Digestibility and oxidative stability of plant lipid assemblies: An underexplored source of potentially bioactive surfactants?

Most lipids in our diet come under the form of triacylglycerols that are often redispersed and stabilized by surfactants in processed foods. In plant however, lipid assemblies constitute interesting sources of natural bioactive and functional ingredients. In most photosynthetic sources, polar lipids rich in ω3 fatty acids are concentrated. The objective of this review is to summarize all the knowledge about the physico-chemical composition, digestive behavior and oxidative stability of plant polar lipid assemblies to emphasize their potential as functional ingredients in human diet and their potentialities to substitute artificial surfactants/antioxidants. The specific composition of plant membrane assemblies is detailed, including plasma membranes, oil bodies, and chloroplast; emphasizing its concentration in phospholipids, galactolipids, peculiar proteins, and phenolic compounds. These molecular species are hydrolyzed by specific digestive enzymes in the human gastrointestinal tract and reduced the hydrolysis of triacylglycerols and their subsequent absorption. Galactolipids specifically can activate ileal break and intrinsically present an antioxidant (AO) activity and metal chelating activity. In addition, their natural association with phenolic compounds and their physical state (Lα state of digalactosyldiacylglycerols) in membrane assemblies can enhance their stability to oxidation. All these elements make plant membrane molecules and assemblies very promising components with a wide range of potential applications to vectorize ω3 polyunsaturated fatty acids, and equilibrate human diet.

[1]  V. Vié,et al.  Stability to oxidation and interfacial behavior at the air/water interface of minimally-processed versus processed walnut oil-bodies. , 2021, Food chemistry.

[2]  F. Laugerette,et al.  Impact of Rapeseed and Soy Lecithin on Postprandial Lipid Metabolism, Bile Acid Profile and Gut Bacteria in Mice. , 2021, Molecular nutrition & food research.

[3]  J. Weiss,et al.  Recent advances in the composition, extraction and food applications of plant-derived oleosomes , 2020 .

[4]  C. Knibbe,et al.  Rapeseed Lecithin Increases Lymphatic Lipid Output and α-Linolenic Acid Bioavailability in Rats. , 2020, The Journal of nutrition.

[5]  P. Villeneuve,et al.  The digestion of galactolipids and its ubiquitous function in Nature for the uptake of the essential α-linolenic acid. , 2020, Food & function.

[6]  D. Vergara,et al.  An in vitro digestion study of encapsulated lactoferrin in rapeseed phospholipid-based liposomes. , 2020, Food chemistry.

[7]  M. Abbasalizad Farhangi,et al.  A Systematic Review of the Potential Effects of Thylakoids in the Management of Obesity and Its Related Issues , 2020 .

[8]  R. Lebrun,et al.  Characterization of all the lipolytic activities in pancreatin and comparison with porcine and human pancreatic juices. , 2020, Biochimie.

[9]  F. Carrière,et al.  In vitro digestion of galactolipids from chloroplast-rich fraction (CRF) of postharvest, pea vine field residue (haulm) and spinach leaves. , 2019, Food & function.

[10]  C. V. Nikiforidis Structure and functions of oleosomes (oil bodies). , 2019, Advances in colloid and interface science.

[11]  M. Michalski,et al.  Vegetable lecithins: a review of their compositional diversity, impact on lipid metabolism and potential in cardiometabolic disease prevention. , 2019, Biochimie.

[12]  Yan-Li Du,et al.  Peanut Oil Body Composition and Stability. , 2019, Journal of food science.

[13]  L. Ouchchane,et al.  Milk polar lipids reduce lipid cardiovascular risk factors in overweight postmenopausal women: towards a gut sphingomyelin-cholesterol interplay , 2019, Gut.

[14]  R. Vettor,et al.  Cardio-Metabolic Disorders in Non-Alcoholic Fatty Liver Disease , 2019, International journal of molecular sciences.

