Antihyperlipidemic effect of the hydroalcoholic extract of Basidiomycete Pycnoporus sanguineus (Fr.) Murr. in streptozotocin-induced diabetic rats

Abstract

One of the consequences of diabetes mellitus is deregulation in lipid metabolism, resulting in an increase in triglyceride and cholesterol levels in the blood. This study evaluated the effect of the Pycnoporus sanguineus hydroalcoholic extract on lipid metabolism in streptozotocin-induced diabetic rats. Rats received P. sanguineus extract for 4 weeks in the drinking water at a dose of 10 mg/Kg/day. Lipid profile, glucose and hepatic damage in normal and streptozotocin-induced diabetic rats were evaluated. Also, the chemical composition of P. sanguineus extract, cytotoxicity and HMG-CoA reductase activity in vitro were evaluated. The treatment significantly reduced triglyceride levels in the group of diabetic rats treated with the extract (DBT Pyc) compared to the group receiving water without extract (DBT H2O). For total cholesterol, reductions in the DBT Pyc group were also observed in relation to the DBT H2O group. The HMG-CoA reductase activity was not affected by P. sanguineus extract. Our findings demonstrated significant anti-hyperlipidaemic activity of P. sanguinues extract in diabetic rats. These results highlight the therapeutic potential of the P. sanguineus extract, which provides a new possibility for development of drugs to control hyperlipidaemia and provides impetus for further studies.

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

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

Availability of data and material

Not applicable.

References

  1. Al-Ansari M, Al-Humaid LA, Vijayaraghavan P et al (2019) Identification of phytochemical components from Aerva lanata (Linn.) medicinal plants and its in-vitro inhibitory activity against drug resistant microbial pathogens and antioxidant properties. Saudi J Biol Sci. https://doi.org/10.1016/j.sjbs.2019.02.010

    Article  PubMed  PubMed Central  Google Scholar 

  2. Anandhi R, Annadurai T, Anitha TS et al (2013) Antihypercholesterolemic and antioxidative effects of an extract of the oyster mushroom, Pleurotus ostreatus, and its major constituent, chrysin, in Triton WR-1339-induced hypercholesterolemic rats. J Physiol Biochem 69:313–323. https://doi.org/10.1007/s13105-012-0215-6

    CAS  Article  PubMed  Google Scholar 

  3. Anyaegbu OC, Ajayi AM, Adedapo ADA (2017) Hypolipidemic and antioxidant effects of the Methanolic stem bark extract of Anacardium occidentale Linn. In triton-X 100 induced hyperlipidemic rats. Orient Pharm Exp Med 17:211–221. https://doi.org/10.1007/s13596-017-0262-1

    CAS  Article  Google Scholar 

  4. Dias DA, Urban S (2009) HPLC and NMR studies of phenoxazone alkaloids from Pycnoporus cinnabarinus. Nat Prod Commun 4:489–498

    CAS  PubMed  Google Scholar 

  5. Eeg-Olofsson K, Gudbjörnsdottir S, Eliasson B et al (2014) The triglycerides-to-HDL-cholesterol ratio and cardiovascular disease risk in obese patients with type 2 diabetes: an observational study from the Swedish National Diabetes Register (NDR). Diabetes Res Clin Pract 106:136–144. https://doi.org/10.1016/j.diabres.2014.07.010

    CAS  Article  PubMed  Google Scholar 

  6. Eggert C (1997) Laccase-catalyzed formation of cinnabarinic acid is responsible for antibacterial activity of Pycnoporus cinnabarinus. Microbiol Res 152:315–318. https://doi.org/10.1016/S0944-5013(97)80046-8

    CAS  Article  PubMed  Google Scholar 

  7. Eidi A, Eidi M, Esmaeili E (2006) Antidiabetic effect of garlic (Allium sativum L.) in normal and streptozotocin-induced diabetic rats. Phytomedicine 13:624–629. https://doi.org/10.1016/j.phymed.2005.09.010

