Skip to main content

Antilipidemic effects and gene expression profiling of the glycosaminoglycans from cricket in rats on a high fat diet

Archives of Pharmacal Research volume 39, pages 926–936 (2016)Cite this article

Abstract

Glycosaminoglycan (GAG) from cricket (Gryllus bimaculatus) was studied as a potential health supplement. Antiatherosclerotic and antilipidemic effects of the GAG of G. bimaculatus (GbG, 5 or 10 mg/kg) were investigated in 15-week old Wistar rats treated with GbG for over a month. GbG produced a meaningful anti-edema effect with inhibition of C-reactive protein (CRP). Also, the weights of abdominal and epididymidal fat were also reduced in conjunction with a mild increase in body weight. Furthermore, the sero-biochemical parameters showed an antihyperlipidemic effect with decreased levels of phospholipid, AST, ALT, total cholesterol and glucose in a dose-dependent manner. In addition anticoagulant and antithrombotic effects were seen: platelet, thrombin time, prothrombin time and Factor I were increased with GbG treatment. Furthermore, the GbG treated rat group (at 10 mg/kg) compared to control, showed that 588 genes (test/control ratio >2.0) including lipocalin 2 (Lcn2) and alpha 2-macroglobulin (A2 m) were up-regulated, and 569 genes (test/control ratio >0.5) including stearoyl-coenzyme A desaturase 1 (Scd1) were down-regulated. Based on these results, GbG could potentially prevent or treat fatty liver or hyperlipidemia in rats on a high-fat diet.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Ahn MY, Ryu KS, Park BY, Kim DW, Kim I, Kim SH (2000) Effects on cricket supplements on the chicken meats and its eggs. Korean J Poult Sci 27:197–202

    Google Scholar 

  • Ahn MY, Lee YW, Ryu KS, Lee HS, Kim IK, Kim JW, Lee YK, Kim ES, Kim YS (2002) Protective effects of water/methanol extracts of cricket on the acute hepatic damages in the ICR-mice induced by administration of CCl4. Korean J Food Sci Technol 34:684–687

    Google Scholar 

  • Ahn KS, Moon KY, Lee JS, Kim YS (2003) Downregulation of NF-κB activation in human keratinocytes by melanogenic inhibitors. J Dematol Sci 31:193–201

    CAS  Article  Google Scholar 

  • Ahn MY, Lee YW, Ryu KS, Lee HS, Kim IK, Kim JW, Lim SS (2004) Effect of water and methanol extracts of cricket (Gryllus bimaculatus) on alcohol metabolism. Korean J Pharmacogn 35:175–178

    Google Scholar 

  • Ahn MY, Jung YS, Jee SD, Kim CS, Lee SH, Moon CH, Cho SI, Lee BM, Ryu KS (2007) Anti-hypertensive effect of the Dongchunghacho, Isaria sinclairii, in the spontaneously hypertensive rats. Arch Pharm Res 30:493–501

    CAS  Article  PubMed  Google Scholar 

  • Ahn MY, Han JW, Hwang JS, Yun EY (2014) Anti-inflammatory effect of glycosaminoglycan derived from G. bimaculatus (a type of cricket, insect) on adjuvant-treated chronic arthritis rat model. J Toxicol Environ Health Part A 77:1332–1345

    CAS  Article  PubMed  Google Scholar 

  • Ahn MY, Kim MJ, Kwon RH, Hwang JS, Park KK (2015) Gene expression profiling and inhibition of adipose tissue accumulation of G. bimaculatus extract in rats on high fat diet. Lipids. Health. doi:10.1186/s12944-015-0113-3

    Google Scholar 

  • Alwahsh SM, Xu M, Seyhan HA, Ahmad S, Mihm S, Ramadori G, Schultze FC (2014) Diet high in fructose leads to an overexpression of lipocalin-2 in rat fatty liver. World J Gastroenterol 20:1807–1821

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • An D, Pulinilkunnil T, Qi D, Ghosh S, Abrahani A, Rodrigues B (2005) The metabolic “switch” AMPK regulates cardiac heparin-releasable lipoprotein lipase. Am J Physiol Endocrinol Metab 288:E246–E253

    CAS  Article  PubMed  Google Scholar 

  • Casu B, Johnson EA, Mantovani M, Mulloy B, Oreste P, Pescador R, Prino G, Torri G, Zoppetti G (1983) Correlation between structure, fat-clearing and anticoagulant properties of heparins and heparan sulphates. Arzneimittelforschung 33:135–142