[15]  I. Desgagné-Penix,et al.  Study of antioxidant properties of thylakoids and application in UV protection and repair of UV‐induced damage , 2019, Journal of cosmetic dermatology.

[16]  Zhang Yan,et al.  Thermally treated soya bean oleosomes: the changes in their stability and associated proteins , 2019, International Journal of Food Science & Technology.

[17]  P. Rougé,et al.  Oil bodies (oleosomes): Occurrence, structure, allergenicity , 2018, Revue Française d'Allergologie.

[18]  Y. Keum,et al.  Omega-3 and omega-6 polyunsaturated fatty acids: Dietary sources, metabolism, and significance - A review. , 2018, Life sciences.

[19]  K. Miyashita,et al.  Comparison of Oxidative Stability of Monogalactosyl Diacylglycerol, Digalactosyl Diacylglycerol, and Triacylglycerol Containing Polyunsaturated Fatty Acids , 2018 .

[20]  A. Shanbhag Utilization of Modified Lecithin to Control Lipid Oxidation in Bulk Oils , 2018 .

[21]  D. Mcclements,et al.  Hurdles in predicting antioxidant efficacy in oil-in-water emulsions , 2017 .

[22]  Chien-Yu Huang,et al.  Unique Motifs and Length of Hairpin in Oleosin Target the Cytosolic Side of Endoplasmic Reticulum and Budding Lipid Droplet1[OPEN] , 2017, Plant Physiology.

[23]  M. Laville,et al.  Emulsifying dietary fat modulates postprandial endotoxemia associated with chylomicronemia in obese men: a pilot randomized crossover study , 2017, Lipids in Health and Disease.

[24]  F. Abbas,et al.  Biochemical and molecular responses of oilseed crops to heavy metal stress , 2017 .

[25]  K. Stenkula,et al.  Thylakoids reduce body fat and fat cell size by binding to dietary fat making it less available for absorption in high-fat fed mice , 2017, Nutrition & Metabolism.

[26]  Jingbo Li,et al.  Identification and quantification of phenolic compounds in rapeseed originated lecithin and antioxidant activity evaluation , 2016 .

[27]  P. Ellis,et al.  A review of the impact of processing on nutrient bioaccessibility and digestion of almonds , 2016, International journal of food science & technology.

[28]  Koichi Kobayashi Role of membrane glycerolipids in photosynthesis, thylakoid biogenesis and chloroplast development , 2016, Journal of Plant Research.

[29]  E. Decker,et al.  Phospholipids in foods: prooxidants or antioxidants? , 2016, Journal of the science of food and agriculture.

[30]  A. Huang,et al.  Bioinformatics Reveal Five Lineages of Oleosins and the Mechanism of Lineage Evolution Related to Structure/Function from Green Algae to Seed Plants1[OPEN] , 2015, Plant Physiology.

[31]  E. Meugnier,et al.  Impact of various emulsifiers on ALA bioavailability and chylomicron synthesis through changes in gastrointestinal lipolysis. , 2015, Food & function.

[32]  D. Mcclements,et al.  Impact of extraneous proteins on the gastrointestinal fate of sunflower seed (Helianthus annuus) oil bodies: a simulated gastrointestinal tract study. , 2015, Food & function.

[33]  J. Jeong,et al.  Beneficial effects of phosphatidylcholine on high-fat diet-induced obesity, hyperlipidemia and fatty liver in mice. , 2014, Life sciences.

[34]  J. Coutinho,et al.  Superactivity induced by micellar systems as the key for boosting the yield of enzymatic reactions , 2014 .

[35]  C. Genot,et al.  Lipid Oxidation in Oil‐in‐Water Emulsions: Involvement of the Interfacial Layer , 2014 .

[36]  Y. Hua,et al.  Macronutrients and micronutrients of soybean oil bodies extracted at different pH. , 2014, Journal of food science.

