Trends in Pharmaceutical Sciences and Technologies

Trends in Pharmaceutical Sciences and Technologies

Hepatoprotective properties of the glycolipoprotein extract from Eisenia foetida

Document Type : Research(Original) Article

Authors
Akram Jamshidzadeh
Fatemeh Dabagh
Omid Farshad
Mohammad Mehdi Ommat
Azadeh Mahdavinia
Negar Azarpira
Maryam Shahbazi
Asma Najibi
Reza Heidari
Shiraz University of Medical Sciences, Pharmaceutical Sciences Research Center
Abstract
The liver is continuously exposed to a variety of xenobiotics. Several xenobiotics are identified which act as hepatotoxicants. Hence, finding protective agents for ameliorating xenobiotics-included liver injury has a great value. Eisenia foetida, a kind of “earthworm,” is a source of a wide range of bioactive components. Several investigations have been evaluated the E. foetida extract (EFX) for biomedical and nutritional applications. The current study was designed to evaluate the potential hepatoprotective properties of EFX in two experimental models of hepatic damage. Acetaminophen (APAP; 1 g/kg, i.p) was administered as the animal model of acute liver injury in mice. Bile duct ligated (BDL) rats were used as the animal model of chronic hepatic damage. Severe elevation in tissue biomarkers of oxidative stress including lipid peroxidation and hepatic glutathione depletion was evident in both APAP-treated and BDL animals. Moreover, serum biomarkers of liver injury were drastically increased in both acute and chronic animal models of hepatotoxicity. Significant liver tissue histopathological alterations including tissue necrosis, vascular congestion, and inflammatory cells infiltration were detected in APAP-treated and BDL animals. On the other hand, it was found that EFX supplementation (100, 200, 500, and 700 mg/kg, i.p) mitigated oxidative stress markers, decreased serum biomarkers of liver injury, and alleviated liver tissue histopathological changes. The hepatoprotection provided by EFX supplementation in the current study might be mediated through its potential antioxidative mechanisms.
  1. Heidari R, Niknahad H, Jamshidzadeh A, Eghbal MA, Abdoli N. An Overview on the Proposed Mechanisms of Antithyroid Drugs-Induced Liver Injury. Adv Pharm Bull. 2015;5;1-11.
  2. Heidari R, Niknahad H, Jamshidzadeh A, Abdoli N. Factors affecting drug-induced liver injury: antithyroid drugs as instances. Clin Mol Hepatol. 2014;20;237-248.
  3. Abboud G, Kaplowitz N. Drug-induced liver injury. Drug Saf. 2007;30;277-294.
  4. Farshad O, Heidari R, Mohammadi H, Akbarizadeh AR, Zarshenas MM. Hepatoprotective effects of Avicennia marina (forssk.) vierh. Trend Pharm Sci. 2017;3;255-266.
  5. Mobasher MA, Jamshidzadeh A, Heidari R, Ghahiri G, Mobasher N. Hepatoprotective effects of Artemia salina L. extract against carbon tetrachloride-induced toxicity. Trend Pharm Sci. 2016;2;259-264.
  6. Niknahad H, Heidari R, Mokhtebaz T, Mansouri S, Dehshahri S, Abdoli N, Najibi A. Evaluating the effects of different fractions obtained from Gundelia tournefortii extract against carbon tetrachloride-induced liver injury in rats. Trend Pharm Sci. 2016;2;25-34.
  7. Jamshidzadeh A, Heidari R, Razmjou M, Karimi F, Moein MR, Farshad O, Akbarizadeh AR, Shayesteh MRH. An in vivo and in vitro investigation on hepatoprotective effects of Pimpinella anisum seed essential oil and extracts against carbon tetrachloride-induced toxicity. Iran J Basic Med Sci. 2015;18;205-211.
  8. Heidari R, Babaei H, Eghbal MA. Cytoprotective effects of organosulfur compounds against methimazole-induced toxicity in isolated rat hepatocytes. Adv Pharm Bull. 2013;3;135-142.
  9. Zhang A, Sun H, Wang X. Recent advances in natural products from plants for treatment of liver diseases. Eur J Med Chem. 2013;63;570-577.
  10. Schuppan D, Jia J-D, Brinkhaus B, Hahn EG. Herbal products for liver diseases: A therapeutic challenge for the new millennium. Hepatology. 1999;30;1099-1104.
