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Pilocarpine and Related Alkaloids in Pilocarpus Vahl (Rutaceae)

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Pilocarpine and Related Alkaloids in Pilocarpus Vahl (Rutaceae) In: Alkaloids: Properties, Applications… ISBN: 978-1-61668-974-2 Editor: N. M. Cassiano, pp. 63-80 © 2010 Nova Science Publishers, Inc. Chapter 3 PILOCARPINE AND RELATED ALKALOIDS IN PILOCARPUS VAHL (RUTACEAE) Alexandra C. H. F. Sawaya1,, Ilka N. Abreu1,2, Nathalia L. Andreazza1, Marcos N. Eberlin3, Paulo Mazzafera1,* 1Plant Biology Department, Institute of Biology, State University of Campinas, UNICAMP, CP 6109, Campinas, 13083-970, SP, Brazil 2Scottish Crop Research Institute, Department of Plant Products and Food Quality, Invergowrie, Dundee, DD2 5DA, Scotland, UK 3Thomson Mass Spectrometry Laboratory, Institute of Chemistry, State University of Campinas, UNICAMP, Campinas, 13083-970, SP, Brazil ABSTRACT Pilocarpine is mainly known as a drug for the treatment of glaucoma and it is also used as a stimulant of sweat and lachrymal glands. Species of the genus Pilocarpus are collectively named jaborandi in Brazil and their leaves are the only known source of this imidazole alkaloid. Pilocarpine is mainly obtained from two species, Pilocarpus microphyllus and Pilocarpus jaborandi and, despite the economical and pharmacological importance of this alkaloid, very little is known about pilocarpine, from basic information on the contents in different jaborandi species and plant tissues to the biosynthetic route and the metabolic * Corresponding author: [email protected] 64 Alexandra C. H. F. Sawaya, Ilka N. Abreu, Nathalia L. Andreazza et al. control. This review will focus briefly on the genus jaborandi, then on what is known about pilocarpine biosynthesis followed by possible biotechnological applications aiming to produce the alkaloid in vitro. Finally, the alkaloids found in this genus, their plant sources and pharmacological applications will be reviewed. Keywords: Biosynthesis; genetic variation; imidazole alkaloid; Jaborandi 1. PILOCARPUS, THE SOURCE OF PILOCARPINE Pilocarpus Vahl (Rutaceae) is a neotropical genus comprising shrubs and trees, with species distributed from the south of Mexico, throughout Central America and the Antilles, as far as the lower latitudes of South America (Kaastra, 1982; Skorupa, 1996). The name of the genus is probably based on the shape of the mericarps, as pilos means felt hat in Greek and carpos means fruit (Kaastra, 1982). The genus has 17 species and 14 of them are found in the Brazilian territory, with the majority in the oriental part of the country identified as the genetic diversity center of the species (Oliveira, 2007). Several species of Pilocarpus are popularly known in Brazil as jaborandi, which comes from the name of these plants in the Tupi-Guaraní language (ya- mbor-endi) meaning ―the one who causes mouth dripping (Holmstead et al., 1979). Pilocarpus is the only source of pilocarpine, an imidazole alkaloid with pharmacological activity, used in eye-drops for the treatment of glaucoma, and also for the stimulation of sweat and lachrymal glands (Goodman and Gilman, 2001; Valdez et al., 1993). Other imidazole alkaloids were isolated from jaborandi but little is known about their pharmacological properties (Abreu et al., 2007a; Abreu et al., 2007b; Andrade-Neto et al., 1996; Kaastra, 1982; Link and Bernauer, 1972; Santos and Moreno, 2004; Sawaya et al., 2008). Apparently, all Pilocarpus species have pilocarpine but in varied concentrations (Joseph, 1967; Sawaya et al., 2010; Sousa et al., 1991; Voigtlander et al., 1978). However, only two species: Pilocarpus microphyllus Stapf ex Holmes and Pilocarpus jaborandi Holmes have economical importance as they are known to have a high pilocarpine concentration in the leaves and also because they have a broad geographical distribution (Joseph, 1967; Kaastra, 1982; Sousa et al., 1991). The distribution is an important aspect, as the leaves used for pilocarpine extraction were (until some years ago) exclusively obtained from native plants growing in the wild and the Pilocarpine and Related Alkaloids in Pilocarpus Vahl (Rutaceae) 65 intensive collection made some Pilocarpus species to be included in a list of endangered Brazilian plants (IBAMA, 1992). The Brazilian state of Maranhão was the main producer of jaborandi leaves and P. jaborandi, P. microphyllus, P. alatus and P. trachylophus were the species in the endangered list (Pinheiro, 1997, 2002). The leaves were harvested by people living in or near the forest and the pharmaceutical company Merck was the only buyer. Repeated leaf collection induced plant death, vigor and plant height reduction, as well as decrease in leaf size (Pinheiro, 1997). Curiously, from a phylogenetic point of view the above mentioned four species form a unique clade and their phylogenetic relationships are in a certain degree associated with their geographical distribution (Oliveira, 2007). The uncontrolled exploitation accelerated actions for domestication of native jaborandi species, an initiative by Merck (SUDEMA, 1970), which was undertaken in the Maranhão state starting in 1969 (Vieira, 1999). A notable annual mark of 4,000 kg of leaves/ha was reached in the Merck farm but in recent years the production is about 1,400 Kg of leaves/ha. In 2002, the Centroflora Group (Vegeflora Extrações do Nordeste Ltda - www.centroflora.com.br) became responsible for the pilocarpine extraction from the jaborandi leaves but Merck still carries out the purification and trades the alkaloid. 