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Tocopherol from Seeds of Cucurbita Pepo Against Diabetes: Validation by in Vivo Experiments Supported by Computational Docking

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Tocopherol from Seeds of Cucurbita Pepo Against Diabetes: Validation by in Vivo Experiments Supported by Computational Docking Journal of the Formosan Medical Association (2013) 112, 676e690 Available online at www.sciencedirect.com ScienceDirect journal homepage: www.jfma-online.com ORIGINAL ARTICLE Tocopherol from seeds of Cucurbita pepo against diabetes: Validation by in vivo experiments supported by computational docking Sudhanshu Kumar Bharti a,f, Amit Kumar b,f, Neeraj Kumar Sharma a, Om Prakash b, Sudhir Kumar Jaiswal a, Supriya Krishnan c, Ashok Kumar Gupta a,d,*, Awanish Kumar d,e,** a Department of Biochemistry, Patna University, Patna, Bihar, India b School of Computational and Integrative Sciences, Jawaharlal Nehru University, New Delhi, India c Department of Psychology, Banaras Hindu University, Varanasi, Uttar Pradesh, India d Department of Biotechnology, National Institute of Pharmaceutical Education and Research (NIPER), Hajipur, Bihar, India e Department of Biotechnology, National Institute of Technology, Raipur, Chhattisgarh, India Received 25 January 2013; received in revised form 13 August 2013; accepted 13 August 2013 KEYWORDS Background/purpose: Tocopherol from raw pumpkin seeds has been reported to be effective in antidiabetic; the alleviation of diabetes through its antioxidant activities. This study evaluates the antidia- Cucurbita pepo seed; betic activities of the tocopherol fraction of raw seeds of Cucurbita pepo L. (CPSE) in a dia- docking; betic rat model. In addition, the putative action mechanisms of its botanicals were HPLC; computationally investigated. PPAR-g Methods: Seed water activity (Aw) was assessed. Tocopherol was extracted and quantified from raw seed oil. The effect of CPSE was studied in poloxamer-407 (PX-407)-induced type 2 diabetic Wistar rats. Glycemic, insulinemic, and lipid profiles, as well as lipid peroxidation sta- tus, were evaluated. Glucagon like peptide-1 (GLP-1) content in the cecum was evaluated and * Corresponding author. Department of Biochemistry, Patna University, Patna, Bihar, India. ** Corresponding author. Department of Biotechnology, National Institute of Pharmaceutical Education and Research (NIPER), Hajipur, Bihar, India. E-mail addresses: [email protected] (A.K. Gupta), [email protected] (A. Kumar). URL: URL: http://awanikbt.nitrr.ac.in.http://awanikbt.nitrr.ac.in. f These authors contributed equally to this work. 0929-6646/$ - see front matter Copyright ª 2013, Elsevier Taiwan LLC & Formosan Medical Association. All rights reserved. http://dx.doi.org/10.1016/j.jfma.2013.08.003 In vivo and in silico validation of Cucurbita pepo tocopherol 677 histopathological analysis of the pancreas was performed. Further, HYBRID and FRED docking were performed for 10 documented CPSE botanicals, for putative action mechanisms concern- ing three proteins [protein-tyrosine phosphatase 1B (PTP-1B), peroxisome proliferator- activated receptor gamma (PPAR-g), and dipeptidyl peptidase IV (DPP-IV)] known to have dia- betic therapeutic potential. Results: The Aw of raw seeds was found to be 0.544 Æ 0.002. Using tocopherol standards, HPLC determination of CPSE revealed the presence of tocopherol isomers (a, b, g,andd). The tocopherol content was found to be 107.4 Æ 2.9 mg/100 g of CPSE. When compared to diabetic control (DC) rats, the CPSE-treated diabetic rats presented a significant amelioration of glyce- mia, insulinemia, and lipid dysmetabolism. A remarkable reduction in oxidative markers and improved cecal and pancreatic characteristics were also observed. Tocopherol isomers have shown a considerable interaction potential with the aforesaid proteins in docking. Conclusion: The results provide pharmacological evidence of CPSE as an antihyperglycemic mediated by the interaction of various botanicals with multiple targets operating in diabetes mellitus (DM). Copyright ª 2013, Elsevier Taiwan LLC & Formosan Medical Association. All rights reserved. Introduction nutraceutical due to its macro- and micro-constituent composition. The seed oil is a rich source of proteins, diverse fatty acids, and antioxidant vitamins, such as Type 2 diabetes mellitus (T2DM) is a chronic metabolic dis- 12e14 order characterized by abnormalities of glucose homeostasis carotenoids and tocopherols. It has been documented by various organs. It accounts for about 85e95% of all diag- that the tocopherol content of the oil ranged from 27 mg/ nosed cases of diabetes and is associated with considerable gto75mg/g of oil for a-tocopherol, from 75 mg/g to 493 mg/g for g-tocopherol, and from 35 mg/g to 1110 mg/g morbidity and mortality. Several treatment strategies are 14,15 being adopted to ameliorate T2DM by therapeutic inter- for d-tocopherol. So far, several pharmacological 