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Ulomoides Dermestoides) Fat Improves Diabetes: Effect on Liver and Pancreatic Architecture and on Pparg Expression

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Ulomoides Dermestoides) Fat Improves Diabetes: Effect on Liver and Pancreatic Architecture and on Pparg Expression Brazilian Journal of Medical and Biological Research (2018) 51(6): e7238, http://dx.doi.org/10.1590/1414-431X20187238 ISSN 1414-431X Research Article 1/12 Beetle (Ulomoides dermestoides) fat improves diabetes: effect on liver and pancreatic architecture and on PPARg expression E.I. Jasso-Villagomez1, M. Garcia-Lorenzana2, J.C. Almanza-Perez1, M.A. Fortis-Barrera1, G. Blancas-Flores1, R. Roman-Ramos1, L.A. Prado-Barragan3* and F.J. Alarcon-Aguilar1* 1Laboratory of Pharmacology, Department of Health Sciences, Division of Health and Biological Sciences, Metropolitan Autonomous University of Iztapalapa, Mexico City, Mexico 2Laboratory of Tissue Neurobiology, Department of Reproduction Biology, Division of Health and Biological Sciences, Metropolitan Autonomous University of Iztapalapa, Mexico City, Mexico 3Laboratory of Solid State Fermentation, Department of Biotechnology, Division of Health and Biological Sciences, Metropolitan Autonomous University of Iztapalapa, Mexico City, Mexico Abstract Ulomoides dermestoides is a beetle traditionally consumed to treat diabetes. In this study, we performed a composition analysis of U. dermestoides to obtain the principal fractions, which were used to assess the effect on glycemia, liver and pancreatic architecture, and PPARg and GLUT4 expression. Normal mice and alloxan-induced diabetic mice were administered fractions of chitin, protein or fat, and the acute hypoglycemic effect was evaluated. A subacute study involving daily administration of these fractions to diabetic mice was also performed over 30 days, after which the liver and pancreas were processed by conventional histological techniques and stained with hematoxylin and eosin to evaluate morphological changes. The most active fraction, the fat fraction, was analyzed by gas chromatography–mass spectrometry (GC–MS), and PPARg and GLUT4 mRNA expressions were determined in 3T3-L1 adipocytes. The protein and fat fractions exhibited hypoglycemic effects in the acute as well as in the 30-day study. Only the fat fraction led to elevated insulin levels and reduced glycemia, as well as lower intake of water and food. In the liver, we observed recovery of close hepatic cords in the central lobule vein following treatment with the fat fraction, while in the pancreas there was an increased density and percentage of islets and number of cells per islet, suggesting cellular regeneration. The GC–MS analysis of fat revealed three fatty acids as the major components. Finally, increased expression of PPARg and GLUT4 was observed in 3T3-L1 adipocytes, indicating an antidiabetic effect. Key words: Diabetes; Ulomoides dermestoides; Hypoglycemic agent; Insulin-sensitizing agent; Fatty acids; PPARg Introduction Diabetes mellitus is a metabolic disorder characterized the mobilization of GLUT4, and increases insulin by hyperglycemia, caused by a deficit in the secretion or sensitivity (4). function of insulin (1). Although exogenous insulin and Ulomoides dermestoides Chevrolat, a beetle also other drugs such as peroxisome proliferator-activated known as the ‘‘peanut weevil’’, is used in the traditional receptor gamma (PPARg) agonists may help control medicine of Argentina, Brazil, China, Colombia, Japan, diabetes (1), long-term patients develop progressive com- and Mexico to treat backache, cough, asthma, and diabetes, plications including retinopathy, nephropathy, neuropathy, among others (5,6). The main compounds of the cuticle and cardiovascular disease (2). The worldwide cost of (alkenes and terpenes) and the defensive secretion diabetes is increasing every year (3). Therefore, the (benzoquinones) of this beetle have been characterized development of new treatments to prevent this illness is in previous chemical studies (7), and its adverse anti- important. PPARg is a member of the nuclear hormone inflammatory, cytotoxic, and genotoxic activities have receptor superfamily that regulates glucose and fat been described (6–9). Concerning its use in the control metabolism, ameliorates insulin resistance through of diabetes, it is thought that ingestion of the live adult Correspondence: F.J. Alarcon-Aguilar: <[email protected]> | L.A. Prado Barragan: <[email protected]> *These authors contributed equally to this study. Received October 20, 2017 | Accepted January 15, 2018 Braz J Med Biol Res | doi: 10.1590/1414-431X20187238 Beetle (Ulomoides dermestoides) fat improves diabetes 2/12 beetle induces pancreatic regeneration. However, it remains Isolation of the protein fraction unclear whether U. dermestoides has an effect on glycemia, The resultant supernatant from the chitin extraction and if it is associated with