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Review Article Natural Products and Biological Activity of the Pharmacologically Active Cauliflower Mushroom Sparassis Crispa

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Review Article Natural Products and Biological Activity of the Pharmacologically Active Cauliflower Mushroom Sparassis Crispa Hindawi Publishing Corporation BioMed Research International Volume 2013, Article ID 982317, 9 pages http://dx.doi.org/10.1155/2013/982317 Review Article Natural Products and Biological Activity of the Pharmacologically Active Cauliflower Mushroom Sparassis crispa Takashi Kimura Research&DevelopmentCenter,UnitikaLtd.,23Uji-Kozakura,Uji,Kyoto611-0021,Japan Correspondence should be addressed to Takashi Kimura; [email protected] Received 4 October 2012; Accepted 25 February 2013 Academic Editor: Fabio Ferreira Perazzo Copyright © 2013 Takashi Kimura. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Sparassis crispa, also known as cauliflower mushroom, is an edible mushroom with medicinal properties. Its cultivation became popular in Japan about 10 years ago, a phenomenon that has been attributed not only to the quality of its taste, but also to its potential for therapeutic applications. Herein, I present a comprehensive summary of the pharmacological activities and mechanisms of action of its bioactive components, such as beta-glucan, and other physiologically active substances. In particular, the immunomodulatory mechanisms of the beta-glucan components are presented herein in detail. 1. Introduction 2. Chemical Constituents and Bioactive Components of S. crispa Medicinal mushrooms have an established history of use in traditional Asian therapies. Over the past 2 to 3 decades, Scientific investigation has led to the isolation of many com- scientific and medical research in Japan, China, and Korea, pounds from S. crispa that have been shown to have health- and more recently in the United States, has increasingly promoting activities. The fruiting bodies of S. crispa contain demonstrated the potent and unique properties of com- approximately 90% water, protein, lipid, carbohydrate, ash, pounds extracted from mushrooms for the prevention and and dietary fiber (Table 1)[3]. Furthermore, the content of treatment of cancer and other chronic diseases. Various vitamin D2, which aids intestinal calcium absorption, was important pharmaceutical products with proven medicinal shown to be 0.17 mg per 100 g of dry weight, a concentration applications have been derived from mushrooms [1]. that is higher than that observed in other mushrooms [4]. Sparassis crispa Wulf.:Fr. (Figure 1), also known as Also S. crispa contained a relatively large amount of glucosyl cauliflower mushroom, is an edible mushroom with various ceramide (approximately 0.2%), which is a glycoside of medicinal properties whose cultivation has recently become ceramide. It was demonstrated that the moiety of sphingoid popularinJapan.ThetaxonomyofS. crispa is as follows: king- base was characterized by the unique structure [5]. Though dom, Fungi; phylum, Basidiomycota; class, Agaricomycetes; S. crispa has a scent of its own, the results of headspace order, Polyporales; family, Sparassidaceae; genus, Sparassis; analyses showed that 3-octanone, DL-3-octanol, and 1-octen- and species, crispa.Itisabrown-rotfungusthatprimarily 3-ol contributed mutually to the particular aroma of this growsonthestumpsofconiferoustreesandiswidely mushroom [6]. It is noteworthy that the beta-glucan content distributed throughout the North Temperate Zone. S. crispa of S. crispa is more than 40% of the dry weight of the fruiting has been reported to have many biological activities, which bodies, as measured by the enzyme method of the Japan Food are detailed below. Research Laboratories (Tokyo) [3]. 2 BioMed Research International shown to stimulate leukocytes to produce cytokines such as IL-8 in whole-cell cultures of human peripheral blood [13] and in mouse splenocytes [14]. Yamamoto et. al reported antiangiogenic and anti- metastatic effects of SCG on neoplasm by using different animal models [8]. Oral administration of SCG suppressed B16-F10 cell-induced angiogenesis in a dorsal air sac assay using ICR mice and suppressed vascular endothelial growth factor induced neovascularization in a Matrigel plug assay using C57BL/6J mice. Furthermore, it suppressed the growth and number of metastatic tumor foci in the lung, along with primary tumor growth in a C57BL/6J mice model of spontaneous metastasis. From these findings, it is apparent that the oral administration of SCG exerts a suppressive effect on tumor growth and metastasis in the lung through the inhibition of tumor-induced angiogenesis. Taken together, these results demonstrate that SCG ex- 10 cm hibits various biological activities, including antitumor effects, enhancement of the hematopoietic response, and Figure 1: Sparassis crispa Wulf.:Fr. [2]. induction of cytokine production in vivo and in vitro. Table 1: Approximate composition of Sparassis crispa (per 100 g dry sample). 