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Biologically Active Metabolites of the Genus Ganoderma: Three Decades of Myco-Chemistry Research

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Biologically Active Metabolites of the Genus Ganoderma: Three Decades of Myco-Chemistry Research Biologically active metabolites of the genus Ganoderma: Three decades of myco-chemistry research Ángel Trigos 1,2 Jorge Suárez Medellín 1,3 1 Laboratorio de Alta Tecnología de Xalapa, Universidad Veracruzana. Calle Médicos, 5, Col. Unidad del Bosque. C.P. 91010, Xalapa, Veracruz, México. 2 Instituto de Ciencias Básicas, Universidad Veracruzana, Av. Dos Vistas s/n, Carretera Xalapa-Las Trancas, 91000 Xalapa, Veracruz, México. 3 Unidad de Investigación y Desarrollo en Alimentos, Instituto Tecnológico de Veracruz. Av. Miguel A. de Quevedo # 2779 Col. Formando Hogar, C. P. 91680 Veracruz, Veracruz, México 1 1 0 Metabolitos biológicamente activos del género Ganoderma: tres décadas de 2 , investigación mico-química 3 8 - 3 6 Resumen. Desde la antigüedad en la medicina tradicional de oriente, hasta los tiempos : 4 modernos, los hongos pertenecientes al género Ganoderma se han utilizado para el 3 A tratamiento y la prevención de diversas enfermedades como cáncer, hipertensión y Í G diabetes, entre muchas otras afecciones. Así, a partir de los cuerpos fructíferos, micelio y O L O esporas de diferentes especies de Ganoderma se han aislado más de 140 triterpenoides C I M biológicamente activos y 200 polisacáridos, al igual que proteínas y otros metabolitos E diversos. Por lo que el objetivo de este trabajo, es mostrar un panorama general de los D A principales metabolitos biológicamente activos aislados de los miembros de este género N A C hasta la fecha, aunque sin pretender constituir una revisión exhaustiva, ya que tal cosa sería I X imposible dado el impresionante dinamismo del tema de investigación. E M Palabras clave: compuestos bioactivos, hongos medicinales, metabolitos terapeúticos, A T S polisacáridos, triterpenoides. I V E R Abstract. The fungi belonging to the genus Ganoderma have been used since ancient times / in Eastern traditional medicine in the treatment and prevention of several diseases such as o cancer, hypertension and diabetes, among many other conditions. More than 140 c i x biologically active triterpenoids and 200 polysaccharides, as well as proteins and é M n miscellaneous metabolites have been isolated from the fruiting bodies, mycelium and spores e a of different species of Ganoderma. The aim of this study is to summarize the main biologically s e r active metabolites isolated from members of this genus to date, yet without pretending to be p m I . an exhaustive review, since that would be impossible due the dynamism of the field. a í g o Key words: bioactive compounds, medicinal mushrooms, polysaccharides, therapeutic l o c metabolites, triterpenoids. i M e d a n Recibido 17 de marzo 2011; aceptado 17 de noviembre 2011. a c i x Received 17 March 2011; accepted 17 November 2011. e M a t s i v Introduction e as well as being a key ingredient in the formulation of tonics R 1 1 and sedatives (Lee et al., 2005). More recently, different 0 2 The fungi belonging to the genus Ganoderma (especially G. preparations made from mycelium, fruiting bodies and spores © lucidum), have been used since ancient times in Eastern of G. lucidum have been marketed as nutriceuticals or dietary traditional medicine, until modern days in the treatment and supplements due their antitumor, immunomodulatory and prevention of several diseases such as cancer, hypertension, free radical scavenging abilities (Mau et al., 2002; Wachtel- chronic bronchitis and asthma, among many other conditions, Galor et al., 2004; Wasser et al., 2000). The market for dietary Autor para correspondencia: Ángel Trigos supplements made from G. lucidum has been estimated at [email protected] N about 5 to 6 billion dollars per year, of which 1.6 billion Ó I S I V E R correspond only to its consumption within the United States Ganoderma lucidum complex, including non-polar although the latter show strong activity against lipid Triterpenoids derived from lanosterol (ganoderic acids N Ó I S (Zjawiony, 2004). In addition to G. lucidum, some other metabolites (mostly lanosterol derivatives and related peroxidation as well as scavenging hydroxyl and superoxide and related compounds) I V E species belonging to this genus have be seen to exert diverse compounds) and polar metabolites (polysaccharides, free radicals, among other properties (Jones and Janardhanan, From the non-polar fractions of G. lucidum extracts, more R salutary effects on human health, including G. tsugae, G. peptides and proteins). Then are listed the metabolites 2000; Lu et al., 2003). than 130 different triterpenoids have been isolated. All of applanatum, G. colossum, G. concinna, G. pfeifferi and G. isolated from other members of this genus, yet without them are