Skip to main content
SpringerLink
Log in

Protective effect of Ganoderma lucidum polysaccharide against carbon tetrachloride-induced hepatic damage in precision-cut carp liver slices

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The aim of the present study was to investigate the protective effects of Ganoderma lucidum polysaccharide (GLPS) against carbon tetrachloride (CCl4)-induced hepatotoxicity in vitro in common carp. Precision-cut liver slices (PCLSs), which closely resemble the organ from which they are derived, were employed as an in vitro model system. GLPS (0.1, 0.3, and 0.6 mg/ml) was added to PCLS culture system before the exposure to 12 mM CCl4. The supernatants and slices were collected to detect molecular and biochemical responses to CCl4 and PCLS treatments. The levels of CYP1A, CYP3A, and CYP2E1 were measured by ELISA; the mRNA expressions of TNF-α, IL-1β, IL-6, and iNOS were determined by RT-PCR; and the relative protein expressions of c-Rel and p65 were analyzed by western blotting. Results showed that GLPS inhibited the elevations of the marker enzymes (GOT, GPT, LDH) and MDA induced by CCl4; it also enhanced the suppressed activity of antioxidant enzymes (SOD, CAT, GSH-Px, T-AOC). The treatment with GLPS resulted in significant downregulation of NF-κB and inflammatory cytokine mRNA levels and significant decreases in the hepatic protein levels of CYP1A, CYP3A, and CYP2E1. These results suggest that GLPS can protect CCl4-induced PCLS injury through inhibiting lipid peroxidation, elevating antioxidant enzyme activity, and suppressing immune inflammatory response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

GLPS:

Ganoderma lucidum polysaccharide

PCLS:

Precision-cut liver slice

LDH:

Lactate dehydrogenase

GPT:

Glutamate pyruvate transaminase

GOT:

Glutamate oxalate transaminase

SOD:

Superoxide dismutase;

GSH-Px:

Glutathione peroxidase

CAT:

Catalase

T-AOC:

Total antioxidant capacity

MDA:

Malondialdehyde

References

  • Balunas MJ, Kinghorn AD (2005) Drug discovery from medicinal plants. Life Sci 78(5):431–441

    Article  CAS  PubMed  Google Scholar 

  • Basu S (2011) Carbon tetrachloride-induced hepatotoxicity: a classic model of lipid peroxidation and oxidative stress. In: Basu S, Wiklund L (eds) Studies on experimental models. Humana Press, Totowa, pp 467–480

    Chapter  Google Scholar 

  • Bhakar AL, Tannis L-L, Zeindler C, Russo MP, Jobin C, Park DS, MacPherson S, Barker PA (2002) Constitutive nuclear factor-κB activity is required for central neuron survival. J Neurosci 22(19):8466–8475

    CAS  PubMed  Google Scholar 

  • Boess F, Kamber M, Romer S, Gasser R, Muller D, Albertini S, Suter L (2003) Gene expression in two hepatic cell lines, cultured primary hepatocytes, and liver slices compared to the in vivo liver gene expression in rats: possible implications for toxicogenomics use of in vitro systems. Toxicol Sci 73(2):386–402

    Article  CAS  PubMed  Google Scholar 

  • Braunbeck T, Storch V, Bresch H (1990) Species-specific reaction of liver ultrastructure in zebrafish (Brachydanio rerio) and trout (Salmo gairdneri) after prolonged exposure to 4-chloroaniline. Arch Environ Contam Toxicol 19(3):405–418

    Article  CAS  PubMed  Google Scholar 

  • Brown SJ, Desmond PV (2002) Hepatotoxicity of antimicrobial agents. Semin Liver Dis 22:157–168

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Chen Y, Li S, Chen Y, Lan J, Liu L (2009) Free radical scavenging of Ganoderma lucidum polysaccharides and its effect on antioxidant enzymes and immunity activities in cervical carcinoma rats. Carbohydr Polym 77(2):389–393

    Article  CAS  Google Scholar 

  • Dong D, Zhang S, Yin L, Tang X, Xu Y, Han X, Qi Y, Peng J (2013) Protective effects of the total saponins from Rosa laevigata Michx fruit against carbon tetrachloride-induced acute liver injury in mice. Food Chem Toxicol 62:120–130. doi:10.1016/j.fct.2013.08.050

    Article  CAS  PubMed  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers P, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–356

    Article  CAS  Google Scholar 

  • Elferink M, Olinga P, Draaisma A, Merema M, Bauerschmidt S, Polman J, Schoonen W, Groothuis G (2008) Microarray analysis in rat liver slices correctly predicts in vivo hepatotoxicity. Toxicol Appl Pharmacol 229(3):300–309

    Article  CAS  PubMed  Google Scholar 

  • Farkas D, Tannenbaum SR (2005) In vitro methods to study chemically-induced hepatotoxicity: a literature review. Curr Drug Metab 6(2):111–125

