Ganoderma lucidum as a cosmeceutical: antiradical potential and inhibitory effect on hyperpigmentation and skin extracellular matrix degradation enzymes

Authors

  • Maja Kozarski Department of Chemistry and Biochemistry, Institute of Food Technology and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade http://orcid.org/0000-0002-3576-5551
  • Anita Klaus Department of Industrial Microbiology, Institute of Food Technology and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
  • Dragica Jakovljević Institute of Chemistry, Technology and Metallurgy, University of Belgrade, Njegoševa 12, 11001 Belgrade
  • Nina Todorović Institute of Chemistry, Technology and Metallurgy, University of Belgrade, Njegoševa 12, 11001 Belgrade
  • Wan Abd Al Qadr Imad Wan-Mohtar Functional Omics and Bioprocess Development Laboratory, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur
  • Miomir Nikšić Department of Industrial Microbiology, Institute of Food Technology and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade

Keywords:

Ganoderma lucidum, cosmeceutical, maturate skin, oxidative stress, polysaccharide extracts

Abstract

Paper description:

  • Ganoderma lucidum (Curtis) P. Karst is a source of bioactive molecules with various medical activities.
  • The polysaccharide extracts of G. lucidum at different levels of purification protects skin from aging without cytotoxicity to HaCaT keratinocytes. Naturally-sourced inhibitors of collagenase, elastase and tyrosinase do not belong to polyphenolic extracts. Polysaccharide extracts are more efficient inhibitors of lipid peroxidation than additives commonly used in cosmeceutical formulations.
  • The results of this study point to the need for evaluating polysaccharide extracts in cosmeceutical studies as multi-functional and non-toxic natural products.

Abstract: Three different polysaccharide extracts of a wild European source of the mushroom Ganoderma lucidum were screened for their free radical-blocking potential, which could strengthen the skin’s barrier function, and provide a skin-lightening effect via potential inhibition of tyrosinase. The anti-collagenase and anti-elastase activities, which can help to restore skin elasticity and tensile strength, were also evaluated for the three extracts. Carbohydrates were the most abundant components of the extracts, followed by smaller quantities of proteins, phenols and flavonoids. The glucan fraction represented between 48% and 61% of carbohydrate content in all three extracts. None of the analyzed extracts showed overt toxicity to spontaneously-transformed immortal human keratinocytes (HaCaT) at concentrations up to 2 mg/mL, and displayed superior scavenging ability on 2,2′-azinobis(3-ethylbenzothiazoline-6-sulfonic acid (ABTS) and 1,1-diphenyl-2-picrylhydrazyl (DPPH) radicals. The hot water crude polysaccharide extract (HWCP) and partially purified fraction (HWPP) were found to be effective inhibitors of lipid peroxidation (LPx), with an almost two-fold increased inhibition of LPx compared with ascorbic acid (EC50=1.65±0.08 mg/mL), a common additive in cosmeceutical formulations and used at mg levels. Among the investigated extracts, HWCP showed the strongest inhibition potential on tyrosinase and skin extracellular matrix (ECM) degradation enzymes. These diverse functionalities indicate that G. lucidum may represent a promising source of natural cosmeceutical ingredients.

https://doi.org/10.2298/ABS181217007K 

Received: December 17, 2018; Revised: January 30, 2019; Accepted: January 31, 2019; Published online: March 5, 2019

How to cite this article: Kozarski M, Klaus A, Jakovljević D, Todorović N, Wan-Mohtar WAAQI, Nikšić M. Ganoderma lucidumas a cosmeceutical: Antiradical potential and inhibitory effect on hyperpigmentation and skin extracellular matrix degradation enzymes. Arch Biol Sci. 2019;71(2):253-64.

Downloads

Download data is not yet available.

Author Biography

Nina Todorović, Institute of Chemistry, Technology and Metallurgy, University of Belgrade, Njegoševa 12, 11001 Belgrade

References

Rinnerthaler M, Bischof J, Streubel MK, Trost A, Richter K. Oxidative stress in aging human skin. Biomolecules. 2015;5(2):545-89.

Haydont V, Bernard BA, Fortunel NO. Age-related evolutions of the dermis: Clinical signs, fibroblast and extracellular matrix dynamics. Mech Ageing Dev. 2019;177:150-6.

Poljšak B, Dahmane R. Free radicals and extrinsic skin aging. Dermatol Res Pract. 2012;2012:135206.

Kruk J, Duchnik E. Oxidative stress and skin diseases: possible role of physical activity. Asian Pac J Cancer Prev. 2014;15(2):561-8.

Naidoo K, Birch-Machin MA. Oxidative Stress and Ageing: The influence of environmental pollution, sunlight and diet on skin. Cosmetics. 2017;4:4.

Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrovic P, Niksic M, Vrvic MM, Van Griensven L. Antioxidants of edible mushrooms. Molecules. 2015;20(10):19489-525.