    CAS  PubMed  Google Scholar 

  • Cui Z, Ahn MY, Lee YB, Ryu KS (2002) Materia medica from insects. Shinilbooks, Seoul

    Google Scholar 

  • Dudley KJ, Sloboda DM, Connor KL, Beltrand J, Vickers MH (2011) Offspring of mothers fed a high fat diet display hepatic cell cycle inhibition and associated changes in gene expression and DNA methylation. PLoS ONE. doi:10.1371/journal.pone.0021662

    Google Scholar 

  • El-Sayed MM, Ghareeb DA, Talat HA, Sarhan EM (2013) High fat diet induced insulin resistance and elevated retinol binding protein 4 in female rats; treatment and protection with Berberis vulgaris extract and vitamin A. Pak J Pharm Sci 26:1189–1195

    CAS  PubMed  Google Scholar 

  • Fogelstrand P, Borén J (2013) Hyaluronan accumulates with high-fat feeding and contributes to insulin resistance. Diabetes 62:1816–1817

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Fukatsu Y, Noguchi T, Hosooka T, Ogura T, Kotani K, Abe T, Shibakusa T, Inoue K, Sakai M, Tobimatsu K, Inagaki K, Yoshioka T, Matsuo M, Nakae J, Matsuki Y, Hiramatsu R, Kaku K, Okamura H, Fushiki T, Kasuga M (2009) Muscle-specific overexpression of heparin-binding epidermal growth factor-like growth factor increases peripheral glucose disposal and insulin sensitivity. Endocrinology 150:2683–2691

    CAS  Article  PubMed  Google Scholar 

  • Han LK, Sumiyoshi M, Takeda T, Chihara H, Nishikioro T, Tsujita T, Kimura Y, Okuda H (2000) Inhibitory effects of chondroitin sulfate prepared from salmon nasal cartilage on fat storage in mice fed a high-fat diet. Int J Obes Metab Disord 21:1131–1138

    Article  Google Scholar 

  • Hoffmann E, Konkar A, Dziadek S, Josel HP, Conde-Knape K, Kropp H, Kling L, Stubenrauch K, Thorey I, Dengl S, Brinkmann U (2013) PK modulation of haptenylated peptides via non-covalent antibody complexation. J Control Release 171:48–56

    CAS  Article  PubMed  Google Scholar 

  • Hosaka T, Sasaga S, Yamasaka Y, Nii Y, Edazawa K, Tsutsumi R, Shuto E, Okahisa N, Iwata S, Tomotake H, Sakai T (2014) Treatment with buckwheat bran extract prevents the elevation of serum triglyceride levels and fatty liver in KK-A(y) mice. J Med Invest 61:345–352

    Article  PubMed  Google Scholar 

  • Hu SW, Tian YY, Chang YG, Li ZJ, Xue CH, Wang YM (2014) Fucosylated chondroitin sulfate from sea cucumber improves glucose metabolism and activates insulin signaling in the liver of insulin-resistant mice. J Med Food 17:749–757

    CAS  Article  PubMed  Google Scholar 

  • Karaman S, Hollmén M, Robciuc MR, Alitalo A, Nurmi H, Morf B, Buschle D, Alkan HF, Ochsenbein AM, Alitalo K, Wolfrum C, Detmar M (2015) Blockade of VEGF-C and VEGF-D modulates adipose tissue inflammation and improves metabolic parameters under high-fat diet. Mol Metab 4:93–105

    CAS  Article  PubMed  Google Scholar 

  • Karamanos NK, Tzanakakis GN (2012) Glycosaminoglycans: from ‘‘cellular glue’’ to novel therapeutical agents. Curr Opin Pharmacol 12:220–222

    CAS  Article  PubMed  Google Scholar 

  • Karlsson-Lindahl L, Schmidt L, Haage D, Hansson C, Taube M, Egecioglu E, Tan YX, Admyre T, Jansson JO, Vlodavsky I, Li JP, Lindahl U, Dickson SL (2012) Heparanase affects food intake and regulates energy balance in mice. PLoS ONE. doi:10.1371/journal.pone.0034313

