Lipid-lowering effect of molluscan (Katelysia opima) glycosaminoglycan (GAG) in hypercholesterolemic induced rats
-
Vijayabaskar Pandian
, Natarajan Aravindan
Abstract
Identifying pharmacologically safe lipid-lowering ‘deliverables’ could potentiate therapeutic outcome for diet-induced atherogenesis. Accordingly, we investigated the potential of molluscan (Katelysia opima) glycosaminoglycan (GAG) in modulating the early lipid changes in atherogenesis. Wistar rats were fed a diet with (n=24) or without (n=6) hypercholesterolemic atherogenic CCT (rat chow supplemented with 4% cholesterol, 1% cholic acid, and 0.5% thiouracil) for 17 days. CCT-fed rates were (i) treated with isolated molluscan GAG (40 mg/kg/day, s.c.) for 10 days after the introduction of CCT diet, (ii) cotreated with GAG (40 mg/kg/day, s.c.) for 17 days, or (iii) treated with heparin (200 units/kg/day, s.c.) for 10 days after the introduction of CCT. The increases induced by CCT diet in the plasma levels of cholesterol, triglycerides, high-density lipoprotein, very-low-density lipoprotein, and low-density lipoprotein were completely attenuated with GAG treatment. Consistently, alterations induced by CCT diet in the levels of plasma lecithin cholesterol acyltransferase and lipoprotein lipase activities were restored to baseline levels with GAG treatment. Coherently, histology revealed a decrease associated with GAG treatment in the CCT-diet-induced foam cells (in aorta), tubular damages (kidney), and lipid accumulations (liver). Together, these results suggest that GAG may exert antiatherogenesis potential by significantly attenuating lipid modulations derived by a high-fat diet. Further, the data imply that the GAG extracts may comprehensively prevent hypercholesterolemia-associated tissue damage and could thus serve as a therapeutic deliverable for hypercholesterolemia.
References
Barbara, M. (2005). The specificity of interactions between proteins and sulfated polysaccharides. Ann. Braz. Acad. Sci. 77, 651–664.10.1590/S0001-37652005000400007Search in Google Scholar
Bertani, T., Poggi, A., Pozzoni, R., Delaini, F., Sacchi, G., Thoua, Y., Mecca, G., Remuzzi, G., and Donati, M.B. (1982). Adriamycin-induced nephrotic syndrome in rats: sequence of pathologic events. Lab. Invest. 46, 16–23.Search in Google Scholar
Boobalan, R., Murugesan, S., and Gopal, S. (2012). Veratric acid ameliorates hyperlipidemia and oxidative stress in Wistar rats fed an atherogenic diet. Mol. Cell. Biochem. 366, 21–30.10.1007/s11010-012-1278-ySearch in Google Scholar
Burstein, M., Scholnick, H.R., and Morfin, R. (1970). Method for isolation of lipoproteins from human serum by precipitation with polyanions. J. Lipid Res. 11, 583–595.10.1016/S0022-2275(20)42943-8Search in Google Scholar
Carl, A.B. and Edward, R.A. (1999). Tietz Textbook of Clinical Chemistry, 3rd edition, (Philadelphia, PA: W.B. Saunders), pp. 579.Search in Google Scholar
Carlson, L.A. and Holmquist, L. (1985). Evidence for the presence in human plasma of lecithin-cholesterol acyltransferase activity (β-LCAT) specifically esterifying free cholesterol of combined pre-β- and β-lipoproteins: studies of fish eye patients and control subjects. Acta Med. Scand. 218, 197–205.10.1111/j.0954-6820.1985.tb08847.xSearch in Google Scholar
Christudas, S., Savarimuthu, I., and Chidambaram, K. (2012). Hypolipidemic activity of Symplocos cochinchinensis S. moore leaves in hyperlipidemic rats. J. Nat. Med. 66, 32–38.10.1007/s11418-011-0548-4Search in Google Scholar
Deepa, P.R. and Varalakshmi, P. (2003). The cytoprotective role of a low-molecular-weight heparin fragment studied in an experimental model of glomerulotoxicity. Eur. J. Pharmacol. 478, 199–205.10.1016/j.ejphar.2003.08.084Search in Google Scholar