Mukherjee PK, Maity N, Nema NK, Sarkar BK. Bioactive compounds from natural resources against skin aging. Phytomedicine. 2011;19(1):64-73.

Diehl C. Melanocytes and Oxidative Stress. J Pigment Disord. 2014;1:127.

Ahmad MF. Ganoderma lucidum: Persuasive biologically active constituents and their health endorsement. Biomed Pharmacother. 2018;107:507-19.

Bishop KS, Kao CHJ, Xu Y, Glucina MP, Paterson RRM, Ferguson LR. From 2000 years of Ganoderma lucidum to recent developments in nutraceuticals. Phytochemistry. 2015;114:56-65.

Wasser SP. Reishi or Ling Zhi (Ganoderma lucidum). In: Wasser SP, Coates P, Blackman M, Cragg G, Levine M, Moss J, White J, editors. Encyclopedia of Dietary Supplements. New York: Marcel Dekker; 2005. p. 680-90.

Hyde KD, Bahkali AH, Moslem MA. Fungi-an unusual source for cosmetics. Fungal Divers. 2010;43(1):1-9.

Taofiq O, González-Paramás AM, Martins A, Barreiro MF, Ferreira ICFR. Mushrooms extracts and compounds in cosmetics, cosmeceuticals and nutricosmetics. Ind Crops Prod. 2016;90:38-48.

Wu Y, Choi MH, Li J, Yang H, Shin HJ. Mushroom cosmetics: The present and future. Cosmetics. 2016;3(3):22.

Phillips R. Mushrooms and other fungi of Great Britain & Europe. New York: Macmillan; 1979.

Klaus A, Kozarski M, Niksic M, Jakovljevic D, Todorovic N, Van Griensven LJLD. Antioxidative activities and chemical characterization of polysaccharides extracted from the basidiomycete Schizophyllum commune. LWT-Food Sci Technol. 2011;44(10):2005-11.

Dubois M, Gilles KA, Hamilton JK, Reders PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28(3):350-6.

Bradford MM. A refined and sensitive method for the quantitation of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem. 1976;72(1-2):248-55.

Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Niksic M, Vrvic MM, Van Griensven LJLD. Dietary polysaccharide extracts of Agaricus brasiliensis fruiting bodies: chemical characterization and bioactivities at different levels of purification. Food Res Int. 2014;64:53-64.

Kozarski M, Klaus A, Niksic M, Vrvic MM, Todorovic N, Jakovljevic D. Van Griensven LJLD. Antioxidative activities and chemical characterization of polysaccharide extracts from the widely used mushrooms Ganoderma applanatum, Ganoderma lucidum, Lentinus edodes and Trametes versicolor. J Food Comp Anal. 2012;26:144-53.

Jansson PE, Stenutz R, Widmalm G. Sequence determination of oligosaccharides and regular polysaccharides using NMR spectroscopy and a novel Web-based version of the computer program CASPER. Carbohyd Res. 2006;341(8):1003-10.

Wei L, Zhang W, Yin L, Yan F, Xu Y, Chen F. Extraction optimization of total triterpenoids from Jatropha curcas leaves using response surface methodology and evaluations of their antimicrobial and antioxidant capacities. Electron J Biotechnol. 2015;18(2):88-95.

Masuda T, Yamashita D, Takeda Y, Yonemori S. Screening for tyrosinase inhibitors among extracts of seashore plants and identification of potent inhibitors from Garcinia subelliptica. Biosci Biotechnol Biochem. 2005;69(1):197-201.

Azmi N, Hashim P, Hashim DM, Halimoon N, Majid NMN. Anti-elastase, anti-tyrosinase and matrix metalloproteinase-1 inhibitory activity of earthworm extracts as potential new anti-aging agent. Asian Pac J Trop Biomed. 2014;4(Suppl 1):S348-52.

Van Wart HE, Steinbrink DR. A continuous spectrophotometric assay for Clostridium histolyticum collagenase. Anal Biochem. 1981;113(2):356-65.

Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1-2):55-63.

Karaman M, Janjušević Lj, Jakovljević D, Šibul F, Pejin B. Anti-hydroxyl radical activity, redox potential and anti-AChE activity of Amanita strobiliformis polysaccharide extract. Nat Prod Res. 2018; 10.1080/14786419.2017.1422183

Pejin B, Tešanović K, Jakovljević D, Kaišarević S, Šibul F, Rašeta M, Karaman M. The polysaccharide extracts from the fungi Coprinus comatus and Coprinellus truncorum do exhibit AChE inhibitory activity. Nat Prod Res. 2017; 10.1080/14786419. 2017.1405417

Wang ZB, Pei JJ, Ma HL, Cai PF, Yan JK. Effect of extraction media on preliminary characterizations and antioxidant activities of Phellinus linteus polysaccharides. Carbohydr Polym. 2014;109:49 -55.

Silva D. Ganoderma lucidum in cancer research. Leuk Res. 2006;30(7):767-8.

