Antithrombotic and Antiatherosclerotic Properties of  Olive Oil and Olive Pomace Polar Extracts in Rabbits

Tsantila, Nektaria; Karantonis, Haralabos C.; Perrea, Despina N.; Theocharis, Stamatios E.; Iliopoulos, Dimitrios G.; Antonopoulou, Smaragdi; Demopoulos, Constantinos A.

doi:https://doi.org/10.1155/2007/36204

Mediators of Inflammation

On this page

Abstract References Copyright Related Articles

Research Article | Open Access

Volume 2007 | Article ID 036204 | https://doi.org/10.1155/2007/36204

Antithrombotic and Antiatherosclerotic Properties of Olive Oil and Olive Pomace Polar Extracts in Rabbits

Nektaria Tsantila,¹Haralabos C. Karantonis,²Despina N. Perrea,³Stamatios E. Theocharis,⁴Dimitrios G. Iliopoulos,³Smaragdi Antonopoulou,²and Constantinos A. Demopoulos¹

Received30 Jan 2007

Revised12 Apr 2007

Accepted06 May 2007

Published24 Jul 2007

Abstract

Olive oil polar lipid (OOPL) extract has been reported to inhibit atherosclerosis development on rabbits. Olive pomace polar lipid (PPL) extract inhibits PAF activity in vitro and the most potent antagonist has been identified as a glycerylether-sn-2-acetyl glycolipid with common structural characteristics with the respective potent antagonist of OOPL. The aim of this study was to investigate the effect of PPL on early atherosclerosis development on rabbits and to compare it with the antiatherosclerotic effect of OOPL. OOPL and PPL inhibition potency, towards both PAF action and PAF binding, was tested in vitro on washed rabbit platelets. Consequently, rabbits were divided into three groups (A, B, and C). All groups were fed atherogenic diet for 22 days. Atherogenic diets in groups B and C were enriched with OOPL and PPL, respectively. At the end of the experimental time, rabbits were euthanized and aortic samples were examined histopathologically. OOPL and PPL inhibited PAF-induced aggregation, as well as specific PAF binding, with PPL being more potent. Free and bound PAF levels and PAF-AH activity were significantly elevated at the end of the experimental time. Plasma total cholesterol, HDL cholesterol, LDL cholesterol, and triglycerides levels were also found increased. Groups B and C exhibited significantly increased values of EC50 compared to group A. Histopathological examination revealed that the development of early atherosclerosis lesions in groups B and C were significantly inhibited compared to group A. Significant differences were noted in the early atherosclerosis lesions between groups B and C, thus indicating that PPL exhibit its anti-atherosclerotic activity by blocking PAF receptor. Specific PAF antagonists with similar in vitro and in vivo bioactivity to those that have been previously reported in OOPL exist in PPL.