Deepa, P.R. and Varalakshmi, P. (2004). Protective effects of certoparin sodium, a low molecular weight heparin derivative, in experimental atherosclerosis. Clin. Chim. Acta 339, 105–115.10.1016/j.cccn.2003.09.021Search in Google Scholar
Dietrich, C.P., Nader, H.B., de Paiva, J.F., Santose, E.A., Holme, K.R., and Perlin, A.S. (1989). Heparin in molluscs: chemical, enzymatic degradation and 13C and 1H NMR spectroscopical evidence for the maintenance of the structure through evolution. Int. J. Biol. Macromol. 11, 361–366.10.1016/0141-8130(89)90008-1Search in Google Scholar
Dominick, M. (2003). Aquaculture of three phyla of marine invertebrates to yield bioactive metabolites: process developments and economics. Biomol. Eng. 20, 441–458.10.1016/S1389-0344(03)00075-3Search in Google Scholar
Editorial. (1992). Antibodies to oxidized LDL in atherosclerosis. The Lancet 339, 899–900.10.1016/0140-6736(92)90933-TSearch in Google Scholar
Engelberg, H. (1984). Heparin and the atherosclerotic process. Pharmacol. Rev. 36, 91–110.Search in Google Scholar
Engelberg, H. (1988). Update on the relationship of heparin to atherosclerosis and its thrombotic complications. Semin. Thromb. Hemost. 14, 88–105.Search in Google Scholar
Engelberg, H. (1996). Actions of heparin in the atherosclerotic process. Pharmacol. Rev. 48, 327–352.Search in Google Scholar
Fielding, C.J., Shore, V.G., and Fielding, P.E. (1972). Lecithin: cholesterol acyltransferase: effects of substrate composition upon enzyme activity. Biochim. Biophys. Acta 270, 513–518.10.1016/0005-2760(72)90116-6Search in Google Scholar
Friedewalds, W.T., Levy, R.I., and Fredrickson, D.S. (1972). Estimation of the concentration of low-density lipoprotein cholesterol without the use of the preparative ultracentrifuge. Clin. Chem. 18, 499–502.10.1093/clinchem/18.6.499Search in Google Scholar
Glomset, J.A. (1968). The plasma lecithins: cholesterol acyltransferase reaction. J. Lipid Res. 9, 155–167.10.1016/S0022-2275(20)43114-1Search in Google Scholar
Grant, A.C., Linhardt, R.J., Fitzerald, G.L., Park, J.J., and Langer, R. (1984). Metachromatic activity of heparin and heparin fragments. Anal. Biochem. 137, 25–32.10.1016/0003-2697(84)90341-5Search in Google Scholar
Handley, D.A. (1988). Heparin and related molecules as future drugs in the control of atherosclerosis. Heparin and Related Polysaccharides, Conferences Documentation (London, United Kingdom: London Hilton on Park Lane), pp. 1–9.Search in Google Scholar
Hansson, G.K., Bondjers, G., and Nilsson, L.A. (1979). Plasma protein accumulation in injured endothelial cells. Immunofluorescent localization of IgG and fibrinogen in the rabbit aortic endothelium. Exp. Mol. Pathol. 30, 12–26.10.1016/0014-4800(79)90078-9Search in Google Scholar
Hitz, J., Steinmetz, J., and Siest, G. (1983). Lecithin: cholesterol acyltransferase reference values and effects of xenobiotics. Clin. Chim. Acta 133, 85–86.10.1016/0009-8981(83)90023-2Search in Google Scholar
Holick, M.F., Judkiewicz, A., Walworth, N., and Wang, M.H. (1985). Recovery of heparin from fish wastes. In: Biotechnology of Marine Polysaccharide, R.R. Cowell, E.R. Pariser, and A.J. Sinskey, eds. (New York, NY, USA: Hemisphere Publishing Corporation), pp. 389–397.Search in Google Scholar
Hongli, G., Zhaochun, L., Wenju, W., Xiaolan, Q., and Meihua, C. (2013). Aqueous extract of yerba mate tea lowers atherosclerotic risk factors in a rat hyperlipidemia model. Phytother. Res. 27, 1225–1231.10.1002/ptr.4856Search in Google Scholar
Jaques, L.B. (1987). Drug prophylaxis in atherosclerosis. Artery 14, 209–215.Search in Google Scholar
Johnson, E.A. and Mulloy, B. (1976). The molecular-weight range of mucosal heparin preparations. Carbohydr. Res. 51, 119–127.10.1016/S0008-6215(00)84041-0Search in Google Scholar
