Abstract
Arachidonic acid (20∶4n−6, ArA) and its eicosanoid metabolites have been demonstrated to be implicated in immune functions of vertebrates, fish, and insects. Thus, the aim of this study was to assess the impact of ArA supplementation on the FA composition and hemocyte parameters of oysters Crassostrea gigas. Oyster dietary conditioning consisted of direct addition of ArA solutions at a dose of 0, 0.25, or 0.41 μg ArA per mL of seawater into tanks in the presence or absence of T-Iso algae. Results showed significant incorporation of ArA into gill polar lipids when administered with algae (up to 19.7%) or without algae (up to 12.1%). ArA supplementation led to an increase in hemocyte numbers, phagocytosis, and production of reactive oxygen species by hemocytes from ArA-supplemented oysters. Moreover, the inhibitory effect of Vibrio aestuarianus extracellular products on the adhesive proprieties of hemocytes was lessened in oysters fed ArA-supplemented T-Iso. All changes in oyster hemocyte parameters reported in the present study suggest that ArA and/or eicosanoid metabolites affect oyster hemocyte functions.
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Abbreviations
- AASH:
-
anti-aggregant solution for hemocytes
- ArA:
-
arachidonic acid
- AU:
-
arbitrary units
- DCFH-DA:
-
2′7′-dichlorofluorescein diacetate
- DPI:
-
diphenylene iodonium chloride
- DW:
-
dry weight
- ECP:
-
extracellular products
- FSSW:
-
filtered sterile seawater
- ROS:
-
reactive oxygen species
- WW:
-
wet weight
References
Calder, P.C. (2001) n−3 Polyunsaturated Fatty Acids, Inflammation and Immunity: Pouring Oil on Troubled Waters or Another Fishy Tale?, Nutr. Res. 21, 309–341.
Harbige, L.S. (2003) Fatty Acids, the Immune Response, and Autoimmunity: A Question of n−6 Essentiality and the Balance Between n−6 and n−3, Lipids 38, 323–341.
Borda, E.S., Tenenbaum, A., Sales, M.E., Rumi, L., and Sterin-Borda, L. (1998) Role of Arachidonic Acid Metabolites in the Action of a Beta-Adrenergic Agonist on Human Monocyte Phagocytosis, Prostaglandins Leukot. Essent. Fatty Acids 58, 85–90.
Bailie, M.B., Standiford, T.J., Laichalk, L.L., Coffey, M.J., Strieter, R., and Peters-Golden, M. (1996) Leukotriene-Deficient Mice Manifest Enhanced Lethality from Klebseilla pneumonia in Association with Decreased Alveolar Macrophage Phagocytic and Bactericidal Activities, J. Immunol. 157 (12), 5221–5224.
Davidson, J., Kerr, A., Guy, K., and Rotondo, D. (1998) Prostaglandin and Fatty Acid Modulation of Escherichia coli O157 Phagocytosis by Human Monocytic Cells, Immunol. 94, 228–234.
Lloret, S., and Moreno, J.J. (1996) Role of Kinases and G-Proteins on Arachidonate Release Induced by Zymosan in Mouse Peritoneal Macrophages, Internat. J. Biochem. Cell. Biol. 28, 465–472.
Mancuso, P., Standiford, T.J., Marshall, T., and Peters-Golden, M. (1985) 5-Lipoxygenase Reaction Products Modulate Alveolae Macrophage Phagocytosis of Klebsiella pneumoniae, Infect. Immun. 66, 5140–5146.
Lennartz, M.R. (1999) Phospholipases and Phagocytosis: The Role of Phospholipid-Derived Second Messengers in Phagocytosis, Internat. J. Biochem. Cell. Biol. 31, 415–430.
Sheldon, W.M.J., and Blazer, V.S. (1991) Influence of Dietary Lipid and Temperature on Bactericidal Activity of Channel Catfish Macrophages, J. Aquat. Anim. Health 3, 87–93.
