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      Cholesterol and Lipoprotein Dynamics in a Hibernating Mammal

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          Abstract

          Hibernating mammals cease feeding during the winter and rely primarily on stored lipids to fuel alternating periods of torpor and arousal. How hibernators manage large fluxes of lipids and sterols over the annual hibernation cycle is poorly understood. The aim of this study was to investigate lipid and cholesterol transport and storage in ground squirrels studied in spring, summer, and several hibernation states. Cholesterol levels in total plasma, HDL and LDL particles were elevated in hibernators compared with spring or summer squirrels. Hibernation increased plasma apolipoprotein A-I expression and HDL particle size. Expression of cholesterol 7 alpha-hydroxylase was 13-fold lower in hibernators than in active season squirrels. Plasma triglycerides were reduced by fasting in spring but not summer squirrels. In hibernators plasma β-hydroxybutyrate was elevated during torpor whereas triglycerides were low relative to normothermic states. We conclude that the switch to a lipid-based metabolism during winter, coupled with reduced capacity to excrete cholesterol creates a closed system in which efficient use of lipoproteins is essential for survival.

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          A rapid method of total lipid extraction and purification.

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            Natural hypometabolism during hibernation and daily torpor in mammals.

            Daily torpor and hibernation are the most powerful measures of endotherms to reduce their energy expenditure. During entrance into these torpid states metabolic rate is suppressed to a fraction of euthermic metabolism, paralleled by reductions in ventilation and heart rate. Body temperature gradually decreases towards the level of ambient temperature. In deep torpor body temperature as well as metabolic rate are controlled at a hypothermic and hypometabolic level. Torpid states are terminated by an arousal where metabolic rate spontaneously returns to normal levels again and euthermic body temperature is established by a burst of heat production. In recent years some of the cellular mechanisms which contribute to hypometabolism have been disclosed. Transcription, translation, as well as protein synthesis are largely suppressed. Cell proliferation in highly proliferating epithelia like the intestine is suspended. ATP production from glucose is reduced and lipids serve as the major substrate for remaining energy requirements. All these changes are rapidly reverted to normometabolism during arousal. Hibernation and daily torpor are found in small mammals inhabiting temperate as well as tropical climates. It indicates that this behaviour is not primarily aimed for cold defense, instead points to a general role of hypometabolism, as a measure to cope with a timely limited or seasonal bottleneck of energy supply.
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              A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism.

              Plasma high density lipoprotein (HDL), which protects against atherosclerosis, is thought to remove cholesterol from peripheral tissues and to deliver cholesteryl esters via a selective uptake pathway to the liver (reverse cholesterol transport) and steroidogenic tissues (e.g., adrenal gland for storage and hormone synthesis). Despite its physiologic and pathophysiologic importance, the cellular metabolism of HDL has not been well defined. The class B, type I scavenger receptor (SR-BI) has been proposed to play an important role in HDL metabolism because (i) it is a cell surface HDL receptor which mediates selective cholesterol uptake in cultured cells, (ii) its physiologically regulated expression is most abundant in the liver and steroidogenic tissues, and (iii) hepatic overexpression dramatically lowers plasma HDL. To test directly the normal role of SR-BI in HDL metabolism, we generated mice with a targeted null mutation in the SR-BI gene. In heterozygous and homozygous mutants relative to wild-type controls, plasma cholesterol concentrations were increased by approximately 31% and 125%, respectively, because of the formation of large, apolipoprotein A-I (apoA-I)-containing particles, and adrenal gland cholesterol content decreased by 42% and 72%, respectively. The plasma concentration of apoA-I, the major protein in HDL, was unchanged in the mutants. This, in conjunction with the increased lipoprotein size, suggests that the increased plasma cholesterol in the mutants was due to decreased selective cholesterol uptake. These results provide strong support for the proposal that in mice the gene encoding SR-BI plays a key role in determining the levels of plasma lipoprotein cholesterol (primarily HDL) and the accumulation of cholesterol stores in the adrenal gland. If it has a similar role in controlling plasma HDL in humans, SR-BI may influence the development and progression of atherosclerosis and may be an attractive candidate for therapeutic intervention in this disease.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                15 December 2011
                : 6
                : 12
                : e29111
                Affiliations
                [1 ]Department of Comparative Biosciences, University of Wisconsin, Madison, Wisconsin, United States of America
                [2 ]Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, United States of America
                [3 ]Department of Nutritional Sciences, University of Wisconsin, Madison, Wisconsin, United States of America
                The University of Queensland, Australia
                Author notes

                Conceived and designed the experiments: JPO DS VAD CLEY HVC. Performed the experiments: JPO DS. Analyzed the data: JPO DS VAD CLEY HVC. Contributed reagents/materials/analysis tools: DS VAD CLEY HVC. Wrote the paper: JPO HVC.

                Article
                PONE-D-11-15849
                10.1371/journal.pone.0029111
                3240636
                22195001
                8846a7b5-d165-4d6f-aef4-e3a037b4b6a5
                Otis et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 13 August 2011
                : 21 November 2011
                Page count
                Pages: 10
                Categories
                Research Article
                Biology
                Biochemistry
                Lipids
                Fats
                Fatty Acids
                Lipid Metabolism
                Sterols
                Metabolism
                Lipid Metabolism
                Proteins
                Lipoproteins
                Apolipoproteins
                Zoology
                Animal Physiology
                Mammalogy

                Uncategorized
                Uncategorized

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