cellular regeneration at the was subjected to acidification (HClconc.) until the iso- pancreatic level or with the activation of PPARg. electric point of the proteins was reached (pH 3). Then, the In the present study, alloxan-induced diabetic mice sample was filtered through Whatman no. 4 filter paper were given the principal fractions of U. dermestoides (chitin, and the insoluble protein fraction was dried and stored at protein, and fat) to evaluate their effects on glycemia after a 2–4°C until use (13). single administration (acute study) and after daily adminis- tration for 30 days (subacute study) for histological analyses Experimental animals of the liver and pancreas. In addition, with the fat fraction, a Male Mus musculus mice of the CD1 strain (35–45 g) gas chromatography-mass spectrometry analysis (CG-MS) were purchased and bred in the Experimental Animal was performed and the changes in mRNA expression of Center at Metropolitan Autonomous University, Mexico. PPARg and GLUT4 were evaluated. Six mice per cage were maintained under a 12/12 h light/ dark period at 22±1°C and relative humidity of 55±3%. Material and Methods Mice were fed a rodent diet containing 18.6% protein, 44.2% carbohydrates, and 6.2% fat (2018s Teklad Global U. dermestoides 18% protein; Harlan Laboratories, USA) and received U. dermestoides beetles were grown to adulthood in a water ad libitum. The handling of the laboratory animals sanitary bed (natural wheat bran) at 25±2°C and fed a and experimental procedures were performed according diet consisting of banana peels and bread. The taxonomic to national and international standards including the authentication of the beetle was performed at the Entomol- Official Mexican Standard (NOM-062-ZOO-999, revised ogy and Acarology Center, Phyto-Sanitary Institute, Post- 2001) and the National Institutes of Health (NIH publica- graduate College of Agricultural Sciences, COLPOS tion No. 8023, revised 1996) for the health, safety and (Mexico). comfort of experimental animals. Additionally, the inter- nal committee of the Metropolitan Autonomous Univer- Composition analysis of U. dermestoides sity approved the experimental animal handling protocol A sample of U. dermestoides was subjected to com- (DCBS.949.2017). position analysis. The moisture, protein, fat, crude fiber, and ash contents were determined according to the Evaluation of the acute hypoglycemic effect of the methods reported by the Association of Official Analytical different fractions of U. dermestoides in normal mice Chemists (10). The moisture content was determined in In previous in vivo assays performed with U. dermes- a thermal scale (OHAUS MB45MR, Switzerland), and the toides, the tested doses of the active extracts ranged from ash content in a muffle (Thermo Scientific, Germany) at 0.6, 3, 8, and 16 mg/kg (9,14). Therefore, in the present 550°C for 4 h. Total protein content was determined by study, only the highest dose (16 mg/kg) was selected to total digestion (Buchi K-350 Distillation Unit, Switzerland). perform all experiments. Thirty experimental animals were The ether extraction of crude fat was performed using fasted for 12 h and grouped as follows: group 1 (control), a Soxhlet extractor (Barlsteadt; Thermo Scientific), and treated with isotonic saline solution (ISS, 4 mL/kg); group crude fiber was quantified using the method described by 2, treated with the fat fraction (16 mg/kg); group 3, treated Hernandez et al. (11). with the protein fraction (16 mg/kg); group 4, treated with the chitin fraction (16 mg/kg); and group 5, positive control, Isolation of the fat fraction treated with glibenclamide (10 mg/kg), a sulphonyl urea Live adult beetles were frozen at –80°C, dehydrated at agent with hypoglycemic action that acts at the pancreatic 60°C and ground to a fine powder. The total fat fraction level as an insulin secretagogue. All treatments were was obtained from 10 g of dried beetle sample by Soxhlet administered by the intraperitoneal (ip) route and glycemia extraction using petroleum ether as the solvent (12). The was quantified from tail vein blood samples at 0, 120, 240, fat fraction was recovered in a rotary evaporator (B490; and 360 min by the dehydrogenase method (Accu-Chekt Buchi, Switzerland). Performa; Roche Diagnostics, USA). Isolation of the chitin fraction Induction of diabetes in mice The defatted sample (7.6 g) was ground and mixed Mice were intravenously administrated a single dose of with 300 mL of 10% NaOH. After incubation at 60°C 70 mg/kg of alloxan (Sigma-Aldrich, USA) dissolved in ISS for 3 h, the slurry was filtered through Whatman no. 4 (15). The control group was treated with ISS only. After filter paper. The precipitate (chitin fraction) was dried at 8 days of drug administration, glycemia was quantified. 60°C and stored in an airtight container at 2–4°C until Only those alloxan-treated mice with blood glucose levels use (11). The supernatant
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