  11. Niknahad H, Jamshidzadeh A, Heidari R, Zarei M, Ommati MM. Ammonia-induced mitochondrial dysfunction and energy metabolism disturbances in isolated brain and liver mitochondria, and the effect of taurine administration: relevance to hepatic encephalopathy treatment. Clin Exp Hepatol. 2017;3;141-151.
  12. Heidari R, Jamshidzadeh A, Niknahad H, Safari F, Azizi H, Abdoli N, Ommati MM, Khodaei F, Saeedi A, Najibi A. The hepatoprotection provided by taurine and glycine against antineoplastic drugs induced liver injury in an ex vivo model of normothermic recirculating isolated perfused rat liver. Trend Pharm Sci. 2016;2;59-76.
  13. Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Ommati MM, Abdoli N, Aghaei F, Esfandiari A, Azarpira N, Niknahad H. Mitochondria protection as a mechanism underlying the hepatoprotective effects of glycine in cholestatic mice. Biomed Pharmacother. 2018;97;1086-1095.
  14. Jamshidzadeh A, Abdoli N, Niknahad H, Azarpira N, Mardani E, Mousavi S, Abasvali M, Heidari R. Taurine alleviates brain tissue markers of oxidative stress in a rat model of hepatic encephalopathy. Trend Pharm Sci. 2017;3;181-192.
  15. Jamshidzadeh A, Heidari R, Abasvali M, Zarei M, Ommati MM, Abdoli N, Khodaei F, Yeganeh Y, Jafari F, Zarei A, Latifpour Z, Mardani E, Azarpira N, Asadi B, Najibi A. Taurine treatment preserves brain and liver mitochondrial function in a rat model of fulminant hepatic failure and hyperammonemia. Biomed Pharmacother. 2017;86;514-520.
  16. Akram J, Reza H, Farzaneh A, Maral R, Forouzan K, Mohammad Mehdi O, Maryam A, Roya F, Arastoo S, Negar A, Asma N. Antimalarial drugs-induced hepatic injury in rats and the protective role of carnosine. Pharm Sci. 2016;22;170-180.
  17. Heidari R, Niknahad H, Jamshidzadeh A, Azarpira N, Bazyari M, Najibi A. Carbonyl traps as potential protective agents against methimazole-induced liver injury. J Biochem Mol Toxicol. 2015;29;173-181.
  18. Jamshidzadeh A, Heidari R, Latifpour Z, Ommati MM, Abdoli N, Mousavi S, Azarpira N, Zarei A, Zarei M, Asadi B, Abasvali M, Yeganeh Y, Jafari F, Saeedi A, Najibi A, Mardani E. Carnosine ameliorates liver fibrosis and hyperammonemia in cirrhotic rats. Clinic Res Hepatol Gastroenterol. 2017;41;424-434.
  19. Jamshidzadeh A, Abdoli N, Niknahad H, Azarpira N, Mousavi S, Mardani E, Abasvali M, Heidari R. Carnosine supplementation mitigates brain tissue markers of oxidative stress in a rat model of fulminant hepatic failure. Trend Pharm Sci. 2017;3;149-160.
  20. Heidari R, Abdoli N, Ommati MM, Jamshidzadeh A, Niknahad H. Mitochondrial impairment induced by chenodeoxycholic acid: The protective effect of taurine and carnosine supplementation. Trend Pharm Sci. 2018;4;99-108.
  21. Adzet T, Camarasa J, Laguna JC. Hepatoprotective activity of polyphenolic compounds from Cynara scolymus against CCl4 toxicity in isolated rat hepatocytes. J Nat Prod. 1987;50;612-617.
  22. Heidari R, Ghanbarinejad V, Mohammadi H, Ahmadi A, Esfandiari A, Azarpira N, Niknahad H. Dithiothreitol supplementation mitigates hepatic and renal injury in bile duct ligated mice: Potential application in the treatment of cholestasis-associated complications. Biomed Pharmacother. 2018;99;1022-1032.
  23. Lee S-P, Yang S-C, Cheng Y-S, Lien W-J, Ng L-T. Hepatoprotection by palm tocotrienol‐rich fraction. Eur J Lipid Sci Technol. 2010;112;712-719.