References

J. F. Keaney Jr., “Atherosclerosis: from lesion formation to plaque activation and endothelial dysfunction,” Molecular Aspects of Medicine, vol. 21, no. 4-5, pp. 99–166, 2000.
View at: Publisher Site | Google Scholar
C. A. Demopoulos, H. C. Karantonis, and S. Antonopoulou, “Platelet activating factor—a molecular link between atherosclerosis theories,” European Journal of Lipid Science and Technology, vol. 105, no. 11, pp. 705–716, 2003.
View at: Publisher Site | Google Scholar
M. de Lorgeril, P. Salen, F. Paillard, F. Laporte, F. Boucher, and J. de Leiris, “Mediterranean diet and the French paradox: two distinct biogeographic concepts for one consolidated scientific theory on the role of nutrition in coronary heart disease,” Cardiovascular Research, vol. 54, no. 3, pp. 503–515, 2002.
View at: Publisher Site | Google Scholar
H. C. Karantonis, S. Antonopoulou, and C. A. Demopoulos, “Antithrombotic lipid minor constituents from vegetable oils. Comparison between olive oils and others,” Journal of Agricultural and Food Chemistry, vol. 50, no. 5, pp. 1150–1160, 2002.
View at: Publisher Site | Google Scholar
M. González-Santiago, E. Martín-Bautista, J. J. Carrero et al., “One-month administration of hydroxytyrosol, a phenolic antioxidant present in olive oil, to hyperlipemic rabbits improves blood lipid profile, antioxidant status and reduces atherosclerosis development,” Atherosclerosis, vol. 188, no. 1, pp. 35–42, 2006.
View at: Publisher Site | Google Scholar
R. P. Mensink and M. B. Katan, “An epidemiological and an experimental study on the effect of olive oil on total serum and HDL cholesterol in healthy volunteers,” European Journal of Clinical Nutrition, vol. 43, Supplement 2, pp. 43–48, 1989.
View at: Google Scholar
J. P. de La Cruz, M. A. Villalobos, J. A. Carmona, M. Martín-Romero, J. M. Smith-Agreda, and F. S. de la Cuesta, “Antithrombotic potential of olive oil administration in rabbits with elevated cholesterol,” Thrombosis Research, vol. 100, no. 4, pp. 305–315, 2000.
View at: Publisher Site | Google Scholar
S. M. Cardoso, A. M. S. Silva, and M. A. Coimbra, “Structural characterisation of the olive pomace pectic polysaccharide arabinan side chains,” Carbohydrate Research, vol. 337, no. 10, pp. 917–924, 2002.
View at: Publisher Site | Google Scholar
G. Brunetti, C. Plaza, and N. Senesi, “Olive pomace amendment in Mediterranean conditions: effect on soil and humic acid properties and wheat (Triticum turgidum L.) yield,” Journal of Agricultural and Food Chemistry, vol. 53, no. 17, pp. 6730–6737, 2005.
View at: Publisher Site | Google Scholar
A. Saviozzi, R. Levi-Minzi, R. Cardelli, A. Biasci, and R. Riffaldi, “Suitability of moist olive pomace as soil amendment,” Water, Air, and Soil Pollution, vol. 128, no. 1-2, pp. 13–22, 2001.
View at: Publisher Site | Google Scholar
R. Borja, A. Martín, B. Rincón, and F. Raposo, “Kinetics for substrate utilization and methane production during the mesophilic anaerobic digestion of two phases olive pomace (TPOP),” Journal of Agricultural and Food Chemistry, vol. 51, no. 11, pp. 3390–3395, 2003.
View at: Publisher Site | Google Scholar
B. Muik, B. Lendl, A. Molina-Díaz, L. Pérez-Villarejo, and M. J. Ayora-Cañada, “Determination of oil and water content in olive pomace using near infrared and Raman spectrometry. A comparative study,” Analytical & Bioanalytical Chemistry, vol. 379, no. 1, pp. 35–41, 2004.
View at: Publisher Site | Google Scholar
M. Brenes, C. Romero, A. García, F. J. Hidalgo, and M. V. Ruiz-Méndez, “Phenolic compounds in olive oils intended for refining: formation of 4-ethylphenol during olive paste storage,” Journal of Agricultural and Food Chemistry, vol. 52, no. 26, pp. 8177–8181, 2004.
View at: Publisher Site | Google Scholar
M. S. Haddadin, S. M. Abdulrahim, G. Y. Al-Khawaldeh, and R. K. Robinson, “Solid state fermentation of waste pomace from olive processing,” Journal of Chemical Technology and Biotechnology, vol. 74, no. 7, pp. 613–618, 1999.
View at: Publisher Site | Google Scholar
E. Ninio, “Phospholipid mediators in the wall: involvement in atherosclerosis,” Current Opinion in Clinical Nutrition and Metabolic Care, vol. 8, no. 2, pp. 123–131, 2005.
View at: Publisher Site | Google Scholar
D. M. Stafforini, T. M. McIntyre, G. A. Zimmerman, and S. M. Prescott, “Platelet-activating factor, a pleiotrophic mediator of physiological and pathological processes,” Critical Reviews in Clinical Laboratory Sciences, vol. 40, no. 6, pp. 643–672, 2003.
View at: Google Scholar
