The impact of puffball autolysis on selected chemical and biological properties: puffball extracts as potential ingredients of skin-care products


  • Predrag Petrović Innovation Center of the Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, 11060 Belgrade
  • Katarina Ivanović NIC Pharmaceutical doo, Osme crnogorske brigade 3, 11090 Belgrade
  • Aleksandra Jovanović Innovation Center of the Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, 11060 Belgrade
  • Milica Simović Department of Biochemical Engineering and Biotechnology, Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, 11060 Belgrade
  • Violeta Milutinović Department of Pharmacognosy, Faculty of Pharmacy, University of Belgrade, Vojvode Stepe 450, 11221 Belgrade
  • Maja Kozarski Institute for Food Technology and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
  • Miloš Petković Department of Organic Chemistry, Faculty of Pharmacy, University of Belgrade,Vojvode Stepe 450, 11221 Belgrade
  • Anka Cvetković Laboratory for Gas Chromatography, Institute for Public Health of Belgrade, Bulevar despota Stefana 54A, 11000 Belgrade
  • Anita Klaus Institute for Food Technology and Biochemistry, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11080 Belgrade
  • Branko Bugarski Department of Chemical Engineering, Faculty of Technology and Metallurgy, University of Belgrade, Karnegijeva 4, 11060 Belgrade


puffballs, mushrooms, tyrosinase inhibitory activity, antioxidant, cosmeceutical


Paper description:

  • Mature puffballs have been used in traditional medicine as haemostyptics.
  • Methanol extracts of young and mature fruiting bodies of Handkea excipuliformis and Vascellum pratense were subjected to chemical analysis, with accent on the compounds involved in skin care and regeneration, and screened for their antioxidant, tyrosinase-inhibitory and antimicrobial activities which could have a role in treatments of various skin conditions.
  • Mature fruiting body extracts are generally richer in N-acetylglucosamine, phenolics, α-tocopherol, ergosterol, linoleic acid and exhibited better antioxidant and tyrosinase-inhibitory activities.
  • Mature puffballs can be used as ingredients in medical and cosmetic skin products.

Abstract: Puffballs are fungi that produce globose fruiting bodies that undergo autolysis, transforming their insides into a spore bearing, powdery mass. Mature fruiting bodies are traditionally used to treat open skin wounds. In this study, methanol extracts of two puffball species, Handkea excipuliformis and Vascellum pratense, were examined and compared in order to provide insight into the changes these mushrooms undergo during maturation, with respect to their potential use in skin care and wound treatment. Some compounds involved in skin care and regeneration were quantified, and it was found that maturation increases the concentrations of almost all of these compounds. Antioxidant activity was also more pronounced in mature fruiting body extracts, which was in correlation with the higher content of antioxidants. Tyrosinase inhibition was vastly improved with autolysis, correlating with the higher phenolic content in mature fruiting body extracts. Antimicrobial activity was negatively affected by autolysis in the case of H. excipuliformis, whereas autolysis had little effect on the antimicrobial activity of V. pratense. Autolysis generally improved the biological activity and increased the concentrations of compounds involved in skin care, which justifies the traditional use of puffballs and makes them good candidates for various potential cosmetic and medicinal skin-care products.

Received: July 25, 2019; Revised: August 26, 2019; Accepted: August 28, 2019; Published online: September 5, 2019

How to cite this article: Petrović P, Ivanović K, Jovanović A, Simović M, Milutinović V, Kozarski M, Petković M, Cvetković A, Klaus A, Bugarski B. The impact of puffball autolysis on selected chemical and biological properties: Puffball extracts as potential ingredients of skin-care products. Arch Biol Sci. 2019;71(4):721-33.


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Larsson E, Jeppson M. Phylogenetic relationships among species and genera of Lycoperdaceae based on ITS and LSU sequence data from north European taxa. Mycol Res. 2008;112(1):4-22.

Coetzee J, van Wyk A. The genus Calvatia (Gasteromycetes, Lycoperdaceae): A review of its ethnomycology and biotechnological potential. Afr J Biotechnol. 2009;8(22):6007-15.

Læssøe T, Spooner B. The uses of ‘Gasteromycetes’. Mycologist. 1994;8(4):154-9.

Petrović P, Vunduk J, Klaus A, Carević M, Petković M, Vuković N, Cvetković A, Žižak Ž, Bugarski B. From mycelium to spores: A whole circle of biological potency of mosaic puffball. S Afr J Bot. 2019;123:152-60.

