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Structural Classification and Biological Activities of Stemona Alkaloids

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Structural Classification and Biological Activities of Stemona Alkaloids Phytochem Rev https://doi.org/10.1007/s11101-019-09602-6 (0123456789().,-volV)( 0123456789().,-volV) Structural classification and biological activities of Stemona alkaloids Harald Greger Received: 11 February 2019 / Accepted: 27 February 2019 Ó The Author(s) 2019 Abstract Stemona alkaloids represent a unique class pyridoazepines characterized by a six-membered of natural products exclusively known from the three piperidine ring. Stimulated by the great interest in genera Stemona, Stichoneuron, and Croomia of the the antitussive activity of Stemona alkaloids, differ- monocotyledonous family Stemonaceae. Structurally ences in transport mechanisms and potencies via they are characterized by a central pyrroloazepine core different administrative routes were investigated. usually linked with two butyrolactone rings. The great Follow-up studies on the significant insecticidal diversity, comprising 215 derivatives, is created by the activities focused on the mode of action by using formation of additional C–C linkages and oxygen biochemical and electrophysiological approaches. bridges together with ring cleavages and eliminations Screening for acetylcholinesterase inhibitory proper- of the lactone rings. Based on biosynthetic consider- ties revealed a much higher potency for stemofoline ations they can be grouped into three structural types derivatives compared to pyridoazepines, but showed represented by the croomine, stichoneurine, and also significant activity for isomers of stenine with a protostemonine skeleton. Due to the formation of stichoneurine skeleton. Evaluating synergistic growth characteristic terminal lactone rings and the central inhibitory effects with cancer chemotherapeutic pyrrolidine ring pandanamine and pandamarilac- agents stemofoline exhibited the most potent effect tonine, isolated from Stichoneuron calcicola, were in the reversal of permeability glycoprotein-mediated suggested to represent biogenetic precursors. The multidrug resistance. The anti-inflammatory activity taxonomically complex S. tuberosa group can be of some derivatives was identified as an inhibition of clearly segregated by the formation of stichoneurines, the expression of inflammatory mediators. Comparing while the other Stemona species are characterized by the diverse bioactivities of Stemona alkaloids stemo- protostemonine derivatives. Croomine derivatives are foline-type derivatives are the most versatile com- more widespread found in both groups and in the pounds representing promising lead structures for genus Croomia. Of chemotaxonomic significance are further development as commercial agents in agricul- the different transformations of protostemonine into ture and medicine. stemofolines with a cage-type structure or into Keywords Stemona alkaloids Á Structural classification Á Biogenetic trends Á Antitussive H. Greger (&) activity Á Insecticidal and nematicidal activity Á Chemodiversity Research Group, Faculty of Life Acetylcholinesterase inhibition Multidrug resistance Sciences, University of Vienna, Rennweg 14, Á 1030 Vienna, Austria e-mail: [email protected] 123 Phytochem Rev reversing properties Á Anti-inflammatory activities Á different suggestions regarding the origin of the Chemotaxonomy central building blocks have been published (Seger et al. 2004; Greger et al. 2009; Wang and Chen 2014). Structural classifications were based either on pure chemical perspectives (Pilli et al. 2010)oron Introduction biosynthetic considerations (Greger 2006; Wang and Chen 2014). As a result, Stemona alkaloids were In the framework of UNESCOs program ‘‘Man and classified either into eight groups by Pilli et al. the Biosphere’’ (MAB) broad-based phytochemical (2010), or into two classes with fourteen types by investigations within tropical plant families were Wang and Chen (2014). By contrast, only three carried out in our laboratory to find a replenishing basic skeletons were discriminated by Greger source of naturally occurring insecticides or fungi- (2006). The present review provides an updated cides. Besides highly active sulfur-containing classification of 215 Stemona alkaloids including all amides from the genus Glycosmis of the Rutaceae newly described derivatives. In spite of the many (Greger et al. 1996; Hofer and Greger 2000) and new structures the overview supports the previous flavaglines from Aglaia of the Meliaceae (Brader classification into three basic skeletons (Tables 1, 2, et al. 1998; Bacher et al. 1999) we found very 3) based on presumed biosynthetic connections and promising biological activities in the genus Stemona on the distribution of specific structures in related of the small monocotyledonous family Stemonaceae