highly oxygenated lanosterol derivatives with neo-japonicum (Gan et al., 1998; González et al., 2002; pretending to be an exhaustive review, since that would be Kleinwätcher et al., 2001; Lee et al., 2005; Mau et al., 2002; impossible due the dynamism of the field. Mothana et al., 2000; Zjawiony, 2004). The genus Ganoderma has been studied from many Biologically active compounds isolated from Ganoderma different points of view, depending on the interests of each lucidum complex research group: The most studied members of Ganodermataceae family are a) As a source of drugs and nutraceuticals (Boh, et al., 2007; without any doubt, the laccate species belonging to Fujita et al., 2005; Han and Yuan, 2005; Joseph et al., 2009; Ganoderma lucidum (Curtis) complex. These fungi, named Lindequist et al., 2005; Mau et al., 2002; Mizuno et al., 1995; Reishi in Japan and Ling-zhi in China, have been known since a m r Suárez-Medellín et al., 2007; Sliva et al., 2003; Tang et al., ancient times, and were even mentioned in the famous e d o 2005; Tasaka et al., 1988; Trigos and Suárez-Medellín, 2010; medical books Shen Nong Ben Cao Jing, (written during the n a G Wachtel-Galor et al., 2004; Wang et al., 2005; Wasser et al., Eastern Han Dynasty) and Ben Cao Gang Mu (written around s u n e 2000; Yang, 2005). 1590 A.C.). Among the wide range of diseases claimed to be g e h t b) As plant pathogens on crops like oil palm, coconut, rubber, successfully treated by G. lucidum are found be: hepatitis, f o tea, coffee, cocoa and forest trees (Karthikeyan et al., 2009; h y p e r c h o l e s t e r o l e m i a , d i a b e t e s , n e o p l a s m , s e t i l Paterson, 2007; Zakaria et al., 2005). immunodeficiency, leukopenia, atherosclerosis, o b a t c) As a cause of asthma due to the airborne dispersal of spores hemorrhoids, chronic fatigue, insomnia and dizziness caused e m e 1 (Craig and Levetin, 2000). by neurasthenia, in addition to the previously mentioned v 1 i t 0 c 2 d) As a source of ligninolytic enzymes with potential cancer, bronchitis and hypertension (Bao et al., 2001; Fujita et a , y l 4 l a 3 applications in pulping, textile dyes, detoxification of al., 2005; Gao et al., 2002; Hajjaj et al., 2005; Lu et al., 2003; c i A g Í o G polluted water and other biotechnological procedures (Hong Sliva et al., 2003;You and Lin, 2002). l o O i L B O and Jung, 2004; Songulashvili et al., 2006; Teerapatsakul et This surprising versatility is due to the large number . C n I í l l M al., 2007; Wang and Ng, 2006). of bioactive compounds isolated from this fungus. Overall, e d E e D e) And even as a dietary supplement for farm chickens (Ogbe most of the biologically active metabolites reported for G. M A z N e et al., 2008). lcidum fall into two main groups: those derived from r A á C I u X The aim of this study, is to summarize the main lanosterol (mostly ganoderic acids and related compounds) S . E J M , . biologically active metabolites isolated from members of and polysaccharides (Cole and Schweikert, 2003; Paterson, Á A , T s S I Ganoderma genus to date, in order to show an overview of the 2006). However, there are also reports of low molecular o V g i E r R state of art about the mycochemical research of this genus and weight peptides and proteins (Sripuan et al., 2003; Sun et al., T its potential use as a natural resource. 2004; Wang and Ng, 2006). It has been shown that aqueous The text is divided into two main sections. First are extracts of G. lucidum are particularly effective in inhibiting presented the biologically active metabolites isolated from the growth of sarcoma, while non-polar extracts are not, Figure 1. Some metabolites isolated from Ganoderma lucidum. 5 4 6 6 Table1. Biological activity of some non-polar metabolites isolated from Ganoderma lucidum Continue Table1 N Ó Metabolite Bioactivity Reference I Metabolite Bioactivity Reference S I V Ganoderic acids R, T, U, V, Cytotoxic-based carcinostatic effects on Toth et al., 1983; Sliva, 2003; Yuen E Ergosterol Inhibition of angiogenesis induced by solid Wiseman, 1993; Yazawa et al., 2000 R tumors; growth-inhibition of bladder cancer in Takaku et al., 2001; Yuan et al., W, X, Y and Z, lucidimol A cancer cells and Gohel, 2005 rats; inhibition of iron-dependent lipidic 2006; Kobori et al., 2007; Seo et al., and B, and ganodermanondiol peroxidation of membranes; reduction of pain 2009 associated to inflammation; reduction in the Ganoderic acids C1, G, g, Direct cytotoxicity on Meth-A and LLC Min et al., 2000; Yuen and Gohel, incidence of cardiovascular diseases and e and q, ganolucidic acid A, tumor cell lines 2005 antimicrobial activity; Anti-complement lucidenic acid a, lucidimol B; activity ganodermanondiol, against the classical pathway of the ganodermenonol, complement system ganodermadiol, lucialdehydes Ergosterol peroxide Cytostatic effect on HT29 cells; suppression Yuen and Gohel, 2005; Kobori et
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