, F. In Vitro and In Vivo Studies on Hexane Fraction of Nitzschia palea, a Freshwater Diatom for Oxidative Damage Protective and Anti-inflammatory Response. Rev. Bras. Farm. 2020, 30, 189–201.
  61. Conde, T.A.; Couto, D.; Melo, T.; Costa, M.; Silva, J.; Domingues, M.R.; Domingues, P. Polar lipidomic profile shows Chlorococcum amblystomatis as a promising source of value-added lipids. Sci. Rep. 2021, 11, 1–23.
  62. Sibi, G.; Rabina, S. Inhibition of Pro-inflammatory mediators and cytokines by Chlorella vulgaris extracts. Pharmacogn. Res. 2016, 8, 118–122.
  63. Abu-Serie, M.M.; Habashy, N.H.; Attia, W.E. In vitro evaluation of the synergistic antioxidant and anti-inflammatory activities of the combined extracts from Malaysian Ganoderma lucidum and Egyptian Chlorella vulgaris. BMC Complement. Altern. Med. 2018, 18, 1–13.
  64. Neumann, U.; Louis, S.; Gille, A.; Derwenskus, F.; Schmid-Staiger, U.; Briviba, K.; Bischoff, S.C. Anti-inflammatory effects of Phaeodactylum tricornutum extracts on human blood mononuclear cells and murine macrophages. J. Appl. Phycol. 2018, 30, 2837–2846.
  65. Suh, S.-S.; Hong, J.-M.; Kim, E.J.; Jung, S.W.; Chae, H.; Kim, J.E.; Kim, J.H.; Kim, I.-C.; Kim, S. Antarctic freshwater microalga, Chloromonas reticulata, suppresses inflammation and carcinogenesis. Int. J. Med. Sci. 2019, 16, 189–197.
  66. Jo, W.S.; Choi, Y.J.; Kim, H.J.; Nam, B.H.; Hong, S.H.; Lee, G.A.; Lee, S.W.; Seo, S.Y.; Jeong, M.H. Anti-inflammatory effect of microalgal extracts from Tetraselmis suecica. Food Sci. Biotechnol. 2010, 19, 1519–1528.
  67. Banskota, A.H.; Stefanova, R.; Gallant, P.; McGinn, P.J. Mono- and digalactosyldiacylglycerols: Potent nitric oxide inhibitors from the marine microalga Nannochloropsis granulata. Environ. Boil. Fishes 2012, 25, 349–357.
  68. Kagan, M.L.; Levy, A.; Leikin-Frenkel, A. Comparative study of tissue deposition of omega-3 fatty acids from polar-lipid rich oil of the microalgae Nannochloropsis oculata with krill oil in rats. Food Funct. 2014, 6, 185–191.
  69. Natarajan, K.; Abraham, P.; Kota, R.; Isaac, B. NF-κB-iNOS-COX2-TNF α inflammatory signaling pathway plays an important role in methotrexate induced small intestinal injury in rats. Food Chem. Toxicol. 2018, 118, 766–783.
  70. Zhang, J.-M.; An, J. Cytokines, Inflammation and Pain. Int. Anesth. Clin. 2007, 45, 27–37.
  71. Choi, W.Y.; Sim, J.-H.; Lee, J.-Y.; Kang, D.H.; Lee, H.Y. Increased Anti-Inflammatory Effects on LPS-Induced Microglia Cells by Spirulina maxima Extract from Ultrasonic Process. Appl. Sci. 2019, 9, 2144.
  72. De Los Reyes, C.; Ávila-Román, J.; Ortega, M.J.; De La Jara, A.; García-Mauriño, S.; Motilva, V.; Zubía, E. Oxylipins from the microalgae Chlamydomonas debaryana and Nannochloropsis gaditana and their activity as TNF-α inhibitors. Phytochemistry 2014, 102, 152–161.
  73. Lauritano, C.; Helland, K.; Riccio, G.; Andersen, J.H.; Ianora, A.; Hansen, E.H. Lysophosphatidylcholines and Chlorophyll-Derived Molecules from the Diatom Cylindrotheca closterium with Anti-Inflammatory Activity. Mar. Drugs 2020, 18, 166.
  74. Novichkova, E.; Chumin, K.; Eretz-Kdosha, N.; Boussiba, S.; Gopas, J.; Cohen, G.; Khozin-Goldberg, I. DGLA from the Microalga Lobosphaera Incsa P127 Modulates Inflammatory Response, Inhibits iNOS Expression and Alleviates NO Secretion in RAW264.7 Murine Macrophages. Nutrients 2020, 12, 2892.
  75. Caroprese, M.; Albenzio, M.; Ciliberti, M.G.; Francavilla, M.; Sevi, A. A mixture of phytosterols from Dunaliella tertiolecta affects proliferation of peripheral blood mononuclear cells and cytokine production in sheep. Vet. Immunol. Immunopathol. 2012, 150, 27–35.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
This entry is offline, you can click here to edit this entry!
Video Production Service
Feedback