Nutrition Research and Practice

The Korean Nutrition Society (한국영양학회)
권호 표지
DOI QR코드

DOI QR Code

Lutein decreases oxidative stress and inflammation in liver and eyes of guinea pigs fed a hypercholesterolemic diet

  • Kim, Jung-Eun (Department of Nutritional Sciences, University of Connecticut) ;
  • Clark, Richard M. (Department of Nutritional Sciences, University of Connecticut) ;
  • Park, Young-Ki (Department of Nutritional Sciences, University of Connecticut) ;
  • Lee, Ji-Young (Department of Nutritional Sciences, University of Connecticut) ;
  • Fernandez, Maria Luz (Department of Nutritional Sciences, University of Connecticut)
  • Received : 2011.10.19
  • Accepted : 2012.02.03
  • Published : 2012.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Guinea pigs were fed a hypercholesterolemic diet (0.25 g/100 g cholesterol) and randomly allocated either to a Control group (n = 9) or to a Lutein (0.1 g/100 g) group (n = 10) for 12 weeks to evaluate oxidative stress and inflammation in both liver and eyes. Malondialdehyde (MDA) concentrations and inflammatory cytokines were measured as well as hepatic nuclear factor-kappaB (NF-${\kappa}B$) binding. Lutein concentrations were greater in eyes ($P$ < 0.01) and liver ($P$ < 0.001) in the Lutein group. All guinea pigs had high concentrations of hepatic cholesterol as well as high plasma ALT and AST levels indicative of liver injury. However, the Lutein group had 43% lower hepatic free cholesterol than the Controls ($P$ < 0.05). Hepatic MDA and MDA in the eye were lower in the Lutein compared to the Control group ($P$ < 0.05). Hepatic tumor necrosis factor-${\alpha}$ was 32% lower in the Lutein group ($P$ < 0.05). Lastly, the Lutein group presented lower NF-${\kappa}B$ DNA binding activity than the Control group ($P$ < 0.001). These results suggest that in the presence of high cholesterol, lutein exerts both antioxidant and anti-inflammatory effects, which can be explained by attenuated NF-${\kappa}B$ DNA binding activity. Furthermore, results also suggest that lutein accumulates in the eyes of guinea pigs to protect against oxidative stress.