1.1. Biosynthesis of Pilocarpine It has long been suggested (Cordell, 1981) that pilocarpine and other analogous imidazole alkaloids in plants are derived from histidine but no proof was given. Dewick (1997) also indicated that pilocarpine is probably derived from histidine and additional carbon atoms would come from acetate and threonine, but again without any experimental confirmation. Both suggestions come from the similarity of this amino acid structure and the imidazole ring (Fig. 1). However, this may not be a rule as the imidazole alkaloid anosmine is originated from two lysine molecules (Hemscheidt and Spenser, 1991). (3-3H-Threonine and (3-3H)histidine were used to study the biosynthesis of pilocarpine in calli obtained from leaf peduncle (Abreu and Mazzafera, unpublished results). After 12, 24 and 48 h of incubation pilocarpine was extracted (Avancini et al., 2003) and analysed in HPLC coupled to a UV and radioactivity detectors (pumping a scintillation cocktail). Radioactivity was detected in the pilocarpine peak in all analyzed incubation periods and with 66 Alexandra C. H. F. Sawaya, Ilka N. Abreu, Nathalia L. Andreazza et al. both labeled amino acids, suggesting indeed that both amino acids may be involved in the biosynthesis of pilocarpine. However the radioactivity incorporation was very low, varying from 0.02 to 0.06%. Labeled amino acids (14C-histidine, 14C-arginine and 14C-ornitine) were also used to study the biosynthesis route of the imidazole alkaloid stevensine in Teichaxinella morchella and about 0.2% incorporation was observed (Andrade et al., 1999). Such low radioactivity incorporation in the target alkaloid might be due to the destination of part of the labeled amino acids to the synthesis of proteins and other amino acid derived compounds. Indeed, in our analysis of the jaborandi extracts in HPLC described above, several other peaks of radioactivity were identified (Abreu and Mazzafera, unpublished results). L-Theronine OH O OH O NH2 CH R N 3 OH + N OR NH O N 2 O N L-Histidine O Pilocarpine C CoA CH3 Acetyl-CoA Figure 1. Probable biosynthesis of pilocarpine from histidine and additional C atoms from acetyl-CoA and threonine (Adapted from Dewick, 1997). Interested in finding a model to study the biosynthesis route of pilocarpine in jaborandi, different approaches to increase the alkaloid content in seedlings have been tested (Avancini et al., 2003) and then in calli (Abreu et al., 2005) or cell suspension cultures (Abreu et al., 2007b; Andreazza et al., 2008). When calli were half-immersed in a liquid medium containing 0.05, 0.15, and 0.75 mM of threonine or histidine there was a significant increase of the alkaloid content (medium + cells) at the highest amino acid concentration, supporting the hypothesis that both amino acids may participate in or act as precursors of pilocarpine biosynthesis in jaborandi (Abreu et al., 2005). A comparison of the mass spectrometry fingerprint [ESI (+) - MS] of alkaloid extracts from leaves and cell suspension cultures of P. microphyllus identified 3-nor-8(11)-dihydropilocarpine, pilocarpine, anhydropilosine, Pilocarpine and Related Alkaloids in Pilocarpus Vahl (Rutaceae) 67 pilosine and three new alkaloids (Abreu et al., 2007a). A further and more detailed study (Abreu et al., 2007b) on the alkaloid profile of P. microphyllus in different seasons and parts of the plant by electrospray ionization mass spectrometry fingerprinting allowed the identification of these and other new alkaloids: (1) pilocarpine, (2) pilosine, (3) 3-anhydropilosine, (4) 13-nor- 8(11)-dihydropilocarpine, (5) 3-(3-methyl-3H-imidazol-4-ylmethyl)-1-phenyl- but-3-en-1-one, (6) 3-hydroxymethyl-4-(3-methyl-3H-imidazol-4-yl)-1- phenyl-butan-1-one, (7) 3-benzoyl-4-(3-methyl-3H-imidazol-4-ylmethyl)- dihydro-furan-2-one and (8) pilosinine. Based on the dissociation patterns of the main compounds found in the extracts it was possible to separate the identified alkaloids into three structurally related groups of compounds (Group A = 1, 4 and 8; Group B = 2 and 3; Group C = 5, 6 and 7), which varied with the seasons of the year. But, more interestingly, these results indicated that these three groups could belong to
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