Paraoxonase 1 (PON1) attenuates diabetes development in mice through its antioxidative properties

Free Radical Biology and Medicine

Volumn 44, Issue 11, 2008, Pages 1951-1959

  Rozenberg, Orit ^a   Shiner, Maayan ^a   Aviram, Michael ^a   Hayek, Tony ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Antioxidants; Diabetes mellitus; Macrophages; Oxidative stress; Paraoxonase

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; APOLIPOPROTEIN E; ARYLDIALKYLPHOSPHATASE 1; PROTEIN P47;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; DIABETES MELLITUS; DISEASE COURSE; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; HYPERLIPOPROTEINEMIA TYPE 3; MACROPHAGE; MALE; MORTALITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOZOCIN DIABETES; TRANSGENIC MOUSE; VITAMIN SUPPLEMENTATION;

ANIMALS; ANTIOXIDANTS; APOLIPOPROTEINS E; ARYLDIALKYLPHOSPHATASE; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; HUMANS; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NADPH OXIDASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STREPTOZOCIN;

MUS; MUS MUSCULUS;

EID: 43049162677     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.02.012     Document Type: Article

References (70)

1. Kaneto H., Katakami N., Kawamori D., Miyatsuka T., Sakamoto K., Matsuoka T.A., Matsuhisa M., and Yamasaki Y. Involvement of oxidative stress in the pathogenesis of diabetes. Antioxid. Redox Signal. 9 (2007) 355-366
2. Ceriello A., and Motz E. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 816-823
3. Hayek T., Hussein K., Aviram M., Coleman R., Keidar S., Pavoltzky E., and Kaplan M. Macrophage foam-cell formation in streptozotocin-induced diabetic mice: stimulatory effect of glucose. Atherosclerosis 183 (2005) 25-33
4. Ahmed F.N., Naqvi F.N., and Shafiq F. Lipid peroxidation and serum antioxidant enzymes in patients with type 2 diabetes mellitus. Ann. N. Y. Acad. Sci. 1084 (2006) 481-489
5. Wahlberg G., Adamson U., and Svensson J. Pyridine nucleotides in glucose metabolism and diabetes: a review. Diabetes Metab. Res. Rev. 16 (2000) 33-42
6. Naka Y., Bucciarelli L.G., Wendt T., Lee L.K., Rong L.L., Ramasamy R., Yan S.F., and Schmidt A.M. RAGE axis: animal models and novel insights into the vascular complications of diabetes. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1342-1349
7. Chung S.S., Ho E.C., Lam K.S., and Chung S.K. Contribution of polyol pathway to diabetes-induced oxidative stress. J. Am. Soc. Nephrol. 14 (2003) S233-S236
8. Lapolla A., Piarulli F., Sartore G., Ceriello A., Ragazzi E., Reitano R., Baccarin L., Laverda B., and Fedele D. Advanced glycation end products and antioxidant status in type 2 diabetic patients with and without peripheral artery disease. Diabetes Care 30 (2007) 670-676
9. Ceriello A., Taboga C., Tonutti L., Quagliaro L., Piconi L., Bais B., Da Ros R., and Motz E. Evidence for an independent and cumulative effect of postprandial hypertriglyceridemia and hyperglycemia on endothelial dysfunction and oxidative stress generation: effects of short- and long-term simvastatin treatment. Circulation 106 (2002) 1211-1218
10. Aviram M., and Rosenblat M. Paraoxonases and cardiovascular diseases: pharmacological and nutritional influences. Curr. Opin. Lipidol. 16 (2005) 393-399
11. Ng C.J., Shih D.M., Hama S.Y., Villa N., Navab M., and Reddy S.T. The paraoxonase gene family and atherosclerosis. Free Radic. Biol. Med. 38 (2005) 153-163
12. Aviram M., Billecke S., Sorenson R., Bisgaier C., Newton R., Rosenblat M., Erogul J., Hsu C., Dunlop C., and La Du B. Paraoxonase active site required for protection against LDL oxidation involves its free sulfhydryl group and is different from that required for its arylesterase/paraoxonase activities: selective action of human paraoxonase allozymes Q and R. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 1617-1624
