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Egg Oil from Portunus Trituberculatus Improves Insulin Resistance Through Activation of Insulin Signaling in Mice

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Egg Oil from Portunus Trituberculatus Improves Insulin Resistance Through Activation of Insulin Signaling in Mice Applied Physiology, Nutrition, and Metabolism Egg oil from Portunus trituberculatus improves insulin resistance through activation of insulin signaling in mice Journal: Applied Physiology, Nutrition, and Metabolism Manuscript ID apnm-2018-0718.R7 Manuscript Type: Article Date Submitted by the 20-Feb-2019 Author: Complete List of Authors: Hu, Shiwei; Zhejiang Ocean University Wang, Jingfeng; Ocean University of China Yan, Xiaojun; Zhejiang Ocean University Li, Shijie; Zhejiang Ocean University Jiang, Wei;Draft Zhejiang Ocean University Liu, Yu; Zhejiang Ocean University Egg oil, Portunus trituberculatus, constituents, insulin resistance < Keyword: insulin resistance, insulin signaling, obesity < obesity Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? : https://mc06.manuscriptcentral.com/apnm-pubs Page 1 of 34 Applied Physiology, Nutrition, and Metabolism Draft 67x100mm (300 x 300 DPI) https://mc06.manuscriptcentral.com/apnm-pubs Applied Physiology, Nutrition, and Metabolism Page 2 of 34 1 Egg oil from Portunus trituberculatus alleviates insulin 2 resistance through activation of insulin signaling in mice 3 Shiwei Hua, Jingfeng Wangb, Xiaojun Yana*, Huicheng Yangc, Shijie Lia, Wei Jianga, 4 Yu Liua 5 6 aInnovation Application Institute, Zhejiang Ocean University, Zhoushan, Zhoushan, 316022, China. 7 bCollege of Food Science and Engineering, Ocean University of China, Qingdao, Shandong Province 8 266003, China. 9 cZhejiang Marine Development Research Institute, Zhoushan 316021, China Running title: Pt-egg oil improves insulin resistance Corresponding author at: Institute of InnovationDraft & Application, Zhejiang Ocean University, Zhoushan 316002, Chian. Fax: +86 0580 2262063; Tel: +86 0580 2262589; E-mail: [email protected], [email protected]. 1 https://mc06.manuscriptcentral.com/apnm-pubs Page 3 of 34 Applied Physiology, Nutrition, and Metabolism 11 Abstract 12 Marine bioactive lipids have been utilized to overcome insulin resistance. However, oil from 13 swimming crab has never been studied. Here, we analyzed the constituents of egg oil from Portunus 14 trituberculatus (Pt-egg oil) and investigated its protective effects against insulin resistance in mice on a 15 high-fat diet. The results showed that Pt-egg oil contained 52.05% phospholipids, 8.61% free fatty 16 acids (especially eicosapentaenoic acid and docosahexaenoic acid), 32.38% triglyceride, 4.79% total 17 cholesterol, and ditissimus astaxanthin. Animal experiments showed that Pt-egg oil significantly 18 mitigated insulin resistance and was associated with reductions in blood glucose, insulin, glucose 19 tolerance, insulin tolerance, serum lipids, and hepatic glycogen. Pt-egg oil activated the 20 phosphatidylinositol 3-hydroxy kinase (PI3K)/proteinDraft kinase B (Akt)/glucose transporter 4 (Glut4) 21 pathway in skeletal muscle both at the transcriptional level and at the translational level. Pt-egg oil also 22 promoted hepatic glycogen synthesis through activation of the PI3K/Akt/glycogen synthase kinase-3 23 beta (GSK3β) pathway. These indicate that Pt-egg oil can be used as an alternative to marine bioactive 24 lipids, to improve insulin resistance. 25 Keywords: Egg oil; Portunus trituberculatus; constituents; insulin resistance; insulin signaling; obesity 2 https://mc06.manuscriptcentral.com/apnm-pubs Applied Physiology, Nutrition, and Metabolism Page 4 of 34 27 Introduction 28 Insulin resistance underlies the development of several metabolic disorders, such as 29 obesity, cardiovascular disease, type 2 diabetes mellitus, and certain cancers (Czech 30 2017). Insulin resistance occurs when the normal circulating concentration of insulin 31 fails to balance body glucose homeostasis in its target tissues-mainly the liver, skeletal 32 muscle, and adipose tissues (Macdonald 2016). Insulin-dependent glucose disposal 33 primarily takes place in the skeletal muscle: approximately 75%, including glucose 34 translocation (Saltiel and Kahn 2001). The liver precedes resistance in these 35 peripheral tissues, and defects in hepatic glycogen synthesis result from insufficient 36 insulin, which finally causes theDraft disruption of glucose-glycogen homeostasis and 37 hyperinsulinemia (Prada et al. 2018). Therefore, numerous studies on the impaired 38 glucose homeostasis in insulin resistant individuals have been performed in the 39 skeletal muscle and liver (Bai et al. 2015; Wang et al. 2016; Li et al. 2015). 