The Effect of Eicosapentaenoic Acid on the Serum Levels and Enzymatic Activity of Paraoxonase 1 in the Patients With Type 2 Diabetes Mellitus
-
Mohammad Hassan Golzari
,
Saeed Hosseini
,
Fariba Koohdani
,
Ali-Akbar Saboor Yaraghi
,
Mohammad Hassan Javanbakht
,
Niyaz Mohammadzadeh-Honarvar
,
Mahmoud Djalali
Abstract
Paraoxonase 1 is known as one of the most important ant oxidative enzymes associated with HDL-c, and because of its antioxidant and antiinflammatory activities. EPA has the antioxidant, anti inflammatory, antithrombogenic, and antiarteriosclerotic properties. Therefore, we investigated the effect of EPA supplementation on the serum levels and activity of PON1 in type 2 diabetic patients. This study was designed as a randomized, double-blind, and placebo-controlled clinical trial. Thirty-six patients with type 2 diabetes were given written; informed consent randomly was classified into 2 groups. They were supplemented with 2 g/day of the capsules of EPA or placebo for eight weeks. Blood sample was given for measurement of the serum levels of lipids, the activity of PON1, FBS and HbA1c. The patients supplemented with EPA showed a significant increase in the serum levels and activity of PON1 and the serum ratio of PON1/HDL-c. There were no significant differences between the two groups regarding any demographic, clinical or biochemical data, total energy intake, and macronutrient intake at the baseline during the intervention, except for a significant increase of protein intake and the levels of HbA1c in the placebo group, and a significant increase of HDL-c, as well as a slight reduction of total cholesterol, LDL-c, TG and FBS in the supplement group. EPA is atheroprotective via increase in the serum levels and activity of PON1, as well as change in the serum levels of lipids, FBS and HbA1c.
Adeghate, E., P. Schattner, and E. Dunn, An update on the etiology and epidemiology of diabetes mellitus. Ann N Y Acad Sci, 2006. 1084: p. 1-29.
Freeman, J.S., The increasing epidemiology of diabetes and review of current treatment algorithms. J Am Osteopath Assoc, 2010. 110(7 Suppl 7): p. eS2-6.
Wild, S., et al., Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care, 2004. 27(5): p. 1047-53.
King, H., R.E. Aubert, and W.H. Herman, Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care, 1998. 21(9): p. 1414-31.
Shaw, J.E., R.A. Sicree, and P.Z. Zimmet, Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract, 2010. 87(1): p. 4-14.
Hossain, P., B. Kawar, and M. El Nahas, Obesity and diabetes in the developing world--a growing challenge. N Engl J Med, 2007. 356(3): p. 213-5.
Esteghamati, A., et al., Prevalence of diabetes and impaired fasting glucose in the adult population of Iran: National Survey of Risk Factors for Non-Communicable Diseases of Iran. Diabetes Care, 2008. 31(1): p. 96-8.
Davies, H.G., et al., The effect of the human serum paraoxonase polymorphism is reversed with diazoxon, soman and sarin. Nat Genet, 1996. 14(3): p. 334-6.
Costa, L.G., et al., Measurement of paraoxonase (PON1) status as a potential biomarker of susceptibility to organophosphate toxicity. Clin Chim Acta, 2005. 352(1-2): p. 37-47.
Cole, T.B., et al., Toxicity of chlorpyrifos and chlorpyrifos oxon in a transgenic mouse model of the human paraoxonase (PON1) Q192R polymorphism. Pharmacogenet Genomics, 2005. 15(8): p. 589-98.
Teiber, J.F., et al., Estrogen esters as substrates for human paraoxonases. Arch Biochem Biophys, 2007. 461(1): p. 24-9.
Teiber, J.F., D.I. Draganov, and B.N. La Du, Lactonase and lactonizing activities of human serum paraoxonase (PON1) and rabbit serum PON3. Biochem Pharmacol, 2003. 66(6): p. 887-96.
Draganov, D.I. and B.N. La Du, Pharmacogenetics of paraoxonases: a brief review. Naunyn Schmiedebergs Arch Pharmacol, 2004. 369(1): p. 78-88.
Biggadike, K., et al., Selective plasma hydrolysis of glucocorticoid gamma-lactones and cyclic carbonates by the enzyme paraoxonase: an ideal plasma inactivation mechanism. J Med Chem, 2000. 43(1): p. 19-21.
Mackness, B., et al., Paraoxonase-1 inhibits oxidised LDL-induced MCP-1 production by endothelial cells. Biochem Biophys Res Commun, 2004. 318(3): p. 680-3.
Ozer, E.A., et al., Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorum-sensing. FEMS Microbiol Lett, 2005. 253(1): p. 29-37.
Durrington, P.N., B. Mackness, and M.I. Mackness, Paraoxonase and atherosclerosis. Arterioscler Thromb Vasc Biol, 2001. 21(4): p. 473-80.
Aviram, M. and M. Rosenblat, Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development. Free Radic Biol Med, 2004. 37(9): p. 1304-16.