2.1.3. Mechanisms. Harada et al. reported strain-specific Components Amount (g) differences of the reactivity of mice to SCG, with DBA/1 and Protein 13.4 DBA/2 mice being highly sensitive to SCG. In splenocytes Fat 2.0 derived from various inbred strains of mice, interferon- Ash 1.8 (IFN-) production was not induced by SCG. However, Carbohydrate 21.5 splenocytes from na¨ıve DBA/1 and DBA/2 mice strongly Dietary fiber (DF) 61.2 react with SCG to produce IFN- [14]. Furthermore, Beta-glucan from DF 43.5 in addition to IFN-, cytokines induced by SCG were screened for and found to include tumor necrosis factor- (TNF-), granulocyte-macrophage colony-stimulating factor 2.1. Polysaccharide (Beta-Glucan) (GM-CSF), and interleukin-12 (IL-12p70) [15]. Since the sera of na¨ıve DBA/1 and DBA/2 mice contain significantly higher 2.1.1. Primary Structure. Using chemical, enzymatic, and titers of antibody against SCG than other strains of mice [16], NMR analyses, it was shown that the primary structure it seems likely that these mice strains are sensitive to SCG. of a purified beta-glucan (designated SCG), obtained from Thus, DBA/1 and DBA/2 mice would be useful models for cultured fruiting bodies of S. crispa is a 6-branched 1,3-beta- future studies of SCG. glucan, with one branch in approximately every 3 main chain Harada et al. further demonstrated that GM-CSF was one units (Figure 2)[7–9]. of the key factors in reactivity to SCG in DBA/2 mice [15, 17]. Neutralizing GM-CSF using an anti-GM-CSF monoclonal 2.1.2. Biological Activities. Tumor size in cancerous (Sarcoma antibody significantly inhibited IFN-,TNF-,andIL-12p70 180) ICR mice was dose-dependently decreased after 5 weeks elicited by SCG. The splenocytes in various strains of mice of oral administration of S. crispa (10 or 100 mg/kg) in showedsimilarpatternsofcytokineproductioninresponse comparison to a control group. Furthermore, the survival rate toSCGcotreatmentinthepresenceofrecombinantmurine of these model mice was higher when similarly treated with GM-CSF. The high sensitivity to SGG shown by DBA/1 S. crispa [2]. Since SCG content in dry powder of S. crispa was and DBA/2 mice may be attributable to differences of their measured to be more than 40%, SCG was likely be responsible regulation of GM-CSF compared with that in other mice. for this antitumor effect. Harada and Ohno also proposed an interesting model for Ohno et al. prepared polysaccharide fractions from the the mechanism of cytokine induction by SCG in DBA/2 mice fruiting bodies of cultured S. crispa andshowedtheiranti- [18]. Broadly speaking, SCG directly induces adherent cells tumor activity against the solid form of Sarcoma 180 in ICR to produce TNF- and IL-12p70, whereas cell-cell contact + mice with strong vascular dilation and hemorrhage reactions mediated by the association of CD4 T cells expressing LFA-1 [7]. Furthermore, intraperitoneal and oral SCG over a wide and antigen-presenting cells such as dendritic cells expressing range of concentrations enhanced hematopoietic responses ICAM-1 is required for the induction of IFN- and GM-CSF in mice with leukopenia induced by cyclophosphamide (CY, by SCG. aDNA-alkylatingagent)[10, 11]. This effect was augmented Neutrophils, macrophages, and dendritic cells express in combination with isoflavone aglycone [12]. SCG was also several receptors capable of recognizing beta-glucan in its BioMed Research International 3 H HO OH HO H H H O OH H O OH H OH H H H H H O O O HO HO HO O O O O H H H OH OH OH H H H H H H Figure 2: Chemical structure of SCG [9]. various forms. Dectin-1, complement receptor 3, lactosylce- production and dectin-1 expression, such as CY, can control ramide, and scavenger and Toll-like receptors are all candi- reactivity to SCG and the expression of various cytokines. dates that have been reported thus far [19–23]. Among these, Shibata et al. found that both GM-CSF and TNF- dectin-1, which is a C-type lectin, is an archetypical non-Toll- synthesis in DBA/2 mouse splenocytes stimulated with SCG, like pattern recognition receptor expressed predominantly but not with lipopolysaccharide, were significantly enhanced by myeloid cells. Dectin-1 can induce its own intracellular inthepresenceofcytochalasinD(CytD),aninhibitorof signaling and can mediate a variety of cellular responses, such actin polymerization [27]. On the other hand, Kim et al. as cytokine production [24]. pointed out the importance of the role of Toll-like recep- The magnitude of cytokine induction from bone- tor 4 (TLR4) [28]. They examined the effect of SCG on marrow-derived dendritic cells (BMDCs) by SCG and the adherent monocytes, such as macrophages and
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