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Galantamine Quantity and Alkaloid Profile in the Bulbs of Narcissus

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Galantamine Quantity and Alkaloid Profile in the Bulbs of Narcissus H OH metabolites OH Article Galantamine Quantity and Alkaloid Profile in the Bulbs of Narcissus tazetta and daffodil cultivars (Amaryllidaceae) Grown in Israel Dana Atrahimovich 1,2, Raviv Harris 1, Ron Eitan 3, Menashe Cohen 3 and Soliman Khatib 1,2,4,* 1 Department of Natural Compounds and Analytical Chemistry, Migal-Galilee Research Institute, Kiryat Shmona 11016, Israel; [email protected] (D.A.); [email protected] (R.H.) 2 Department of Biotechnology, Tel-Hai College, Upper Galilee 1220800, Israel 3 Northern R&D, Migal-Galilee Research Institute, Kiryat Shmona 11016, Israel; [email protected] (R.E.); [email protected] (M.C.) 4 Analytical Chemistry Laboratory, Tel-Hai College, Upper Galilee 1220800, Israel * Correspondence: [email protected]; Tel.: +972-4-695-3512; Fax: +972-4-694-4980 Abstract: Alkaloids produced by the bulbs of the Amaryllidaceae are a source of pharmaceutical compounds. The main alkaloid, galantamine, is a reversible acetylcholinesterase inhibitor and allosteric nicotinic receptor modulator, which slows cognitive and functional decline in mild to moderate dementia due to Alzheimer’s disease. Having a complex stereochemistry, the organic synthesis of galantamine for pharmaceutical uses is highly challenging and not always economically viable, and it is therefore isolated from Amaryllidaceae bulbs. In the present study, galantamine was extracted and quantified in Narcissus bulbs from five cultivars (cvs.), Fortune, Carlton, Ice Follies, Galilee and Ziva, which were grown in Israel under various conditions. Results show that the cvs. Fortune, Carlton and Ice Follies bulbs contained 285 ± 47, 452 ± 73 and 69 ± 17 µg g−1 Citation: Atrahimovich, D.; Harris, galantamine, respectively, while the Galilee and Ziva bulbs contained relatively low concentrations R.; Eitan, R.; Cohen, M.; Khatib, S. µ −1 Galantamine Quantity and Alkaloid of galantamine (1–20 g g ). Irrigation levels and pruning conditions did not affect the galantamine Profile in the Bulbs of Narcissus tazetta contents. Additionally, the alkaloids profile of the five cvs. was analyzed and characterized using LC- and daffodil cultivars (Amaryllidaceae) MS/MS showing that galantamine-type alkaloids were mainly detected in the Fortune and Carlton Grown in Israel. Metabolites 2021, 11, bulbs, lycorine-type alkaloids were mainly detected at the Galilee and Ziva bulbs and vittatine-type 185. https://doi.org/10.3390/ alkaloids were mainly detected in the Ice Follies bulbs. The present research is the first to characterize metabo11030185 the alkaloids profile in the Narcissus bulbs of Galilee and Ziva, indigenous cvs. grown in Israel. The antiviral and anticancer alkaloids lycorine and lycorinine were the main alkaloids detected in the Academic Editor: Robert D. Hall bulbs of those cultivars. Received: 1 March 2021 Keywords: Amaryllidaceae; Narcissus; alkaloids; galantamine; lycorine Accepted: 19 March 2021 Published: 21 March 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- Amaryllidaceae is a family of bulbous flowering plants, characterized by the presence iations. of a biogenetically related group of alkaloids derived from norbelladine. Over 300 different alkaloids have been identified from its species [1]. Narcissus is a genus of the most important spring-flowering plants of the amaryllis family, Amaryllidaceae, widely cultivated worldwide [2]. Physiologically, Narcissus species can be divided into two main groups: one that requires low temperatures for flowering and Copyright: © 2021 by the authors. Narcissus tazetta Licensee MDPI, Basel, Switzerland. another that does not [3]. Most species belong to the first group, whereas This article is an open access article cultivars (cvs.) belong to the latter. Two N. tazetta cvs., Galilee and Ziva, are characterized distributed under the terms and by 3–20 flowers per stem and low cold temperature requirements for flowering. Carlton, conditions of the Creative Commons Fortune and Ice Follies cvs. from the large-cupped division are characterized by a single Attribution (CC BY) license (https:// flower per stem and high cold requirements for flowering [3]. The difference between these creativecommons.org/licenses/by/ two groups is reflected in their popular names. While the large-cupped plants are called 4.0/). daffodils, the common name for plants from the tazetta group is Narcissus. Metabolites 2021, 11, 185. https://doi.org/10.3390/metabo11030185 https://www.mdpi.com/journal/metabolites Metabolites 2021, 11, 185 2 of 14 Metabolites 2021, 11, 185 a single flower per stem and high cold requirements for flowering [3]. The difference2 ofbe- 13 tween these two groups is