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Cideb Regulates Diet-Induced Obesityˈliver Steatosis and Insulin Sensitivity by Controlling Lipogenesis and Fatty Acid Oxidation

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Cideb Regulates Diet-Induced Obesityˈliver Steatosis and Insulin Sensitivity by Controlling Lipogenesis and Fatty Acid Oxidation Diabetes Publish Ahead of Print, published online July 23, 2007 Cideb regulates diet-induced obesityˈliver steatosis and insulin sensitivity by controlling lipogenesis and fatty acid oxidation John Zhong Li1*, Jing Ye2, 3 *, Bofu Xue1, Jingzhong Qi2, Jing Zhang3, Zhihong Zhou4, Qing Li3, Zilong Wen4, and Peng Li1, 2# 1Department of Biology, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong; 2Department of Biological Sciences and Biotechnology, Tsinghua University, Beijing,100084, China; 3Department of Pathology, Fourth Military Medical University, Xi’an, China; 4Institute of Molecular and Cell Biology, Singapore; *Those authors contribute equally to this work. # To whom correspondence should be addressed: Dr. Peng Li: Department of Biological Sciences and Biotechnology, Tsinghua University, Beijing, China [email protected] Received for publication 11 January 2007 and accepted in revised form 29 June 2007. Additional information for this article can be found in an online appendix at http://diabetes.diabetesjournals.org. Copyright American Diabetes Association, Inc., 2007 Abstract Our previous study suggests that Cidea, a member of Cide family proteins that share sequence homology with the DNA fragmentation factor and expressed at high levels in brown adipose tissue, plays an important role in the development of obesity. Cideb, another member of Cide family protein, is highly expressed in the liver. Objective˖We would like to understand the physiological role of Cideb in the regulation of energy expenditure and lipid metabolism. Research design and Method: We generated Cideb-null mice by homologues recombination and then fed both wild type and Cideb-null mice with high-fat diet (58% fat). We then characterized the animals’ adiposity index, food intake, whole body metabolic rate, liver morphology, rate of fatty acid synthesis and oxidation, insulin sensitivity and gene expression profile. Result: Cideb-null mice had lower levels of plasma triglycerides, free fatty acids, and are resistant to high-fat diet– induced obesity and live steatosis. In addition, Cideb mutant mice displayed significantly increased insulin sensitivity and enhanced rate of whole body metabolism and hepatic fatty acid oxidation. More importantlyˈCideb-null mice showed decreased lipogenesis and reduced expression levels of acetyl-CoA carboxylaseˈfatty acid synthase and stearol-CoA desaturase. We further demonstrated that expression levels of sterol response element binding protein 1c (SREBP1c) was significantly decreased in Cideb deficient mice. Conclusion: Our data demonstrated that Cideb is a novel important regulator in lipid metabolism in the liver. Cideb may represent a new therapeutic target for the treatment of obesity, diabetes and liver steatosis. Key words: Cideb, obesity, insulin sensitivity, liver steatosis, fatty acid oxidationˈlipogenesis, SREBP1c, ACC2 Obesity represents excessive amount of diabetes and liver steatosis. For example, body fat and is a result of imbalance ACC2-/- mice have a higher rate of fatty between energy intake and expenditure. acid oxidation (7) and are resistant to high It affects a large population in the world fat diet-induced obesity and diabetes (3). and is a major risk for many metabolic Mice with stearol-CoA desaturase (SCD1) diseases such as hypertension, stroke, deficiency, an enzyme catalyzing the liver steatosis and even cancer. In desatuation process of palmitic acid to particular, obesity has been closely unsaturated fatty acids, have an increased associated with insulin resistance and the fatty acid oxidation, reduced body development of type 2 diabetes. Liver adiposity, increased insulin sensitivity, and plays a central role in energy are resistant to diet-induced obesity and homeostasis as it is the main organ for liver steatosis (8,9). Targeted over lipid de novo synthesis, lipid uptake and expression of a constitutively active nuclear secretion, fatty acid oxidation, as well as form of SREBP-1c in the liver resulted in the production of ketone bodies (1). It is the activation of an array of downstream also an important organ for glucose target genes and fatty liver formation (10). synthesis (gluconeogenesis) and storage (glycogen synthesis). Fatty acid Cide proteins, including Cidea, Cideb and oxidation in the liver begins with the Fsp27 (Cidec), share homology with the formation of fatty acyl-CoA, which is DNA fragmentation factor DFF40/45 at the subsequently transported into the N-terminal region (11). Our previous data mitochondria by the carnitine palmitoyl- revealed that Cidea is expressed at high transferase (CPT1/CPT2) shuttle-system levels in brown adipose tissues (BAT) and (2). CPT1 activity is inhibited by Cidea null mice exhibit higher energy malonyl-CoA, the product of acetyl-CoA expenditure, enhanced lipolysis in BAT, and carboxylase-2 (ACC2) in mitochondria are resistant to high-fat-diet induced obesity (3). Hepatic mitochondrial ȕ-oxidation and diabetes (12). Recently, Cidea was of fatty acids provides energy, especially shown to mediate human obesity by during fasting conditions. The regulation regulating human adipocyte lipolysis (13) of lipid metabolism in liver is controlled and a V115F polymorphism in human was by several classes of transcription found to be associated with obesity in factors, such as peroxisome certain population (14). Cideb mRNAs proliferators-activated receptors were detected in various other tissues with (PPARs) (4) and sterol regulatory high expression levels in the liver element-binding proteins (SREBPs) (5). previously (11); however, its biological role SREBP1c is crucial for triacylglycerol is unclear. When over-expressed in synthesis by regulating the expression of heterologous cells, Cideb proteins can form several downstream target genes such as homo-dimmer and induce caspase ACC, fatty acid synthase (FAS) and independent cell death (15). In the present stearol-CoA desaturase1 (SCD1) (5,6). study, we generated Cideb knock-out mice and showed that mice with Cideb Changes of lipid homeostasis in the liver deficiency exhibited increased energy by over-expression or genetic mutation expenditure, improved insulin sensitivity, of a variety of factors often result in and are resistant to high fat diet-induced metabolic defects such as obesity, obesity, hyper-lipidemia, or liver steatosis. Our data reveal a novel pathway in PCR reactions were performed with ABI controlling lipogenesis and fatty acid SYBR® GREEN PCR Master Mix in the oxidation in the liver by Cideb. MX3000PTM real-time PCR system (Stratagene) according to the Research Design and Methods manufacturer’s instruction. The results were Generation of Cideb-null mice and normalized to E-actin level in each sample. maintaining animals. Procedures for Primer sequences are available upon the isolation of genomic clones, request. generation of Cideb deficient mice and Whole-body oxygen consumption, food routine maintenance of mouse strain intake, glucose/insulin tolerance test, were essentially the same as previously adiposity index and blood chemistry. described (12). AnimalV were fed either Whole-body oxygen consumption, normal chow diet (5053, PicoLab® respiration exchange ratio, daily food Rodent Diet 20,) or high-fat diet (HFD, intake, glucose and insulin tolerance tests D12331, 58% of kilocalories from fat, (GTT and ITT, respectively), adiposity Research Diets). During a HFD index were performed as previously treatment, 3-week-old mice were described (12). For blood chemistry, we subjected to HFD feeding for 19 weeks. measured serum levels of triglycerides For fasting and re-feeding experiments, (TAG), non-esterified fatty acids (NEFA), mice in the fasting group were fasted for insulin, leptin and glucose as previously 24h, in refeeding group were fasted for described (12). We using commercial kit to 24h and then allowed access to food and determine serum levels of ketone bodies water for 12h before analysis (16). All (Wako Chemical), adiponectin and resistin mouse research activities were reviewed (LINCO Research, USA), respectively. and approved by the animal research Western blot analysis, ACC activity and committee in the Hong Kong University Insulin infusion. Rabbit polyclonal of Science and Technology and Tsinghua antibody against mouse Cideb was University. generated by injecting His-tagged truncated Southern-blot, genotyping by PCR Cideb protein (aa 1-176) to rabbit as analysis, RNA extraction and real- previously described (18). Western blot time quantitative RT-PCR analysis. analysis was performed essentially the same Genomic DNA was isolated from mouse as previously described (12). Liver nuclear tails and was subjected Southern-blot and membrane extracts were prepared as analysis as previously described (17). previously described (19). Detail The DNA fragment between the AvrII information of antibodies used for western and NcoI sites (Fig. 1A) of Cideb blot analysis was shown on-line appendix. genomic DNA were used as a probe. :estern blot signal was quantified by PCR analysis was used as a routine AlphaEase software (Alpha Innotech, San method for genotyping. Total RNA was Leandro, CA). A&& activity was determined isolated using the TRIzol reagent using the [14C] bicarbonate fixation assay (Invitrogen, Carlsbad, CA). The First- (20). Insulin infusion experiment was strand cDNA were synthesized from 1 performed using mice that were fasted for μg of total RNA with oligo-(dT)20 fours through portal vein for 3 min as primers using Superscript
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