40 Insulin-stimulated glucose disposal is mainly mediated through phosphatidylinositol 41 3-hydroxy kinase (PI3K)/ protein kinase B (Akt) signal transduction (Nandipati et al. 42 2017). Activated Akt protein promotes translocation of glucose transporter 4 (Glut4) 43 from the cytoplasm to the cytomembrane, which provides a tunnel for glucose to enter 44 into cells (Zhang et al. 2017). The phosphorylated Akt also triggers the inactivation of 45 glycogen synthase kinase-3 beta (GSK3β) and subsequent activation of glycogen 46 synthase (GS), finally accelerating glycogen synthesis (Rong Guo et al. 2016). 47 The swimming crab, Portunus trituberculatus, is widely distributed in the coastal 48 waters of China, Japan, Korea, and other East Asian countries (Lv et al. 2017a). This 3 https://mc06.manuscriptcentral.com/apnm-pubs Page 5 of 34 Applied Physiology, Nutrition, and Metabolism 49 crustacean species has become one of the most important economic marine products 50 based on its high nutritive value and high production: more than 100,000 tons in 51 China in 2015 (Lv et al. 2017b). Recent studies on Portunus trituberculatus have 52 focused on its gene sequence analysis or aquaculture (Pan et al. 2016; Ng'ambi et al. 53 2016). Few studies have involved its processing or utilization. Swimming crab eggs 54 contain abundant bioactive lipids, and the biological functions of these lipids have not 55 been revealed, including the effects on insulin resistance. However, inspirations can 56 be taken from the favorable activities of fish oil and shrimp oil (de Castro et al. 2015; 57 Nair et al. 2017). Here, we first separated egg oil from Portunus trituberculatus 58 (Pt-egg oil) and described its composition.Draft The effects of Pt-egg oil on alleviation of 59 insulin resistance were also investigated, especially the molecular mechanism of 60 insulin signal cascades. These may provide some theoretical basis for the utilization of 61 Pt-egg oil as a potent functional ingredient against insulin resistance. 62 Materals and methods 63 Materials and regents 64 Portunus trituberculatus eggs were obtained from Tongqu Aquatic Food Company 65 (Zhoushan, Zhejiang, China). Triglyceride (TG), total cholesterol (TC), free fatty 66 acids (FFAs), glucose, glycosylated haemoglobin (HbA1c), glycogen, and BSA kits 67 were purchased from Biosino (Beijing, China). Insulin ELISA kit was form Invitrogen 68 (Carlsbad, CA, USA). Antibody proteins used in this study were all Cell Signaling 69 products (Beverly, MA, USA). The primers of genes for PCR were synthesized by 70 ShanGon (Shanghai, China). 4 https://mc06.manuscriptcentral.com/apnm-pubs Applied Physiology, Nutrition, and Metabolism Page 6 of 34 71 Preparation of Pt-egg oil 72 Pt-egg oil was extracted from dry Portunus trituberculatus eggs with 95% ethanol 73 (1:6 m/V) for 10 h. After centrifugation, the supernatant was disposed by vacuum 74 concentration to obtain crude lipids. Pt-egg oil was gained through a series of process, 75 including re-concentration, blowing with nitrogen, and dehydration with Na2SO4. 76 Pt-egg oil was stored at -20℃ under nitrogen. 77 Composition of Pt-egg oil 78 TG, TC, and FFAs concentrations in Pt-egg oil were detected using commercial 79 kits. Phospholipid and astaxanthin contents were determined according to the methods 80 described by Xie et al. (2017). Draft 81 Free fatty acids composition analysis in Pt-egg oil 82 FFAs composition in Pt-egg oil was analyzed based on methods described in the 83 literature (Yin et al. 2016). Briefly, esterified Pt-egg oil was produced using 2 M 84 KOH in methanol at 80℃ for 1 h. After cooling to 25℃, further transesterification 85 was performed using 2 M H2SO4 under the same conditions. The upper organic layer 86 was diluted with n-hexane after centrifugation for analysis. The esterifiable Pt-egg oil 87 was analyzed using a gas chromatographic system (7820A, Agilent, Santa Clara, CA, 88 USA) equipped with a hydrogen flame ionization detector (FID) and a FFAP-fused 89 silica capillary column (30 m × 0.53 mm, 1μm). The conditions were as follows: oven 90 temperature, 50 to 100℃ (10℃/min, 1 min), 100 to 150℃ (5℃/min, 5min), and 150 91 to 200℃ (20℃/min); nitrogen (carrier gas), 1 mL/min; FID and injector temperature, 92 250℃; injection volume, 2.0 μL. Fatty acids in the samples were identified by 5 https://mc06.manuscriptcentral.com/apnm-pubs Page 7 of 34 Applied Physiology, Nutrition, and Metabolism 93 comparing the retention times of the sample peaks with those of a mixture of fatty 94 acid methyl ester standards. The FFAs contents were expressed as the weight 95 percentage (% w/w) of the total FFAs detected with chain lengths of 4-22 carbon 96 atoms. 97 Animal experiments 98 Male C57BL/6J mice (licensed ID SCXK2016-0001), 16-18 g, were purchased 99 from Vital River Laboratory Animal Center (Beijing, China). Animals were housed in 100 normal cages at 23 ± 1 ℃ with a 12:12 h light-dark schedule. All experimental 101 protocols used in this study were approved by the ethical committee for experimental 102 animal care at Zhejiang Ocean University.Draft
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