Fracalossi, D.M., and Lowell, R.T. (1994) Dietary Lipid Sources Influence Responses of Channel Catfish (Ictalurus punctatus) to Challenge with the Pathogen Edwardsiella ictaluri, Aquaculture 98, 363–379.
Kiron, V., Fuduka, H., Takeushi, T., and Watanabe, T. (1995) Essential Fatty Acids Nutrition and Defense in Rainbow Trout Oncorhynchus mykiss, Comp. Biochem. Physiol. 111A, 361–367.
Lingenfelser, J.T., Blazer, V.S., and Gay, J. (1995) Influence of Fish Oils in Production Catfish Feeds on Selected Disease Resistance Factors, J. Appl. Aquaculture 5(2), 37–48.
Lin, Y.H., and Shiau, S.Y. (2003) Dietary Lipid Requirement of Grouper, Epinephelus malabaricus, and Effects on Immune Responses, Aquaculture 225, 243–250.
Thompson, K.D., Tatner, M.F., and Henderson, R.J. (1996) Effects of Dietary (n−3) and (n−6) Polyunsaturated Fatty Acid Ratio on the Immune Response of Atlantic Salmon, Salmo salar L., Aquaculture Nutr. 2, 21–31.
Wu, F.C., Ting, Y.Y., and Chen, H.Y. (2003) Dietary Docosahexaenoic Acid Is More Optimal Than Eicosapentaenoic Acid Affecting the Level of Cellular Defence Responses of the Juvenile Grouper Epinephelus malabaricus, Fish Shellfish Immunol. 14, 223–238.
Tafalla, C., Figueras, A., and Novoa, B. (2002) Possible Role of LTB4 in the Antiviral Activity of Turbot (Scophthalmus maximus) Leukocyte-Derived Supernatants Against Viral Hemorrhagic Septicemia Virus (VHSV), Develop. Comp. Immunol. 26, 283–293.
Wikfors, G.H., Patterson, G.W., Ghosh, P., Lewin, R.A., Smith, B.C., and Alix, J.H. (1996) Growth of Post-Set Oysters, Crassostrea virginica, on High-Lipid Strains of Algal Flagellates Tetraselmis spp., Aquaculture 143, 411–419.
Brown, M.R., McCausland, M.A., and Kowalski, K. (1998) The Nutritional Value of Four Australian Microalgal Strains Fed to Pacific Oyster Crassostrea gigas Spat, Aquaculture 165, 281–293.
Knauer, J., and Southgate, P.C. (1997) Growth and Fatty Acid Composition of Pacific Oyster (Crassostrea gigas) Spat Fed a Spray-Dried Freshwater Microalga (Spongiococcum excentricum) and Microencapsulated Lipids, Aquaculture 154, 293–303.
Knuckey, R.M., Brown, M.R., Barrett, S.M., and Hallegraeff, G.M. (2002) Isolation of New Nanoplanktonic Diatom Strains and Their Evaluation as Diets for Juvenile Pacific Oysters (Crassostrea gigas), Aquaculture 211, 253–274.
McCausland, M.A., Brown, M.R., Barrett, S.M., Diemar, J.A., and Heasman, M.P. (1999) Evaluation of Live Microalgae and Microalgal Pastes as Supplementary Food for Juvenile Pacific Oysters (Crassostrea gigas), Aquaculture 174, 323–342.
Martinez-Fernandez, E., Acosta-Salmon, H., and Rangel-Davalos, C. (2004) Ingestion and Digestion of 10 Species of Microalgae by Winged Pearl Oyster Pteria sterna (Gould, 1851) Larvae, Aquaculture 230, 417–423.
Hendriks, I.E., van Duren, L.A., and Herman, P.M.J. (2003) Effect of Dietary Polyunsaturated Fatty Acids on Reproductive Output and Larval Growth of Bivalves, J. Exp. Mar. Biol. Ecol. 296, 199–213.