13. Navab M., Berliner J.A., Watson A.D., Hama S.Y., Territo M.C., Lusis A.J., Shih D.M., Van Lenten B.J., Frank J.S., Demer L.L., Edwards P.A., and Fogelman A.M. The Yin and Yang of oxidation in the development of the fatty streak. Arterioscler. Thromb. Vasc. Biol. 16 (1996) 831-842
14. Aviram M., Rosenblat M., Bisgaier C.L., Newton R.S., Primo-Parmo S.L., and La Du B.N. Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. J. Clin. Invest. 101 (1998) 1581-1590
15. Rozenberg O., Shih D.M., and Aviram M. Paraoxonase 1 (PON1) attenuates macrophage oxidative status: studies in PON1 transfected cells and in PON1 transgenic mice. Atherosclerosis 181 (2005) 9-18
16. Shih D.M., Xia Y.R., Wang X.P., Miller E., Castellani L.W., Subbanagounder G., Cheroutre H., Faull K.F., Berliner J.A., Witztum J.L., and Lusis A.J. Combined serum paraoxonase knockout/apolipoprotein E knockout mice exhibit increased lipoprotein oxidation and atherosclerosis. J. Biol. Chem. 275 (2000) 17527-17535
17. Rozenberg O., Rosenblat M., Coleman R., Shih D.M., and Aviram M. Paraoxonase (PON1) deficiency is associated with increased macrophage oxidative stress: studies in PON1-knockout mice. Free Radic. Biol. Med. 34 (2003) 774-784
18. Tward A., Xia Y.R., Wang X.P., Shi Y.S., Park C., Castellani L.W., Lusis A.J., and Shih D.M. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation 106 (2002) 484-490
19. Nguyen S.D., and Sok D.E. Oxidative inactivation of paraoxonase1, an antioxidant protein and its effect on antioxidant action. Free Radic. Res. 37 (2003) 1319-1330
20. Karabina S.A., Lehner A.N., Frank E., Parthasarathy S., and Santanam N. Oxidative inactivation of paraoxonase-implications in diabetes mellitus and atherosclerosis. Biochim. Biophys. Acta 1725 (2005) 213-221
21. Mastorikou M., Mackness M., and Mackness B. Defective metabolism of oxidized phospholipid by HDL from people with type 2 diabetes. Diabetes 55 (2006) 3099-3103
22. Sampson M.J., Braschi S., Willis G., and Astley S.B. Paraoxonase-1 (PON-1) genotype and activity and in vivo oxidized plasma low-density lipoprotein in type II diabetes. Clin. Sci. (Lond.) 109 (2005) 189-197
23. Lakshman M.R., Gottipati C.S., Narasimhan S.J., Munoz J., Marmillot P., and Nylen E.S. 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 55 (2006) 1201-1206
24. Buege J.A., and Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 52 (1978) 302-310
25. LeBel C.P., Ischiropoulos H., and Bondy S.C. Evaluation of the probe 2′,7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5 (1992) 227-231
26. Zulueta J.J., Sawhney R., Yu F.S., Cote C.C., and Hassoun P.M. Intracellular generation of reactive oxygen species in endothelial cells exposed to anoxia-reoxygenation. Am. J. Physiol. 272 (1997) L897-L902
27. Johnston R.B., Keele B.B., Misra H.P., Lehmeyer J.E., Webb L.S., and Baehner R.L. The role of superoxide anion generation in phagocytic bactericidal activity. Studies with normal and chronic granulomatous disease leukocytes. J. Clin. Invest. 55 (1975) 1357-1372
28. Lowry O.H., Rosebrough N.J., Farr L., and Randall R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Griffith O.W., and Meister A. Excretion of cysteine and gammaglutamyl cysteine moieties in human and experimental animal with gamma glutamyl transpeptidase deficiency. Proc. Natl. Acad. Sci. U. S. A. 77 (1980) 3384-3387
30. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: application to mammalian blood and other tissues. Anal. Biochem. 27 (1969) 502-522
31. Rees D.A., and Alcolado J.C. Animal models of diabetes mellitus. Diabetes Med. 22 (2005) 359-370
32. Davignon J.S., Cohn L., Mabile L., and Bernier L. Apolipoprotein E and atherosclerosis: insights from animal and human studies. Clin. Chim. Acta 286 (1999) 115-143
33. Palinski W., Ord V.A., Plump A.S., Breslow J.L., Steinberg D., and Witztum J.L. ApoE-deficient mice are a model of lipoprotein oxidation in atherosclerosis. Demonstration of oxidation-specific epitopes in lesions and high titers of autoantibodies to malondialdehyde-lysine in serum. Arterioscler. Thromb. 14 (1994) 605-616
