Top

BMC Complementary Medicine and Therapies

Published in:

01-12-2020 | Metformin | Research article

Anti-diabetic activity of field cricket glycosaminoglycan by ameliorating oxidative stress

Authors: Mi Young Ahn, Ban Ji Kim, Ha Jeong Kim, Jang Mi Jin, Hyung Joo Yoon, Jae Sam Hwang, Byung Mu Lee

Published in: BMC Complementary Medicine and Therapies | Issue 1/2020

Abstract

Background

Field cricket (Gryllus bimaculatus) is newly emerged as an edible insect in several countries. Anti-inflammatory effect of glycosaminoglycan derived from this cricket on chronic disease animal model such as diabetic mouse has not been fully investigated yet. Thus, the objective of this study was to determine the anti-oxidative effect of such glycosaminoglycan on diabetic mouse.

Methods

To discover potential therapeutic agents, field cricket glycosaminoglycan (GbG) was tested in the present study. Its anti-oxidative activities in diabetic mice were determined based on its abilities to reduce glucose, ALT, AST, ALP, LDL-cholesterol and BUN levels. Dung beetle (C. molossus) glycosaminoglycan (CaG) was used as a positive control. Db mice were intraperitoneally administered for 1 month according to their group assignments: 1) normal (DB-Hetero); 2) control (DB-Homo); 3) 5 mg/kg treatment of CaG (CaG5); 4) 5 mg/kg treatment of GbG (GbG5); and 5) 10 mg/kg treatment of metformin (Metformin 10).

Results

Blood glucose level decreased after 1st week of treatment with GbG. LDL-cholesterol and alkaline phosphatase levels were also inhibited by GbG. Markers of oxidative damage, such as protein carbonyl content and levels of hepatocellular biomarkers, were reduced in db mice treated with GbG. Especially anti-oxidative activities of catalase, superoxide dismutase and glutathione peroxidase were significantly increased in GbG treated group compared to those in the control (Db Homo). GbG was composed of heparin disaccharides. Its main N-glycan was identified as Hex₉GlcNAc₂ (m/z 1905.7) with neutral mono-sugar mainly comprising of hexose and L (+) rhamnose by mass spectroscopy.

Conclusions

Sero-biochemical and hepatocellular anti-oxidant assay results in db mice suggest that cricket (G. bimaculatus) glycosaminoglycan might possess anti-oxidative effect in diabetic state.

Ahn MY, Lee YW, Ryu KS, Lee HS, Kim I, Kim JW. Effect of water and methanol extracts of cricket (Gyryllus bimaculatus) on alcohol metabolism. Korean J Pharmacogn. 2004;35(2):175–8.

Ahn MY, Kim MJ, Kwon RH, Hwang JS, Park KK. Gene expression profiling and inhibition of adipose tissue accumulation of G. bimaculatus extract in rats on high fat diet. Lipid Health Dis. 2015;14:116.CrossRef

Stull VJ, Finer E, Bergmans RS, Febvre HP, Longhurst C, Manter DK, Patz JA, Weir TL. Impact of edible cricket consumption on gut microbiota in healthy adults, a double-blind randomized crossover trial. Scientic Rep. 2018;8(1):10762.CrossRef

Robson R, Kundur AR, Singh I. Oxidative stress biomarkers in type 2 diabetes mellitus for assessment of cardiovascular disease risk. Diabetes Metab Syndr. 2018;12(3):455–62.PubMedCrossRef

Zielińska E, Baraniak B, Karaś M. Antioxidant and anti-inflammatory activities of hydrolysates and peptide fractions obtained by enzymatic hydrolysis of selected heat-treated edible insects. Nutrients. 2017;9(9):970. https://doi.org/10.3390/nu9090970.PubMedCentralCrossRef

Uchimido R, Schmidt EP, Shapiro NI. The glycocalyx: a novel diagnostic and therapeutic target in sepsis. Crit Care. 2019;23(1):16.PubMedPubMedCentralCrossRef

Yang L, Wu S, Cooper JC, Paul MK, Cummings AL, Eletr ZM, Ben-Arye SL, Padler-Karavani V, Samli KN, Woods RJ. High-specificity affinity reagents for the detection of glycan sialylation. FASEB J. 2018;32(1 supplement):544.16 https://www.fasebj.org/doi/10.1096/fasebj.2018.32.1_supplement.544.16.

