10.6092/issn.2531-7342/12542
The edible and medicinal agaricoid and polyporoid mushrooms (phylum Basidiomycota, order Agaricomycetes) have long been known by humans as valuable food and medicines. They are producers of different groups of high- and low-molecular weight bioactive compounds (alkaloids, phenolics, polysaccharides, proteins, terpenoids, vitamins etc.) with around 130 therapeutic effects, including neuroprotective. Mushroom-derived biotech products are reported as effective neuroprotectants, however their potential to prevent or mitigate several neurodegenerative pathologies, such as Alzheimer and Parkinson diseases, epilepsy, depression and others has not been fully explored. This review discusses the neuroprotective potential of Agaricomycetes fungi and possibilities for their application as natural neuroprotectants.
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Agaricomycetes mushrooms (Basidiomycota) as potential neuroprotectants
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Zhao C, Zhang C, Xing Z, Ahmad Z, Li JS, Chang MW (2019) Pharmacological effects of natural Ganoderma and its extracts on neurological diseases: a comprehensive review. International Journal of Biological Macromolecules 121:1160–1178. https://doi.org/10.1016/j.ijbiomac.2018.10.076
Agaricomycetes mushrooms (Basidiomycota) as potential neuroprotectants
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                IJM - Italian Journal of Mycology
                ISSN 2531-7342 - Vol. 50 (2021): 30-43
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Review

                   Agaricomycetes mushrooms (Basidiomycota)
                          as potential neuroprotectants

                             Susanna M. Badalyan1* and Sylvie Rapior2*
1 Laboratory of Fungal Biology and Biotechnology, Institute of Pharmacy, Department of Biomedicine, Yerevan State
University, Yerevan, Armenia - E-mail: s.badalyan@ysu.am
2 Laboratoire de Botanique, Phytochimie et Mycologie, CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier,
France - E-mail: sylvie.rapior@umontpellier.fr

Corresponding author e-mail: s.badalyan@ysu.am, sylvie.rapior@umontpellier.fr


Article info
Received 22/2/2021; accepted 14/4/2021
https://doi.org/10.6092/issn.2531-7342/12542

Abstract
The edible and medicinal agaricoid and polyporoid mushrooms (phylum Basidiomycota, order Agaricomycetes) have
long been known by humans as valuable food and medicines. They are producers of different groups of high- and low-
molecular weight bioactive compounds (alkaloids, phenolics, polysaccharides, proteins, terpenoids, vitamins etc.)
with around 130 therapeutic effects, including neuroprotective. Mushroom-derived biotech products are reported as
effective neuroprotectants, however their potential to prevent or mitigate several neurodegenerative pathologies, such
as Alzheimer and Parkinson diseases, epilepsy, depression and others has not been fully explored. This review discusses
the neuroprotective potential of Agaricomycetes fungi and possibilities for their application as natural neuroprotectants.

Keywords
Agaricomycetes, antioxidant, anti-inflammatory, bioactive compounds, neurodegenerative, neuroprotective


Introduction
Neurodegeneration is incurable pathological process of progressive loss of structure and function of
nerve cells, which lead to their death. In recent years age-related neurodegenerative diseases (NDD),
such as Alzheimer’s, Parkinson’s and Meniere’s diseases, multiple sclerosis affecting more than
35 million people worldwide. Available scientific data support the theory that the oxidative stress-
derived neuro-inflammation in the neuron-glia system, as well as mitochondrial dysfunction are early
pathological conditions and key points in the pathogenesis of NDD (Lin and Beal, 2006; Kozarski
et al., 2015; Chen et al., 2016b; Trovato Salinaro et al., 2018). The functional role of mitochondria
and reactive oxygen species (ROS) formation are positively implicated in cellular stress response
mechanisms and highly regulated process controlled by different intracellular signalling pathways,
including vitagenes (Cornelius et al., 2013). The strategy to prevent the development of NDD is
a stress-free lifestyle, physical activity, and healthy diet, enriched with different natural products,
including mushroom supplements (Brandalise et al., 2017; Rossi et al., 2018; Bai et al., 2019; Fan et
al., 2019).
    Despite the advancement of pharmacological treatment of age-related NDD, their management
remains largely ineffective. Moreover, available drugs have always been associated with several side
effects, while natural products have gained recognition to prevent development of patho-neurological

