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A Review of Fungal Protoilludane Sesquiterpenoid Natural Products

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A Review of Fungal Protoilludane Sesquiterpenoid Natural Products antibiotics Review A Review of Fungal Protoilludane Sesquiterpenoid Natural Products Melissa M. Cadelis 1,2,* , Brent R. Copp 1 and Siouxsie Wiles 2 1 School of Chemical Sciences, University of Auckland, 23 Symonds Street, Auckland 1010, New Zealand; [email protected] 2 Bioluminescent Superbugs Lab, School of Medical Sciences, University of Auckland, 85 Park Road, Grafton, Auckland 1023, New Zealand; [email protected] * Correspondence: [email protected] Received: 1 December 2020; Accepted: 18 December 2020; Published: 19 December 2020 Abstract: Natural products have been a great source for drug leads, due to a vast majority possessing unique chemical structures. Such an example is the protoilludane class of natural products which contain an annulated 5/6/4-ring system and are almost exclusively produced by fungi. They have been reported to possess a diverse range of bioactivities, including antimicrobial, antifungal and cytotoxic properties. In this review, we discuss the isolation, structure elucidation and any reported bioactivities of this compound class, including establishment of stereochemistry and any total syntheses of these natural products. A total of 180 protoilludane natural products, isolated in the last 70 years, from fungi, plant and marine sources are covered, highlighting their structural diversity and potential in drug discovery. Keywords: sesquiterpenoid; natural products; protoilludanes 1. Introduction Fungi remain an untapped source of bioactive natural products with an estimate of over 1.5 million species of fungi worldwide, of which only approximately 7% have been chemically investigated [1–6]. Over 90% of the recorded species are higher fungi which are considered one of the largest biodiverse resources on Earth. With the development of fungal natural product isolation techniques and a better understanding of biosynthetic pathways, higher fungi have become an abundant source for drug discovery. Ascomycota, the largest phylum of fungi, is one of the two divisions of higher fungi along with Basidiomycota. Both divisions of higher fungi, having undergone evolution to survive harsh and unfavourable environments, are well known producers of an array of structurally diverse natural products that possess a variety of bioactivities. These natural products can be divided into several groups by their chemical structures, one of which are the terpenoids. Representative terpenoid scaffolds in higher fungi include sesquiterpenoids, diterpenoids and triterpenoids which are all derived from common precursors [1–6]. Fungal terpenoid natural products are derived from isoprene units (C5) and are classified by the number of isoprene units in the structure [7–11]. Higher terpenoids such as monoterpenoids (C10), sesquiterpenoids (C15) and diterpenoids (C20) are synthesised from two isoprene intermediates, dimethylallyl pyrophosphate (DMAPP) and isopentenyl pyrophosphate (IPP), in the mevalonate pathway. The mevalonate pathway begins with the phosphorylation of mevalonic acid, derived from acetyl-CoA, by two molecules of adenosine triphosphate (ATP). Subsequent decarboxylation forms IPP, the stereospecific isomerisation of which affords DMAPP (Scheme1). Loss of diphosphate from DMAPP forms an allylic cation which undergoes nucleophilic attack by IPP to afford geranyl diphosphate. Reaction of geranyl diphosphate with another unit of IPP gives farnesyl diphosphate Antibiotics 2020, 9, 928; doi:10.3390/antibiotics9120928 www.mdpi.com/journal/antibiotics Antibiotics 2020, 9, 928 2 of 29 Antibiotics 2020, 9, 928 2 of 29 from which sesquiterpenoids (C15) are derived. Repetition of this process results in the formation of terpenoidfrom which chains sesquiterpenoids of different (C length.15) are derived. Linear terpenoidsRepetition of can this undergo process results cyclisation in the formation by a number of of terpenoid chains of different length. Linear terpenoids can undergo cyclisation by a number of different terpene cyclases which can generate numerous terpenoid scaffolds [7–11]. different terpene cyclases which can generate numerous terpenoid scaffolds [7–11]. SchemeScheme 1. Biosynthesis 1. Biosynthesis of sesquiterpenoidsof sesquiterpenoids from from isopentenylisopentenyl pyrophosphate pyrophosphate (IPP) (IPP) and and dimethylallyl dimethylallyl pyrophosphate (DMAPP) through the mevalonate pathway. pyrophosphate (DMAPP) through the mevalonate pathway. Cyclisation of farnesyl diphosphate can produce a wide range of natural products, many of Cyclisation of farnesyl diphosphate can produce a wide range of natural products, many of which are biosynthesised through a cyclisation pathway involving a humulyl cation [12–15]. The which are biosynthesised through a cyclisation pathway involving a humulyl cation [12–15]. humulene pathway proceeds through 1,11-cyclisation of 2E,6E-farnesyl diphosphate to afford the The humulenetrans-humulyl pathway cation proceedswhich can throughthen undergo 1,11-cyclisation rearrangement of to 2E produce,6E-farnesyl a number diphosphate of different to classes afford the trans-humulylof sesquiterpenoid cation which carbon can skeletons then undergo including rearrangement α-humulene and to produce (E)-β-caryophyllene. a number of Of di ffinteresterent classesis of sesquiterpenoidthe 2,9 and 3,6-cyclisation carbon skeletons product, protoilludyl including α cation,-humulene the precursor and (E to)- βvarious-caryophyllene. protoilludane Of natural interest is the 2,9products and 3,6-cyclisation [12–15]. product, protoilludyl cation, the precursor to various protoilludane natural products [Sesquiterpenoid12–15]. protoilludane natural products contain a characteristic annulated 5/6/4-ring Sesquiterpenoidsystem and have protoilludanebeen reported naturalto possess products a diverse contain range aof characteristic bioactivities. annulatedThey have 5been/6/4-ring systempredominantly and have been isolated reported from to higher possess fungi a diverse (96%) with range very of bioactivities. few examples Theyfrom marine have been (1%) predominantly and plant (3%) sources (Figure 1). A total of 180 examples of this class have been isolated over a span of 70 years isolated from higher fungi (96%) with very few examples from marine (1%) and plant (3%) sources with almost half of these natural products being isolated in the last 20 years (Figure 2). (Figure1). A total of 180 examples of this class have been isolated over a span of 70 years with almost The purpose of this review is to give an overview of sesquiterpenoid protoilludane natural half ofproducts these natural bearing products an annulated being 5/6/4-ring isolated system in the and last does 20 years not cover (Figure the 2structurally). related illudins Thewhich purpose are derived of this from review protoilludane is to give precursors. an overview In this review, of sesquiterpenoid we will first discuss protoilludane the isolation, natural productsstructure bearing elucidation, an annulated establishment 5/6/4-ring of stereo systemchemistry and does and notsummarise cover thethe structurallybioactivities relatedof illudinssesquiterpenoid which are derivedprotoilludan frome natural protoilludane products isolated precursors. to date Infrom this fungal review, origins we beginning will first with discuss the isolation,those isolated structure from elucidation, Basidiomycota establishment followed ofby stereochemistry Ascomycota. We and will summarise then briefly the bioactivities cover of sesquiterpenoidprotoilludanes protoilludaneisolated from other natural sources. products We isolatedwill acknowledge to date from any fungalknown originssyntheses beginning of these with thosenatural isolated products from Basidiomycota but will not elaborate followed on bythese, Ascomycota. as a comprehensive We will overview then briefly of synthetic cover protoilludanes attempts towards this class of natural products has been reported previously [14]. A short discussion on the isolated from other sources. We will acknowledge any known syntheses of these natural products but biosynthetic studies conducted on these natural products has also been included. will not elaborate on these, as a comprehensive overview of synthetic attempts towards this class of natural products has been reported previously [14]. A short discussion on the biosynthetic studies conducted on these natural products has also been included. Antibiotics 2020, 9, 928 3 of 29 AntibioticsAntibiotics 2020 2020, 9,, 9928, 928 3 of3 of29 29 Figure 1. Isolation sources of protoilludane natural products. FigureFigure 1. 1.Isolation Isolation sources sources of of protoilludane protoilludane natural natural products. products. FigureFigureFigure 2. Timeline2. 2.Timeline Timeline of of of thethe the discovery discovery discovery of of ofprotoilludane protoilludane protoilludane na naturaltural natural products products products from from marine, marine, from plantmarine, plant and and fungal plant fungal and fungalsources. sources. 2. Basidiomycota2.2. Basidiomycota Basidiomycota The BasidiomycotaTheThe Basidiomycota Basidiomycota account account account for for for approximately approximately approximately 30% 30% of of of the the the described describeddescribed species species species of of higher of higher higher fungi fungi fungi and and and includeincludeinclude the smuts, the the smuts, smuts, rusts, rusts, rusts, jelly jelly jelly fungi, fungi, fungi, bracket bracket bracket fungi,fungi, fungi, stinkhorns, stinkhorns, fairy fairyfairy clubs, clubs, clubs, bird’s bird’s bird’s
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