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Glycosaminoglycan Derived from Field Cricket and Its Inhibition Activity of Diabetes Based on Anti-Oxidative Action

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Glycosaminoglycan Derived from Field Cricket and Its Inhibition Activity of Diabetes Based on Anti-Oxidative Action Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 Glycosaminoglycan derived from field cricket and its inhibition 2 activity of diabetes based on anti-oxidative action 3 1 1 1 2 4 Mi Young Ahn , Ban Ji Kim , Ha Jeong Kim , Jang Mi Jin , Hyung Joo 1 1 3 5 Yoon , Jae Sam Hwang and Byung Mu Lee 1 6 Department of Agricultural Biology, National Academy of Agricultural Science, RDA, 7 Wanju-Gun 55365, South Korea; [email protected] (MYA); [email protected] (BJK.); 8 [email protected] (HJK); [email protected] (HJY); [email protected] (JSH) 2 9 Korean Basic Science Institute, Ochang 863-883, South Korea; [email protected] 3 10 Division of Toxicology, College of Pharmacy, Sungkyunkwan University, Suwon, 440-746, 11 South Korea; [email protected] 12 Running title: Anti-oxidative effect of cricket glycan in db mice 13 14 Prepared for Nutrients 15 *Address correspondence to: Mi Young Ahn, 16 Department of Agricultural Biology, 17 National Academy of Agricultural Science, RDA, 166 18 Nongsaengmyung-Ro, Iseo-Myun, Wanju-Gun, 55365, South Korea, 19 Telephone: 82-63-238-2975. 20 Fax: 82-63-238-3833. 21 E-mail: [email protected] 22 1 © 2019 by the author(s). Distributed under a Creative Commons CC BY license. Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 Abstract: Field cricket (Gryllus bimaculatus) is newly emerged as an edible insect in 2 several countries. Anti-inflammatory effect of glycosaminoglycan derived this cricket was 3 not fully investigated on chronic disease animal model such as diabetic mouse. 4 For potential therapeutic agents, anti-diabetic activities of field cricket glycosaminoglycan 5 (GbG) was evaluated in diabetic mice based on their abilities to reduce glucose, ALT, AST, 6 LDL-cholesterol, and BUN levels, compared with dung beetle (Catharsius molossus) 7 glycosaminoglycan (CaG) as a positive control glycosaminoglycan. Db mice were orally 8 administered for one month according to their groups: Db Hetero (normal), Db Homo (type-2 9 diabetic), CaG (5 mg/kg), GbG (5 mg/kg), and metformin (10 mg/kg). 10 Blood glucose level was decreased after 1st week treatment with GbG. It also inhibited LDL- 11 cholesterol and alkaline phosphatase levels. Regarding oxidative damage of diabetic state, 12 levels of hepatocellular biomarkers levels and protein carbonyl content were reduced in db 13 mice treated with GbG. Especially anti-oxidative activities of catalase, superoxide dismutase, 14 and glutathione peroxidase were significantly increased in GbG treated group compared to 15 those in the control. GbG was composed of heparin disaccharides and main N-glycan was 16 identified as Hex9GlcNAc2 (m/z 1905.7) of with neutral mono-sugar mainly comprising of 17 hexose, L (+) rhamnose by mass spectroscopy. 18 These results from sero-biochemical, hepatocellular anti-oxidant assay in db mice data 19 suggest cricket (G. bimaculatus) glycosaminoglycan might play a role in its anti-diabetic 20 action. 21 Keywords: cricket glycosaminoglycan, N-glycan, homo db mice, anti-oxidant enzyme. 22 2 Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 1. Introduction 2 The custom of eating of insects has come to be spread worldwide. Edible crickets acquired 3 from industrial rearing systems are an alternative food increasingly used in countries 4 including the Netherlands and several others. Gryllus bimaculatus (field cricket, Gb) water 5 extract has been used in Oriental medicine as a crude drug for an antifebrile and lowering 6 agent for high blood pressure. Recently, this extracts from this cricket, have the lowering 7 activity of blood ethanol metabolite concentrations by enhancing the liver mitochondrial 8 alcohol and acetaldehyde dehydrogenases [1] and anti-obesity effect through the inhibition of 9 adipose tissue accumulation in high fat diet rats [2]. Recently, we found a significant report 10 on showing good result effects by consuming crickets: edible cricket consumption on gut 11 microbiota in healthy adults [3]. We are concerned about the type-2 diabetes is related with 12 oxidative stress and influenced vascular disease such as a chronic disease, atherosclerosis, 13 hypertension and nephropathy [4]. 14 The antioxidant and anti-inflammatory activities of enzymatic hydrolysates and peptide 15 fractions from selected heat-treated edible insects including cricket have been ascertained [5] 16 with exception of other carbohydrate components of field cricket. Indeed, all human cells 17 were coated with an array of glycoproteins, glycolipids and polysaccharides named 18 glycocalyx, the surface proteoglycan/glycoprotein layer [6]. Therefore, glycans can appeal 19 distinct properties as biomarker targets [7]; especially N-glycans are also ubiquitous in nature 3 Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 providing structural and functional stability to N-linked glycoprotein, with flexibility [8]. 