    CAS  Article  PubMed  Google Scholar 

  8. Gambato G, Todescato K, Pavão EM et al (2016) Evaluation of productivity and antioxidant profile of solid-state cultivated macrofungi Pleurotus albidus and Pycnoporus sanguineus. Bioresour Technol 207:46–51. https://doi.org/10.1016/j.biortech.2016.01.121

    CAS  Article  PubMed  Google Scholar 

  9. Gambato G, Pavão EM, Chilanti G et al (2018) Pleurotus albidus Modulates mitochondrial metabolism disrupted by hyperglycaemia in EA.hy926 endothelial cells. Biomed Res Int 2018:1–10. https://doi.org/10.1155/2018/2859787

    CAS  Article  Google Scholar 

  10. Garcia TA, Santiago MF, Ulhoa CJ (2006) Properties of laccases produced by Pycnoporus sanguineus induced by 2,5-xylidine. Biotechnol Lett 28:633–636. https://doi.org/10.1007/s10529-006-0026-3

    CAS  Article  PubMed  Google Scholar 

  11. Ikewuchi JC, Ikewuchi CC, Ifeanacho MO et al (2013) Moderation of hematological and plasma biochemical indices of sub-chronic salt-loaded rats by aqueous extract of the sclerotia of Pleurotus tuberregium (Fr) Sing’s: implications for the reduction of cardiovascular risk. J Ethnopharmacol 150:466–476. https://doi.org/10.1016/j.jep.2013.09.002

    CAS  Article  PubMed  Google Scholar 

  12. Jahn MP, Gomes LF, Jacob MHVM et al (2011) The effect of dehydroepiandrosterone (DHEA) on renal function and metabolism in diabetic rats. Steroids 76:564–570. https://doi.org/10.1016/j.steroids.2011.02.006

    CAS  Article  PubMed  Google Scholar 

  13. Li I-C, Chen Y-L, Lee L-Y et al (2014) Evaluation of the toxicological safety of erinacine A-enriched Hericium erinaceus in a 28-day oral feeding study in Sprague–Dawley rats. Food Chem Toxicol 70:61–67. https://doi.org/10.1016/j.fct.2014.04.040

    CAS  Article  PubMed  Google Scholar 

  14. Liang B, Guo Z, Xie F, Zhao A (2013) Antihyperglycemic and antihyperlipidemic activities of aqueous extract of Hericium erinaceus in experimental diabetic rats. BMC Complement Altern Med 13:253. https://doi.org/10.1186/1472-6882-13-253

    Article  PubMed  PubMed Central  Google Scholar 

  15. Liu S, You L, Zhao Y, Chang X (2018) Wild Lonicera caerulea berry polyphenol extract reduces cholesterol accumulation and enhances antioxidant capacity in vitro and in vivo. 107:73–83. https://doi.org/10.1016/j.foodres.2018.02.016

  16. Lowe MM, Mold JE, Kanwar B et al (2014) Identification of cinnabarinic acid as a novel endogenous aryl hydrocarbon receptor ligand that drives IL-22 production. PLoS ONE 9:e87877. https://doi.org/10.1371/journal.pone.0087877

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Manninen V, Tenkanen L, Koskinen P et al (1992) Joint effects of serum triglyceride and LDL cholesterol and HDL cholesterol concentrations on coronary heart disease risk in the Helsinki Heart Study. Implications for treatment. Circulation 85:37–45

    CAS  Article  Google Scholar 

  18. Megson IL, Whitfield PD, Zabetakis I (2016) Lipids and cardiovascular disease: where does dietary intervention sit alongside statin therapy? Food Funct 7:2603–2614. https://doi.org/10.1039/c6fo00024j

    CAS  Article  PubMed  Google Scholar 

  19. Molina S, Rencoret J, del Río JC et al (2008) Oxidative degradation of model lipids representative for main paper pulp lipophilic extractives by the laccase–mediator system. Appl Microbiol Biotechnol 80:211–222. https://doi.org/10.1007/s00253-008-1547-6