    PubMed  Google Scholar 

  • Kim YS, Jo YY, Chang IM, Toida T, Park Y, Linhardt RJ (1996) A new glycosaminoglycan from the giant african snail Achatina fulica. J Biol Chem 271:11750–11755

    CAS  Article  PubMed  Google Scholar 

  • Lee CY (2013) The effect of high-fat diet-induced pathophysiological changes in the gut on obesity: What should be the ideal treatment? Clin Transl Gastroenterol 4:e39

    Article  Google Scholar 

  • Oh TS, Yun JW (2012) DNA microarray analysis reveals differential gene expression in the soleus muscle between male and female rats exposed to a high fat diet. Mol Biol Rep 39:6569–6580

    CAS  Article  PubMed  Google Scholar 

  • Pandian V, Aravindan N, Subramanian S, Somasundaran ST (2014) Lipid-lowering effect of molluscan (Katelysia opima) glycosaminoglycan (GAG) in hypercholesterolemic induced rats. Biol Chem 395:355–364

    CAS  Article  PubMed  Google Scholar 

  • Park Y, Pariza MW (2001) Lipoxygenase inhibitors inhibit heparin-releasable lipoprotein lipase activity in 3T3-L1 adipocytes and enhance body fat reduction in mice by conjugated linoleic acid. Biochim Biophys Acta 1534:27–33

    CAS  Article  PubMed  Google Scholar 

  • Song J, Liu H, Ressom HW, Tiwari S, Ecelbarger CM (2008) Chronic Rosigiltazone therapy normalizes expression of ACE1, SCD1 and other genes in the kidney of obese Zucker rats as determined by microarray by microarray analysis. Exp Clin Endocrinol Diabetes 116:315–325

    CAS  Article  PubMed  Google Scholar 

  • Srinroch C, Srisomsap C, Chokchaichamnankit D, Punyarit P, Phiriyangkul P (2015) Identification of novel allergen in edible insect, Gryllus bimaculatus and its cross-reactivity with Macrobrachium spp. allergens. Food Chem 184:160–166

    CAS  Article  PubMed  Google Scholar 

  • Sun H, Yuan Y, Sun ZL (2013) Cholesterol contributes to diabetic nephropathy through SCAP-SREBP-2 pathway. Int J Endocrinol. doi:10.1155/2013/592576

    Google Scholar 

  • Ueno T, Fukuda N, Nagase H, Tsunemi A, Tahira K, Matsumoto T, Hiraoka-Yamamoto J, Ikeda K, Mitsumata M, Sato Y, Soma M, Matsumoto K, Yamori Y (2009) Atherogenic dyslipidemia and altered hepatic gene expression in SHRSP.Z-Leprfa/IzmDmer rats. Int J Mol Med 23:313–320

    CAS  Article  PubMed  Google Scholar 

  • Yunoki K, Sasaki G, Tokuji Y, Kinoshita M, Naito A, Aida K, Ohnishi M (2008) Effect of dietary wine pomace extract and oleanolic acid on plasma lipids in rats fed high-fat diet and its DNA microarray analysis. J Agric Food Chem 56:12052–12058

    CAS  Article  PubMed  Google Scholar 

  • Zhao D, Wang SR, Ma WW, Liu LJ, Sun CH (2008) Alpha1-macroglobulin: a potential obesity-related factor in serum. Med Sci Monitor 14:BR57–BR61

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Rural Development Administration National Research Project, PJ009827.

Author information

Affiliations

  1. Department of Agricultural Biology, National Academy of Agricultural Science, RDA, 166 Nongsaengmyung-Ro, Iseo-Myun, Wanju-Gun, 55365, South Korea

    Mi Young Ahn, Jae Sam Hwang & Min-Ji Kim

  2. Pharmacogenechips Inc., Chuncheon, 200-160, South Korea

    Kun-Koo Park

Authors
  1. Mi Young Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jae Sam Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min-Ji Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kun-Koo Park
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mi Young Ahn.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ahn, M.Y., Hwang, J.S., Kim, MJ. et al. Antilipidemic effects and gene expression profiling of the glycosaminoglycans from cricket in rats on a high fat diet. Arch. Pharm. Res. 39, 926–936 (2016). https://doi.org/10.1007/s12272-016-0749-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-016-0749-1

Keywords

  • Antilipidemic effect
  • G. bimaculatus
  • Glycosaminoglycan
  • Wistar rats
  • High fat diet