reflected in their popular names. While the large-cupped plants are called daffodils, the common name for plants from the tazetta group is Narcissus. Galantamine is the most studied alkaloid from Amaryllidaceae bulbs [4]. The discov- Galantamine is the most studied alkaloid from Amaryllidaceae bulbs [4]. The discovery ery that it is a reversible inhibitor of acetylcholinesterase, and that it can cross the blood– that it is a reversible inhibitor of acetylcholinesterase, and that it can cross the blood–brain brain barrier, led to its clinical use for neurological conditions. Galantamine is also recog- barrier, led to its clinical use for neurological conditions. Galantamine is also recognized as nizedan allosteric as an allosteric modulator modulator of the neuronal of the neuronal nicotinic nicotinic acetylcholine acetylcholine receptors receptors [5]. It has [5] been. It hasshown, been both shown,in vitro bothand in vitroin vivo and, to in have vivo, a to neuroprotective have a neuroprotecti effect onve braineffect tissueson brain subjected tissues subjectedto, for instance, to, for instance, oxidative oxidative stress, or stress, oxygen or oxygen and glucose and glucose deprivation deprivation [1]. The [1]. projected The pro- jectedincrease increase in the numberin the number of patients of patients with Alzheimer’s with Alzheimer’s disease disease due to an due aging to an population aging popu- [6], lationand the [6], use and of the galantamine use of galantamine to treat otherto treat medical other medical conditions, conditions, are likely are likely to result to result in an inincreased an increased demand demand for thisfor this compound. compound.Narcissus Narcissusbulbs bulbs are are considered considered one one ofof thethe most importantimportant natural natural sources sources of of galantamine galantamine other other than than synthetic synthetic production. production. Nevertheless, Nevertheless, thethe potential potential utility of thethe NarcissusNarcissus speciesspecies is is not not just just restricted restricted to to galantamine, galantamine, the theAmaryl- Ama- rlidaceaeyllidaceaesynthesize synthesize a diversea diverse array array of of alkaloids alkaloids (Figure (Figure1) with 1) with pharmacological pharmacological activities, activi- ties,and compoundsand compounds like lycorine, like lycorine, lycorinine, lycor homolycorine,inine, homolycorine, haemanthamine, haemanthamine, narciclasine narci- and clasinetazettine and are tazettine known forare theirknown anticancer for their propertiesanticancer [1properties]. [1]. FigureFigure 1. 1. BiosyntheticBiosynthetic pathway pathway leading leading to to multiple multiple Amaryllidaceae alkaloidsalkaloids.. TThehe alkaloid alkaloid pattern, pattern, as as well well as as galantamine content content and and percentage percentage in in the alkaloid mixture,mixture, varies varies widely widely with with geographical geographical location location and and plant plant genotype genotype [7]. [Obviously,7]. Obviously, ad- ditionaladditional growth growth conditions conditions,, such such as nutrition, as nutrition, humidity, humidity, irrigation, irrigation, pest pestcontrol, control, light lightlev- els,levels, pruning pruning and andharvest harvest time time might might affect affect chemical chemical concentrations concentrations and composition. and composition. The alkaloidThe alkaloid pattern pattern and andgalantami galantaminene content contentss in the in the bulbs bulbs of ofthe the five five cultivars cultivars of of NNarcissusarcissus,, Carlton,Carlton, For Fortune,tune, Ice Ice Follies, Follies, Galilee Galilee and and Z Ziva,iva, grown grown in in Israel under various irrigation levellevelss were were characterized. characterized. To To our our knowledge, knowledge, no no investigation investigation has has reported reported on on Amarylli-Amaryl- lidaceae alkaloids diversity and accumulation in Narcissus bulbs of the Galilee and Ziva cultivars grown in Israel. Hence, our aim was to quantify the galantamine content in the investigated Narcissus cvs. bulbs and to analyze their alkaloid profile in order to broaden the variety of cvs. known in the literature and to benefit their pharmacological potential. Metabolites 2021, 11, 185 3 of 13 2. Results 2.1. Extraction and Quantification of Galantamine from Narcissus Bulbs—Method Optimization and Validation Three methods were used for the extraction of galantamine from Narcissus bulbs. Each of the methods was optimized as described in Materials and Methods and validated by measuring recovery and repeatability. Narcissus bulbs were lyophilized, ground and galantamine-d3 was added as the internal standard. Then, the pulverized bulbs were extracted with methanol, and galantamine was further extracted using liquid–liquid extrac- tion (LLE) and solid-phase
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