1e3 properties of pumpkin have been reported including vention. Synthetic drugs, despite having excellent po- 16,17 17 18 tencies, had offered unwanted therapeutic profiles marked lipid-lowering, hepatoprotective, anticarcinogenic, antimicrobial,19 and treatment of urination disorders,20 in by fluid retention, drug-induced hypoglycemia, liver mal- 20e25 functioning, weight gain, and cardiac dysfunction.4 addition to antidiabetic and antioxidant activities. Extensive research has been carried out worldwide on Despite of the folkloric use of seed extract of C. pepo, rational drug design,5 to identify and optimize new leads there is insufficient supporting scientific data forming the for molecular targets of T2DM, such as nuclear receptor basis of the present investigation. It systematically evalu- peroxisome proliferator-activated receptor gamma (PPAR- ates the beneficial effects of the tocopherol fraction of g),6,7 human incretin-degrading enzyme dipeptidyl pepti- pumpkin seed oil in vivo in poloxamer-407 (PX-407)-induced dase IV (DPP-IV),5,8 and protein-tyrosine phosphatase 1B diabetic Wistar rats. Intraperitoneal administration of the (PTP1 B).5,9 The PPAR-g regulates glucose metabolism and nonionic copolymer PX-407 in rats induces hyperglycemia fatty acid storage by enhancing the insulin action.5e7 The with impaired response and loss of b-cell sensitivity to glucose, which is considered as a useful diabetic model to DPP-IV is a membrane-bound, serine protease ectoenzyme 26 responsible for the degradation and inactivation of a study the activity of antihyperglycemic agents. In addi- tion, in silico molecular docking was performed using number of glucose regulating incretin hormones, like 27 28 glucagon like peptide-1 (GLP-1). GLP-1 causes an increase HYBRID and FRED programs, to propose the interaction in the amount of insulin released from pancreatic b- potential of 10 botanicals from C. pepo seeds, documented cells.5e8 Thus, diabetic conditions can be reduced either by hitherto concerning three proteins (PTP-1B, PPAR-g, and injecting an excess of GLP-1 or its analogues, inhibiting the DPP-IV) known to have diabetic therapeutic potential. action of DPP-IV.10 PTP-1B inhibitors have emerged as a promising potential therapeutic target for T2DM, as they are negative regulators of the insulin signaling pathway and Methods regulate lipogenesis and hypertriglyceridemia.5,9 These therapeutic targets may improve the efficacy-to- Chemicals safety ratio, resulting in durable maintenance of glycemic control in the majority of people with diabetes. Numerous PX-407, heparin, glucose oxidase, peroxidase, o-dia- structurally unrelated natural products, including alkaloids and nisidine, bovine serum albumin, Coomassie brilliant blue G- flavonoids, have been described to interact with these target 250, cysteine hydrochloride, thiosemicarbazide, and proteins in micromolar concentrations.5,11 Therefore, there is diacetyl monoxime were purchased from Sigma Chemical much scope for herbal medicines, which have emerged as a Co. (St Louis, MO, USA). Tocopherol isomers were pur- safe and relatively economical therapy found to be effective as chased as follows: a-tocopherol e Fluka (Sigma-Aldrich, St. add on therapy, in the long-term management of T2DM.11 Louis, MO, USA), b-tocopherol e Matreya, LLC (Matreya Pumpkin [Cucurbita pepo (C. pepo)] seed oil (about LLC, 168 Tressler St, Pleasant Gap, PA 16823, United 11e31% of total seed content) has been implicated as a States), g-tocopherol and d-tocopherol e Supelco (Sigma- 678 S.K. Bharti et al. Aldrich, St. Louis, MO, USA). The blood glucose diagnostic thermostatted column compartment, an FLD G1321 A kit was purchased from Span Diagnostic Limited, Surat, fluorescence detector (Agilent Technologies, Hewlett- India and the glycosylated hemoglobin (HbA1c) diagnostic Packard-Strasse 8, Waldbronn, Germany) operating at an kit was from Monozyme India Limited, Secunderabad, India. excitation wavelength of 290 nm and an emission wave- The biochemical kits for measuring the lipid profiles were length of 330 nm. The analytical column used was a Phe- procured from Biosys, Bangalore, India and ketamine was nomenex (Torrance, CA, USA) Luna (250 Â 4.60 mm), from Neo Pharmaceuticals, Bangalore, India. The enzyme- packed with 5 mm silica, S/N 00G-4274-E0. The mobile linked immunosorbent assay (ELISA) kit for insulin assay phase used was heptane-THF (1000 þ 40 v/v) at a constant and GLP 1 determination was purchased from Millipore flow rate of 1.0 mL/minute. The injection volume was in Corporation (Linco Research, Inc., St. Charles, MO, USA, the range of 5e100 mL in order for all the tocopherol iso- 63304). Casein (refined grade) was procured from Nimesh mers to elute in the calibration range. The retention times Corporation (Mumbai, India). The salt mixture was procured of a-tocopherol and g-tocopherol were in the range of from SISCO Research Laboratories
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