Kanchan, K. and Balbir, S. (2002). Cerebral Atherosclerosis an Autopsy Study. Current Advances in Atherosclerosis Research. Proceeding of XV Annual Conferences of the Indian Society for Atherosclerosis, Tirupati, India. 5. pp. 72–91.Search in Google Scholar
Leffler, H.H. and McDougald, C.H. (1963). Estimation of cholesterol in serum. Am. J. Clin. Pathol. 39, 311–315.10.1093/ajcp/39.3_ts.311Search in Google Scholar
Legraud, A., Guillansseav, R.J., and Land, J. (1979). Method of colorimetric simple determination del activit de la Lecithin: cholesterol acyltransferase (LCAT) plasma tique interest on diabetoeligic. In: Biologic. Prospectives. G, Siest and M.M. Glateau, eds. (Paris, France: Masson), pp. 368–371.Search in Google Scholar
Lenmann, R., Engler, H., Honegger, R., Riesen, W., and Spinas, G.A. (2001). Alterations of lipolytic enzymes and high-density lipoprotein subfractions induced by physical activity in type 2 diabetes mellitus. Eur. J. Clin. Invest. 31, 37–44.10.1046/j.1365-2362.2001.00752.xSearch in Google Scholar PubMed
Liu, H.H., Ko, W.C., and Hu, M.L. (2002). Hypolipidemic effect of glycosaminoglycans from the sea cucumber Metriatyla scabra in rats fed a cholesterol-supplemented diet. J. Agric. Food Chem. 50, 3602–3606.10.1021/jf020070kSearch in Google Scholar
Martha, F., Graciela, C., Luis, R., Juan, C.R., Aida, M., Claudia, H.G., Serafin, R., Luis, F.M., Carlos, P.R., and Oscar, P.M. (2003). Decreased activity of lecithin:cholesterol acyltransferase and hepatic lipase in chronic hypothyroid rats: implications for reverse cholesterol transport. Mol. Cell. Biochem. 246, 51–56.10.1023/A:1023451811547Search in Google Scholar
McComb, R.B. and Bowers, G.N. (1972). Study of optimum buffer conditions for measuring alkaline phosphatase activity in human serum. Clin. Chem. 18, 97–104.10.1093/clinchem/18.2.97Search in Google Scholar
Medeiros, G.F., Menden, A., Castro, R.A., Bau, E.C., Nader, H.B., and Dietrich, C.P. (2000). Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochim. Biophys. Acta 1475, 287–294.10.1016/S0304-4165(00)00079-9Search in Google Scholar
Mirhadi, S.A., Singh, S., and Gupta, P.P. (1991). Effect of garlic supplementation to cholesterol rich diet on development of atherosclerosis in rabbits. Indian J. Exp. Biol. 29, 162–168.Search in Google Scholar
Mohamad, W., Eman, G.G., Toshihiko, T., Lianli, C., and Robert, J.L. (2003). Isolation and characterization of raw heparin from dromedary intestine: evaluation of a new source of pharmaceutical heparin. Comp. Biochem. Physiol. Part C 136, 357–365.Search in Google Scholar
Naik, S.R. and Sheth, U.K. (1978). Studies on two new derivatives of N-aralkyl-o-ethoxybenzamides: part II – biochemical studies on their anti-inflammatory activity. Indian J. Exp. Biol. 16, 1175–1179.Search in Google Scholar
Nelson, R.M., Cecconi, O., Roberts, W.G., Aruffo, A., Linhardt, R.J., and Bevilacqua, M.P. (1993). Heparin oligosaccharides bind L- and P-selectin and inhibit acute inflammation. Blood 82, 3253–3258.10.1182/blood.V82.11.3253.3253Search in Google Scholar
Owen, J.K., Iggo, B., Scandrett, F.J., and Stemart, C.P. (1954). Determination of creatinine in plasma or serum and in urine. A critical examination. Biochem. J. 58, 426–437.Search in Google Scholar
Panneerselvam, V., Kannan, M., Jayaraja, S., and Vasanthi, N. (2013). Antihyperlipidemic activity of Cassia auriculata flowers in triton WR 1339 induced hyperlipidemic rats. Exp. Toxicol. Pathol. 65, 135–141.10.1016/j.etp.2011.07.001Search in Google Scholar
Penumathsa, S.V., Thirunavukkarasu, M., Koneru, S., Juhasz, B., Zhan, L., Pant, R., Menon, V.P., Otani, H., and Maulik, N. (2007). Statin and resveratrol in combination induces cardioprotective against myocardial infarction in hypercholesterolemic rat. J. Mol. Cell. Cardiol. 42, 508–516.10.1016/j.yjmcc.2006.10.018Search in Google Scholar