  24. Tong J, Yao X, Zeng H, Zhou G, Chen Y, Ma B, Wang Y. Hepatoprotective activity of flavonoids from Cichorium glandulosum seeds in vitro and in vivo carbon tetrachloride-induced hepatotoxicity. J Ethnopharmacol. 2015;174;355-363.
  25. Ravikumar S, Gnanadesigan M. Hepatoprotective and antioxidant activity of a mangrove plant Lumnitzera racemosa. Asian Pacific J Trop Biomed. 2011;1;348-352.
  26. Sabine JR. Earthworms as a source of food and drugs. Earthworm ecology: Springer; 1983. p. 285-296.
  27. Cooper EL, Balamurugan M, Huang C-Y, Tsao CR, Heredia J, Tommaseo-Ponzetta M, Paoletti MG. Earthworms dilong: Ancient, inexpensive, noncontroversial models may help clarify approaches to integrated medicine emphasizing neuroimmune systems. Evid Based Complement Alternat Med. 2012;2012.
  28. Hanušova R, Bilej M, Brys L, De-Baetselier P, Beschin A. Identification of a coelomic mitogenic factor in Eisenia foetida earthworm. Immunol Lett. 1999;65;203-211.
  29. Hrẑenjak M, Kobrehel Ddj, Levanat S, Jurin M, Hrẑenjak T. Mitogenicity of the earthworm's ( eisenia foetida) insulin-like proteins. Comp Biochem Physiol Part B: Comp Biochem. 1993;104;723-729.
  30. Aldarraji QM, Halimoon N, Majid NM. Antioxidant activity and total phenolic content of earthworm paste of Lumbricus rubellus (red worm) and Eudrilus eugenia (African night crawler). J Entomol Nematol. 2013;5;33-37.
  31. Prakash M, Gunasekaran G, Elumalai K. Effect of earthworm powder on antioxidant enzymes in alcohol induced hepatotoxic rats. Eur Rev Med Pharmacol Sci. 2008;12;237-243.
  32. Grdisa M, Popovic M, Hrzenjak T. Glycolipoprotein extract (G-90) from earthworm< i> Eisenia foetida exerts some antioxidative activity. Comp Biochem Physiol Part A: Mol Integ Physiol 2001;128;821-825.
  33. Zhao H, Dong J, Lu J, Chen J, Li Y, Shan L, Lin Y, Fan W, Gu G. Effects of extraction solvent mixtures on antioxidant activity evaluation and their extraction capacity and selectivity for free phenolic compounds in barley (Hordeum vulgare L.). J Agric Food Chem. 2006;54;7277-7286.
  34. Li W, Wang C, Sun Z. Vermipharmaceuticals and active proteins isolated from earthworms. Pedobiologia. 2011;54;S49-S56.
  35. Liu Y-Q, Sun Z-J, Wang C, Li S-J, Liu Y-Z. Purification of a novel antibacterial short peptide in earthworm Eisenia foetida. Acta Biochimica Biophysica. 2004;36;297-302.
  36. Jamshidzadeh A, Heidari R, Golzar T, Derakhshanfar A. Effect of Eisenia foetida Extract against Cisplatin-Induced Kidney Injury in Rats. J Diet Suppl. 2016;13;551-559.
  37. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Anti-inflammatory and anti-pyretic activities of earthworm extract— Lampito mauritii (Kinberg). J Ethnopharmacol. 2009;121;330-332.
  38. Nafisi S, Heidari R, Ghaffarzadeh M, Ziaee M, Hamzeiy H, Garjani A, Eghbal MA. Cytoprotective effects of silafibrate, a newly-synthesised siliconated derivative of clofibrate, against acetaminophen-induced toxicity in isolated rat hepatocytes. Arh Hig Rada Toksikol. 2014;1-10.
  39. Heidari R, Jamshidzadeh A, Niknahad H, Mardani E, Ommati MM, Azarpira N, Khodaei F, Zarei A, Ayarzadeh M, Mousavi S, Abdoli N, Yeganeh BS, Saeedi A, Najibi A. Effect of taurine on chronic and acute liver injury: Focus on blood and brain ammonia. Toxicol Rep. 2016;3;870-879.
  40. Ommati MM, Jamshidzadeh A, Niknahad H, Mohammadi H, Sabouri S, Heidari R, Abdoli N. N-acetylcysteine treatment blunts liver failure-associated impairment of locomotor activity. PharmaNutrition. 2017;5;141-147.