    Article  CAS  PubMed  Google Scholar 

  • Ikatsu H, Shinoda S, Nakajima T (1998) CYP2E1 level in rat liver injured by the interaction between carbon tetrachloride and chloroform. J Occup Health 40:223–229

    Article  CAS  Google Scholar 

  • Jia R, Cao L-P, Du J-L, Wang J-H, Liu Y-J, Jeney G, Xu P, Yin G-J (2014) Effects of carbon tetrachloride on oxidative stress, inflammatory response and hepatocyte apoptosis in common carp (Cyprinus carpio). Aquat Toxicol 152:11–19

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Gao M, Sun S, Bi A, Xin Y, Han X, Wang L, Yin Z, Luo L (2012) Protective effect of L-theanine on carbon tetrachloride-induced acute liver injury in mice. Biochem Biophys Res Commun 422(2):344–350. doi:10.1016/j.bbrc.2012.05.022

    Article  CAS  PubMed  Google Scholar 

  • Klassen LW, Thiele GM, Duryee MJ, Schaffert CS, DeVeney AL, Hunter CD, Olinga P, Tuma DJ (2008) An in vitro method of alcoholic liver injury using precision-cut liver slices from rats. Biochem Pharmacol 76(3):426–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemaire B, Beck M, Jaspart M, Debier C, Calderon PB, Thomé J-P, Rees J-F (2011) Precision-cut liver slices of Salmo salar as a tool to investigate the oxidative impact of CYP1A-mediated PCB 126 and 3-methylcholanthrene metabolism. Toxicol in Vitro 25(1):335–342

    Article  CAS  PubMed  Google Scholar 

  • Li H, Wang G, Liu S, An Q, Zheng Q, Li B, Li Z (2014) Comparative changes in the antioxidant system in the flag leaf of early and normally senescing near-isogenic lines of wheat (Triticum aestivum L.). Plant cell reports 1–12

  • Liu Q, Tan Q, Chen X, Du Y, Xia J, Yang Q, Ma Y (2009) Changes of biochemical characteristics and organization structure in liver of grass carp (Ctenopharyngodon idellus) with hepatobiliary syndrome. Joumal of Anhui Agricultual Sciences 37:6463–6467

    CAS  Google Scholar 

  • Lin S, Zhu K, Song D, Shaoping N, Mingyong X (2013) Protective Effect of Polysaccharide from Ganoderma atrum against Oxidative Stress-induced Liver Injury in Type II Diabetic Rats. Food Science 34, 300–304

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582(1):67–78

    Article  CAS  PubMed  Google Scholar 

  • Parrish AR, Gandolfi AJ, Brendel K (1995) Precision-cut tissue slices: applications in pharmacology and toxicology. Life Sci 57(21):1887–1901

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Gordillo K, Segovia J, Shibayama M, Vergara P, Moreno MG, Muriel P (2007) Curcumin protects against acute liver damage in the rat by inhibiting NF-κB, proinflammatory cytokines production and oxidative stress. Biochimica et Biophysica Acta (BBA)-General Subjects 1770(6):989–996

    Article  CAS  Google Scholar 

  • Robbins M, Zhao W (2004) Chronic oxidative stress and radiation-induced late normal tissue injury: a review. Int J Radiat Biol 80(4):251–259

    Article  CAS  PubMed  Google Scholar 

  • Rudd PM, Elliott T, Cresswell P, Wilson IA, Dwek RA (2001) Glycosylation and the immune system. Science 291(5512):2370–2376

    Article  CAS  PubMed  Google Scholar 

  • Schaffert CS, Duryee MJ, Bennett RG, DeVeney AL, Tuma DJ, Olinga P, Easterling KC, Thiele GM, Klassen LW (2010) Exposure of precision-cut rat liver slices to ethanol accelerates fibrogenesis. American Journal of Physiology Gastrointestinal and Liver Physiology 299(3):G661–G668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shanmugasundaram P, Venkataraman S (2006) Hepatoprotective and antioxidant effects of Hygrophila auriculata (K. Schum) Heine Acanthaceae root extract. J Ethnopharmacol 104(1):124–128

    Article  CAS  PubMed  Google Scholar 

  • Shilling A, Williams D (2000) Determining relative estrogenicity by quantifying vitellogenin induction in rainbow trout liver slices. Toxicol Appl Pharmacol 164(3):330–335

    Article  CAS  PubMed  Google Scholar 

  • Smith P, Krack G, McKee R, Johnson D, Gandolfi A, Hruby V, Krumdieck C, Brendel K (1986) Maintenance of adult rat liver slices in dynamic organ culture. In vitro Cellular & Developmental Biology 22(12):706–712