Department of Agricultural and Food Science in partnership with the Italian Mycological Society (UMI).
The journal is hosted and mantained by ABIS-AlmaDL. © 2021 The Authors. This work is licensed under CC BY 4.0
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symptoms. Therefore, it is urgent to explore neuroprotectants with natural, including plant and
mushroom origin.
   Agaricomycetes mushrooms (phylum Basidiomycota) are widely distributed worldwide and
have been appreciated in traditional medicine for thousands of years for nutritional and medicinal
properties, as well as a part of human culture and religious attribute (Hobbs, 2004; Chang and Miles,
2004; Badalyan, 2012; Chang and Wasser, 2017; Badalyan and Zambonelli, 2019; Badalyan et al.,
2019).
   According to a large number of chemical and myco-pharmacological studies, mushrooms are
producer of different bioactive compounds (BAC) with neuroprotective effect (NPE) (Friedman,
2015; Chen et al., 2018a,b; Gupta et al., 2018; Badalyan et al., 2019; Lee et al., 2019; Yadav et al.,
2020; Badalyan and Rapior, 2021). Although the mechanism of neuroprotective action of mushroom-
derived BAC has not been thoroughly investigated, recent literature and research reviews reveal
their potential to prevent the development and mitigate the symptoms of NDD (Sabaratnam and
Phan, 2018; Yadav et al., 2020; Badalyan and Rapior, 2021). Several mushroom-derived biotech
products (pharmaceuticals, nutraceuticals and nutriceuticals) currently available in the market have
been demonstrated to be effective as neuroprotectants (Wang et al., 2014; Friedman, 2015; Bandara
et al., 2015; Phan et al., 2015; Thangthaeng et al., 2015; Brandalise et al., 2017; Rathore et al., 2017;
Rossi et al., 2018; Yin et al., 2018; Ho et al., 2020).
   The review discusses recent advances in research on the neuroprotective potential of
Agaricomycetes mushrooms belonging to different ecological and taxonomic groups and
perspectives of their biomedical application as neuroprotectants.

Neuroprotective potential of Agaricomycetes mushrooms
Agaricomycetes mushrooms have been used by humans from ancient times as food and medicine
(Chang and Miles, 2004; Hobbs, 2004; Badalyan, 2012; Chang and Wasser, 2017; Badalyan and
Zambonelli, 2019; Badalyan et al., 2019; Badalyan and Rapior, 2021). They are a source of different
BAC (β-glucans, lectins, phenolics, terpenoids, vitamins, etc.) possessing around 130 therapeutic
effects (i.e., antitumor, anti-inflammatory, anti-oxidant, anti-microbial, hypocholesterolemic,
hypoglycemic, etc.) (Badalyan, 2012; Gargano et al., 2017; Gupta et al., 2018; Morel et al., 2018;
Badalyan et al., 2019; Hyde et al., 2019). Scientific data are documented the NPE of several
mushrooms [i.e. Agaricus bisporus (J.E. Lange) Imbach, Ganoderma lucidum (Curtis) P. Karst.,
Hericium erinaceus (Bull.) Pers., Pleurotus ostreatus (Jacq.) P. Kumm., etc.] which could be highly
efficient in complementary therapy of neurological disorders (Park et al., 2012; Phan et al., 2017;
Sabaratnam and Phan, 2018; Chen et al., 2018a,b; Cui and Zhang, 2019; Lew et al., 2020; Badalyan
and Rapior, 2021). However, further myco-pharmacological studies, pre-clinical and clinical trials
are still required for the comprehensive evaluation of NPE of mushroom-derived products in the form
of approved clinical drugs (Badalyan et al., 2019; Lucius, 2020).
   Nowadays, dozens of mushroom species from different ecological (saprotrophs, xylotrophs,
mycorrhizal) and taxonomic (agaricoid, polyporoid, russuloid, hymenochaetoid, and others) groups are
biotechnologically cultivated and used as medicine however genetic mechanisms of their bioactivity
and medicinal effect have not been fully exploited, yet (Kües and Badalyan, 2017). The recent advances
in study of nutritional and medicinal values of Agaricomycetes, biotechnological production of
mycelial biomass and mushrooms have been reported, innovative biological, biochemical and genetic
approaches to produce health-enhancing mushroom-derived biotech products have been developed
(Chang and Wasser, 2017; Gargano et al., 2017; Gupta et al., 2018; Badalyan and Zambonelli, 2019;
Badalyan et al., 2019; Hyde et al., 2019; Badalyan and Rapior, 2021).