Hégaret, H., Wikfors, G.H., Soudant, P., Delaporte, M., Alix, J.H., Smith, B.C., Dixon, M.S., Quere, C., Le Coz, J.R., and Paillard, C. (2004) Immunological Competence of Eastern Oysters, Crassostrea virginica, Fed Different Microalgal Diets and Challenged with a Temperature Elevation, Aquaculture 234, 541–560.
Delaporte, M. (2005) Modulation des paramètres hémocytaires par la nutrition chez l'huître creuse Crassostrea gigas. Implication dans les mortalités estivales. Ph.D. Thesis, University of Rennes 1, Rennes, France, 358 pp. (in French).
Delaporte, M., Soudant, P., Moal, J., Lambert, C., Quéré, C., Miner, P., Choquet, G., Paillard, C., and Samain, J.-F. (2003) Effect of a Mono-specific Algal Diet on Immune Functions in Two Bivalves Species Crassostrea gigas and Ruditapes philippinarum, J. Exp. Biol. 206, 3053–3064.
Séguineau, C., Soudant, P., Moal, J., Delaporte, M., Miner, P., Quéré, C., and Samain, J.-F. (2005) Techniques for Delivery of Arachidonic Acid to Pacific Oyster, Crassostrea gigas Spat, Lipids 40, 931–939.
Walne, P.R., and Mann, R. (1975) Growth and Biochemical Composition in Ostrea edulis and Crassostrea gigas, in Ninth European Marine Biology Symposium (Barnes, H., ed.), pp. 587–607.
Delaporte, M., Soudant, P., Soundant, P., Moal, J., Kraffe, E., Marty, Y., and Samain, J.F. (2005) Incorporation and Modification of Dietary Fatty Acids in Gill Polar Lipids by Two Bivalve Species Crassostrea gigas and Ruditapes philippinarum, Comp. Biochem. Physiol. 140A, 460–470.
Bligh, E.G., and Dyer, W.J. (1959) A Rapid Method of Total Lipid Extraction and Purification., Can. J. Biochem. Physiol. 37, 911–917.
Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., and Smith, F. (1956) Colorimetric Method for Determination of Sugars and Related Substances, Anal. Chem. 28, 350–356.
Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent., J. Biol. Chem. 193, 265–275.
Marty, Y., Delaunay, F., Moal, J., and Samain, J.F. (1992) Change in the Fatty Acid Composition of Pecten maximus (L.), J. Exp. Mar. Biol. Ecol. 163, 221–234.
Metcalfe, L.D., and Schmitz, A.A. (1961) The Rapid Preparation of Fatty Acid Esters for Gas Chromatographic Analysis. Anal. Chem. 33, 363–364.
Allen, W.V., and Conley, H. (1982) Transport of Lipids in the Blood of the Pacific Oyster, Crassostrea gigas (Thunberg), Comp. Biochem. Physiol. 71B, 201–207.
Auffret, M., and Oubella, R. (1995) Cytological and Cytometric Analysis of Bivalve Mollusc Hemocytes, in Techniques in Fish Immunology, Stolen, J.S., Fletcher, C., Smith, S.A., Zelikoff, J.T., Kaattari, S.L., Anderson, R.S., Soderhall, K., and Weeks-Perkins, B.A., eds., pp. 55–64, Fair Haven: SOS Publication.
Choquet, G., Soudant, P., Lambert, C., Nicolas, J.L., and Paillard, C. (2003) Reduction of Adhesion Properties on Ruditapes philippinarum Hemocytes Exposed to Vibrio tapetis, Dis. Aquat. Org. 57, 109–116.
Labreuche, Y., Soudant, P., Goncalves, M., Lambert, C., and Nicolas, J.L. (2006) In vitro Effects of Extracellular Products (ECPs) from the Pathogenic Vibrio aestuarianus Strain 01/32 on the Oyster Crassostrea gigas Cellular Immune Responses, Develop. Comp. Immunol. 30, 367–379.
Lambert, C., Soudant, P., Choquet, G., and Paillard, C. (2003) Measurement of Crassostrea gigas Hemocyte Oxidative Metabolism by Flow Cytometry. A Tool to Evaluate Pathogenic Vibrio Inhibiting Capacity, Fish Shellfish Immunol. 15, 225–240.