[37]  C. V. Nikiforidis,et al.  Composition, properties and potential food applications of natural emulsions and cream materials based on oil bodies , 2014 .

[38]  D. Leister,et al.  Structure and dynamics of thylakoids in land plants. , 2014, Journal of experimental botany.

[39]  E. Maréchal,et al.  Contribution of galactoglycerolipids to the 3‐dimensional architecture of thylakoids , 2014, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[40]  M. Walla,et al.  Reducing the Dietary Omega-6:Omega-3 Utilizing α-Linolenic Acid; Not a Sufficient Therapy for Attenuating High-Fat-Diet-Induced Obesity Development Nor Related Detrimental Metabolic and Adipose Tissue Inflammatory Outcomes , 2014, PloS one.

[41]  C. Brennan,et al.  Bioavailability and Potential Uses of Vegetarian Sources of Omega-3 Fatty Acids: A Review of the Literature , 2014, Critical reviews in food science and nutrition.

[42]  Claire Bourlieu,et al.  Specificity of Infant Digestive Conditions: Some Clues for Developing Relevant In Vitro Models , 2011, Critical reviews in food science and nutrition.

[43]  Tong Wang,et al.  Oxidative stability of soybean oil in oleosomes as affected by pH and iron. , 2013, Food chemistry.

[44]  F. Kraemer,et al.  Lipid droplet metabolism , 2013, Current opinion in clinical nutrition and metabolic care.

[45]  M. Bonn,et al.  The role of intact oleosin for stabilization and function of oleosomes. , 2013, The journal of physical chemistry. B.

[46]  C. Lopez,et al.  Multiscale structures of lipids in foods as parameters affecting fatty acid bioavailability and lipid metabolism. , 2013, Progress in lipid research.

[47]  C. V. Nikiforidis,et al.  Effect of recovery methods on the oxidative and physical stability of oil body emulsions. , 2013, Food chemistry.

[48]  Y. Gohon,et al.  Fold of an oleosin targeted to cellular oil bodies. , 2013, Biochimica et biophysica acta.

[49]  E. Scholten,et al.  Oil bodies: An insight on their microstructure — maize germ vs sunflower seed , 2013 .

[50]  R. Zhu,et al.  The Oil Bodies of Liverworts: Unique and Important Organelles in Land Plants , 2013 .

[51]  Harjinder Singh,et al.  In vitro gastric and intestinal digestion of a walnut oil body dispersion. , 2013, Journal of agricultural and food chemistry.

[52]  E. Scholten,et al.  Purified oleosins at air–water interfaces , 2013 .

[53]  C. Marinangeli,et al.  Critical Reviews in Food Science and Nutrition , 2013 .

[54]  D. Lairon,et al.  Modulating absorption and postprandial handling of dietary fatty acids by structuring fat in the meal: a randomized crossover clinical trial. , 2013, The American journal of clinical nutrition.

[55]  C. Spickett,et al.  Chemistry of phospholipid oxidation. , 2012, Biochimica et biophysica acta.

[56]  Robert V Farese,et al.  Lipid droplets and cellular lipid metabolism. , 2012, Annual review of biochemistry.

[57]  D. Mcclements,et al.  Physical and oxidative stability of pre-emulsified oil bodies extracted from soybeans. , 2012, Food chemistry.

[58]  G. Tucker,et al.  Phytochemical Composition of Oryza sativa (Rice) Bran Oil Bodies in Crude and Purified Isolates , 2012 .

[59]  E. Meugnier,et al.  Coupling in vitro gastrointestinal lipolysis and Caco-2 cell cultures for testing the absorption of different food emulsions. , 2012, Food & function.

[60]  Harjinder Singh,et al.  Behavior of almond oil bodies during in vitro gastric and intestinal digestion. , 2012, Food & function.

[61]  F. Carrière,et al.  Understanding the lipid-digestion processes in the GI tract before designing lipid-based drug-delivery systems. , 2012, Therapeutic delivery.