Kerdudo A, Burger P, Merck F, Dingas A, Rolland Y, Michel T, Fernandez X. Development of a natural ingredient-Natural preservative: A case study. C R Chimie. 2016;19:1077-89.

Yang S, Sun Y, Geng Z, Ma K, Sun X, Fu X. Abnormalities in the basement membrane structure promote basal keratinocytes in the epidermis of hypertrophic scars to adopt a proliferative phenotype. Int J Mol Med. 2016;37(5):1263-73.

Kishk YFM, Al-Sayed HMA. Free-radical scavenging and antioxidative activities of some polysaccharides in emulsions. LWT- Food Sci Technol. 2007;40:270-7.

Pillai R, Redmond M, Roding J. Anti-wrinkle therapy: significant new findings in the non-invasive cosmetic treatment of skin wrinkles with beta-glucan. IFSCC Magazine. 2005;8(1):1-6.

Prior R., Wu X, Schaich K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem. 2005;53(10):4290-302.

Aioi A. Sirtuins in wound healing. Trends Immunother. 2017;1(3):114-20.

Blander G, Bhimavarapu A, Mammone T, Maes D, Elliston K, Reich C, Matsui MS, Guarente L, Loureiro JJ. SIRT1 promotes differentiation of normal human keratinocytes. J Invest Dermatol. 2009;129(1):41-9.

Rawlings ND, Barrett AJ, Thomas PD, Huang X, Bateman A, Finn RD. The MEROPS database of proteolytic enzymes, their substrates and inhibitors in 2017 and a comparison with peptidases in the PANTHER database. Nucleic Acids Res. 2018;46(D1):D624-32.

Cherrak SA, Mokhtari-Soulimane N, Berroukeche F, Bensenane B, Cherbonnel A, Merzouk H. Elhabiri M. In Vitro antioxidant versus metal ion chelating properties of flavonoids: a structure-activity investigation. PLoSOne. 2016;11(10):e0165575.

Lanigan RS, Yamarik TA. Final report on the safety assessment of EDTA, calcium disodium EDTA, diammonium EDTA, dipotassium EDTA, disodium EDTA, TEA-EDTA, tetrasodium EDTA, tripotassium EDTA, trisodium EDTA, HEDTA, and trisodium HEDTA. Int J Toxicol. 2002;21(Suppl 2):95-142.

Saewan N, Jimtaisong A. Photoprotection of natural flavonoids. J Appl Pharm Sci. 2013;3(09):129-41.

Glumac M, Pejin B, Karaman M, Mojović M, Matavulj M. Lignicolous fungi hydrodistilled extracts may represent a promising source of natural phenolics. Nat Prod Res. 2017;31(1):104-7.

Janjušević Lj, Pejin B, Kaišarević S, Gorjanović S, Pastor F, Tešanović K, Karaman M. Trametes versicolor ethanol extract, a promising candidate for health-promoting food supplement. Nat Prod Res. 2018;32(8):963-7.

Tešanović K, Pejin B, Šibul F, Matavulj M, Rašeta M, Janjušević Lj, Karaman M. A comparative overview of antioxidative properties and phenolic profiles of different fungal origins: fruiting bodies and submerged cultures of Coprinus comatus and Coprinellus truncorum J Food Sci Technol. 2017;54(2):430-8.

Janjušević Lj, Karaman M, Šibul F, Tommonaro G, Iodice C, Jakovljević D, Pejin B. The lignicolous fungus Trametes versicolor (L.) Lloyd (1920): a promising natural source of antiradical and AChE inhibitory agents. J Enzyme Inhib Med Chem. 2017;32(1):355-62.

Marcuse R. Antioxidative effect of amino-acids. Nature. 1960;186:886-7.

Schagen SK. Topical peptide treatments with effective anti-aging results. Cosmetics. 2017;4:16.

Klaus A, Kozarski M, Nikšić M, Jakovljević D, Todorović N, Stefanoska I, Van Griensven LJLD. The edible mushroom Laetiporus sulphureus as potential source of natural antioxidants. Int J Food Sci Nutr. 2013;64:599-610.

Jia RZ, Ding GC, Gu CM, Huang T, Rui C, Wang YX, Lu Q. CDX2 enhances HTR-8/SVneo trophoblast cell invasion by altering the expression of matrix metalloproteinases. Cell Physiol Biochem. 2014;34(3):628-36.

Downloads

Published

2019-06-04

How to Cite

1.
Kozarski M, Klaus A, Jakovljević D, Todorović N, Wan-Mohtar WAAQI, Nikšić M. Ganoderma lucidum as a cosmeceutical: antiradical potential and inhibitory effect on hyperpigmentation and skin extracellular matrix degradation enzymes. Arch Biol Sci [Internet]. 2019Jun.4 [cited 2024Nov.21];71(2):253-64. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/3759

Issue

Vol. 71 No. 2 (2019)

Section

Articles

License

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.

Most read articles by the same author(s)