Peric-Golia, L. and Peric-Golia, M. (1983). Aortic and renal lesions in hypercholesterolemic adult, male, virgin Sprague-Dawley rats. Atherosclerosis 46, 57–65.10.1016/0021-9150(83)90164-8Search in Google Scholar
Persson, B., Bjorntorp, P., and Hood, B. (1966). Lipoprotein lipase activity in human adipose tissue. I. Conditions for release and relationship to triglycerides in serum. Metabolism 15, 730–741.10.1016/S0026-0495(66)80009-4Search in Google Scholar
Petitou, M., Casu, B., and Lindahl, U. (2003). 1976–1983, a critical period in the history of heparin: the discovery of the antithrombin binding site. Biochimie 85, 83–89.10.1016/S0300-9084(03)00078-6Search in Google Scholar
Ragazzi, E. and Chinellato, A. (1995). Heparin: pharmacological potentials from atherosclerosis to asthma. Gen. Pharmacol. 26, 697–701.10.1016/0306-3623(94)00170-RSearch in Google Scholar
Rajeevkumar, J. and Xu, Z.-R. (2004). Biomedical compounds from marine organisms. Mar. Drugs 2, 123–146.10.3390/md203123Search in Google Scholar
Rifai, N., Bachorik, P.S., and Albers, J.J. (1999). Lipids, lipoproteins, and apolipoproteins. In: Tietz Textbook of Clinical Chemistry, 3rd ed., C.A. Burtis and E.R. Ashwood, eds. (Philadelphia, PA, USA: WB Saunders Company), pp. 809–861.Search in Google Scholar
Rodkey, F.L. (1964). Autozyme albumin reagent set for determination of albumin in serum/plasma based on BCG method. Clin. Chem. 10, 606.10.1093/clinchem/10.7.606Search in Google Scholar
Ross, R. (1986). The pathogenesis of atherosclerosis – an update. N. Engl. J. Med. 314, 488–500.10.1056/NEJM198602203140806Search in Google Scholar
Ross, R. (1993). The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 362, 801–809.10.1038/362801a0Search in Google Scholar
Ross, R. (1999). Atherosclerosis – an inflammatory disease. N. Engl. J. Med. 340, 115–126.10.1056/NEJM199901143400207Search in Google Scholar
Sable-Amplis, R. and Sicart, R. (1983). Relationship between aorta cholesterol content and plasma lipids in guinea pigs fed an atherogenic diet. Atherosclerosis 48, 295–299.10.1016/0021-9150(83)90047-3Search in Google Scholar
Saravanan, R., Vairamani, S., and Shanmugam, A. (2010). Glycosaminoglycans from marine clam Meretrix meretrix (LINNE) are an anticoagulant. Prepar. Biochem. Biotechnol. 40, 305–315.10.1080/10826068.2010.488998Search in Google Scholar
Schrecker, O. and Greten, H. (1979). Activation and inhibition of lipoprotein lipase. Studies with artificial lipoproteins. Biochim. Biophys. Acta 572, 244–256.10.1016/0005-2760(79)90040-7Search in Google Scholar
Shim, J.Y., Lee, Y.S., Jung, S.H., Choi, H.S., Shin, K.H., and Kinm, Y.S. (2002). Pharmacological activities of a new glycosaminoglycan, acharan sulfate isolated from the giant African snail Achatina fulica. Arch. Pharm. Res. 25, 889–894.10.1007/BF02977010Search in Google Scholar PubMed
Shulman, A.G. (1990). Heparin and atherosclerosis an investigative report on the treatment of atherosclerosis. Biomed. Pharmacother. 44, 303–306.10.1016/0753-3322(90)90133-TSearch in Google Scholar
Siedel, J., Schlumberger, H., Klose, S., Ziegenhorn, J., and Wahlefeld, A.W. (1981). Improved reagent for enzymatic determination of serum cholesterol. J. Clin. Chem. Clin. Biochem. 19, 838–839.Search in Google Scholar
Silkworth, J.B., McLean, B., and Stehbens, W.E. (1975). The effect of hypercholesterolemia on aortic endothelium studied en face. Atherosclerosis 22, 335–348.10.1016/0021-9150(75)90015-5Search in Google Scholar
Somasundaram, S.T. and Vijayabaskar, P. (2007). Histological and analytical evaluation of glycosaminoglycan from the clam Katelysia opima. Trends Med. Res. 2, 167–175.10.3923/tmr.2007.167.175Search in Google Scholar
Somasundaram, S.T., Dey, A., Manavalan, R., and Subramanian, A. (1989). Heparin from some bivalve mollusks. Curr. Sci. 58, 264.Search in Google Scholar