[62]  K. Miyashita,et al.  Oxidative stability of glyceroglycolipids containing polyunsaturated fatty acids. , 2012, Journal of oleo science.

[63]  M. Rayner,et al.  Chloroplast thylakoid membrane-stabilised emulsions. , 2011, Journal of the science of food and agriculture.

[64]  D. Mcclements,et al.  Mechanisms of lipid oxidation in food dispersions , 2011 .

[65]  S. Mongrand,et al.  Lipids of the Plant Plasma Membrane , 2011 .

[66]  F. Shahidi,et al.  Lipid oxidation and improving the oxidative stability. , 2010, Chemical Society reviews.

[67]  D. Mcclements,et al.  Oxidative stability of Echium plantagineum seed oil bodies , 2010 .

[68]  Yeming Chen,et al.  Simple extraction method of non-allergenic intact soybean oil bodies that are thermally stable in an aqueous medium. , 2010, Journal of agricultural and food chemistry.

[69]  M. Golding,et al.  The influence of emulsion structure and stability on lipid digestion , 2010 .

[70]  P. Villeneuve,et al.  Lipolysis of natural long chain and synthetic medium chain galactolipids by pancreatic lipase-related protein 2. , 2010, Biochimica et biophysica acta.

[71]  J. Rehfeld,et al.  Thylakoids suppress appetite by increasing cholecystokinin resulting in lower food intake and body weight in high‐fat fed mice , 2009, Phytotherapy research : PTR.

[72]  F. Carrière,et al.  Continuous measurement of galactolipid hydrolysis by pancreatic lipolytic enzymes using the pH-stat technique and a medium chain monogalactosyl diglyceride as substrate. , 2009, Biochimica et biophysica acta.

[73]  P. Wilde,et al.  Modulating pancreatic lipase activity with galactolipids: effects of emulsion interfacial composition. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[74]  J. Rehfeld,et al.  Thylakoids promote release of the satiety hormone cholecystokinin while reducing insulin in healthy humans , 2009, Scandinavian Journal of Gastroenterology.

[75]  M. Lad,et al.  Oxidative stability of sunflower oil bodies , 2008 .

[76]  C. Cambillau,et al.  Structure of human pancreatic lipase-related protein 2 with the lid in an open conformation. , 2008, Biochemistry.

[77]  G. Márquez‐Ruiz,et al.  Changes and Effects of Dietary Oxidized Lipids in the Gastrointestinal Tract , 2008 .

[78]  R. Lebrun,et al.  Occurrence of pancreatic lipase-related protein-2 in various species and its relationship with herbivore diet. , 2008, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[79]  C. Dijkema,et al.  Phase behavior of phosphatidylglycerol in spinach thylakoid membranes as revealed by 31P-NMR. , 2008, Biochimica et biophysica acta.

[80]  V. Vié,et al.  Galactosyl headgroup interactions control the molecular packing of wheat lipids in Langmuir films and in hydrated liquid-crystalline mesophases. , 2007, Biochimica et biophysica acta.

[81]  J. Rehfeld,et al.  Chloroplast membranes retard fat digestion and induce satiety: effect of biological membranes on pancreatic lipase/co-lipase. , 2007, The Biochemical journal.

[82]  K. Miyashita,et al.  Unsaturated phosphatidylethanolamine as effective synergist in combination with alpha-tocopherol. , 2007, Journal of oleo science.

[83]  Ian D Fisk,et al.  Tocopherol—An intrinsic component of sunflower seed oil bodies , 2006 .

[84]  I. Konopka,et al.  Differences in content and composition of free lipids and carotenoids in flour of spring and winter wheat cultivated in Poland , 2006 .

[85]  B. Borgström Phosphatidylcholine as substrate for human pancreatic phospholipase A2. Importance of the physical state of the substrate , 1993, Lipids.