34. Hayek T., Oikinine J., Brook J.G., and Aviram M. Increased plasma and lipoprotein lipid peroxidation in apoE deficient mice. Biochem. Biophys. Res. Commun. 201 (1994) 1567-1574
35. 0-mice and from human carotid artery contain lipid peroxides and oxysterols. Biochem. Biophys. Res. Commun. 269 (2000) 775-780
36. Jackson S.H., Gallin J.I., and Holland S.M. The p47phox mouse knock-out model of chronic granulomatous disease. J. Exp. Med. 182 (1995) 751-758
37. Cathcart M.K. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: contributions to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 23-28
38. Babior B.M. Phagocytes and oxidative stress. Am. J. Med. 109 (2000) 33-44
39. Wu J.H., Ward N.C., Indrawan A.P., Almeida C.A., Hodgson J.M., Proudfoot J.M., Puddey I.B., and Croft K.D. Effects of alpha-tocopherol and mixed tocopherol supplementation on markers of oxidative stress and inflammation in type 2 diabetes. Clin. Chem. 53 (2007) 511-519
40. Al-Shamsi M., Amin A., and Adeghate E. Vitamin E ameliorates some biochemical parameters in normal and diabetic rats. Ann. N. Y. Acad. Sci. 1084 (2006) 411-431
41. Wautier M.P., Chappey O., Corda S., Stern D.M., Schmidt A.M., and Wautier J.L. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am. J. Physiol. Endocrinol. Metab. 280 (2001) E685-E694
42. San Martin A., Foncea R., Laurindo F.R., Ebensperger R., Griendling K.K., and Leighton F. Nox1-based NADPH oxidase-derived superoxide is required for VSMC activation by advanced glycation end-products. Free Radic. Biol. Med. 42 (2007) 1671-1679
43. Rosenblat M., Karry R., and Aviram M. Paraoxonase 1 (PON1) is a more potent antioxidant and stimulant of macrophage cholesterol efflux, when present in HDL than in lipoprotein-deficient serum: relevance to diabetes. Atherosclerosis 187 (2006) 74-81
44. Rosenblat M., Hayek T., and Aviram M. Anti-oxidative effects of pomegranate juice (PJ) consumption by diabetic patients on serum and on macrophages. Atherosclerosis 187 (2006) 363-371
45. Rozenberg O., and Aviram M. S-Glutathionylation regulates HDL-associated paraoxonase 1 (PON1) activity. Biochem. Biophys. Res. Commun. 351 (2006) 492-498
46. James R.W., Leviev I., Ruiz J., Passa P., Froguel P., and Garin M.C. Promoter polymorphism T(-107)C of the paraoxonase PON1 gene is a risk factor for coronary heart disease in type 2 diabetic patients. Diabetes 49 (2000) 1390-1393
47. Mackness B., Hine D., McElduff P., and Mackness M. High C-reactive protein and low paraoxonase1 in diabetes as risk factors for coronary heart disease. Atherosclerosis 186 (2006) 396-401
48. Aviram M. Macrophage foam cell formation during early atherogenesis is determined by the balance between pro-oxidants and anti-oxidants in arterial cells and blood lipoprotein. Antioxid. Redox Signal. 1 (1999) 585-594
49. Draganov D.I., Teiber J.F., Speelman A., Osawa Y., Sunahara R., and La Du B.N. Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificities. J. Lipid Res. 46 (2005) 1239-1247
50. Teiber J.F., Draganov D.I., and La Du B.N. Purified human serum PON1 does not protect LDL against oxidation in the in vitro assays initiated with copper or AAPH. J. Lipid Res. 45 (2004) 2260-2268
51. Khersonsky O., and Tawfik D.S. Structure-reactivity studies of serum paraoxonase PON1 suggest that its native activity is lactonase. Biochemistry 44 (2005) 6371-6382
52. Rosenblat M., Gaidukov L., Khersonsky O., Vaya J., Oren R., Tawfik D.S., and Aviram M. The catalytic histidine dyad of high density lipoprotein-associated serum paraoxonase-1 (PON1) is essential for PON1-mediated inhibition of low density lipoprotein oxidation and stimulation of macrophage cholesterol efflux. J. Biol. Chem. 281 (2006 17) 7657-7665
53. Evans J.L., Maddux B.A., and Goldfine I.D. The molecular basis for oxidative stress-induced insulin resistance. Antioxid. Redox Signal. 7 (2005) 1040-1052