    Article  CAS  Google Scholar 

  • Sun R, Liu D, Chen J, Liu Z, Liu F, Li X, Pu X (2005) Extraction of Astragalus polysaccharides in Astragalus. Acta Scientiarun Naturaltium Universitatis Nankaiensis 38:33–36

    CAS  Google Scholar 

  • Thiim M, Friedman LS (2003) Hepatotoxicity of antibiotics and antifungals. Clinics in liver disease 7(2):381

    Article  PubMed  Google Scholar 

  • Visen P, Saraswat B, Dhawan B (1998) Curative effect of picroliv on primary cultured rat hepatocytes against different hepatotoxins: an in vitro study. J Pharmacol Toxicol Methods 40(3):173–179

    Article  CAS  PubMed  Google Scholar 

  • Webb D, Gagnon MM, Rose T (2008) Hepatic metabolism of contaminants in the terapontid fish, yellowtail trumpeter (Amniataba caudavittata Richardson). Environ Toxicol 23(1):68–76

    Article  CAS  PubMed  Google Scholar 

  • Weber L, Boll M, Stampfl A (2003) Hepatotoxicity and mechanism of action of haloalkanes: carbon tetrachloride as a toxicological model. Crit Rev Toxicol 33(2):105–136

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Bai D, Yang G, Ning B, Zhang X, Sun L (2011) Effects of ganoderma lucidum polysaccharides on the activation of immunological cells of the yellow catfish (Pelteobagrus fulvidraco). Acta Agriculturae Boreali-Sinica 26:195–198

    Google Scholar 

  • Xie Y, Hao H, Wang H, Guo C, Kang A, Wang G (2014) Reversing effects of lignans on CCl4-induced hepatic CYP450 down regulation by attenuating oxidative stress. J Ethnopharmacol 155(1):213–221. doi:10.1016/j.jep.2014.05.016

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Li Y, Wang F, Wu C (2010) Hepatoprotective effects of apple polyphenols on CCl4-induced acute liver damage in mice. J Agric Food Chem 58(10):6525–6531

    Article  CAS  PubMed  Google Scholar 

  • Yeh C-H, Chen H-C, Yang J-J, Chuang W-I, Sheu F (2010) Polysaccharides PS-G and protein LZ-8 from Reishi (Ganoderma lucidum) exhibit diverse functions in regulating murine macrophages and T lymphocytes. J Agric Food Chem 58(15):8535–8544

    Article  CAS  PubMed  Google Scholar 

  • Yin G, Cao L, Xu P, Jeney G, Nakao M, Lu C (2011) Hepatoprotective and antioxidant effects of Glycyrrhiza glabra extract against carbon tetrachloride (CCl4)-induced hepatocyte damage in common carp (Cyprinus carpio). Fish Physiol Biochem 37(1):209–216

    Article  CAS  PubMed  Google Scholar 

  • Zhao Z, Park SM, Guan L, Wu Y, Lee JR, Kim SC, Kim YW, Zhao R (2015) Isoliquiritigenin attenuates oxidative hepatic damage induced by carbon tetrachloride with or without buthionine sulfoximine. Chem Biol Interact 225:13–20. doi:10.1016/j.cbi.2014.10.030

    Article  CAS  PubMed  Google Scholar 

  • Zhonghui Z, Xiaowei Z, Fang F (2014) Ganoderma lucidum polysaccharides supplementation attenuates exercise-induced oxidative stress in skeletal muscle of mice. Saudi Journal of Biological Sciences 21(2):119–123

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was funded by Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (2016GH05, 2012A08YQ01) and National Natural Science Foundation of China (31202002, 31200918).

Author information

Authors and Affiliations

  1. Wuxi Fisheries College, Nanjing Agricultural University, Wuxi, 214081, China

    Yingjuan Liu, Chunyun Zhang & Guojun Yin

  2. Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, China

    Jinliang Du, Rui Jia, Liping Cao, Pao Xu & Guojun Yin

  3. International Joint Research Laboratory for Fish Immunopharmacology, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, China

    Jinliang Du, Rui Jia, Liping Cao, Pao Xu & Guojun Yin

  4. Research Institute for Fisheries, Aquaculture and Irrigation, Anna Light 8, Szarvas, 4440, Hungary

    Galina Jeney

  5. Department of Toxicology, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, 069-8501, Japan

    Hiroki Teraoka

Authors
  1. Yingjuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunyun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jinliang Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rui Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Liping Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Galina Jeney
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hiroki Teraoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guojun Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pao Xu or Guojun Yin.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Yingjuan Liu and Chunyun Zhang contributed equally to this study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Zhang, C., Du, J. et al. Protective effect of Ganoderma lucidum polysaccharide against carbon tetrachloride-induced hepatic damage in precision-cut carp liver slices. Fish Physiol Biochem 43, 1209–1221 (2017). https://doi.org/10.1007/s10695-016-0333-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-016-0333-0

Keywords

Search

Navigation