Berntsson, K.M., Jonsson, P.R., Wängberg, S.A., and Carlsson, A.S. (1997) Effects of Broodstock Diets on Fatty Acid Composition, Survival and Growth Rates in Larvae of the European Flat Oyster, Ostrea edulis, Aquaculture 154, 139–153.
Delaunay, F., Marty, Y., Moal, J., and Samain, J.F. (1992) Growth and Lipid Class Composition of Pecten maximus (L.) Larvae Grown Under Hatchery Conditions, J. Exp. Mar. Biol. Ecol. 163, 209–219.
Langdon, C.J., and Waldock, M.J. (1981) The Effect of Algal and Artificial Diets on the Growth and Fatty Acid Composition of Crassostrea gigas Spat, J. Mar. Biol. Assoc. U.K. 61, 431–448.
Fernandez-Reiriz, M.J., Labarta, U., Albentosa, M., and Perez-Camacho, A. (1998) Effect of Microalgal Diets and Commercial Wheatgerm Flours on the Lipid Profile of Ruditapes decussatus Spat, Comp. Biochem. Physiol. 124B, 369–377.
Fernandez-Reiriz, M.J., Labarta, U., Albentosa, M., and Perez-Camacho, A. (1999) Lipid Profile and Growth of the Clam Spat, Ruditapes decussatus (L), Fed with Microalgal Diets and Cornstarch, Comp. Biochem. Physiol. 124B, 309–318.
Soudant, P., Marty, Y., Moal, J., Robert, R., Quéré, C, Le Coz, J.R., and Samain, J.F. (1996) Effect of Food Fatty Acid and Sterol Quality on Pecten maximus Gonad Composition and Reproduction Process, Aquaculture 143, 361–378.
Soudant, P., Moal, J., Marty, Y., and Samain, J.F. (1997) Composition of Polar Lipid Classes in Male Gonads of Pecten maximus (L.). Effect of nutrition, J. Exp. Mar. Biol. Ecol. 215, 103–114.
Soudant, P., Van Ryckeghem, K., Marty, Y., Moal, J., Samain, J.F., and Sorgeloos, P. (1999) Comparison of the Lipid Class and Fatty Acid Composition Between a Reproductive Cycle in Nature and a Standard Hatchery Conditioning of the Pacific Oyster Crasostrea gigas, Comp. Biochem. Physiol. 123B, 209–222.
Bunde, T.A., and Fried, M. (1978) The Uptake of Dissolved Free Fatty Acids from Seawater by a Marine Filter Feeder, Crassostrea virginica, Comp Biochem. Physiol. 60A, 139–144.
Cheng, T.C., (1996) Hemocytes: Forms and Functions, in The Eastern Oyster Crassostrea virginica, Newell, R.I.E., Kennedy, V.S., and Eble, A.F., eds., pp. 299–329, Maryland Sea Grant College.
Chu, F.L.E. (2000) Defense Mechanisms of Marine Bivalves, in Recent Advances in Marine Biotechnology, Immunology and Pathology, Fingerman, M.N., and Nagabhushanam, R., eds., pp. 1–42, Enfield, NH, Plymouth, UK: Sciences Publishers.
Pipe, R.K. (1992) Generation of Reactive Oxygen Metabolites by the Haemocytes of the Mussel Mytilus edulis, Develop. Comp. Immunol. 16, 111–122.
Peres, C.M., Otton, R., and Curi, R. (2005) Modulation of Lymphocyte Proliferation by Macrophages and Macrophages Loaded with Arachidonic Acid, Cell Biochem. Funct. 23, 373–381.
Peters-Golden, M., C.C., Mancuso, P., and Cofrey, M.J. (2004) Leukotrienes: Underappreciated Mediators of Innate Immune Responses, J. Immunol. 173, 589–594.