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   Study of Agaricomycetes biodiversity, assessment of bioresources and creation of specialized culture
collections will have an incredible impact on fundamental and applied myco-pharmacological and
biotechnological research to develop novel mushrooms-derived products, including neuroprotectants
(Badalyan and Gharibyan, 2016, 2017, 2020; Badalyan and Borhani, 2019a,b; Badalyan and
Zambonelli, 2019; Badalyan, 2020).

Neuroprotective compounds of Agaricomycetes mushrooms
Agaricomycetes, particularly agaricoid (order Agaricales) and polyporoid (order Polyporales) species
[Flammulina velutipes (Curtis) Singer, Lentinula edodes (Berk.) Pegler, Pleurotus (Fr.) P. Kumm.,
Ganoderma P. Karst., and Trametes Fr. species, etc.], as well as russuloid (order Russulales) species
Hericium erinaceus (Bull.) Pers. are recognized as rich source of neuroprotective compounds, such
as polysaccharides, terpenoids, phenolics, steroids, alkaloids, etc. (Badalyan, 2012; Phan et al.,
2012; Zhang et al., 2016b; Chen et al., 2018a,b; Ćilerdžić et al., 2018, 2019; Lemieszek et al., 2018;
Sabaratnam and Phan, 2018; Badalyan et al., 2019; Wang et al., 2019b; Badalyan and Rapior, 2021).
    Polysaccharides or β-glucans are one of the major BAC in mushrooms. Except immunomodulating
and antitumor activities they also possess significant antioxidant, anti-inflammatory, and
neuroprotective activities allowing to use them as potential neuroprotectants (Wasser and Didukh,
2005; Khan et al., 2014; Kozarski et al., 2015; He et al., 2017; Wang et al., 2019a; Badalyan et
al., 2019; Wu et al., 2019). The NPE of polysaccharides isolated from polyporoid chaga mushroom
Inonotus obliquus (Fr.) Pilát (Ning et al., 2014), and agaricoid [Agaricus bisporus, Coprinus comatus
(O. F. Müll.) Pers., Coprinellus truncorum (Scop.) Redhead, Vilgalys & Moncalvo and Pleurotus
eryngii (DC.) Quél.] and cantharelloid (Cantharellus cibarius Fr.) species have also been reported
(Mahmoud et al., 2014; Lemieszek et al., 2018; Pejin et al., 2019; Zhang et al., 2020). The NPE
of bioactive polysaccharides from well-known edible medicinal mushroom H. erinaceus and new
prospects for their usage as neuroprotectant is proposed (Friedman, 2015; Cheng et al., 2016; He et
al., 2017; Wang et al., 2019a).
    Agaricomycetes are also source of bioactive terpenoids, steroids, and sterols with neurotrophic and
anti-neuroinflammatory activity. Hericenones, hericipins and erinacines have been isolated from H.
erinaceus (Rupcic et al., 2018; Lee et al., 2020), cyathane diterpenes with from Cyathus africanus H.J.
Brodie and C. hookeri Berk. (Tang et al., 2019; Yin et al., 2019), lanostane triterpenes, ganoderic acid,
lucidone A, and aromatic meroterpenoids from G. lucidum (Wang et al., 2019b) and other Ganoderma
species [G. applanatum (Pers.) Pat., G. leucocontextum T. H. Li, W. Q. Deng, Sheng H. Wu, Dong M.
Wang & H. P. Hu, G. microsporum R. S. Hseu, G. resinaceum Boud.] (Chen et al., 2018a; Ćilerdžić
et al., 2018; Lai et al., 2019; Zhao et al., 2019). Anti-neuroinflammatory polyoxygenated lanostanoids
from Chaga mushroom I. obliquus were recently reported (Kou et al., 2021).
    Phenolics, such as hispidin and derivatives were isolated from G. applanatum, Phellinus baumii
Pilát, Trametes versicolor (L.) Lloyd, and T. gibbosa (Pers.) Fr. They possess diverse pharmacological
effects, including anti-inflammatory, antioxidant and neuroprotective (Palacios et al., 2011; Khatua et
al., 2013; Kozarski et al., 2015; Pop et al., 2018; Jiang et al., 2020).