Keywords

References

  1. Khachik F, Beecher GR, Smith JC Jr. Lutein, lycopene, and their oxidative metabolites in chemoprevention of cancer. J Cell Biochem Suppl 1995;22:236-46.
  2. Krinsky NI, Landrum JT, Bone RA. Biologic mechanisms of the protective role of lutein and zeaxanthin in the eye. Annu Rev Nutr 2003;23:171-201. https://doi.org/10.1146/annurev.nutr.23.011702.073307
  3. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2006;51:137-52. https://doi.org/10.1016/j.survophthal.2005.12.001
  4. Hollyfield JG, Bonilha VL, Rayborn ME, Yang X, Shadrach KG, Lu L, Ufret RL, Salomon RG, Perez VL. Oxidative damageinduced inflammation initiates age-related macular degeneration. Nat Med 2008;14:194-8. https://doi.org/10.1038/nm1709
  5. Dwyer JH, Navab M, Dwyer KM, Hassan K, Sun P, Shircore A, Hama-Levy S, Hough G, Wang X, Drake T, Merz CN, Fogelman AM. Oxygenated carotenoid lutein and progression of early atherosclerosis: the Los Angeles atherosclerosis study. Circulation 2001;103:2922-7. https://doi.org/10.1161/01.CIR.103.24.2922
  6. Dwyer JH, Paul-Labrador MJ, Fan J, Shircore AM, Merz CN, Dwyer KM. Progression of carotid intima-media thickness and plasma antioxidants: the Los Angeles Atherosclerosis Study. Arterioscler Thromb Vasc Biol 2004;24:313-9. https://doi.org/10.1161/01.ATV.0000109955.80818.8a
  7. Sindhu ER, Firdous AP, Preethi KC, Kuttan R. Carotenoid lutein protects rats from paracetamol-, carbon tetrachloride- and ethanolinduced hepatic damage. J Pharm Pharmacol 2010;62:1054-60. https://doi.org/10.1111/j.2042-7158.2010.01123.x
  8. Sindhu ER, Preethi KC, Kuttan R. Antioxidant activity of carotenoid lutein in vitro and in vivo. Indian J Exp Biol 2010; 48:843-8.
  9. Jin XH, Ohgami K, Shiratori K, Suzuki Y, Hirano T, Koyama Y, Yoshida K, Ilieva I, Iseki K, Ohno S. Inhibitory effects of lutein on endotoxin-induced uveitis in Lewis rats. Invest Ophthalmol Vis Sci 2006;47:2562-8. https://doi.org/10.1167/iovs.05-1429
  10. Kim JH, Na HJ, Kim CK, Kim JY, Ha KS, Lee H, Chung HT, Kwon HJ, Kwon YG, Kim YM. The non-provitamin A carotenoid, lutein, inhibits NF-kappaB-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-kappaB-inducing kinase pathways: role of H(2)O(2) in NF-kappaB activation. Free Radic Biol Med 2008;45:885-96. https://doi.org/10.1016/j.freeradbiomed.2008.06.019
  11. Shanmugasundaram R, Selvaraj RK. Lutein supplementation alters inflammatory cytokine production and antioxidant status in F-line turkeys. Poult Sci 2011;90:971-6. https://doi.org/10.3382/ps.2010-01150
  12. He G, Karin M. NF-kappaB and STAT3 - key players in liver inflammation and cancer. Cell Res 2011;21:159-68. https://doi.org/10.1038/cr.2010.183
  13. Luedde T, Schwabe RF. NF-kappaB in the liver--linking injury, fibrosis and hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 2011;8:108-18. https://doi.org/10.1038/nrgastro.2010.213
  14. Robinson SM, Mann DA. Role of nuclear factor kappaB in liver health and disease. Clin Sci (Lond) 2010;118:691-705. https://doi.org/10.1042/CS20090549
  15. Fernandez ML. Guinea pigs as models for cholesterol and lipoprotein metabolism. J Nutr 2001;131:10-20. https://doi.org/10.1093/jn/131.1.10
  16. Roy S, Vega-Lopez S, Fernandez ML. Gender and hormonal status affect the hypolipidemic mechanisms of dietary soluble fiber in guinea pigs. J Nutr 2000;130:600-7. https://doi.org/10.1093/jn/130.3.600
  17. Torres-Gonzalez M, Shrestha S, Sharman M, Freake HC, Volek JS, Fernandez ML. Carbohydrate restriction alters hepatic cholesterol metabolism in guinea pigs fed a hypercholesterolemic diet. J Nutr 2007;137:2219-23. https://doi.org/10.1093/jn/137.10.2219
  18. Anstee QM, Goldin RD. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 2006;87:1-16. https://doi.org/10.1111/j.0959-9673.2006.00465.x
  19. Kim JE, Leite JO, DeOgburn R, Smyth JA, Clark RM, Fernandez ML. A lutein-enriched diet prevents cholesterol accumulation and decreases oxidized LDL and inflammatory cytokines in the aorta of guinea pigs. J Nutr 2011;141:1458-63. https://doi.org/10.3945/jn.111.141630
