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Bulb Alkaloids of the Reputedly Psychoactive Brunsvigia Radulosa (Amaryllidaceae)

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Bulb Alkaloids of the Reputedly Psychoactive Brunsvigia Radulosa (Amaryllidaceae) South African Journal of Botany 2002, 68: 86–89 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY ISSN 0254–6299 Bulb alkaloids of the reputedly psychoactive Brunsvigia radulosa (Amaryllidaceae) NR Crouch*1,2, J Chetty2, DA Mulholland2 and E Ndlovu2,3 1 Ethnobotany Unit, National Botanical Institute, PO Box 52099, Berea Road, Durban 4007, South Africa 2 Natural Products Research Group, Department of Chemistry, University of Natal, Durban 4041, South Africa 3 Kwamalulekoes Nursery and Herbalist, PO Box 11409, Mooi River 3300, South Africa * Corresponding author, e-mail: [email protected] Received 8 August 2001, accepted in revised form 23 October 2001 Brunsvigia radulosa Herb. is a bulbous ethnomedicinal and its usefulness in the traditional treatment of cancer. herb, widespread from the Great Karoo northwards The identification of anhydrolycorinium chloride, the through the grasslands of southern Africa. Earlier work- second ever isolation of this compound from a plant, ers have previously identified a total of ten isoquinoline supports earlier observations for antineoplastic activity alkaloids from this taxon, including 1-O-acetylnorpluvi- of bulb and leaf extracts of B. radulosa in a mouse P-388 ine which is only known from B. radulosa. The current lymphocytic leukaemia system. In the current study, 1- report investigates the suggestions of earlier workers O-acetyllcorine was also isolated from the bulbs. relating to the psychoactivity of the bulb constituents, Introduction As one of the most widespread amaryllids in the Flora of cells. Among extracts of 60 ethnomedicinal taxa investigat- southern Africa region (Dyer 1950) it is not surprising that ed for such activity, only B. radulosa and the related the variable Brunsvigia radulosa Herb. (syn. B. cooperi Amaryllis belladona L. (Amaryllidaceae) showed antineo- Baker in Fl. Cap. 6: 207) has been incorporated into tradi- plastic activity in a mouse P-388 lymphocytic leukaemia tional medicine across much of its range. In Swaziland, assay. Although Charlson (1980) demonstrated that lycorine where it is known as lilula, it is used to straighten bones in accounted for some of the observed antileukaemic activity in children (Dlamini 1981) and in Lesotho barren women are the P-388 mice (3PS, 35% life extension at dose levels of treated with B. radulosa (Sotho name is lematla), alone or in 75mg kg-1 in vivo), the more potent agent was not isolated. combination with other plants (Phillips 1917). This Sotho Subsequent bioassay-directed fractionation of A. belladona application may relate to the Doctrine of Signatures principle bulb extracts by Pettit et al. (1984) led to the isolation and as the plant resembles the human female pubic region in a identification of anhydrolycorinium chloride as the principal manner similar to that shown for Haemanthus deformis antineoplastic component against murine P-388 lymphocyt- Hook.f. (Amaryllidaceae). This latter taxon is known to the ic leukaemia (3PS, 64–69% life extension at dose levels of -1 -1 Zulu as the ‘female’ uzeneke, distinct from the phallic-like H. 10–20mg kg in vivo, ED50 1.4mg ml in vitro). Pettit et al. albiflos Jacq. traded as the ‘male’ uzeneke. The Sotho fur- (1984) posited that this same constituent was responsible ther employ the plant in difficult confinement cases (Jacot for the observed 3PS in vivo activity of B. radulosa extracts; Guillarmod 1971) and wash divining bones in a decoction of the current investigation tested this hypothesis. the plant to impart them with greater accuracy (Phillips Earlier phytochemical investigations of Brunsvigia radu- 1917). Loubser and Zietsman (1994) postulated a close link losa (Dry et al. 1958, Laing and Clark 1974, Campbell et al. between B. radulosa and altered states of consciousness. 2000) collected in Dargyle and Otto’s Bluff (KwaZulu-Natal) They interpreted a rock painting at Thaba Bosiu in western and near the Gariep Dam (Free State, South Africa) respec- Lesotho as a San depiction of this species, and suggested tively yielded nine alkaloids (Figure 1): brunsvigine, 1, its historic use in inducing hallucinations and trance states. lycorine, 2, crinamine, 3, crinine, 4, hamayne, 5, stern- Based on the report by Watt and Breyer-Brandwijk (1962) bergine, 6, 1-O-acetylnorpluviine, 7, 1-epideacetylbowden- that an enema of an infusion of the bulb of a Brunsvigia sp. sine, 8, and anhydrolycorin-6-one, 9. A radioimmunoassay was used by the Zulu for abdominal troubles, Charlson survey by Tanahashi et al. (1990) has further revealed that (1980) investigated B. radulosa for pharmacological activity galanthamine, 10, is also produced by this taxon. in arresting the maturation and proliferation of malignant South African Journal of Botany 2002, 68: 86–89 87 OH OH OR RO OH O H OH O O H O H N NH N O O 1. Brunsvigine 2. Lycorine (R=H) 3. Crinamine (R=Me) 11. 