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Phylogenetic Selection of Target Species in Amaryllidaceae Tribe

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Phylogenetic Selection of Target Species in Amaryllidaceae Tribe South African Journal of Botany 77 (2011) 175–183 www.elsevier.com/locate/sajb Phylogenetic selection of target species in Amaryllidaceae tribe Haemantheae for acetylcholinesterase inhibition and affinity to the serotonin reuptake transport protein M.G.K. Bay-Smidt a, A.K. Jäger a, K. Krydsfeldt a, A.W. Meerow b,c, G.I. Stafford a,d, ⁎ J. Van Staden d, N. Rønsted a, a Department of Medicinal Chemistry, University of Copenhagen, Universitetsparken 2, DK-2100 Copenhagen, Denmark b USDA-ARS-SHRS, National Germplasm Repository, 13601 Old Cutler Road, Miami, Florida, USA c Fairchild Tropical Garden, Miami, Florida, USA d Research Centre for Plant Growth and Development, School of Biological and Conservation Sciences, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville 3201, South Africa Received 25 April 2010; received in revised form 14 July 2010; accepted 28 July 2010 Abstract We present phylogenetic analyses of 37 taxa of Amaryllidaceae, tribe Haemantheae and Amaryllis belladonna L. as an outgroup, in order to provide a phylogenetic framework for the selection of candidate plants for lead discoveries in relation to Alzheimer's disease and depression. DNA sequences from the nuclear ribosomal internal transcribed spacer (ITS) and the plastid trnL-F regions were used. Maximum parsimony analyses provide increased support for the sister relationship of Haemanthus and Scadoxus. Within Haemanthus, a well supported clade (89% BS) corresponds to a summer rainfall group (mainly Eastern Cape) with white-pale pink flowers. A second strongly supported clade (100% BS) corresponds to a winter rainfall group (mainly Western Cape) with red-pale pink flowers. Haemanthus montanus, which is from the summer rainfall region, is sister to the winter rainfall group. Alkaloid profiles and bioactivity profiles were investigated for 16 taxa using gas chromatography-mass spectrometry (GC–MS) and assays measuring acetylcholinesterase (AChE) inhibition and affinity to the serotonin reuptake transport protein (SERT). No alkaloids were detected by GC–MS in extracts of the two species of Gethyllis included in the present study suggesting that Gethyllis (and possibly Apodolirion) species may not produce the alkaloids characteristic for the family. AChE inhibitory activity was found in all investigated clades except the Apodolirion–Gethyllis clade, which can be explained by the apparent lack of alkaloids in this clade. In spite of infra-specific variability of alkaloid profiles observed, dose-dependent SERT activity appears to be pronounced and restricted to the genus Haemanthus within tribe Haemantheae. Three of eight Haemanthus species tested had IC50 b10 μg/ml. Two of the most active extracts in the present study contained primarily montanine type alkaloids which have not been tested for SERT affinity previously. Simultaneous evaluation of bioactivity and alkaloid profiles in a phylogenetic framework can potentially be used to select candidate species for phytotherapy and drug discovery. © 2010 SAAB. Published by Elsevier B.V. All rights reserved. Keywords: Acetylcholinesterase; Amaryllidaceae; Drug discovery; Internal transcribed spacer; Phylogeny; Serotonin-reuptake-transport-protein; trnL-F 1. Introduction significant part of health care problems everywhere and are increasing as human life-expectancy increases in many Mental health problems such as epilepsy, convulsions, de- countries (WHO, 2010a). Plants provide a large number of pression, dementia and age-related diseases constitute a herbal remedies to treat mental illnesses. Many people are largely dependent on plants as the only readily available medicine (WHO, 2010b). In southern Africa well over 300 ⁎ Corresponding author. Tel.: +45 35 336504; fax: +45 35336001. species are used by traditional healers to treat mental illnesses E-mail address: [email protected] (N. Rønsted). (Sobiecki, 2002; Stafford et al., 2008). 0254-6299/$ - see front matter © 2010 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2010.07.016 176 M.G.K. Bay-Smidt et al. / South African Journal of Botany 77 (2011) 175–183 Several Amaryllidaceae are used in traditional medicine for first isolated from the Caucasian snowdrop Galanthus wor- various illnesses (Neuwinger, 2000) including mental illnesses onowii Losinsk. and since from a range of other Amaryllidaceae (Sobiecki, 2002; Stafford et al., 2008). African Amaryllidaceae species, is approved as an AChE inhibitor in a number of constitutes 280–300 species in 20 genera, which are divided countries (Heinrich and Teoh, 2004). Galanthamine is a into three major clades corresponding to the tribes Amarylli- selective, reversible and competitive inhibitor