Effect of long-term ingestion of weakly oxidised flaxseed oil on biomarkers of oxidative stress in LDL-receptor knockout mice

British Journal of Nutrition

Volumn 116, Issue 2, 2016, Pages 258-269

  Nogueira, M S ^a   Kessuane, M C ^a   Lobo Ladd, A A B ^a   Lobo Ladd, F V ^a   Cogliati, B ^a   Castro, I A ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Atherosclerosis; Flaxseeds; Malondialdehyde; Mice; Oxidation

Indexed keywords

ARACHIDONIC ACID; BIOLOGICAL MARKER; GLUCOSE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; ICOSAPENTAENOIC ACID; LINOLEIC ACID; LINSEED OIL; LIPID HYDROPEROXIDE; LOW DENSITY LIPOPROTEIN RECEPTOR; MALONALDEHYDE; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; FAT INTAKE; FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTERY DIAMETER; ARTICLE; ATHEROSCLEROSIS; BODY WEIGHT; CALORIC INTAKE; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID BLOOD LEVEL; IN VIVO STUDY; LIVER HOMOGENATE; LIVER LEVEL; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; AORTA; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECTS; FAT INTAKE; FLAX; GENETICS; KNOCKOUT MOUSE; LIPID DIET; LIVER; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; PHARMACOLOGY;

ANIMALS; AORTA; ATHEROSCLEROSIS; BIOMARKERS; DIET, HIGH-FAT; DIETARY FATS; FATTY ACIDS; FLAX; LINSEED OIL; LIVER; MALE; MALONDIALDEHYDE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; OXIDATION-REDUCTION; OXIDATIVE STRESS; RECEPTORS, LDL;

EID: 84969638889     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114516001513     Document Type: Article

References (70)