A. M. Evangelou, “Platelet-activating factor (PAF): implications for coronary heart and vascular diseases,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 50, no. 1, pp. 1–28, 1994.
View at: Publisher Site | Google Scholar
R. Quarck, B. de Geest, D. Stengel et al., “Adenovirus-mediated gene transfer of human platelet-activating factor-acetylhydrolase prevents injury-induced neointima formation and reduces spontaneous atherosclerosis in apolipoprotein E-deficient mice,” Circulation, vol. 103, no. 20, pp. 2495–2500, 2001.
View at: Google Scholar
S. Antonopoulou, C. E. Semidalas, S. Koussissis, and C. A. Demopoulos, “Platelet-activating factor (PAF) antagonists in foods: a study of lipids with PAF or anti-PAF-like activity in cow's milk and yogurt,” Journal of Agricultural and Food Chemistry, vol. 44, no. 10, pp. 3047–3051, 1996.
View at: Publisher Site | Google Scholar
S. Koussissis, C. E. Semidalas, E. C. Hadzistavrou, V. G. Kalyvas, S. Antonopouloy, and C. A. Demopoulos, “PAF antagonists in foods: isolation and identification of PAF in honey and wax,” Revue Française des Corps Gras, vol. 41, no. 5-6, pp. 127–132, 1994.
View at: Google Scholar
E. Fragopoulou, T. Nomikos, S. Antonopoulou, C. A. Mitsopoulou, and C. A. Demopoulos, “Separation of biologically active lipids from red wine,” Journal of Agricultural and Food Chemistry, vol. 48, no. 4, pp. 1234–1238, 2000.
View at: Publisher Site | Google Scholar
E. Fragopoulou, T. Nomikos, N. Tsantila, A. Mitropoulou, I. Zabetakis, and C. A. Demopoulos, “Biological activity of total lipids from red and white wine/must,” Journal of Agricultural and Food Chemistry, vol. 49, no. 11, pp. 5186–5193, 2001.
View at: Publisher Site | Google Scholar
E. Fragopoulou, S. Antonopoulou, and C. A. Demopoulos, “Biologically active lipids with antiatherogenic properties from white wine and must,” Journal of Agricultural and Food Chemistry, vol. 50, no. 9, pp. 2684–2694, 2002.
View at: Publisher Site | Google Scholar
A. Panayiotou, D. Samartzis, T. Nomikos et al., “Lipid fractions with aggregatory and antiaggregatory activity toward platelets in fresh and fried cod (Gadus morhua): correlation with platelet-activating factor and atherogenesis,” Journal of Agricultural and Food Chemistry, vol. 48, no. 12, pp. 6372–6379, 2000.
View at: Publisher Site | Google Scholar
J. Rementzis, S. Antonopoulou, D. Argyropoulos, and C. A. Demopoulos, “Biologically active lipids from S. scombrus,” Advances in Experimental Medicine and Biology, vol. 416, pp. 65–72, 1997.
View at: Google Scholar
S. Koussissis, C. E. Semidalas, S. Antonopoulou, V. Kapoulas, C. A. Demopoulos, and V. G. Kalyvas, “PAF antagonists in foods: isolation and identification of PAF in virgin olive oil,” Revue Française des Corps Gras, vol. 40, no. 9-10, pp. 323–327, 1993.
View at: Google Scholar
H. C. Karantonis, S. Antonopoulou, D. N. Perrea et al., “In vivo antiatherogenic properties of olive oil and its constituent lipid classes in hyperlipidemic rabbits,” Nutrition, Metabolism & Cardiovascular Diseases, vol. 16, no. 3, pp. 174–185, 2006.
View at: Publisher Site | Google Scholar
H. C. Karantonis, N. Tsantila, G. Stamatakis et al., “Bioactive polar lipids in olive oil, pomace and waste by products,” to appear in Journal of Food Biochemistry.
View at: Google Scholar
H. C. Karantonis, I. Zabetakis, T. Nomikos, and C. A. Demopoulos, “Antiatherogenic properties of lipid minor constituents from seed oils,” Journal of the Science of Food and Agriculture, vol. 83, no. 12, pp. 1192–1204, 2003.
View at: Publisher Site | Google Scholar
C. A. Demopoulos, R. N. Pinckard, and D. J. Hanahan, “Platelet-activating factor. Evidence for 1- $O$ -alkyl-2-acetyl-sn-glyceryl-3-phosphorylcholine as the active component (a new class of lipid chemical mediators),” The Journal of Biological Chemistry, vol. 254, no. 19, pp. 9355–9358, 1979.
View at: Google Scholar
S. Antonopoulou, C. A. Demopoulos, and C. Iatrou, “Blood cardiolipin in haemodialysis patients. Its implication in the biological action of platelet-activating factor,” International Journal of Biochemistry and Cell Biology, vol. 28, no. 1, pp. 43–51, 1996.
View at: Publisher Site | Google Scholar
G. R. Bartlett, “Phosphorus assay in column chromatography,” The Journal of Biological Chemistry, vol. 234, no. 3, pp. 466–468, 1959.
View at: Google Scholar
D. S. Galanos and V. M. Kapoulas, “Preparation and analysis of lipid extracts from milk and other tissues,” Biochimica et Biophysica Acta, vol. 98, no. 5, pp. 278–292, 1965.
View at: Google Scholar