  20. Fernandez ML, McNamara DJ. Regulation of cholesterol and lipoprotein metabolism in guinea pigs mediated by dietary fat quality and quantity. J Nutr 1991;121:934-43. https://doi.org/10.1093/jn/121.7.934
  21. Clark RM, Herron KL, Waters D, Fernandez ML. Hypo- and hyperresponse to egg cholesterol predicts plasma lutein and betacarotene concentrations in men and women. J Nutr 2006;136:601-7. https://doi.org/10.1093/jn/136.3.601
  22. Carr TP, Andresen CJ, Rudel LL. Enzymatic determination of triglyceride, free cholesterol, and total cholesterol in tissue lipid extracts. Clin Biochem 1993;26:39-42. https://doi.org/10.1016/0009-9120(93)90015-X
  23. Schaffer MW, Sinha Roy S, Mukherjee S, Das SK. Identification of lutein, a dietary antioxidant carotenoid in guinea pig tissues. Biochem Biophys Res Commun 2008;374:378-81. https://doi.org/10.1016/j.bbrc.2008.07.030
  24. Lin EC, Fernandez ML, McNamara DJ. Dietary fat type and cholesterol quantity interact to affect cholesterol metabolism in guinea pigs. J Nutr 1992;122:2019-29. https://doi.org/10.1093/jn/122.10.2019
  25. Shanmugasundaram R, Selvaraj RK. Dietary lutein and fish oil interact to alter atherosclerotic lesions in a Japanese quail model of atherosclerosis. J Anim Physiol Anim Nutr (Berl) 2011;95:762-70. https://doi.org/10.1111/j.1439-0396.2010.01106.x
  26. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, Cheung O, Sargeant C, Contos MJ, Sanyal AJ. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 2007;46:1081-90. https://doi.org/10.1002/hep.21763
  27. Sanyal AJ, Campbell-Sargent C, Mirshahi F, Rizzo WB, Contos MJ, Sterling RK, Luketic VA, Shiffman ML, Clore JN. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 2001;120:1183-92. https://doi.org/10.1053/gast.2001.23256
  28. Nair S, V PC, Arnold C, Diehl AM. Hepatic ATP reserve and efficiency of replenishing: comparison between obese and nonobese normal individuals. Am J Gastroenterol 2003;98:466-70.
  29. McClain CJ, Mokshagundam SP, Barve SS, Song Z, Hill DB, Chen T, Deaciuc I. Mechanisms of non-alcoholic steatohepatitis. Alcohol 2004;34:67-79. https://doi.org/10.1016/j.alcohol.2004.07.007
  30. Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990;9:515-40. https://doi.org/10.1016/0891-5849(90)90131-2
  31. Young AJ, Lowe GM. Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 2001;385:20-7. https://doi.org/10.1006/abbi.2000.2149
  32. Ribaya-Mercado JD, Blumberg JB. Lutein and zeaxanthin and their potential roles in disease prevention. J Am Coll Nutr 2004;23:567S-587S. https://doi.org/10.1080/07315724.2004.10719427
  33. Debril MB, Renaud JP, Fajas L, Auwerx J. The pleiotropic functions of peroxisome proliferator-activated receptor gamma. J Mol Med (Berl) 2001;79:30-47. https://doi.org/10.1007/s001090000145
  34. Selvaraj RK, Shanmugasundaram R, Klasing KC. Effects of dietary lutein and PUFA on PPAR and RXR isomer expression in chickens during an inflammatory response. Comp Biochem Physiol A Mol Integr Physiol 2010;157:198-203. https://doi.org/10.1016/j.cbpa.2010.06.172
  35. Mai J, Shen X, Shi D, Wei Y, Shen H, Wu M. Effect of lutein on relieving oxidative stress in mice induced by D-galatose. Wei Sheng Yan Jiu 2010;39:430-2.
  36. Ruhl CE, Everhart JE. Relation of elevated serum alanine aminotransferase activity with iron and antioxidant levels in the United States. Gastroenterology 2003;124:1821-9. https://doi.org/10.1016/S0016-5085(03)00395-0
  37. Preethi KC, Kuttan R. Hepato and reno protective action of Calendula officinalis L. flower extract. Indian J Exp Biol 2009;47:163-8.
  38. Catala A. Lipid peroxidation of membrane phospholipids in the vertebrate retina. Front Biosci (Schol Ed) 2011;3:52-60.
  39. Ham WT Jr, Mueller HA, Sliney DH. Retinal sensitivity to damage from short wavelength light. Nature 1976;260:153-5. https://doi.org/10.1038/260153a0
  40. Beatty S, Koh H, Phil M, Henson D, Boulton M. The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv Ophthalmol 2000;45:115-34. https://doi.org/10.1016/S0039-6257(00)00140-5