1. Libby P, Ridker PM &Hansson GK (2011) Progress and challenges in translating the biology of atherosclerosis. Nature 473, 317-325
2. Zaina S &Lund G (2011) Epigenetics: a tool to understand diet-related cardiovascular risk? J Nutrigenet Nutrigenomics 4, 261-274
3. Rezvan A, Ni CW, Alberts-Grill N, et al. (2011) Animal, in vitro, and ex vivo models of flow-dependent atherosclerosis: role of oxidative stress. Antioxid Redox Signal 15, 1433-1448
4. Ishibashi S, Herz J, Maeda N, et al. (1994) The two-receptor model of lipoprotein clearance: tests of the hypothesis in 'knockout' mice lacking the low density lipoprotein receptor, apolipoprotein E, or both proteins. Proc Natl Acad Sci U S A 91, 4431-4435
5. Higley NA, Beery JT, Taylor SL, et al. (1986) Comparative atherogenic effects of cholesterol and cholesterol oxides. Atherosclerosis 62, 91-104
6. Yu R &Schellhorn HE (2013) Recent applications of engineered animal antioxidant deficiency models in human nutrition and chronic disease. J Nutr 143, 1-11
7. Lloyd K, Franklin C, Lutz C, et al. (2015) Reproducibility: use mouse biobanks or lose them. Nature 522, 151-153
8. Russell JC &Proctor SD (2006) Small animal models of cardiovascular disease: tools for the study of the roles of metabolic syndrome, dyslipidemia, and atherosclerosis. Cardiovasc Pathol 15, 318-330
9. Hansson GK &Libby P (2006) The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6, 508-519
10. Oikawa D, Akai R, Tokuda M, et al. (2012) A transgenic mouse model for monitoring oxidative stress. Sci Rep 2, 229
11. Ding T, Yao Y &Praticò D (2005) Increase in peripheral oxidative stress during hypercholesterolemia is not reflected in the central nervous system: evidence from two mouse models. Neurochem Int 46, 435-439
12. Sakata N, Yoshimatsu G, Tsuchiya H, et al. (2012) Animal models of diabetes mellitus for islet transplantation. Exp Diabetes Res 2012, 256707
13. Kunitomo M, Yamaguchi Y, Kagota S, et al. (2009) Biochemical evidence of atherosclerosis progression mediated by increased oxidative stress in apolipoprotein E-deficient spontaneously hyperlipidemic mice exposed to chronic cigarette smoke. J Pharmacol Sci 110, 354-361
14. Kuiper HC, Miranda CL, Sowell JD, et al. (2008) Mercapturic acid conjugates of 4-hydroxy-2-nonenal and 4-oxo-2-nonenal metabolites are in vivo markers of oxidative stress. J Biol Chem 283, 17131-17138
15. Rosa DP, Martinez D, Picada JN, et al. (2011) Hepatic oxidative stress in an animal model of sleep apnoea: effects of different duration of exposure. Comp Hepatol 10, 1
16. Hermans N, Cos P, De Meyer GR, et al. (2007) Study of potential systemic oxidative stress animal models for the evaluation of antioxidant activity: status of lipid peroxidation and fat-soluble antioxidants. J Pharm Pharmacol 59, 131-136
17. Flora SJS (2011) Arsenic-induced oxidative stress and its reversibility. Free Radic Biol Med 51, 257-281
18. Breslow JL (1996) Mouse models of atherosclerosis. Science 272, 685-688
19. Jawien J, Nastalek P &Korbut R (2004) Mouse models of experimental atherosclerosis. J Physiol Pharmacol 55, 503-517
20. Jové M, Pamplona R, Prat J, et al. (2013) Atherosclerosis prevention by nutritional factors: a meta-analysis in small animal models. Nutr Metab Cardiovasc Dis 23, 84-93
21. Khan-Merchant N, Penumetcha M, Meilhac O, et al. (2002) Oxidized fatty acids promote atherosclerosis only in the presence of dietary cholesterol in low-density lipoprotein receptor knockout mice. J Nutr 132, 3256-3262
22. Eder K (1999) The effects of a dietary oxidized oil on lipid metabolism in rats. Lipids 34, 717-725
23. Kämmerer I, Ringseis R &Eder K (2011) Feeding a thermally oxidised fat inhibits atherosclerotic plaque formation in the aortic root of LDL receptor-deficient mice. Br J Nutr 105, 190
24. Awada M, Soulage CO, Meynier A, et al. (2012) Dietary oxidized n-3 PUFA induce oxidative stress and inflammation: role of intestinal absorption of 4-HHE and reactivity in intestinal cells. J Lipid Res 53, 2069-2080
25. Staprans I, Pan X-M, Rapp JH, et al. (1998) Oxidized cholesterol in the diet accelerates the development of aortic atherosclerosis in cholesterol-fed rabbits. Arterioscler Thromb Vasc Biol 18, 977-983
26. Staprans I, Rapp JH, Pan X-M, et al. (1993) The effect of oxidized lipids in the diet on serum lipoprotein peroxides in control and diabetic rats. J Clin Invest 92, 638-643
27. Staprans I, Rapp JH, Pan X-M, et al. (1996) Oxidized lipids in the diet are incorporated by the liver into very low density lipoprotein in rats. J Lipid Res 37, 420-430
28. Staprans I, Pan X-M, Rapp JH, et al. (2000) Oxidized cholesterol in the diet accelerates the development of atherosclerosis in LDL receptor-and apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 20, 708-714
29. Cao J, Zou X-G, Deng L, et al. (2014) Analysis of nonpolar lipophilic aldehydes/ketones in oxidized edible oils using HPLC-QqQ-MS for the evaluation of their parent fatty acids. Food Res Int 64, 901-907
30. Frankel EN (2005) Lipid Oxidation. Bridgwater: The Oily Press
31. Tallman DL &Taylor CG (2003) Effects of dietary fat and zinc on adiposity, serum leptin and adipose fatty acid composition in C57BL/6J mice. J Nutr Biochem 14, 17-23
32. Sampey BP, Vanhoose AM, Winfield HM, et al. (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to highfat diet. Obesity (Silver Spring) 19, 1109-1117
33. Shantha NC &Decker EA (1994) Rapid, sensitive, iron-based spectrophotometric methods for determination of peroxide values of food lipids. J AOAC Int 77, 421-424
34. McDonald RE &Hultin HO (1987) Some characteristics of the enzymic lipid peroxidation system in the microsomal fraction of flounder skeletal muscle. J Food Sci 52, 15-21
35. Garcia-Llatas G, Lagarda M, Romero F, et al. (2007) A headspace solid-phase microextraction method of use in monitoring hexanal and pentane during storage: application to liquid infant foods and powdered infant formulas. Food Chem 101, 1078-1086