2 In the overview of a total insect component survey concept, as one of the functional 3 components, a mucin polysaccharide, glycosaminoglycan as an ingredient, is required to 4 standardize and to manufacture not from a versatile natural source but from the same 5 conditions of insect rearing. The distinctive role of Gb glycosaminoglycan has been reported 6 as an anti-inflammatory effect in arthritis induced rat model [9], anti-obesity [10] and 7 antilipidemic [11] effects in a high-fat diet. Nowadays, some glycosaminoglycans so retained 8 anti-oxidant activity robust enough for that they scavenge free radicals thus repaired cellular 9 oxidative damages [12]. 10 We commonly use db/db mouse model to conduct research in this experiment on type 2 11 diabetes mellitus and its comorbidities including obesity and hypertension [13]. Hence, there 12 are some reports that a kind of glycosaminoglycan, heparin sulfate, plays a crucial role in 13 proliferation, development and maturation of beta-cells thereby contributing to normal 14 glucose hemostasis [14] and mouse cell survival in the autoimmune type 1 diabetes [15]. 15 Here, this G. bimaculatus glycosaminoglycan with anti-oxidant activities endeavored to 16 contribute to anti-diabetic activities thus to repair cellular oxidative damage in protein 17 carbonyl level and anti-oxidant enzyme induction ratios after treatment in db/db mice. 18 As a comparable insect glycosaminoglycan sample, following to a previous report, the 19 dung beetle (Catharsius molossus, Ca) GAG with marked anti-aging activity by reducing 4 Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 oxidative damage in aged rats [16], was used as a positive control. In this work, we also 2 characterized purified N-glycans throughout deglycosylation of GbG and analysis by MS and 3 MS/MS (MALDI TOF MS). In this study, we found that field cricket revealed elements 4 constituting glycosaminoglycan and displayed anti-oxidative activity for use as an anti- 5 diabetic agent with reducing cellular oxidative damages. 6 2. Materials and Methods 7 2.1.Preparation of field cricket glycosaminoglycan 8 Field cricket (Gryllus bimaculatus) was supplied from a cricket farm located in Hwasung, 9 South Korea. These insects were freeze-dried, in the Department of Agricultural Biology, 10 National Academy of Agricultural Science (NAAS), South Korea. Dried dung beetle (C. 11 molossus) was purchased at a local market in China by Chinese phamacognosist and posted 12 to NAAS. 13 These each insect glycosaminoglycan was purified by previous reported method [17] 14 using removal of fat by ethanol and acetone, protein enzymatic hydrolysis by putting Alcalase 15 (Sigma Aldrich, St. Louis, Mo., USA), protein precipitation by trichloroacetic acid (5%), 16 impure materials cleansing with detergent, cetylpyridinium chloride (5%), dissolving of non- 17 glycosaminoglycan with 2.5 M NaCl. We added five volumes of ethanol followed by 18 centrifugation at 8000 g for 30 min. Thus the precipitate was then dissolved in water and then 19 dialyzed against 100 volumes of water and freeze-dried. We loaded crude field cricket or 5 Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 dung beetle GAG onto a DEAE Sephadex A-25 gel chromatography column to be 2 equilibrated with 50 mM phosphate buffer (pH 7.4) using a linear sodium chloride gradient 3 from 0 to 2.5 M NaCl. Dialyzed these glycosaminoglycan was freeze-dried to obtain pure 4 GAG. Main peak of digested GbGAG by co-incubation with heparinase I, II and III was 5 pooled using strong anion exchange (SAX) column (Phenomenex, 5m, 250 x 10.0 mm, 6 Torrance, CA, USA) by high performance liquid chromatography (HPLC), determined its 7 purity and compared with heparin disaccharides or carbohydrate standards by ESI (POS 8 polarity) Mass Spectrometer (SYNAPT G2, Waters, U.K.) chromatogram (Time of flight 9 analyzer 50 ~ 1,500 m/z). 10 2.2. N-glycan preparation derived from insect glycosaminoglycan 11 A purified cricket glycosaminoglycan DEAE Sephadex A-25 gel 0.5 M NaCl fraction (GbG 12 0.5M) was further purified in order to obtain a low molecular weight, N-glycan by enzymatic 13 release, and then enrichment of N-glycan via solid-phase extraction. This GbG was denatured 14 by handling of rapid treatment at 100 °C, for 10 minutes in an aqueous solution of 100 mM 15 ammonium bicarbonate with 5 mM dithiothreitol. After cooling, 2.0 L (or 1000 U) of 16 peptide N-glycosidase F (PNGase F) (New England biolabs, Ipsich, MA, USA) was added in 17 order to release N-glycans. The mixture was then incubated in a 37 °C water bath for 16 18 hours. Graphitized carbon cartridges (Extract clean™ carbo, carbograph, Grace davision 19 discovery Sciences, Deerfield, IL, USA) were then washed with 80% acetonitrile/0.10% 6 Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 12 March 2019 doi:10.20944/preprints201903.0136.v1 1 trifluoroacetic acid (v/v) and conditioned with water.
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