V. L. Singleton and J. A. Rossi Jr., “Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents,” American Journal of Enology and Viticulture, vol. 16, no. 3, pp. 144–158, 1965.
View at: Google Scholar
O. A. Renkonen, “A note on spectrophotometric determination of acyl ester groups in lipids,” Biochimica et Biophysica Acta, vol. 54, no. 2, pp. 361–362, 1961.
View at: Publisher Site | Google Scholar
C. Alasalvar, K. D. A. Taylor, E. Zubcov, F. Shahidi, and M. Alexis, “Differentiation of cultured and wild sea bass (Dicentrarchus labrax): total lipid content, fatty acid and trace mineral composition,” Food Chemistry, vol. 79, no. 2, pp. 145–150, 2002.
View at: Publisher Site | Google Scholar
R. N. Pinckard and J. C. Ludwig, “Determination of PAF-2-acetylhydrolase activity,” Federation Proceedings, vol. 45, p. 856, 1986.
View at: Google Scholar
C. A. Demopoulos, N. K. Andrikopoulos, and S. Antonopoulou, “A simple and precise method for the routine determination of platelet-activating factor in blood and urine,” Lipids, vol. 29, no. 4, pp. 305–309, 1994.
View at: Publisher Site | Google Scholar
E. G. Bligh and W. J. Dyer, “A rapid method of total lipid extraction and purification,” Canadian Journal of Biochemistry and Physiology, vol. 37, no. 8, pp. 911–917, 1959.
View at: Google Scholar
N. K. Andrikopoulos, C. A. Demopoulos, and A. Siafaka-Kapadai, “High-performance liquid chromatographic analysis of platelet activating factor on a cation-exchange column by direct ultraviolet detection,” Journal of Chromatography A, vol. 363, no. 2, pp. 412–417, 1986.
View at: Publisher Site | Google Scholar
C. Aguilera, M. C. Ramírez-Tortosa, M. D. Mesa, C. L. Ramírez-Tortosa, and A. Gil, “Sunflower, virgin-olive and fish oils differentially affect the progression of aortic lesions in rabbits with experimental atherosclerosis,” Atherosclerosis, vol. 162, no. 2, pp. 335–344, 2002.
View at: Publisher Site | Google Scholar
C. M. Aguilera, M. D. Mesa, M. C. Ramírez-Tortosa, J. L. Quiles, and A. Gil, “Virgin olive and fish oils enhance the hepatic antioxidant defence system in atherosclerotic rabbits,” Clinical Nutrition, vol. 22, no. 4, pp. 379–384, 2003.
View at: Publisher Site | Google Scholar
R. Feliste, B. Perret, P. Braquet, and H. Chap, “Protective effect of BN 52021, a specific antagonist of platelet-activating factor (PAF-acether) against diet-induced cholesteryl ester deposition in rabbit aorta,” Atherosclerosis, vol. 78, no. 2-3, pp. 151–158, 1989.
View at: Publisher Site | Google Scholar
J. S. Perona, C. Arcemis, V. Ruiz-Gutierrez, and A. Catalá, “Effect of dietary high-oleic-acid oils that are rich in antioxidants on microsomal lipid peroxidation in rats,” Journal of Agricultural and Food Chemistry, vol. 53, no. 3, pp. 730–735, 2005.
View at: Publisher Site | Google Scholar
E. Ignatowicz and W. Baer-Dubowska, “Resveratrol, a natural chemopreventive agent against degenerative diseases,” Polish Journal of Pharmacology, vol. 53, no. 6, pp. 557–569, 2001.
View at: Google Scholar
E. Jouvin-Marche, E. Ninio, G. Beaurain, M. Tence, P. Niaudet, and J. Benveniste, “Biosynthesis of Paf-acether (platelet-activating factor). VII. Precursors of Paf-acether and acetyl-transferase activity in human leukocytes,” Journal of Immunology, vol. 133, no. 2, pp. 892–898, 1984.
View at: Google Scholar
C. Dentan, P. Lesnik, M. J. Chapman, and E. Ninio, “Phagocytic activation induces formation of platelet-activating factor in human monocyte-derived macrophages and in macrophage-derived foam cells-relevance to the inflammatory reaction in atherogenesis,” European Journal of Biochemistry, vol. 236, no. 1, pp. 48–55, 1996.
View at: Google Scholar
A. D. Tselepis and M. J. Chapman, “Inflammation, bioactive lipids and atherosclerosis: potential roles of a lipoprotein-associated phospholipase A2, platelet activating factor-acetylhydrolase,” Atherosclerosis Supplements, vol. 3, no. 4, pp. 57–68, 2002.
View at: Publisher Site | Google Scholar
L. W. Tjoelker and D. M. Stafforini, “Platelet-activating factor acetylhydrolases in health and disease,” Biochimica et Biophysica Acta, vol. 1488, no. 1-2, pp. 102–123, 2000.
View at: Publisher Site | Google Scholar
S. Blankenberg, D. Stengel, H. J. Rupprecht et al., “Plasma PAF-acetylhydrolase in patients with coronary artery disease: results of a cross-sectional analysis,” Journal of Lipid Research, vol. 44, no. 7, pp. 1381–1386, 2003.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2007 Nektaria Tsantila et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

435

Downloads

1142

Citations