36. Shirai N, Suzuki H &Wada S (2005) Direct methylation from mouse plasma and from liver and brain homogenates. Anal Biochem 343, 48-53
37. Van Vré EA, van Beusekom HM, Vrints CJ, et al. (2007) Stereology: a simplified and more time-efficient method than planimetry for the quantitative analysis of vascular structures in different models of intimal thickening. Cardiovasc Pathol 16, 43-50
38. Jordão MT, Ladd FVL, Coppi AA, et al. (2011) Exercise training restores hypertension-induced changes in the elastic tissue of the thoracic aorta. J Vasc Res 48, 513-524
39. Hong Y-L, Yeh S-L, Chang C-Y, et al. (2000) Total plasma malondialdehyde levels in 16 Taiwanese college students determined by various thiobarbituric acid tests and an improved high-performance liquid chromatographybased method. Clin Biochem 33, 619-625
40. Ewing JF &Janero DR (1995) Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232, 243-248
41. Flohe L &Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105, 114-121
42. Torres LL, Quaglio NB, de Souza GT, et al. (2011) Peripheral oxidative stress biomarkers in mild cognitive impairment and Alzheimer's disease. J Alzheimers Dis 26, 59-68
43. Kleiner DE, Brunt EM, Van Natta M, et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321
44. Zou Y, Li J, Lu C, et al. (2006) High-fat emulsion-induced rat model of nonalcoholic steatohepatitis. Life Sci 79, 1100-1107
45. Ibrahim W, Lee U-S, Yeh C-C, et al. (1997) Oxidative stress and antioxidant status in mouse liver: effects of dietary lipid, vitamin E and iron. J Nutr 127, 1401-1406
46. Staprans I, Rapp JH, Pan X-M, et al. (1994) Oxidized lipids in the diet are a source of oxidized lipid in chylomicrons of human serum. Arterioscler Thromb 14, 1900-1905
47. Grootveld M, Atherton MD, Sheerin AN, et al. (1998) In vivo absorption, metabolism, and urinary excretion of alpha, beta-unsaturated aldehydes in experimental animals. Relevance to the development of cardiovascular diseases by the dietary ingestion of thermally stressed polyunsaturate-rich culinary oils. J Clin Invest 101, 1210-1218
48. Uchida K (2000) Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med 28, 1685-1696
49. Adibhatla RM &Hatcher JF (2010) Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 12, 125-169
50. Viana M, Villacorta L, Bonet B, et al. (2005) Effects of aldehydes on CD36 expression. Free Radic Res 39, 973-977
51. Uchida K (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 42, 318-343
52. Rains JL &Jain SK (2011) Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med 50, 567-575
53. Agência Nacional de Vigilância Sanitária (Anvisa) (2005) Resolução RDC n 270, de 22 de setembro de 2005. In Regulamento técnico para óleos vegetais, gorduras vegetais e creme vegetal (Technical Regulations for Vegetable Oils, Vegetable Fats and Vegetable Cream), Vol. RDC 270, [A-ANdV Sanitária, editor]. Brasilia: Diário Oficial da União; Poder Executivo
54. Dobarganes C &Márquez-Ruiz G (2003) Oxidized fats in foods. Curr Opin Clin Nutr Metab Care 6, 157-163
55. Negre-Salvayre A, Coatrieux C, Ingueneau C, et al. (2008) Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 153, 6-20
56. Esterbauer H, Gebicki J, Puhl H, et al. (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 13, 341-390
57. Vinchi F, Muckenthaler MU, Da Silva MC, et al. (2014) Atherogenesis and iron: from epidemiology to cellular level. Front Pharmacol 5, 328-347
58. Fairweather-Tait SJ, Bao Y, Broadley MR, et al. (2011) Selenium in human health and disease. Antioxid Redox Signal 14, 1337-1383
59. Yin H, Brooks JD, Gao L, et al. (2007) Identification of novel autoxidation products of the-3 fatty acid eicosapentaenoic acid in vitro and in vivo. J Biol Chem 282, 29890-29901
60. Gao L, Wang J, Sekhar KR, et al. (2007) Novel n-3 fatty acid oxidation products activate Nrf2 by destabilizing the association between Keap1 and Cullin3. J Biol Chem 282, 2529-2537
61. Roy J, Le Guennec J-Y, Galano J-M, et al. (2015) Non-enzymatic cyclic oxygenated metabolites of omega-3 polyunsaturated fatty acid: bioactive drugs? Biochimie 120, 56-61
62. Carrepeiro MM, Rogero MM, Bertolami MC, et al. (2011) Effect of n-3 fatty acids and statins on oxidative stress in statintreated hypercholestorelemic and normocholesterolemic women. Atherosclerosis 217, 171-178
63. Penumetcha M, Song M, Merchant N, et al. (2012) Pretreatment with n-6 PUFA protects against subsequent high fat diet induced atherosclerosis-potential role of oxidative stressinduced antioxidant defense. Atherosclerosis 220, 53-58
64. Yang J, Li Y, Wang F, et al. (2010) Hepatoprotective effects of apple polyphenols on CCl4-induced acute liver damage in mice. J Agric Food Chem 58, 6525-6531
65. Zeng T, Guo F-F, Zhang C-L, et al. (2008) The anti-fatty liver effects of garlic oil on acute ethanol-exposed mice. Chem Biol Interact 176, 234-242
66. Botelho PB, Guimarães JP, Mariano KR, et al. (2015) Effect of echium oil combined with phytosterols on biomarkers of atherosclerosis in LDLr-knockout mice: echium oil is a potential alternative to marine oils for use in functional foods. Eur J Lipid Sci Tech 117, 1561-1567
67. Lin C-c &Yin M-c (2008) Effects of cysteine-containing compounds on biosynthesis of triacylglycerol and cholesterol and anti-oxidative protection in liver from mice consuming a highfat diet. Br J Nutr 99, 37-43
68. Prewitt RL, Rice DC &Dobrian AD (2002) Adaptation of resistance arteries to increases in pressure. Microcirculation 9, 295-304
69. Laurent S &Boutouyrie P (2015) The structural factor of hypertension large and small artery alterations. Circ Res 116, 1007-1021
70. van Diepen JA, Berbée JFP, Havekes LM, et al. (2013) Interactions between inflammation and lipid metabolism: relevance for efficacy of anti-inflammatory drugs in the treatment of atherosclerosis. Atherosclerosis 228, 306-315