54. Robertson R.P. Oxidative stress and impaired insulin secretion in type 2 diabetes. Curr. Opin. Pharmacol. 6 (2006) 615-619
55. Kajimoto Y., and Kaneto H. Role of oxidative stress in pancreatic beta-cell dysfunction. Ann. N. Y. Acad. Sci. 1011 (2004) 168-176
56. Kaneto H., Kajimoto Y., Miyagawa J., Matsuoka T., Fujitani Y., Umayahara Y., Hanafusa T., Matsuzawa Y., Yamasaki Y., and Hori M. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 48 (1999) 2398-2406
57. Mensah-Brown E., Shahin A., Parekh K., Hakim A.A., Shamisi M.A., Hsu D.K., and Lukic M.L. Functional capacity of macrophages determines the induction of type 1 diabetes. Ann. N. Y. Acad. Sci. 1084 (2006) 49-57
58. Kolb H., Burkart V., Appels B., Hanenberg H., Kantwerk-Funke G., Kiesel U., Funda J., Schraermeyer U., and Kolb-Bachofen V. Essential contribution of macrophages to islet cell destruction in vivo and in vitro. J. Autoimmun. Suppl1 (1990) 117-120
59. Emre Y., Hurtaud C., Karaca M., Nubel T., Zavala F., and Ricquier D. Role of uncoupling protein UCP2 in cell-mediated immunity: how macrophage-mediated insulitis is accelerated in a model of autoimmune diabetes. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 19085-19090
60. Giannerini F., Giustarini D., Lusini L., Rossi R., and Di Simplicio P. Responses of thiols to an oxidant challenge: differences between blood and tissues in the rat. Chem. Biol. Interact. 134 (2001) 73-85
61. Tchantchou F., Graves M., Ashline D., Morin A., Pimenta A., Ortiz D., Rogers E., and Shea T.B. Increased transcription and activity of glutathione synthase in response to deficiencies in folate, vitamin E, and apolipoprotein E. J. Neurosci. Res. 75 (2004) 508-515
62. Dalton T.P., Dieter M.Z., Yang Y., Shertzer H.G., and Nebert D.W. Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous. Biochem. Biophys. Res. Commun. 279 (2000) 324-329
63. Rosenblat M., Coleman R., and Aviram M. Increased macrophage glutathione content reduces cell-mediated oxidation of LDL and atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 163 (2002) 17-28
64. Kislinger T., Tanji N., Wendt T., Qu W., Lu Y., Ferran Jr. L.J., Taguchi A., Olson K., Bucciarelli L., Goova M., Hofmann M.A., Cataldegirmen G., D'Agati V., Pischetsrieder M., Stern D.M., and Schmidt A.M. Receptor for advanced glycation end products mediates inflammation and enhanced expression of tissue factor in vasculature of diabetic apolipoprotein E-null mice. Arterioscler. Thromb. Vasc. Biol. 21 (2001) 905-910
65. Kim W., Hudson B.I., Moser B., Guo J., Rong L.L., Lu Y., Qu W., Lalla E., Lerner S., Chen Y., Yan S.S., D'Agati V., Naka Y., Ramasamy R., Herold K., Yan S.F., and Schmidt A.M. Receptor for advanced glycation end products and its ligands: a journey from the complications of diabetes to its pathogenesis. Ann. N. Y. Acad. Sci. 1043 (2005) 553-561
66. Wendt T., Harja E., Bucciarelli L., Qu W., Lu Y., Rong L.L., Jenkins D.G., Stein G., Schmidt A.M., and Yan S.F. RAGE modulates vascular inflammation and atherosclerosis in a murine model of type 2 diabetes. Atherosclerosis 185 (2006) 70-77
67. Yamagishi S., and Takeuchi M. Nifedipine inhibits gene expression of receptor for advanced glycation end products (RAGE) in endothelial cells by suppressing reactive oxygen species generation. Drugs Exp. Clin. Res. 30 (2004) 169-175
68. Harja E., Bu D.X., Hudson B.I., Chang J.S., Shen X., Hallam K., Kalea A.Z., Lu Y., Rosario R.H., Oruganti S., Nikolla Z., Belov D., Lalla E., Ramasamy R., Yan S.F., and Schmidt A.M. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE mice. J. Clin. Invest. 118 (2008) 183-194
69. Aragno M., Mastrocola R., Medana C., Restivo F., Catalano M.G., Pons N., Danni O., and Boccuzzi G. Up-regulation of advanced glycated products receptors in the brain of diabetic rats is prevented by antioxidant treatment. Endocrinology 146 (2005) 5561-5567
70. Aviram M., and Fuhrman B. Wine flavonoids protect against LDL oxidation and atherosclerosis. Ann. N. Y. Acad. Sci. 957 (2002) 146-161