Sparks, J.D., Sparks, C.E., and Kritchevsky, D. (1986). Hypercholesterolemia and aortic glycosaminoglycans of rabbits fed semi-purified diets containing sucrose and lactose. Atherosclerosis 60, 183–196.10.1016/0021-9150(86)90010-9Search in Google Scholar
Stemerman, M.B. (1981). Effects of moderate hypercholesterolemia on rabbit endothelium. Arteriosclerosis 1, 25–32.10.1161/01.ATV.1.1.25Search in Google Scholar
Trinder, P. (1969). Determination of glucose in blood using glucose oxidase with an alternative oxygen acceptor. Ann. Clin. Biochem. 6, 24–27.10.1177/000456326900600108Search in Google Scholar
Vijayabaskar, P. and Somasundaram, S.T. (2012). Studies on molluscan glycosaminoglycans (GAG) from backwater clam Donax cuneatus (Linnaeus). Asian Pac. J. Trop. Biomed. 2, S519–S525.10.1016/S2221-1691(12)60265-2Search in Google Scholar
Vijayabaskar, P., Balasubramanian, T., and Somasundaram, S.T. (2008a). Low-molecular weight molluscan glycosaminoglycan from bivalve Katelysia opima (Gmelin). Methods Find Exp. Clin. Pharmacol. 30, 1–6.10.1358/mf.2008.30.3.1159654Search in Google Scholar PubMed
Vijayabaskar, P., Sethupathy, S., and Somasundaram, S.T. (2008b). A comparative study on the atheroprotective potential of heparin and atorvastatin in hypercholesterolemic rats. Afr. J. Biochem. Res. 2, 120–127.Search in Google Scholar
Webster, D. (1977). Autozyme urea reagent set for determination of urea/blood urea nitrogen based on enzymatic method using urease. Clin. Chem. 23, 663.10.1093/clinchem/23.4.663Search in Google Scholar
©2014 by Walter de Gruyter Berlin Boston
Articles in the same Issue
- Masthead
- Masthead
- Guest Editorial
- Highlight issue: membranes in motion
- HIGHLIGHT: MOSBACH COLLOQUIUM 2013 ‘MEMBRANES IN MOTION’
- Remodeling of membrane compartments: some consequences of membrane fluidity
- Reshaping biological membranes in endocytosis: crossing the configurational space of membrane-protein interactions
- Novel intracellular functions of apolipoproteins: the ApoO protein family as constituents of the Mitofilin/MINOS complex determines cristae morphology in mitochondria
- Membranes in motion: mitochondrial dynamics and their role in apoptosis
- Crosstalk of lipid and protein homeostasis to maintain membrane function
- Endocytic Rabs in membrane trafficking and signaling
- Review
- Plasmacytoid dendritic cells and autoimmune inflammation
- Research Articles/Short Communications
- Protein Structure and Function
- Molecular interactions of hemoglobin with resveratrol: potential protective antioxidant role and metabolic adaptations of the erythrocyte
- Membranes, Lipids, Glycobiology
- Lipid-lowering effect of molluscan (Katelysia opima) glycosaminoglycan (GAG) in hypercholesterolemic induced rats
Articles in the same Issue
- Masthead
- Masthead
- Guest Editorial
- Highlight issue: membranes in motion
- HIGHLIGHT: MOSBACH COLLOQUIUM 2013 ‘MEMBRANES IN MOTION’
- Remodeling of membrane compartments: some consequences of membrane fluidity
- Reshaping biological membranes in endocytosis: crossing the configurational space of membrane-protein interactions
- Novel intracellular functions of apolipoproteins: the ApoO protein family as constituents of the Mitofilin/MINOS complex determines cristae morphology in mitochondria
- Membranes in motion: mitochondrial dynamics and their role in apoptosis
- Crosstalk of lipid and protein homeostasis to maintain membrane function
- Endocytic Rabs in membrane trafficking and signaling
- Review
- Plasmacytoid dendritic cells and autoimmune inflammation
- Research Articles/Short Communications
- Protein Structure and Function
- Molecular interactions of hemoglobin with resveratrol: potential protective antioxidant role and metabolic adaptations of the erythrocyte
- Membranes, Lipids, Glycobiology
- Lipid-lowering effect of molluscan (Katelysia opima) glycosaminoglycan (GAG) in hypercholesterolemic induced rats