Banerjee DK, Zhang Z, Baksi K, Serrano-Negrón JE. Dolichol phosphate mannose synthase: a glycosyltransferase with unity in molecular diversities. Glyconj J. 2017;34(4):467–79.CrossRef

Ahn MY, Han JW, Hwang JS, Yun EY, Lee BM. Anti-inflammatory effect of glycosaminoglycan derived from Gryllus bimaculatus (a type of cricket, insect) on adjuvant-treated chronic arthritis rat model. J Toxicol Environ Health A. 2014;77(22–24):1332–45.PubMedCrossRef

10.

Ahn MY, Kim BJ, Kim HJ, Yoon HJ, Jee SD, Hwang JS, Park KK. Anti-obesity effect of Bombus ignitus queen glycosaminoglycans in rats on a high-fat diet. Int J Mol Sci. 2017;18:E681. https://doi.org/10.3390/ijms18030681.PubMedCrossRef

11.

Ahn MY, Hwang JS, Kim MJ, Park KK. Antilipidemic effects and gene expression profiling of the glycosaminoglycans from cricket in rats on a high fat diet. Arch Pharm Res. 2016;39(7):926–36.PubMedCrossRef

12.

Ahn MY, Kim BJ, Yoon HJ, Hwang JS, Park KK. Anti-diabetic effects of dung beetle glycosaminoglycan on db mice and gene expression profiling. Toxicol Res. 2018;34(2):151–62.PubMedPubMedCentralCrossRef

13.

Schramm W, Tuna K, Chacko K, Sanchez V, Ahmed H, Liu L, Alli A. Characterization of urinary exosomes from diabetic hypertensive db/db mice. FASEB J. 2018;32(1 supplement):624.35 https://www.fasebj.org/doi/10.1096/fasebj.2018.32.1_supplement.624.35.

14.

Matsuzawa T, Yoshikawa T, Lida T, Kárpáti A, Kitano H, Harada R, Nakamura T, Sugawara A, Yamaguchi Y, Yanai K. Heparan sulfate in pancreatic cells contributes to normal glucose homeostasis by regulating insulin secretion. Biochem Biophys Res Comm. 2018;499(3):688–95.PubMedCrossRef

15.

Ziolkowski AF, Popp SK, Freeman C, Parish CR, Simeonovic CJ. Heparan sulfate and heparanase play key roles in mouse cell survival and autoimmune diabetes. J Clin Invest. 2012;122(1):132–41.PubMedCrossRef

16.

Ahn MY, Kim BJ, Kim HJ, Hwang JS, Jung YS, Park KK. Anti-aging effect and gene expression profiling of dung beetle glycosaminoglycan in aged rats. Biomater Res. 2017;21:5. https://doi.org/10.1186/s40824-017-0091-9.PubMedPubMedCentralCrossRef

17.

Kim YS, Jo YY, Chang IM, Toida T, Park Y, Linhardt RJ. A new glycosaminoglycan from the giant african snail Achatina fulica. J Biol Chem. 1996;271(20):11750–5.PubMedCrossRef

18.

Ahn MY, Kim BJ, Kim HJ, Jin JM, Yoon HJ, Hwang JS, Park KK. Anti-cancer effect of dung beetle glycosaminoglycans on melanoma. BMC Cancer. 2019;19:9.PubMedPubMedCentralCrossRef

19.

Bae EJ, Cho MJ, Kim SG. Metformin prevents an adaptive increase in GSH and induces apoptosis under the conditions of GSH deficiency in H4IIE cells. J Toxicol Environ Health A. 2007;70(15–16):1371–80.PubMedCrossRef

20.

Fratz EJ, Hunter GA, Ferreira C. Expression of murine 5-aminolevulinate synthase variants causes protoporphyrin IX accumulation and light-induced mammalian cell death. PLoS One. 2014;9(4):e93078.PubMedPubMedCentralCrossRef

21.

Hansen BH, Hallmann A, Altin D, Jenssen BM, Ciesielski TM. Acute hydrogen peroxide (H₂O₂) exposure does not cause oxidative stress in late-copepodite stage of Calanus finmarchicus. J Toxicol Environ Health A. 2017;80(16–18):820–9.PubMedCrossRef

22.