    CAS  Article  PubMed  Google Scholar 

  20. Ochani PC, D’Mello P (2009) Antioxidant and antihyperlipidemic activity of Hibiscus sabdariffa Linn. leaves and calyces extracts in rats. Indian J Exp Biol 47:276–282

    PubMed  Google Scholar 

  21. Padala S, Thompson PD (2012) Statins as a possible cause of inflammatory and necrotizing myopathies. Atherosclerosis 222:15–21. https://doi.org/10.1016/j.atherosclerosis.2011.11.005

    CAS  Article  PubMed  Google Scholar 

  22. Parhofer KG (2015) Interaction between glucose and lipid metabolism: more than diabetic dyslipidemia. Diabetes Metab J 39:353. https://doi.org/10.4093/dmj.2015.39.5.353

    Article  PubMed  PubMed Central  Google Scholar 

  23. Polak J, Jarosz-Wilkolazka A, Szalapata K et al (2016) Laccase-mediated synthesis of a phenoxazine compound with antioxidative and dyeing properties – the optimisation process. N Biotechnol 33:255–262. https://doi.org/10.1016/J.NBT.2015.09.004

    CAS  Article  PubMed  Google Scholar 

  24. Rahman MA, Abdullah N, Aminudin N (2014) Inhibitory effect on in vitro LDL oxidation and HMG Co-A reductase activity of the liquid-liquid partitioned fractions of Hericium erinaceus (Bull.) persoon (Lion’s Mane Mushroom). Biomed Res Int 2014:1–9. https://doi.org/10.1155/2014/828149

    Article  Google Scholar 

  25. Ramachandran S, Faisal TK, Anjumary J et al (2017) Comparative evaluation of hypoglycemic and hypolipidemic activity of various extract of Anogeissus latifolia bark in streptozotocin-induced diabetic rats. J Complement Integr Med 14:. https://doi.org/10.1515/jcim-2016-0130

  26. Ramasubbu K, Estep J, White DL et al (2008) Experimental and clinical basis for the use of statins in patients with ischemic and nonischemic cardiomyopathy. J Am Coll Cardiol 51:415–426. https://doi.org/10.1016/j.jacc.2007.10.009

    CAS  Article  PubMed  Google Scholar 

  27. Ramesh B, Viswanathan P, Pugalendi KV (2007) Protective effect of Umbelliferone on membranous fatty acid composition in streptozotocin-induced diabetic rats. Eur J Pharmacol 566:231–239. https://doi.org/10.1016/j.ejphar.2007.03.045

    CAS  Article  PubMed  Google Scholar 

  28. Roden M (2016) Diabetes mellitus: definition, classification and diagnose. Wien Klin Wochenschr 128:37–40. https://doi.org/10.1007/s00508-015-0931-3

    CAS  Article  Google Scholar 

  29. Smânia A, Marques CJS, Smânia EFA et al (2003) Toxicity and antiviral activity of cinnabarin obtained from Pycnoporus sanguineus (Fr.) Murr. Phyther Res 17:1069–1072. https://doi.org/10.1002/ptr.1304

    CAS  Article  Google Scholar 

  30. Sripradha R, Sridhar MG, Maithilikarpagaselvi N (2016) Antihyperlipidemic and antioxidant activities of the ethanolic extract of Garcinia cambogia on high fat diet-fed rats. J Complement Integr Med 13:9–16. https://doi.org/10.1515/jcim-2015-0020

    CAS  Article  PubMed  Google Scholar 

  31. Staels B, Fruchart J-C (2005) Therapeutic roles of peroxisome proliferator-activated receptor agonists. Diabetes 54:2460–2470

    CAS  Article  Google Scholar 

  32. Sugatani J, Sadamitsu S, Wada T et al (2012) Effects of dietary inulin, statin, and their co-treatment on hyperlipidemia, hepatic steatosis and changes in drug-metabolizing enzymes in rats fed a high-fat and high-sucrose diet. Nutr Metab (Lond) 9:23. https://doi.org/10.1186/1743-7075-9-23