Skotti E, Anastasaki E, Kanellou G, Polissiou M, Tarantilis PA. Total phenolic content, antioxidant activity and toxicity of aqueous extracts from selected Greek medicinal and aromatic plants. Ind Crop Prod. 2014;53:46-54.

DuBois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric Method for Determination of Sugars and Related Substances. Anal Chem. 1956;28(3):350-6.

Petrović P, Vunduk J, Klaus A, Kozarski M, Nikšić M, Žižak Ž, Vuković N, Šekularac G, Drmanić S, Bugarski B. Biological potential of puffballs: A comparative analysis. J Funct Foods. 2016;21:36-49.

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 1999;26(9-10):1231-7.

Özyürek M, Güçlü K, Apak R. The main and modified CUPRAC methods of antioxidant measurement. Trac-Trend Anal Chem. 2011;30(4):652-64.

Barros L, Ferreira M, Queirós B, Ferreira IC, Baptista P. Total phenols, ascorbic acid, β-carotene and lycopene in Portuguese wild edible mushrooms and their antioxidant activities. Food Chem. 2007;103(2):413-9.

Alam N, Yoon KN, Lee JS, Cho HJ, Lee TS. Consequence of the antioxidant activities and tyrosinase inhibitory effects of various extracts from the fruiting bodies of Pleurotus ferulae Saudi J Biol Sci. 2012;19(1):111-8.

CLSI. Performance standards for antimicrobial susceptibility testing: 15th informational supplement. CLSI document M100-S15PA, USA: Wayne. 2005.

Klaus A, Kozarski M, Vunduk J, Todorovic N, Jakovljevic D, Zizak Z, Pavlovic V, Levic S, Niksic M, Van Griensven LJ. Biological potential of extracts of the wild edible Basidiomycete mushroom Grifola frondosa. Food Res Int. 2015;67:272-83.

Thevelein JM. Regulation of Trehalose Metabolism and Its Relevance to cell Growth and Function. In: Brambl R, Marzluf GA, editors. Biochemistry and Molecular Biology. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research). Vol 3. Berlin, Heidelberg: Springer; 1996. p. 395-420.

Wiemken A. Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie van Leeuwenhoek. 1990;58(3):209-17.

Richards A, Krakowka S, Dexter L, Schmid H, Wolterbeek A, Waalkens-Berendsen D, Shigoyuki A, Kurimoto M. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem Toxicol. 2002;40(7):871-98.

Pedrali A, Bleve M, Capra P, Jonsson T, Massolini G, Perugini P, Marrubini G. Determination of N-acetylglucosamine in cosmetic formulations and skin test samples by hydrophilic interaction liquid chromatography and UV detection. J Pharmaceut Biomed. 2015;107:125-30.

Nitschke J, Altenbach H, Malolepszy T, Mölleken H. A new method for the quantification of chitin and chitosan in edible mushrooms. Carbohydr Res. 2011;346(11):1307-10.

Harish Prashanth K, Tharanathan R. Chitin/chitosan: modifications and their unlimited application potential—an overview. Trends Food Sci Technol. 2007;18(3):117-31.

Butkhup L, Samappito W, Jorjong S. Evaluation of bioactivities and phenolic contents of wild edible mushrooms from northeastern Thailand. Food Sci Biotechnol. 2017;27(1):193-202.

Barros L, Venturini BA, Baptista P, Estevinho LM, Ferreira IC. Chemical Composition and Biological Properties of Portuguese Wild Mushrooms: A Comprehensive Study. J Agric Food Chem. 2008;56(10):3856-62.

Barros L, Dueñas M, Ferreira IC, Baptista P, Santos-Buelga C. Phenolic acids determination by HPLC–DAD–ESI/MS in sixteen different Portuguese wild mushrooms species. Food Chem Toxicol. 2009;47(6):1076-9.

Cujic N, Zugic A, Zivkovic J, Zdunic G, Savikin K. Preliminary safety estimate of cosmetic anti-age creams with chokeberry extract, using in vivo bioengineering techniques. Lekovite Sirovine. 2017;37:41-4.

Saini RK, Keum Y. Tocopherols and tocotrienols in plants and their products: A review on methods of extraction, chromatographic separation, and detection. Food Res Int. 2016;82:59-70.

Silva JR, Burger B, Kühl CM, Candreva T, Dos Anjos MB, Rodrigues HG. Wound Healing and Omega-6 Fatty Acids: From Inflammation to Repair. Mediat Inflamm. 2018; 2018:1-17.