Hagiwara, S., et al., Eicosapentaenoic acid ameliorates diabetic nephropathy of type 2 diabetic KKAy/Ta mice: involvement of MCP-1 suppression and decreased ERK1/2 and p38 phosphorylation. Nephrol Dial Transplant, 2006. 21(3): p. 605-15.
Kesavulu, M.M., et al., Effect of omega-3 fatty acids on lipid peroxidation and antioxidant enzyme status in type 2 diabetic patients. Diabetes Metab, 2002. 28(1): p. 20-6.
Figueras, M., et al., Effects of eicosapentaenoic acid (EPA) treatment on insulin sensitivity in an animal model of diabetes: improvement of the inflammatory status. Obesity (Silver Spring), 2011. 19(2): p. 362-9.
Terano, T., et al., Effect of oral administration of highly purified eicosapentaenoic acid on platelet function, blood viscosity and red cell deformability in healthy human subjects. Atherosclerosis, 1983. 46(3): p. 321-31.
Nomura, S., S. Kanazawa, and S. Fukuhara, Effects of eicosapentaenoic acid on platelet activation markers and cell adhesion molecules in hyperlipidemic patients with Type 2 diabetes mellitus. J Diabetes Complications, 2003. 17(3): p. 153-9.
Association, A.D., Clinical practice recommendations. Diabetes Care 2010. 33: p. S1-S100.
Alberti, K.G., P. Zimmet, and J. Shaw, International Diabetes Federation: a consensus on Type 2 diabetes prevention. Diabet Med, 2007. 24(5): p. 451-63.
Lakshman, M.R., et al., Inverse correlation of serum paraoxonase and homocysteine thiolactonase activities and antioxidant capacity of high-density lipoprotein with the severity of cardiovascular disease in persons with type 2 diabetes mellitus. Metabolism, 2006. 55(9): p. 1201-6.
Stark, K.D., et al., Effect of a fish-oil concentrate on serum lipids in postmenopausal women receiving and not receiving hormone replacement therapy in a placebo-controlled, double-blind trial. Am J Clin Nutr, 2000. 72(2): p. 389-94.
Fedor, D. and D.S. Kelley, Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care, 2009. 12(2): p. 138-46.
Mustad, V.A., et al., Differential effects of n-3 polyunsaturated fatty acids on metabolic control and vascular reactivity in the type 2 diabetic ob/ob mouse. Metabolism, 2006. 55(10): p. 1365-74.
Suzukawa, M., et al., Effects of fish oil fatty acids on low density lipoprotein size, oxidizability, and uptake by macrophages. J Lipid Res, 1995. 36(3): p. 473-84.
McVeigh, G.E., et al., Dietary fish oil augments nitric oxide production or release in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia, 1993. 36(1): p. 33-8.
Kobayashi, S., et al., Reduction in blood viscosity by eicosapentaenoic acid. Lancet, 1981. 2(8239): p. 197.
Miyajima, T., et al., Effects of eicosapentaenoic acid on blood pressure, cell membrane fatty acids, and intracellular sodium concentration in essential hypertension. Hypertens Res, 2001. 24(5): p. 537-42.
Verlengia, R., et al., Comparative effects of eicosapentaenoic acid and docosahexaenoic acid on proliferation, cytokine production, and pleiotropic gene expression in Jurkat cells. J Nutr Biochem, 2004. 15(11): p. 657-65.
Martin, R.E., Docosahexaenoic acid decreases phospholipase A2 activity in the neurites/nerve growth cones of PC12 cells. J Neurosci Res, 1998. 54(6): p. 805-13.
Serhan, C.N., et al., Anti-microinflammatory lipid signals generated from dietary N-3 fatty acids via cyclooxygenase-2 and transcellular processing: a novel mechanism for NSAID and N-3 PUFA therapeutic actions. J Physiol Pharmacol, 2000. 51(4 Pt 1): p. 643-54.
Serhan, C.N., et al., Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med, 2002. 196(8): p. 1025-37.
Kim, D.N., J. Schmee, and W.A. Thomas, Dietary fish oil added to a hyperlipidemic diet for swine results in reduction in the excessive number of monocytes attached to arterial endothelium. Atherosclerosis, 1990. 81(3): p. 209-16.
Rozenberg, O., D.M. Shih, and M. Aviram, Paraoxonase 1 (PON1) attenuates macrophage oxidative status: studies in PON1 transfected cells and in PON1 transgenic mice. Atherosclerosis, 2005. 181(1): p. 9-18.
Ng, C.J., et al., The paraoxonase gene family and atherosclerosis. Free Radic Biol Med, 2005. 38(2): p. 153-63.
Mackness, B., et al., High C-reactive protein and low paraoxonase1 in diabetes as risk factors for coronary heart disease. Atherosclerosis, 2006. 186(2): p. 396-401.
Precourt, L.P., et al., The three-gene paraoxonase family: physiologic roles, actions and regulation. Atherosclerosis, 2011. 214(1): p. 20-36.
Ng, D.S., et al., Paraoxonase-1 deficiency in mice predisposes to vascular inflammation, oxidative stress, and thrombogenicity in the absence of hyperlipidemia. Cardiovasc Pathol, 2008. 17(4): p. 226-32.