[86]  T. Sanders,et al.  Influence of triacylglycerol structure of stearic acid-rich fats on postprandial lipaemia , 2005, Proceedings of the Nutrition Society.

[87]  F. Carrière,et al.  Characterization of pancreatic lipase-related protein 2 isolated from human pancreatic juice. , 2004, Biochimica et biophysica acta.

[88]  P. Villeneuve,et al.  Antioxidant effect of soy lecithins on vegetable oil stability and their synergism with tocopherols , 2003 .

[89]  J. Mundy,et al.  Oil bodies and their associated proteins, oleosin and caleosin. , 2001, Physiologia plantarum.

[90]  N. Ferté,et al.  Oil-bodies as substrates for lipolytic enzymes. , 2001, Biochimica et biophysica acta.

[91]  H. Kindl,et al.  Phospholipid monolayer of plant lipid bodies attacked by phospholipase A2 shows 80 nm holes analyzed by atomic force microscopy. , 2000, Biophysical chemistry.

[92]  D. G. Lindsay,et al.  Plant sterols: biosynthesis, biological function and their importance to human nutrition. , 2000 .

[93]  L. Ohlsson Digestion and absorption of galactolipids , 2000 .

[94]  S. K. Han,et al.  Bacterial expression and characterization of human pancreatic phospholipase A2. , 1997, Biochimica et biophysica acta.

[95]  P. Shewry,et al.  Purification and characterization of oil-bodies (oleosomes) and oil-body boundary proteins (oleosins) from the developing cotyledons of sunflower (Helianthus annuus L.) , 1996, The Biochemical journal.

[96]  A. Nilsson,et al.  Hydrolysis of galactolipids by human pancreatic lipolytic enzymes and duodenal contents. , 1995, Journal of lipid research.

[97]  P. Laurent,et al.  Lipids, Proteins, and Structure of Seed Oil Bodies from Diverse Species , 1993, Plant physiology.

[98]  A. Huang,et al.  Oil bodies and oleosins in seeds , 1992 .

[99]  Hyun-Kyung Shin,et al.  Synergistic antioxidative effects of tocopherol and ascorbic acid in fish oil/lecithin/water system , 1991 .

[100]  A. Nilsson,et al.  Pancreatic lipolytic enzymes in human duodenal contents. Radioimmunoassay compared with enzyme activity. , 1991, Scandinavian journal of gastroenterology.

[101]  T. Miyazawa,et al.  The antioxidant effects of phospholipids on perilla oil , 1991 .

[102]  J. Browse,et al.  Glycerolipid Synthesis: Biochemistry and Regulation , 1991 .

[103]  Y. Lai,et al.  Oleosin isoforms of high and low molecular weights are present in the oil bodies of diverse seed species. , 1990, Plant physiology.

[104]  J. Joyard,et al.  Do thylakoids really contain phosphatidylcholine? , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[105]  T. D. Simpson,et al.  Phospholipid degradation in membranes of isolated soybean lipid bodies , 1989 .

[106]  L. Sarda,et al.  Kinetic assay of human gastric lipase on short- and long-chain triacylglycerol emulsions. , 1986, Gastroenterology.

[107]  J. Terao,et al.  Phospholipids plus tocopherols increase soybean oil stability , 1984 .

[108]  M. Frentzen,et al.  Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. , 2005, European journal of biochemistry.

[109]  R. Yamauchi,et al.  Autoxidation products of polyunsaturated galactolipids. , 1983 .

[110]  J. Barber,et al.  Monogalactosyldiacylglycerol: The most abundant polar lipid in nature , 1983 .

[111]  R. Verger,et al.  Pancreatic phospholipase A2 hydrolysis of phosphatidylcholines in various physicochemical states. , 1980, Biochimica et biophysica acta.

[112]  M. Anderson,et al.  The role of galactolipids in spinach chloroplast lamellar membranes: I. Partial purification of a bean leaf galactolipid lipase and its action on subchloroplast particles. , 1974, Plant physiology.