Pereira LM, Hatanaka E, Martins EF, Oliveira F, Liberti EA, Farsky SH, Curi R, Pithon-Curi TC. Effect of oleic and linoleic acids on the inflammatory phase of wound healing in rats. Cell Biochem Funct. 2008;26(2):197-204.

Hobson R. Vitamin E and wound healing: an evidence-based review. Int Wound J. 2014;13(3):331-5.

Ding J, Kwan P, Ma Z, Iwashina T, Wang J, Shankowsky HA, Tredget EE. Synergistic effect of vitamin D and low concentration of transforming growth factor beta 1, a potential role in dermal wound healing. Burns. 2016;42(6):1277-86.

León-González AJ, Auger C, Schini-Kerth VB. Pro-oxidant activity of polyphenols and its implication on cancer chemoprevention and chemotherapy. Biochem Pharmacol. 2015;98(3):371-80.

Amirullah NA, Zainal Abidin N, Abdullah N. The potential applications of mushrooms against some facets of atherosclerosis: A review. Food Res Int. 2018;105:517-36.

Jovanovic A, Petrovic P, Ðordjevic V, Zdunic G, Savikin K, Bugarski B. Polyphenols extraction from plant sources. Lekovite Sirovine. 2017;37:45-9.

Nestorovic-Zivkovic J, Zivkovic S, Siler B, Anicic N, Dmitrovic S, Divac-Rankov A, Giba Z, Misic D. Differences in bioactivity of three endemic Nepeta species arising from main terpenoid and phenolic constituents. Arch Biol Sci. 2018;70(1):63-76.

Min Chang T. Tyrosinase and Tyrosinase Inhibitors. J Biocatal Biotransformation. 2012;1(2):1-2.

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

Zengin, G, Uysal S, Ceylan R, Aktumsek A. Phenolic constituent, antioxidative and tyrosinase inhibitory activity of Ornithogalum narbonense L. from Turkey: A phytochemical study. Ind Crop Prod. 2015;70:1-6.

Paun G, Neagu E, Albu C, Radu GL. Verbascum phlomoides and Solidago virgaureae herbs as natural source for preventing neurodegenerative diseases. J Herb Med. 2016;6(4):180-6.

Arumugam R, Kirkan B, Sarikurkcu C. Phenolic profile, antioxidant and enzyme inhibitory potential of methanolic extracts from different parts of Astragalus ponticus Pall. S Afr J Bot. 2018;120:268-73.

Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Wan-Mohtar W, Niksic M. Ganoderma lucidum as a cosmeceutical: Antiradical potential and inhibitory effect on hyperpigmentation and skin extracellular matrix degradation enzymes. Arch Biol Sci. 2019;71(2):253-64.

Miyake M, Yamamoto S, Sano O, Fujii M, Kohno K, Ushio S, Iwaki K, Fukuda S. Inhibitory Effects of 2-Amino-3H-phenoxazin-3-one on the Melanogenesis of Murine B16 Melanoma Cell Line. Biosci Biotechnol Biochem. 2010;74(4):753-8.

Ariff A, Salleh M, Ghani B, Hassan M, Rusul G, Karim M. Aeration and yeast extract requirements for kojic acid production by Aspergillus flavus link. Enzyme Microb Technol. 1996;19(7):545-50.

Ortonne J, Bissett DL. Latest Insights into Skin Hyperpigmentation. J Invest Derm Symp P. 2008;13(1):10-4.

Darlenski R, Surber C, Fluhr J. Topical retinoids in the management of photodamaged skin: from theory to evidence-based practical approach. Brit J Dermatol. 2010;163(6):1157-65.

Solano F. On the Metal Cofactor in the Tyrosinase Family. Int J Mol Sci. 2018;19(2):633

Gasco A, Serafino A, Mortarini V, Menziani E, Bianco MA, Ceruti Scurti J. An antibacterial and antifungal compound from Calvatia lilacina. Tetrahedron Lett. 1974;15(38):3431-2.

Umezawa H, Takeuchi T, Iinuma H, Ito M, Ishizuka M, Kurakata Y, Umeda Y, Nakanishi Y, Nakamura T, Obayashi A, Tanabe O. A new antibiotic, calvatic acid. J Antibiot. 1975;28(1):87-90.




How to Cite

Petrović P, Ivanović K, Jovanović A, Simović M, Milutinović V, Kozarski M, Petković M, Cvetković A, Klaus A, Bugarski B. The impact of puffball autolysis on selected chemical and biological properties: puffball extracts as potential ingredients of skin-care products. Arch Biol Sci [Internet]. 2019Dec.19 [cited 2024Jul.20];71(4):721-33. Available from:




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