Ruggeri, B.A., and Thoroughgood, C.A. (1985) The Identification of Several Prostaglandin Moieties in Crassostrea virginica and Mytilus edulis by Radioimmunoassay and High Performance Liquid Chromatography, Prostaglandins Leukotr. Med. 20, 69–77.
Saintsing, D.G., Hwang, D.H., and Dietz, T.H. (1983) Production of Prostaglandins E2 and F2 in the Freshwater Mussel Ligumia subrostrata: Relation to Sodium Transport, J. Pharm. Exp. Ther. 226, 455–461.
Osada, M., and Nomura, T. (1990) The Levels of Prostaglandins Associated with the Reproductive Cycle of the Scallop, Patinopecten yessoensis, Prostaglandins 40, 229–239.
Canesi, L., Scarpato, A., Betti, M., Ciacci, C., Pruzzo, C., and Gallo, G. (2002) Bacterial Killing by Mytilus Hemocyte Monolayers as a Model for Investigating the Signaling Pathways Involved in Mussel Immune Defence, Mar. Environ. Res. 54, 547–551.
Dean, P., Gadsden, J.C., Richards, E.H., Edwards, J.P., Keith Charnley, A., and Reynolds, S.E. (2002) Modulation by Eicosanoid Biosynthesis Inhibitors of Immune Responses by the Insect Manduca sexta to the Pathogenic Fungus Metarhizium anisopliae, J. Invertebr. Pathol. 79, 93–101.
Mandato, C.A., Diehl-Jones, W.L., Moore, S.J., and Downer, R.G.H. (1997) The Effects of Eicosanoid Biosynthesis IInhibitors on Prophenoloxidase Activation, Phagocytosis and Cell Spreading in Galleria mellonella, J. Insect. Physiol. 43, 1–8.
Stanley-Samuelson, D.W., and Pedibhotla, V.K. (1996) What Can We Learn from Prostaglandins and Related Eicosanoids in Insects?, Insect Biochem. Mol. Biol. 26, 223–234.
Stanley-Samuelson, D.W., Pedibhotla, V.K., Rana, R.L., Rahim, N.A.A., Hoback, W.W., and Miller, J.S. (1997) Eicosanoids Mediate Nodulation Responses to Bacterial Infections in Larvae of the Silkmoth, Bombyx mori, Comp. Biochem. Physiol. 118A, 83–100.
Lavine, M.D., and Strand, M.R. (2002) Insect Hemocytes and Their Role in Immunity, Insect Biochem. Mol. Biol. 32, 1295–1309.
Tunaz, H., Park, Y., Buyukguzel, K., Bedick, J.C., Aliza, A.R., and Stanley, D.W. (2003) Eicosanoids in Insect Immunity: Bacterial Infection Stimulates Hemocytic Phospholipase A2 Activity in Tobacco Hornworms, Arch. Insect Biochem. Physiol. 52, 1–6.
Brock, T.G., McNish, R.W., Mancuso, P., Coffey, M.J., and Peters-Golden, M. (2003) Prolonged Lipopolysaccharide Inhibits Leukotriene Synthesis in Peritoneal Macrophages: Mediation by Nitric Oxide and Prostaglandins, Prostaglandins and Other Lipid Mediators 71, 131–145.
Miller, J.S. (2005) Eicosanoids Influence in vitro Elongation of Plasmatocytes from the Tobacco Hornworm, Manduca sexta, Arch. Insect Biochem. Physiol. 59, 42–51.
Mazière, C., Conte, M.A., Degonville, J., Ali, D., and Mazière, J.C. (1999) Cellular Enrichment with Polyunsaturated Fatty Acids Induces an Oxidative Stress and Activates the Transcription Factors AP1 and NFkB, Biochem. Biophys. Res. Commun. 265, 116–122.
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Delaporte, M., Soudant, P., Moal, J. et al. Impact of 20∶4n−6 supplementation on the fatty acid composition and hemocyte parameters of the pacific oyster crassostrea gigas . Lipids 41, 567–576 (2006). https://doi.org/10.1007/s11745-006-5006-9
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DOI: https://doi.org/10.1007/s11745-006-5006-9