  41. McGill MR, Williams CD, Xie Y, Ramachandran A, Jaeschke H. Acetaminophen-induced liver injury in rats and mice: comparison of protein adducts, mitochondrial dysfunction, and oxidative stress in the mechanism of toxicity. Toxicol Appl Pharmacol. 2012;264;387-394.
  42. Liu L-C, Wang C-J, Lee C-C, Su S-C, Chen H-L, Hsu J-D, Lee H-J. Aqueous extract of Hibiscus sabdariffa L. decelerates acetaminophen-induced acute liver damage by reducing cell death and oxidative stress in mouse experimental models. J Sci Food Agricult. 2010;90;329-337.
  43. Moezi L, Heidari R, Amirghofran Z, Nekooeian AA, Monabati A, Dehpour AR. Enhanced anti-ulcer effect of pioglitazone on gastric ulcers in cirrhotic rats: The role of nitric oxide and IL-1b. Pharmacol Rep. 2013;65;134-143.
  44. Heidari R, Jamshidzadeh A, Ghanbarinejad V, Ommati MM, Niknahad H. Taurine supplementation abates cirrhosis-associated locomotor dysfunction. Clin Exp Hepatol. 2018;4;72-82.
  45. Heidari R, Niknahad H, Sadeghi A, Mohammadi H, Ghanbarinejad V, Ommati MM, Hosseini A, Azarpira N, Khodaei F, Farshad O, Rashidi E, Siavashpour A, Najibi A, Ahmadi A, Jamshidzadeh A. Betaine treatment protects liver through regulating mitochondrial function and counteracting oxidative stress in acute and chronic animal models of hepatic injury. Biomed Pharmacother. 2018;103;75-86.
  46. Heidari R, Moezi L, Asadi B, Ommati MM, Azarpira N. Hepatoprotective effect of boldine in a bile duct ligated rat model of cholestasis/cirrhosis. PharmaNutrition. 2017;5;109-117.
  47. Ahmadian E, Eftekhari A, Khalili Fard J, Babaei H, Mohajjel Nayebi A, Mohammadnejad D, Eghbal MA. In vitro and in vivo evaluation of the mechanisms of citalopram-induced hepatotoxicity. Arch Pharm Res. 2017;40;1296-1313.
  48. Heidari R, Babaei H, Roshangar L, Eghbal MA. Effects of Enzyme Induction and/or Glutathione Depletion on Methimazole-Induced Hepatotoxicity in Mice and the Protective Role of N-Acetylcysteine. Adv Pharm Bull. 2014;4;21-28.
  49. Heidari R, Babaei H, Eghbal MA. Amodiaquine-induced toxicity in isolated rat hepatocytes and the cytoprotective effects of taurine and/or N-acetyl cysteine. Res Pharm Sci. 2014;9;97-105.
  50. Jamshidzadeh A, Heidari R, Abazari F, Ramezani M, Khodaei F, Ommati MM, Ayarzadeh M, Firuzi R, Saeedi A, Azarpira N, Najibi A. Antimalarial drugs-induced hepatic injury in rats and the protective role of carnosine. Pharm Sci. 2016;22;170-180.
  51. Niknahad H, Heidari R, Firuzi R, Abazari F, Ramezani M, Azarpira N, Hosseinzadeh M, Najibi A, Saeedi A. Concurrent inflammation augments antimalarial drugs-induced liver injury in rats. Adv Pharm Bull. 2016;6;617-625.
  52. Heidari R, Jamshidzadeh A, Keshavarz N, Azarpira N. mitigation of methimazole-induced hepatic injury by taurine in mice. Sci Pharm. 2015;83;143-158.
  53. Ommati MM, Tanideh N, Rezakhaniha B, Wang J, Sabouri S, Vahedi M, Dormanesh B, Koohi Hosseinabadi O, Rahmanifar F, Moosapour S, Akhlaghi A, Heidari R, Zamiri MJ. Is immunosuppression, induced by neonatal thymectomy, compatible with poor reproductive performance in adult male rats? Andrology. 2018;6;199-213.