Aviram, M., et al., Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. J Clin Invest, 1998. 101(8): p. 1581-90.
Mackness, M.I., et al., Protection of low-density lipoprotein against oxidative modification by high-density lipoprotein associated paraoxonase. Atherosclerosis, 1993. 104(1-2): p. 129-35.
Rosenblat, M. and M. Aviram, Paraoxonases role in the prevention of cardiovascular diseases. Biofactors, 2009. 35(1): p. 98-104.
Fuhrman, B., N. Volkova, and M. Aviram, Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis, 2002. 161(2): p. 307-16.
Rozenberg, O., D.M. Shih, and M. Aviram, Human serum paraoxonase 1 decreases macrophage cholesterol biosynthesis: possible role for its phospholipase-A2-like activity and lysophosphatidylcholine formation. Arterioscler Thromb Vasc Biol, 2003. 23(3): p. 461-7.
Rosenblat, M., et al., Paraoxonase 1 (PON1) enhances HDL-mediated macrophage cholesterol efflux via the ABCA1 transporter in association with increased HDL binding to the cells: a possible role for lysophosphatidylcholine. Atherosclerosis, 2005. 179(1): p. 69-77.
Rodrigo, L., et al., Hydrolysis of platelet-activating factor by human serum paraoxonase. Biochem J, 2001. 354(Pt 1): p. 1-7.
Khersonsky, O. and D.S. Tawfik, Structure-reactivity studies of serum paraoxonase PON1 suggest that its native activity is lactonase. Biochemistry, 2005. 44(16): p. 6371-82.
Josse D, B.C., Lockidge O, Masson P, PON1 structure. In Paraoxonase (PON1) in Health and Disease: Basic and Clinical Aspects, ed. F.C.e. Costa LG. 2002: Kluwer Acad: Norwell; MA.
Boemi, M., et al., Serum paraoxonase is reduced in type 1 diabetic patients compared to non-diabetic, first degree relatives; influence on the ability of HDL to protect LDL from oxidation. Atherosclerosis, 2001. 155(1): p. 229-35.
Mackness, B., et al., Serum paraoxonase (PON1) 55 and 192 polymorphism and paraoxonase activity and concentration in non-insulin dependent diabetes mellitus. Atherosclerosis, 1998. 139(2): p. 341-9.
She, Z.G., et al., Human paraoxonase gene cluster transgenic overexpression represses atherogenesis and promotes atherosclerotic plaque stability in ApoE-null mice. Circ Res, 2009. 104(10): p. 1160-8.
Abbott, C.A., et al., Serum paraoxonase activity, concentration, and phenotype distribution in diabetes mellitus and its relationship to serum lipids and lipoproteins. Arterioscler Thromb Vasc Biol, 1995. 15(11): p. 1812-8.
Inoue, M., et al., Serum arylesterase/diazoxonase activity and genetic polymorphisms in patients with type 2 diabetes. Metabolism, 2000. 49(11): p. 1400-5.
Letellier, C., et al., Serum paraoxonase activity and paraoxonase gene polymorphism in type 2 diabetic patients with or without vascular complications. Diabetes Metab, 2002. 28(4 Pt 1): p. 297-304.
Juretic, D., et al., Paraoxonase/arylesterase in serum of patients with type II diabetes mellitus. Acta Pharm, 2006. 56(1): p. 59-68.
Tsuzura, S., et al., Correlation of plasma oxidized low-density lipoprotein levels to vascular complications and human serum paraoxonase in patients with type 2 diabetes. Metabolism, 2004. 53(3): p. 297-302.
Kopprasch, S., et al., Lack of association between serum paraoxonase 1 activities and increased oxidized low-density lipoprotein levels in impaired glucose tolerance and newly diagnosed diabetes mellitus. J Clin Endocrinol Metab, 2003. 88(4): p. 1711-6.
Sampson, M.J., et al., Paraoxonase-1 (PON-1) genotype and activity and in vivo oxidized plasma low-density lipoprotein in Type II diabetes. Clin Sci (Lond), 2005. 109(2): p. 189-97.
Calabresi, L., et al., An omega-3 polyunsaturated fatty acid concentrate increases plasma high-density lipoprotein 2 cholesterol and paraoxonase levels in patients with familial combined hyperlipidemia. Metabolism, 2004. 53(2): p. 153-8.
Patti L, M.A., Iovine C, et al, Long term effects of fish oil on lipoprotein subfractions and low density lipoprotein size in non-insulin-dependent diabetic patients with hypertriglyceridemia. Atherosclerosis, 1999. 146: p. 361-367.
Woodman, R.J., et al., Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension. Am J Clin Nutr, 2002. 76(5): p. 1007-15.
Luo, J., et al., Moderate intake of n-3 fatty acids for 2 months has no detrimental effect on glucose metabolism and could ameliorate the lipid profile in type 2 diabetic men. Results of a controlled study. Diabetes Care, 1998. 21(5): p. 717-24.
| Files | ||
| Issue | Vol 55, No 8 (2017) | |
| Section | Articles | |
| Keywords | ||
| Eicosapentaenoic acid Paraoxonase 1 Type 2 diabetes mellitus | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