of AChE, as deae, Cyrtantheae and Haemantheae (Meerow and Clayton, well as an allosteric modulator of the neural nicotinic receptor 2004; Meerow and Snijman, 1998, 2001, 2006; Meerow et al., for acetylcholine (Heinrich and Teoh, 2004). Crude extracts of a 1999). Most species used in traditional medicine belong to the number of Amaryllidaceae species have shown AChE inhibi- Amaryllidaceae tribe Amaryllideae. For example, Boophone tion, but most tested species belong to Crinum L. (Houghton et disticha (L.f.) Herb., is widely used to induce hallucinations, to al., 2004; Jäger et al., 2004) and Narcissus (López et al., 2002). treat headaches and anxiety, and to sedate hysterical, violent The most active alkaloids reported belong to the lycorine- and and psychotic patients (Neergaard et al., 2009). However, galanthamine types (Elgorashi et al., 2004, 2006a; López et al., Cyrtanthus Aiton (tribe Cyrtantheae) and Scadoxus Raf. (tribe 2002). Haementheae) species are also used in traditional medicine to Depression is associated with reduction of neurotransmitters treat mental illnesses (Stafford et al., 2008). Scadoxus puniceus in the brain. Several antidepressants exert their effect by (L.) Friis & Nordal is known to cause dizziness, visual selective inhibition of serotonin reuptake and affinity to the disturbances, CNS excitation or depression (Veale et al., serotonin reuptake inhibitor (SERT) is associated with possible 1992). In Eastern Tanzania, a bath with root infusion of antidepressant effect (SSRIs; Stahl, 1998). Crude extracts and Scadoxus multiflorus (Martyn) Raf. is used to treat mental isolated alkaloids of Boophone disticha have shown affinity to illness (Chhabra et al., 1987). Activities of plants in SERT (Nielsen et al., 2004; Sandager et al., 2005) as have a Amaryllidaceae related to the central nervous system are number of the tested alkaloids from other Amaryllidaceae ascribed to norbelladine-derived alkaloids restricted to the species, primarily of the crinine-type (Elgorashi et al., 2006b). Amaryllidaceae subfamily Amarylloideae (AGP III, 2009). The purpose of the present study is to use a phylogenetic Over 500 alkaloids have been described from various species hypothesis for Amaryllidaceae tribe Haemantheae to evaluate and have been subdivided into 18 major types based on their the distribution of (a) alkaloids, (b) acetylcholinesterase hypothetical biosynthetic pathways (Jin, 2009). inhibitory activity, and (c) affinity to the serotonin reuptake Efforts are continuously being made to identify and develop transport protein. new and improved herbal remedies and lead compounds for drug discovery. However, identification and isolation of 2. Materials and methods bioactive compounds is both time-consuming and costly and only a few of the Amaryllidaceae species and their alkaloids 2.1. Materials have been evaluated for their CNS-effects. New rational approaches are needed to enable the more effective selection Taxon sampling included representatives of all genera of of the most promising organisms for herbal remedies and drug tribe Haemantheae. Apodolirion was included in the phyloge- discovery programmes (Bohlin et al., 2007). netic analyses, but due to lack of material available for this In a study of Narcissus L. (Amaryllidaceae), we have shown study, no chemical or bioactivity data was obtained. For the that the distribution of alkaloids with AChE inhibitory activity phylogenetic hypothesis, we expanded the matrix of Meerow is significantly restricted within the phylogeny of Narcissus and and Clayton (2004) with 17 samples also used for chemical and can be used to predict the occurrence of active alkaloids in bioactivity evaluation in the present study. Of these, Gethyllis uninvestigated species (Rønsted et al., 2008). In the present afra L., G. grandiflora L.Bolus, Haemanthus amarylloides study we take a phylogenetic approach to explore and select Jacq., H. coccineus L., H. deformis Hook.f., H. hirsutus Baker, potential new target species of tribe Haemantheae for lead H. montanus Baker, H. sanguineus Jacq., and Scadoxus discovery of acetylcholinesterase and serotonin reuptake multiflorus, were not included in the earlier study by Meerow transport protein inhibitors. In the most recent formal and Clayton (2004). We did not include a set of sequences classification of Amaryllidaceae by Meerow and Snijman available in Genbank from Spies and Strydom as these were (1998), tribe Haemantheae included only the genera Clivia unpublished and we did therefore not feel we could trust their Lindl., Cryptostephanus Welw. ex Baker, Haemanthus L. and identity. Amaryllis belladonna L. was used as an outgroup Scadoxus. However, phylogenetic analyses have supported an following Meerow and Clayton (2004). We followed circum- expanded tribe Haemantheae including also the genera scriptions and
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