species (Fig. 1). (Brem et al. 2002; Pacher et al. 2002). As reviewed In continuation of the previous review (Greger previously the high insecticidal activity could be 2006) reports on bioactivties were summarized indi- attributed to family-specific Stemona alkaloids cating remarkable progress in deciphering the mode of (Greger 2006), whereas the antifungal property action. Stimulated by the great interest in the antitus- was caused by different groups of stilbenoids sive activity of Stemona alkaloids, investigations on (Greger 2012). In addition, the accumulation of differences in transport mechanisms and potencies via tocopherols with antioxidant activity was shown to different administrative routes were carried out (Lin represent another chemical character of that family et al. 2008a, b; Leung et al. 2006; Zhou et al. 2009). (Brem et al. 2004). Apart from sporadic reports on Moreover, different ways to prepare structurally iminosugars (Asano et al. 2005) and chlorogenic diverse analogues of active compounds were elabo- acid derivatives (Ge et al. 2007) continuative rated to find an efficient synthetic route (Frankowski investigations mainly focused on Stemona alkaloids et al. 2008, 2011). In continuation of previous inves- due to their unique molecular structures and wide tigations on insecticidal activities (Sakata et al. 1978; range of bioactivities. Synthetic approaches to their Jiwajinda et al. 2001; Brem et al. 2002; Kaltenegger intricate structures were summarized in a microre- et al. 2003) follow-up studies focused on the mode of view by Alibe´s and Figueredo (2009) and more action by using biochemical and electrophysiological recent advances were reviewed by Liu and Wang approaches (Tang et al. 2008). With regard to the (2015). A number of innovative strategies have been acetylcholinesterase inhibiting properties of Stemona developed recently for the construction of the alkaloids, bioassays with naturally-occurring as well as structurally simplest stemoamide (214) (Brito and synthetically prepared derivatives informed about Pirovani 2018). Moreover, extensive chromato- structure–activity relationships (Wang et al. 2007a; graphic comparisons of extracts from wild and Baird et al. 2009; Chaiyong et al. 2010; Sastraruji et al. cultivated Stemona species provided the basis for 2010, 2012; Ramli et al. 2013, 2014; Lai et al. 2013). chemotaxonomic conclusions as well as for hypothe- Following the first report on multidrug resistance ses regarding biosynthetic connections within this properties of an ethanolic extract of Stemona aphylla class of alkaloids (Schinnerl et al. 2007; Kongkiat- (Limtrakul et al. 2007), a series of studies evaluated the paiboon et al. 2011). synergistic growth inhibitory effect of Stemona alka- Although the basic biosynthetic steps in the loids with cancer chemotherapeutic agents (Chanma- formation of Stemona alkaloids are still unknown hasathien et al. 2011a, b; Umsumarng et al. 2013, 2015, 2017, 2018). Furthermore, their anti- 123 Phytochem Rev Table 1 Structures derived from croomine skeleton 123 Phytochem Rev Table 2 Structures derived from stichoneurine skeleton 123 Phytochem Rev Table 2 continued 123 Phytochem Rev Table 2 continued 123 Phytochem Rev Table 2 continued 123 Phytochem Rev Table 2 continued 123 Phytochem Rev Table 2 continued inflammatory activity was investigated and regarded Structural classification as an inhibition of the expression of diverse inflammatory mediators (Hosoya et al. 2011; Lim Stemona alkaloids are characterized by a pyrrolo[1,2- et al. 2015; Jung et al. 2016; Lee et al. 2016;Wu a]azepine core (rings A, B) usually linked with two a- et al. 2018). The present review also reports on the methyl-c-butyrolactone rings (C, D). As shown in the nematicidal activity (Huang et al. 2016;Chenetal. structural overview (Tables 1, 2, 3) they can be 2018) and other miscellaneous properties as well as derived from three basic skeletons differing in the on the pharmacokinetics of that class of alkaloids substitution at C-9 (Fig. 1). This classification was (Dong et al. 2012; Sun et al. 2012; Han et al. 2016). also supported by broad-based chemotaxonomic stud- Formula depictions facilitate an overview of 215 ies within the genus Stemona indicating two clear-cut derivatives demonstrating structural relationships and trends either towards derivatives with a stichoneurine biogenetic trends also serving as a guide for exploit- or protostemonine skeleton (Jiang et al. 2006b; ing these compounds for further development as Schinnerl et al. 2007; Li et al. 2007a; Kongkiatpaiboon useful agents in agriculture and medicine. et al. 2011). In contrast, derivatives with a croomine 123 Phytochem Rev Table 3 Structures derived from protostemonine skeleton 123 Phytochem Rev Table 3 continued 123 Phytochem Rev Table 3 continued 123 Phytochem Rev Table 3 continued Fig. 1 Three basic 13
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