Agaricomycetes mushrooms as neuroprotectants
Medicinal Agaricomycetes species with protective effects against oxidation and inflammation can be
used as neuroprotectants in treatment of various life-style and age-related chronic diseases, including
NDD (Palacios et al., 2011; Thangthaeng et al., 2015; Phan et al., 2015, 2017; Badalyan et al. 2019;
Yadav et al., 2020; Badalyan and Rapior, 2021). It was reported that mushroom-based daily diets can
improve the cognitive abilities in ageing people and prevent the neurodegeneration (Rathore et al.,

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2017; Rossi et al., 2018; Sabaratnam and Phan, 2018; Yin et al., 2018; El Sayed and Ghoneum, 2020).
However, scientific validation and further clinical trials are required to understand the molecular and
biochemical mechanisms involved in the stimulation of neurite outgrowth and consider mushrooms
as neuroprotectants (Badalyan et al., 2019; Cui and Zhang, 2019; Lucius, 2020; Badalyan and Rapior,
2021).
    Several agaricoid, polyporoid, russuloid, cantharelloid and other groups of agaricomycetous
mushrooms, such as A. bisporus (Kozarski et al., 2020), Agaricus brasiliensis Fr. (Qin and Han,
2014), Auricularia polytricha (Mont.) Sacc. (Bennett et al., 2013), Amanita caesarea (Scop.) Pers.
(Li et al., 2017), Cantharellus cibarius (Lemieszek et al., 2018), Laetiporus sulphureus (Bull.)
Murrill, and P. ostreatus (Ćilerdžić et al., 2018, 2019), Fomitopsis betulina (Bull.) B. K. Cui, M.
L. Han & Y. C. Dai, and Fomitopsis officinalis (Vill.) Bondartsev & Singer (Pleszczyńska et al.,
2017; Muszyńska et al., 2020), G. lucidum (Rahman et al., 2020), H. erinaceus (Ma et al., 2010),
Lignosus rhinocerotis [= L. rhinocerus (Cooke) Ryvarden] (Farha et al., 2019), Phellinus linteus
(Berk. & M. A. Curtis) Teng (Chen et al., 2016a), Trametes (= Coriolus) species (Knežević et al.,
2018; Scuto et al., 2020), as well as Flammulina velutipes (Phan et al., 2017; Sabaratnam and Phan,
2018), Grifola frondosa (Dicks.) Gray (Fan et al., 2019), Lentinus edodes (Berg.) Singer (Diallo et
al., 2020) and Pleurotus giganteus (Berk.) Karun. & K. D. Hyde (Phan et al., 2012, 2014) have been
used in traditional medicine as neuroprotective and antidepressant agents against ageing-related NDD
(Fig. 1). Among these, H. erinaceus, G. lucidum, L. edodes and Polyporus umbellatus (Pers.) Fr. are
widely used as bio-ingredients in the formulation of cholesterol-free natural food products (Chang
and Buswell, 1996; Ma et al., 2010; Bandara et al., 2015; Rossi et al., 2018; Sabaratnam and Phan,
2018; Yin et al., 2018; Ho et al., 2020).
    Currently, around 80 different BAC from over 20 brain-improving culinary and medicinal
mushrooms have been reported, molecular mechanisms of neuroprotection and possible clinical
trials are discussed (Phan et al., 2015; Badalyan and Rapior, 2021). Nevertheless, before the clinical
application of mushroom-derived neuroprotectants as preventive and therapeutic drugs the synergistic
effects of isolated biocompounds and stabilization for their administration needs to be appropriately
evaluated (Badalyan et al., 2019; Gründemann et al., 2020; Lucius, 2020; Badalyan and Rapior,
2021).
    One of the major etiological factors of Alzheimer’s disease is oxidative stress, which accelerates
β - amyloid peptide plaque accumulation in the brain. Edible medicinal agaricoid oyster mushrooms
(P. eryngii, P. giganteus, P. ostreatus) contain a high level of antioxidants, including ergothioneine,
adenosine, and polyphenol, which reduce the age-related oxidative stress (Badalyan, 2012; Phan et
al., 2014; Ćilerdžić et al., 2019; Liang et al., 2020; Zhang et al., 2020).
    Several white-rot polyporoid fungi, such as Trametes (= Coriolus) species, have been used for
centuries in the traditional medicine, however only T. versicolor has been comprehensively studied
(Knežević et al., 2018; Pop et al., 2018; Kıvrak et al., 2020). The mycelial extract of T. versicolor was
the most effective inhibitor of acetylcholinesterase activity, while extract of T. gibbosa significantly
inhibited tyrosinase activity. The chemical screening revealed strong synergistic action of content of
BAC produced by studied Trametes species (Knežević et al., 2018). According to research data the
role of the inflammasome and the importance of Coriolus (= Trametes) and Hericium derived nutra-
and nutriceuticals in neuroprotection have been considered (Trovato Salinaro et al., 2018).