    CAS  Article  Google Scholar 

  33. Sun B, Xie Y, Jiang J et al (2015) Pleiotropic effects of fenofibrate therapy on rats with hypertriglycemia. Lipids Health Dis 14:27. https://doi.org/10.1186/s12944-015-0032-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Tai M-H, Chen P-K, Chen P-Y et al (2014) Curcumin enhances cell-surface LDLR level and promotes LDL uptake through downregulation of PCSK9 gene expression in HepG2 cells. Mol Nutr Food Res 58:2133–2145. https://doi.org/10.1002/mnfr.201400366

    CAS  Article  PubMed  Google Scholar 

  35. Takeuchi K, Ueshima K, Ohuchi T, Okabe S (1994) Induction of gastric lesions and hypoglycemic response by food deprivation in streptozotocin-diabetic rats. Dig Dis Sci 39:626–634. https://doi.org/10.1007/BF02088352

    CAS  Article  PubMed  Google Scholar 

  36. Ugwu DI, Okoro UC, Mishra NK, Okafor SN (2018) Novel phenoxazinones as potent agonist of PPAR-α: design, synthesis, molecular docking and in vivo studies. Lipids Health Dis 17:120. https://doi.org/10.1186/s12944-018-0764-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Wang K, Bao L, Xiong W et al (2015) Lanostane triterpenes from the tibetan medicinal mushroom Ganoderma leucocontextum and their inhibitory effects on HMG-CoA reductase and α-glucosidase. J Nat Prod 78:1977–1989. https://doi.org/10.1021/acs.jnatprod.5b00331

    CAS  Article  PubMed  Google Scholar 

  38. Xavier HT, Izar MC, Faria Neto JR et al (2013) V Diretriz Brasileira de Dislipidemias e Prevenção da Aterosclerose. Arq Bras Cardiol 101:01–22. https://doi.org/10.5935/abc.2013S010

    CAS  Article  Google Scholar 

Download references

Acknowledgements

GG and RCF cultivated the mushroom and prepared the extract. AF and ER realized the analysis of the chemical composition of the extract. MCVD and MPJ were responsible for the treatment of the animals and performed and interpretation of the biochemical analyzes and the hematological profile. MCVD was a major contributor in writing the manuscript. Critical revision of the article was done by E.R, MC, MPJ and MS. Conception, experimental design, overall monitoring and final approval of the article was done by ER, MC, MPS and MS. All authors read and approved the final manuscript. This work was supported by the Coordination of Improvement of Higher Education Personnel (CAPES) (Grant Number 3255/2013) and National Council for Scientific and Technological Development (CNPq) (Grant Number 472153/2013-7), and the University of Caxias do Sul (UCS).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Maiza Von Dentz.

Ethics declarations

Ethical statement

The research was approved by the Ethics Committee of Animal Use of the University of Caxias do Sul (013/2015) and was performed according to the international guidelines for performing studies on animals.

Conflict of Interest

Maiza Cristina Von Dentz has no conflict of interest. Gabriela Gambato has no conflict of interest. Andreza Ferrari has no conflict of interest. Roselei Claudete Fontana has no conflict of interest. Eliseu Rodrigues has no conflict of interest. Mirian Salvador has no conflict of interest. Marli Camassola has no conflict of interest. Matheus Parmegiani Jahn has no conflict of interest.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Code availability

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Von Dentz, M., Gambato, G., Ferrari, A. et al. Antihyperlipidemic effect of the hydroalcoholic extract of Basidiomycete Pycnoporus sanguineus (Fr.) Murr. in streptozotocin-induced diabetic rats. ADV TRADIT MED (ADTM) (2020). https://doi.org/10.1007/s13596-020-00459-1

Download citation

Keywords

  • Anti-hyperlipidaemic
  • Hyperlipidaemia
  • Pycnoporus sanguineus
  • Diabetes mellitus
  • Cinnabarin