  54. Heidari R, Ahmadi A, Mohammadi H, Ommati MM, Azarpira N, Niknahad H. Mitochondrial dysfunction and oxidative stress are involved in the mechanism of methotrexate-induced renal injury and electrolytes imbalance. Biomed Pharmacother. 2018;107;834-840.
  55. Heidari R, Babaei H, Eghbal MA. Amodiaquine-induced toxicity in isolated rat hepatocytes and the cytoprotective effects of taurine and/or N-acetyl cysteine. Res Pharm Sci. 2014;9;97-105.
  56. Heidari R, Ahmadi F, Rahimi HR, Azarpira N, Hosseinzadeh M, Najibi A, Niknahad H. Exacerbated liver injury of antithyroid drugs in endotoxin-treated mice. Drug Chem Toxicol. 2018;0;1-9.
  57. Eftekhari A, Ahmadian E, Azarmi Y, Parvizpur A, Hamishehkar H, Eghbal MA. In vitro/vivo studies towards mechanisms of risperidone-induced oxidative stress and the protective role of coenzyme Q10 and N-acetylcysteine. Toxicol Mechanism Method. 2016;26;520-528.
  58. Costa-Neto EM. Animal-based medicines: biological prospection and the sustainable use of zootherapeutic resources. An Acad Bras Cienc. 2005;77;33-43.
  59. Cooper EL, Ru B, Weng N. Earthworms: Sources of antimicrobial and anticancer molecules. Complementary and Alternative Approaches to Biomedicine. Advances in Experimental Medicine and Biology: Springer, Boston, MA; 2004. p. 359-389.
  60. Grdisa M, Popovic M, Hrzenjak T. Glycolipoprotein extract (G-90) from earthworm Eisenia foetida exerts some antioxidative activity. Comp Biochem Physiol Part A: Mol Integ Physiol. 2001;128;821-825.
  61. Hrženjak T, Popović M, Božić T, Grdisa M, Dorde K, Tiška-Rudman L. Fibrinolytic and anticoagulative activities from the earthworm Eisenia foetida. Comp Biochem Physiol Part B: Biochem Mol Biol. 1998;119;825-832.
  62. Xie J, He W, Weng N, Guo Z, Yu M, Liu N, Ru B. Extraction and isolation of the anti-tumor protein components from earthworm (eisenia fetida Andrei) and the anti-tumor activity. Chin J Biochem Mol Biol. 2002;19;359-366.
  63. Yang J-S, Ru B-G. Purification and Characterization of an SDS-Activated Fibrinolytic Enzyme from Eisenia fetida. Comp Biochem Physiol Part B: Biochem Mol Biol. 1997;118;623-631.
  64. Balamurugan M. Restoration of histoarchitecture in the paracetamol-induced liver damaged rat by earthworm extract, Lampito mauritii (Kinberg). Eur Rev Med Pharmacol Sci. 2007;11.
  65. Scalbert A, Johnson IT, Saltmarsh M. Polyphenols: antioxidants and beyond. Am J Clin Nut. 2005;81;215S-217S.
  66. Matausijć-Pisl M, Cupić H, Kasuba V, Mikecin AM, Grdisa M. Tissue extract from Eisenia foetida as a wound-healing agent. Eur Rev Med Pharmacol Sci. 2010;14;177-184.
  67. Grdiša M, Popović M, Hrženjak T. Stimulation of growth factor synthesis in skin wounds using tissue extract (G-90) from the earthworm Eissenia foetida. Cell Biochem Funct. 2004;22;373-378.
  68. Mira G, Terezija H. Glycolipoprotein extract of Esenia foetida (G-90): A source of biological active molecules. Eur J Soil Biol. 2007;43;S104-S109.
  69. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Anti-inflammatory and anti-pyretic activities of earthworm extract— Lampito mauritii (Kinberg). J Ethnopharmacol. 2009;121;330-332.
  70. Blazka ME, Wilmer JL, Holladay SD, Wilson RE, Luster MI. Role of Proinflammatory Cytokines in Acetaminophen Hepatotoxicity. Toxicol Appl Pharmacol. 1995;133;43-52.
  71. Seki E, Schwabe RF. Hepatic inflammation and fibrosis: Functional links and key pathways. Hepatology. 2015;61;1066-1079.
Trends in Pharmaceutical Sciences and Technologies
Volume 4, Issue 3 - Serial Number 3
17
September 2018
Pages 149-160