β-Carotene oxygenase 1 activity modulates circulating cholesterol concentrations in mice and humans
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Background: Plasma cholesterol is one of the strongest risk factors associated with the development of atherosclerotic cardiovascular disease (ASCVD) and myocardial infarction. Human studies suggest that elevated plasma β-carotene is associated with reductions in circulating cholesterol and the risk of myocardial infarction. The molecular mechanisms underlying these observations are unknown. Objective: The objective of this study was to determine the impact of dietary β-carotene and the activity of β-carotene oxygenase 1 (BCO1), which is the enzyme responsible for the conversion of β-carotene to vitamin A, on circulating cholesterol concentration. Methods: In our preclinical study, we compared the effects of a 10-d intervention with a diet containing 50 mg/kg of β-carotene on plasma cholesterol in 5-wk-old male and female C57 Black 6 wild-type and congenic BCO1-deficient mice. In our clinical study, we aimed to determine whether 5 common small nucleotide polymorphisms located in the BCO1 locus affected serum cholesterol concentrations in a population of young Mexican adults from the Universities of San Luis Potosí and Illinois: A Multidisciplinary Investigation on Genetics, Obesity, and Social-Environment (UP AMIGOS) cohort. Results: Upon β-carotene feeding, Bco1−/− mice accumulated >20-fold greater plasma β-carotene and had ∼30 mg/dL increased circulating total cholesterol (P < 0.01) and non-HDL cholesterol (P < 0.01) than wild-type congenic mice. Our results in the UP AMIGOS cohort show that the rs6564851 allele of BCO1, which has been linked to BCO1 enzymatic activity, was associated with a reduction in 10 mg/dL total cholesterol concentrations (P = 0.009) when adjusted for vitamin A and carotenoid intakes. Non-HDL-cholesterol concentration was also reduced by 10 mg/dL when the data were adjusted for vitamin A and total carotenoid intakes (P = 0.002), or vitamin A and β-carotene intakes (P = 0.002). Conclusions: Overall, our results in mice and young adults show that BCO1 activity impacts circulating cholesterol concentration, linking vitamin A formation with the risk of developing ASCVD. Copyright © The Author(s) on behalf of the American Society for Nutrition 2020.
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Atherosclerosis; Genetic variants; Micronutrients; Nutrition; Retinoic acid beta carotene; beta carotene oxygenase 1; carotenoid; cholesterol; glycerol 3 phosphate dehydrogenase; high density lipoprotein cholesterol; plasma retinol binding protein; plasma retinol binding protein 4; retinol; triacylglycerol; unclassified drug; Bco1 protein, mouse; BCO2 protein, human; beta carotene; beta carotene 15,15' monooxygenase; cholesterol; dioxygenase; adult; animal experiment; Article; cholesterol blood level; colorimetry; controlled study; diet composition; enzyme activity; female; food frequency questionnaire; gene linkage disequilibrium; genetic association; high density lipoprotein cholesterol level; high performance liquid chromatography; human; human experiment; male; Mexican; mouse; nonhuman; normal human; triacylglycerol blood level; young adult; adolescent; animal; blood; C57BL mouse; genetics; knockout mouse; metabolism; Adolescent; Animals; beta Carotene; beta-Carotene 15,15'-Monooxygenase; Cholesterol; Dioxygenases; Female; Humans; Male; Mice; Mice, Inbred C57BL; Mice, Knockout
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