1-O-Acetyllycorine (R=Ac) 5. Hamayne (R=H) R OH OH AcO HO O H MeO O N O H N N HO O OMe 4. Crinine 6. Sternbergine (R=OH) 8. 1-Epideacetylbowdensine 7. 1-O-Acetylnorpluviine (R=H) OH O O O MeO N N O O NMe Cl O 9. Anhydrolycorin-6-one 10. Galanthamine 12. Anhydrolycorinium chloride Figure 1: Alkaloids identified from Brunsvigia radulosa Material and Methods (1:1). Thin layer chromatography indicated extracts A, B and C were of similar composition so they were combined to Plant material yield an extract of 3.2g and subjected to column chromatog- raphy over silica gel (Merck 9385), using a dichloromethane- The bulbs of Brunsvigia radulosa Herb. were collected during methanol step gradient (19:1, 18:2, 16:4, 12:8, 10:10, 8:12, March 1999 at Buffelskloof Nature Reserve, Mpumalanga 4:16, 0:20) as the eluant and 30 x 35ml fractions collected and a voucher specimen (Crouch 799, NH) retained. for each gradient step. These yielded crinine 4 (72mg, frac- tions 14–17), 1-O-acetyllycorine 11 (22mg, fractions 22–27), Extraction and fractionation crinamine 3 (107mg, fractions 34–40), hamayne 5 (12mg, fractions 49–54), lycorine 2 (72mg, fractions 53–61), and Dried bulbs (850g) were macerated and extracted with anhydrolycorinium chloride 12 (24mg, fractions 73–77). ethanol on a Labcon shaker for 72 hours to yield, after evap- oration of solvent, a viscous extract. The extract was dis- Structure determinations solved in water (100ml) and acidified (HCl) to pH 4. The acid solution was then extracted with chloroform to provide Compounds were identified using NMR, mass spectrometric extract A. Basifying the solution to pH 8–9 and then extract- and other spectroscopic techniques and then confirmed ing with chloroform gave extract B. Extract C was produced against literature physical and spectroscopic data (given as by extracting the basic solution with chloroform/methanol references below) for these compounds. NMR spectra were 88 Crouch, Chetty, Mulholland and Ndlovu recorded on a Varian Unity Inova 400MHz NMR spectrome- Of this preparation, patients are administered two table- ter in CDCl3 or CD3OD. IR spectra were recorded with a spoons thrice daily. At the higher dosage of five tablespoons Nicolet Impact 400 D spectrometer on sodium chloride thrice daily this same preparation may be used to treat psy- plates and calibrated against an air background. EIMS were chotic patients; for this condition the Brunsvigia material may obtained using an Agilent 6 890 GC with a 5 973N mass be optionally substituted with some outer papery bulb scales selective-MS system. of Boophane disticha (L.f.) Herb. Mentally disturbed patients typically sleep for a couple of hours following this treatment, Results and Discussion after which period an improvement should be noticeable. Despite its use in the treatment of mental disorders, par- The re-investigation of the ethanol extract of the bulb again ticularly as a substitute for Boophane disticha, the authors yielded lycorine, 2 (Kinstle et al. 1966, Evidente et al. 1983a, are unaware of the current use of B. radulosa as an hallu- Evidente 1986), crinamine, 3 (Likhitwitayawuid et al. 1993), cinogen; nor is its historical use in this regard definitely crinine, 4 (Evidente 1986, Vildomat et al. 1995), hamayne, 5 known. However, of the ca. 65 Amaryllidaceae of southern (Vildomat et al. 1993) and a further two alkaloids: 1- Africa that have been investigated phytochemically O–acetyllycorine, 11, and anhydrolycorinium chloride, 12 (Vildomat et al. 1997), seven have yielded crinamine, includ- (Pettit et al. 1984). ing two of the three regional amaryllids considered psy- Lycorine is a ubiquitous alkaloid with significant bioactivi- chotropic. These are Ammocharis coranica (Ker-Gawl.) ties. These include the inhibition of cell growth and division Herb. (Koorbanally et al. 2000) and Brunsvigia radulosa (Dry in higher plants and algae (Evidente et al. 1983b), inhibition et al. 1958). Further, tubers of the Zulu narcotic Dioscorea of cyanide-resistant respiration (Arrigoni et al. 1976, dregeana have also recently been shown to contain Evidente et al. 1983b), inhibition of protein biosynthesis in crinamine (Mulholland et al. 2002). On the basis of these vivo and activity against RNA and DNA viruses (Ieven et al. reports we postulate that crinamine accounts for the psy- 1982, Ieven et al. 1983, Ghosal et al. 1985, Harborne and choactivity which has historically been attributed to B. radu- Baxter 1993). Crinamine shows weak brachycardia activity losa (Loubser and Zietsman 1994). Pharmacological inves- and respiratory depression in dogs (Watt and Breyer- tigation of crinamine is warranted, as information on its psy- Brandwijk 1962). Crinamine has also shown strong cytotox- choactivity is not available. Although the total synthesis of ic and moderate antimalarial activity (Likhitwitayawuid et al. crinamine has been accomplished (Nishimata and Mori 1993). 1998), the pharmaceutical development of this alkaloid Subsequent to the work of Charlson (1980), Pettit et al.
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