Cited by

  1. Effect of dietary supplementation of marigold pigment on immunity, skin and meat color, and growth performance of broiler chickens vol.14, pp.4, 2012, https://doi.org/10.1590/S1516-635X2012000400009
  2. Radical Scavenging Activity-Based and AP-1-Targeted Anti-Inflammatory Effects of Lutein in Macrophage-Like and Skin Keratinocytic Cells vol.2013, pp.1466-1861, 2013, https://doi.org/10.1155/2013/787042
  3. Chemoprevention of nonalcoholic fatty liver disease by dietary natural compounds vol.58, pp.1, 2013, https://doi.org/10.1002/mnfr.201300522
  4. Does Vitamin C Deficiency Promote Fatty Liver Disease Development? vol.6, pp.12, 2014, https://doi.org/10.3390/nu6125473
  5. Egg Intake during Carbohydrate Restriction Alters Peripheral Blood Mononuclear Cell Inflammation and Cholesterol Homeostasis in Metabolic Syndrome vol.6, pp.7, 2014, https://doi.org/10.3390/nu6072650
  6. Cholesterol-induced inflammation and macrophage accumulation in adipose tissue is reduced by a low carbohydrate diet in guinea pigs vol.8, pp.6, 2014, https://doi.org/10.4162/nrp.2014.8.6.625
  7. Effects of lutein or lutein in combination with vitamin C on mRNA expression and activity of antioxidant enzymes and status of the antioxidant system in SD rats vol.31, pp.3, 2015, https://doi.org/10.5625/lar.2015.31.3.117
  8. Lutein Prevents High Fat Diet-Induced Atherosclerosis in ApoE-Deficient Mice by Inhibiting NADPH Oxidase and Increasing PPAR Expression vol.50, pp.3, 2015, https://doi.org/10.1007/s11745-015-3992-1
  9. Lutein derived fragments exhibit higher antioxidant and anti-inflammatory properties than lutein in lipopolysaccharide induced inflammation in rats vol.6, pp.2, 2015, https://doi.org/10.1039/C4FO00606B
  10. Bioactive Egg Components and Inflammation vol.7, pp.9, 2015, https://doi.org/10.3390/nu7095372
  11. Carotenoids: biochemistry, pharmacology and treatment vol.174, pp.11, 2016, https://doi.org/10.1111/bph.13625
  12. Effec t of Freeze-Thaw Cycles on Lipid Oxidation and Myowater in Broiler Chickens vol.18, pp.1, 2016, https://doi.org/10.1590/1516-635x1801035-040
  13. Insights into the Role and Interdependence of Oxidative Stress and Inflammation in Liver Diseases vol.2016, pp.1942-0994, 2016, https://doi.org/10.1155/2016/4234061
  14. Dietary Intake of Lutein and Diabetic Retinopathy in the Atherosclerosis Risk in Communities Study (ARIC) vol.23, pp.2, 2016, https://doi.org/10.3109/09286586.2015.1129426
  15. Effects of dietary marigold extract supplementation on growth performance, pigmentation, antioxidant capacity and meat quality in broiler chickens vol.30, pp.1, 2016, https://doi.org/10.5713/ajas.16.0075
  16. Lutein protects against β-amyloid peptide-induced oxidative stress in cerebrovascular endothelial cells through modulation of Nrf-2 and NF-κb vol.33, pp.1, 2017, https://doi.org/10.1007/s10565-016-9360-y
  17. Effects of dietary supplementation with carnosine on meat quality and antioxidant capacity in broiler chickens vol.58, pp.1, 2017, https://doi.org/10.1080/00071668.2016.1237767
  18. Molecular Anti-inflammatory Mechanisms of Retinoids and Carotenoids in Alzheimer’s Disease: a Review of Current Evidence vol.61, pp.3, 2017, https://doi.org/10.1007/s12031-016-0857-x
  19. Effects of dietary supplementation with carnosine on growth performance, meat quality, antioxidant capacity and muscle fiber characteristics in broiler chickens vol.97, pp.11, 2017, https://doi.org/10.1002/jsfa.8236
  20. The Potential of Non-Provitamin A Carotenoids for the Prevention and Treatment of Non-Alcoholic Fatty Liver Disease vol.5, pp.4, 2016, https://doi.org/10.3390/biology5040042
  21. Potential of Dietary Non-Provitamin A Carotenoids in the Prevention and Treatment of Diabetic Microvascular Complications vol.7, pp.1, 2016, https://doi.org/10.3945/an.115.009803