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                                a                                         b                                              c




                                        d                                     e                                          f




                                    g                                     h                                              i




                                            j                                     k                                      l
Legend
Fig. 1. Agaricoid and polyporoid mushrooms with neuroprotectant potential: (a) Flammulina velutipes (Photo Courtesy
of PM Marty); (b) Laetiporus sulphureus (Photo Courtesy of PM Marty; (c) Auricularia polytricha (Photo Courtesy of
JC Malaval); (d) Ganoderma lucidum (Photo Courtesy of JC Malaval); (e) Trametes versicolor (Photo Courtesy of JC
Malaval); (f) Clitocybe geotropa (Photo Courtesy of JC Malaval); (g) Lentinus edodes (Photo Courtesy of AR Bandara,
(h) Cantharellus cibarius (Photo Courtesy of AR Bandara; (i) Pleurotus ostreatus (Photo Courtesy of C Angelini); (j)
Grifola frondosa (Photo Courtesy of C Angelini); (k) Amanita caesarea (Photo Courtesy of JC Malaval) and (l) russuloid
species Hericium erinaceus (Photo Courtesy of AR Bandara).


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   Well-known maitake mushroom, G. frondosa, contains a high amount of health-enhancing BAC
and possesses nutritional and medicinal values (Badalyan and Zambonelli, 2019; Badalyan et al., 2019;
Bai et al., 2019; Fan et al., 2019). It has been reported that proteoglucan from G. frondosa (PGM) can
improve learning and memory; decrease the loss of neurons and histopathological abnormalities in
mice. Moreover, PGM treatment could activate microglia, astrocytes, promote microglial recruitment
to the β-amyloid plaques and enhance their phagocytosis, thereby alleviating pathological changes
in the cortex and hippocampus. The administration of PGM as a dietary supplement may provide
potential benefits on brain age-related memory dysfunction (Bai et al., 2019; Fan et al., 2019).
   Several other Agaricomycetes species [Antrodia cinnamomea T. T. Chang & W. N. Chou, Armillaria
mellea (Vahl.) P. Kumm., Calocybe indica Purkay. & A. Chandra, Clitocybe geotropa (Bull.) Quél.,
Dictyophora indusiata (Vent.) Desv., Hygrophorus eburneus (Bull.) Fr., Paxillus panuoides (Fr.)
Fr., Polyporus umbellatus, Poria cocos F. A. Wolf, Tremella fuciformis Berk., etc.] have also been
reported as potential neuroprotectants (Lee et al., 2003; Park et al., 2012; Hsieh et al., 2013; Lu et al.,
2013; Bandara et al., 2015, 2019; Zhang et al., 2016b; Rathore et al., 2017; Lee et al., 2019, 2020; Wu
et al., 2019; Huang et al., 2020; Kosanić et al., 2020a,b; Badalyan and Rapior, 2021) (Fig. 1).
   Further studies of biomedical potential of Agaricomycetes mushrooms will assist development
and formulation of novel mushrooms-derived neuroprotectants.

Conclusion
Presently, human age-related neurodegenerative and psychotropic diseases are affecting the adult
population worldwide. Therefore, discovering new resources of natural medicines, including plant-
and mushrooms-derived biotech products is topical. This review discusses the current state of
knowledge and the findings of recent studies on the neuroprotective potential of Agaricomycetes
mushrooms. However, the list of studied species is far from being completed.
   Future interdisciplinary research involving physicians, biologists, chemists, pharmacologists
and mycologists collaborating with social scientists is required to create a scientific framework that
incorporates traditional and clinical knowledge and experience to assist in the use of mushroom
resources for human welfare.

Acknowledgments
This review arises from a long-standing collaboration between two authors (S.M.B. and S.R.) on
research directed to the chemical composition and biotechnological potential of Basidiomycetes
mushrooms. The realization of research work was performed in collaboration between the Yerevan
State University, Armenia and Faculty of Pharmacy of the University of Montpellier, France. We would
like to thank our colleagues Jean-Claude Malaval and Pierre-Michel Marty (Société d’Horticulture
et d’Histoire Naturelle de l’Hérault, Montpellier, France), Claudio Angelini (Pordenone, Italy) and
Asanka R Bandara (Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China)
for kindly providing photos of medicinal mushrooms (Fig. 1).



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