Shao G, Zhang S, Nie J, Li J, Tong J. Effects of melatonin on mechanisms involved in hypertension using human umbilical vein endothelial cells. J Toxicol Environ Health A. 2017;80(23–24):1342–8.PubMedCrossRef

23.

Herseth JI, Volden V, Bolling AK. Particulate matter-mediated release of long pentraxin3 (PTX3) and vascular endothelial growth factor (VEGF) in vitro: limited importance of endotoxin and organic content. J Toxicol Environ Health A. 2017;80(2):105–19.PubMedCrossRef

24.

Yuan C, Liu P, Han X, Cui Q. Hypoglycemic effects of glycosaminoglycan from Urechis unicinctus in diabetic mice. J Med Food. 2015;18(2):190–4.PubMedPubMedCentralCrossRef

25.

Ahn MY, Jung YS, Jee SD, Han JW, Hwang JS, Yun EY, Lee BM. Blood-pressure-lowering effect of glycosaminoglycan derived from Isaria sinclairii in spontaneously hypertensive rats. J Toxicol Environ Health A. 2013;76(6):391–9.PubMedCrossRef

26.

Lopes-Costa E, Abreu M, Gargiulo D, Rocha E, Ramos AA. Anticancer effects of seaweed compounds fucoxanthin and phloroglucinol, alone and in combination with 5-fluorouracil in colon cells. J Toxicol Environ Health A. 2017;80(13–15):776–87.PubMedCrossRef

27.

Krasiński R, Tchórzewski H, Lewkowicz P. Antioxidant effect of hyaluronan on polymorphonuclear leukocyte-derived reactive oxygen species is dependent on its molecular weight and concentration and mainly involves the extracellular space. Postepy Hig MedDosw. 2009;63:205–12.

28.

Nunes KZ, Fioresi M, Marques VB, Vassallo DV. Acute copper overload induces vascular dysfunction in aortic rings due to endothelial oxidative stress and increased nitric oxide production. J Toxicol Environ Health A. 2018;81(8):218–28.PubMedCrossRef

29.

Campo GM, Avenoso A, D’Ascola A, Campo S, Ferlazzo AM, Sama D, Calatroni A. Purified human plasma glycosaminoglycans limit oxidative injury induced by iron plus ascorbate in skin fibroblast cultures. Toxicol in Vitro. 2005;19(5):561–72.PubMedCrossRef

30.

Filippon L, Vanzin CS, Biancini GB, Pereira IN, Manfredini V, Sitta A, Peralba Mdo C, Schwartz IV, Giugliani R, Vargas CR. Oxidative stress in patients with mucopolysaccharidosis type II before and during enzyme replacement therapy. Mol Genet Metab. 2011;103(2):121–7.PubMedCrossRef

31.

Xie N, Huan M, Tian F, Gu Z, Li X. Low molecular weight heparin nebulization attenuates acute lung injury. Biomed Res Int. 2017;2017:3169179.PubMedPubMedCentral

Title: Anti-diabetic activity of field cricket glycosaminoglycan by ameliorating oxidative stress
Authors: Mi Young Ahn
Ban Ji Kim
Ha Jeong Kim
Jang Mi Jin
Hyung Joo Yoon
Jae Sam Hwang
Byung Mu Lee
Publication date: 01-12-2020
Publisher: BioMed Central
Keyword: Metformin
Published in: BMC Complementary Medicine and Therapies / Issue 1/2020
Electronic ISSN: 2662-7671
DOI: https://doi.org/10.1186/s12906-020-03027-x

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Anti-diabetic activity of field cricket glycosaminoglycan by ameliorating oxidative stress

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2020

In vivo analgesic, anti-inflammatory, and sedative activity and a molecular docking study of dinaphthodiospyrol G isolated from Diospyros lotus

In vitro anticandidal potency of Syzygium aromaticum (clove) extracts against vaginal candidiasis

Neuroprotective effect of diosgenin in a mouse model of diabetic peripheral neuropathy involves the Nrf2/HO-1 pathway

Overcoming cisplatin resistance by targeting the MTDH-PTEN interaction in ovarian cancer with sera derived from rats exposed to Guizhi Fuling wan extract

Pao Pereira extract suppresses benign prostatic hyperplasia by inhibiting inflammation-associated NFκB signaling

Decreased overall mortality rate with Chinese herbal medicine usage in patients with decompensated liver cirrhosis in Taiwan