  22. Recent Advances in Studies on the Therapeutic Potential of Dietary Carotenoids in Neurodegenerative Diseases vol.2018, pp.1942-0994, 2018, https://doi.org/10.1155/2018/4120458
  23. Burn-Induced Multiple Organ Injury and Protective Effect of Lutein in Rats vol.41, pp.3, 2018, https://doi.org/10.1007/s10753-018-0730-x
  24. The effect of dietary supplementation with the natural carotenoids curcumin and lutein on pigmentation, oxidative stability and quality of meat from broiler chickens affected by a coccidiosis challeng vol.55, pp.4, 2012, https://doi.org/10.1080/00071668.2014.925537
  25. Incorporation of lutein and docosahexaenoic acid from dietary microalgae into the retina in quail vol.66, pp.2, 2012, https://doi.org/10.3109/09637486.2014.971227
  26. Antioxidative and anti-inflammatory activity of functional foods vol.2, pp.None, 2012, https://doi.org/10.1016/j.cofs.2014.11.002
  27. Effect of Intramuscular Injection on Oxidative Homeostasis in Laboratory Guinea Pig Model vol.59, pp.2, 2012, https://doi.org/10.14712/18059694.2016.90
  28. Ameliorative Effect of Spinach on Non-Alcoholic Fatty Liver Disease Induced in Rats by a High-Fat Diet vol.20, pp.7, 2012, https://doi.org/10.3390/ijms20071662
  29. Comparison of Carotenoids for Their Antifibrogenic Effects in Hepatic Stellate Cells vol.54, pp.6, 2012, https://doi.org/10.1002/lipd.12157
  30. Nutritional Importance of Carotenoids and Their Effect on Liver Health: A Review vol.8, pp.7, 2012, https://doi.org/10.3390/antiox8070229
  31. Effects of Andaliman (Zantoxylumachantopodium, DC) Supplementation on Broiler Immunity vol.1477, pp.None, 2020, https://doi.org/10.1088/1742-6596/1477/7/072009
  32. Dietary Supplementation with Pioglitazone Hydrochloride and Resveratrol Improves Meat Quality and Antioxidant Capacity of Broiler Chickens vol.10, pp.7, 2012, https://doi.org/10.3390/app10072452
  33. Ethanolic extract of mango seed used in the feeding of broilers: effects on phenolic compounds, antioxidant activity, and meat quality vol.100, pp.2, 2012, https://doi.org/10.1139/cjas-2018-0120
  34. Anti-Apoptotic Effects of Carotenoids in Neurodegeneration vol.25, pp.15, 2020, https://doi.org/10.3390/molecules25153453
  35. Consumption of Spinach and Tomato Modifies Lipid Metabolism, Reducing Hepatic Steatosis in Rats vol.9, pp.11, 2020, https://doi.org/10.3390/antiox9111041
  36. Effects of anthocyanin, astaxanthin, and lutein on eye functions: a randomized, double-blind, placebo-controlled study vol.69, pp.1, 2012, https://doi.org/10.3164/jcbn.20-149
  37. Impact of Fermented or Enzymatically Fermented Dried Olive Pomace on Growth, Expression of Digestive Enzyme and Glucose Transporter Genes, Oxidative Stability of Frozen Meat, and Economic Efficiency o vol.8, pp.None, 2012, https://doi.org/10.3389/fvets.2021.644325
  38. Beyond the Liver: Liver-Eye Communication in Clinical and Experimental Aspects vol.8, pp.None, 2012, https://doi.org/10.3389/fmolb.2021.823277
  39. Lutein Exerts Antioxidant and Anti-Inflammatory Effects and Influences Iron Utilization of BV-2 Microglia vol.10, pp.3, 2012, https://doi.org/10.3390/antiox10030363
  40. Dietary supplementation with pioglitazone hydrochloride and l-carnosine improves the growth performance, muscle fatty acid profiles and shelf life of yellow-feathered broiler chickens vol.7, pp.1, 2021, https://doi.org/10.1016/j.aninu.2020.05.011
  41. Lutein as a Modulator of Oxidative Stress-Mediated Inflammatory Diseases vol.10, pp.9, 2012, https://doi.org/10.3390/antiox10091448
  42. Anti-Inflammatory and Anticancer Effects of Microalgal Carotenoids vol.19, pp.10, 2012, https://doi.org/10.3390/md19100531