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Comparative Risk Assessment of Three Native Heliotropium Species in Israel

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Comparative Risk Assessment of Three Native Heliotropium Species in Israel molecules Article Comparative Risk Assessment of Three Native Heliotropium Species in Israel Jakob A. Shimshoni 1,* , Shimon Barel 2 and Patrick P. J. Mulder 3 1 Department of Food Quality & Safety, Institute for Postharvest and Food Sciences, Agricultural Research Organization, Volcani Center, Rishon LeTsyion 753593, Israel 2 Department of Toxicology, Kimron Veterinary Institute, Bet Dagan 50250, Israel; [email protected] 3 Wageningen Food Safety Research, Wageningen University & Research, P.O. Box 230, 6700 AE Wageningen, The Netherlands; [email protected] * Correspondence: [email protected]; Tel.: +972-50-6243961; Fax: +972-3-9681730 Abstract: Pyrrolizidine alkaloids (PAs) are genotoxic carcinogenic phytotoxins mostly prevalent in the Boraginaceae, Asteraceae and Fabaceae families. Heliotropium species (Boraginaceae) are PA-producing weeds, widely distributed in the Mediterranean region, that have been implicated with lethal intoxications in livestock and humans. In Israel, H. europaeum, H. rotundifolium and H. suaveolens are the most prevalent species. The toxicity of PA-producing plants depends on the PA concentration and composition. PAs occur in plants as mixtures of dozens of various PA congeners. Hence, the risk arising from simultaneous exposure to different congeners has to be evaluated. The comparative risk evaluation of the three Heliotropium species was based on recently proposed interim relative potency (iREP) factors, which take into account certain structural features as well as in vitro and in vivo toxicity data obtained for several PAs of different classes. The aim of the present study was to determine the PA profile of the major organ parts of H. europaeum, H. rotundifolium and H. suaveolens in order to assess the plants’ relative toxic potential by utilizing the iREP concept. In total, 31 different PAs were found, among which 20 PAs were described for the first time for Citation: Shimshoni, J.A.; Barel, S.; H. rotundifolium and H. suaveolens. The most prominent PAs were heliotrine-N-oxide, europine-N- Mulder, P.P.J. Comparative Risk oxide and lasiocarpine-N-oxide. Europine-N-oxide displayed significant differences among the three Assessment of Three Native species. The PA levels ranged between 0.5 and 5% of the dry weight. The flowers of the three species Heliotropium Species in Israel. were rich in PAs, while the PA content in the root and flowers of H. europaeum was higher than that Molecules 2021, 26, 689. https:// of the other species. H. europaeum was found to pose a higher risk to mammals than H. rotundifolium, 10.3390/molecules26030689 whereas no differences were found between H. europaeum and H. suaveolens as well as H. suaveolens and H. rotundifolium. Academic Editor: Stefano Dall’Acqua Received: 15 December 2020 Keywords: Heliotropium europaeum; suaveolens; rotundifolium; pyrrolizidine alkaloids; interim Accepted: 25 January 2021 Published: 28 January 2021 relative potency factor Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. Pyrrolizidine alkaloids (PAs) are secondary plant metabolites that function as chemical defense compounds against various herbivores [1–3]. They are highly prevalent in the plant families of Boraginaceae, Asteraceae (Senecio and Eupatorieae tribes) and Fabaceae (Crotalarieae tribe). More than 660 PA and PA-N-oxides have been identified and these Copyright: © 2021 by the authors. have been estimated to occur in over 6000 plants [1–3]. PAs are composed of a saturated or Licensee MDPI, Basel, Switzerland. 1,2-unsaturated necine base esterified with one or two necic acids [1,2]. Common PA types This article is an open access article occurring in the Heliotropium genus are depicted in Figure1[ 3]. In general, PAs occur in distributed under the terms and two forms, namely, as the free tertiary base and their corresponding N-oxide. conditions of the Creative Commons Many PAs exhibit genotoxic effects in humans and farm animals targeting mainly Attribution (CC BY) license (https:// the liver [4–7]. Most 1,2-dehydro PAs are pro-toxins, requiring metabolic activation by creativecommons.org/licenses/by/ cytochrome P450 to generate a pyrrolic ester as the reactive electrophilic intermediate that 4.0/). Molecules 2021, 26, 689. https://doi.org/10.3390/molecules26030689 https://www.mdpi.com/journal/molecules Molecules 2021, 26, 689 2 of 12 subsequently reacts with proteins and nucleic acids [6,7]. Since, upon ingestion, PA-N- oxides are reduced in the gut/liver to their corresponding free bases, both PA forms are considered to be toxic [2,7,8]. The toxicity of PA-producing plants mostly depends on the absolute PA concentration but also on the plants’ PA composition, as the toxic potential of Molecules 2021, 26, 689 individual PAs and their N-oxides widely differs [4,7]. The structural features determining2 of 14 the toxic potencies of PAs have been extensively studied and reviewed [2,4,9]. 1 1 R R 5' CH 3 CH3 CH3 CH3 O 3' O O O 1 2 2' R OH R O CH3 9 OH OH OH OH O O O HO O H HO H HO H H 7 1 6 2 N N N N 5 3 R1 = H Supinine (1) Echinatine (3)RR1 = H, R2= OH Rinderine (4) 1 = H Heliotrine (7) R1 = OH Heleurine (2) R1 = H, R2 = OAc 3'-Acetylrinderine (5) R1 = OH Europine (8) R1 = OH, R2 = OH 5'-Hydroxyrinderine (6) R1 = OAc 5'-Acetyleuropine (9) 1 1 OH R R CH3 CH3 CH3 O O O O O O 1 R O CH3 O CH3 O OH O OH O OH O H O H O H N N N R1 = OH Heliosupine (10) R1 = H 7-Angeloylheliotrine (12) R1 = OH 7-Tigloyleuropine (15) R1 = OAc 3'-Acetylheliosupine (11) R1 = OH Lasiocarpine (13) R1 = OAc 5'-Acetyl-7-tigloyleuropine (16) R1 = OAc 5'-Acetyllasiocarpine (14) OH OH O O CH 3 CH3 CH3 CH3 CH3 O O O O O OH OH CH OH OH O CH3 OH O 3 HO OH HO OH HO OH HO OH HO OH Angelic acid (-)-Viridifloric acid (+)-Trachelantic acid Tiglic acid Heliotric acid Echimidinic acid Lasiocarpic acid FigureFigure 1. PyrrolizidinePyrrolizidine alkaloids alkaloids (PAs) (PAs) and and corresponding corresponding necic necic acids acids commonly commonly found found in Heliotropium in Heliotropium species.species. The cor- The correspondingresponding PA- PA-N-oxideN-oxide forms forms are arenot not shown. shown. ManyPA-containing PAs exhibit plants genotoxic commonly effects grow in inhu pasturesmans and and farm agricultural animals targeting fields, resulting mainly in theoccasional liver [4–7]. cross-contamination Most 1,2-dehydro of PAs crops are and pro- agriculturaltoxins, requiring produce metabolic [1,3,4]. As activation PAs occur by as cytochromemixtures of P450 dozens to generate of various a pyrrolic PA congeners, ester as the the risk reactive arising electrophilic from simultaneous intermediate exposure that subsequentlyto different congeners reacts with has prot toeins be evaluatedand nucleic [9 acids,10]. [6,7]. Although Since, the upon genotoxic ingestion, potency PA-N- of oxidesdifferent are congeners reduced in may the varygut/liver substantially to their corresponding by several orders free bases, of magnitude, both PA forms the current are consideredapproach to to assess be toxic the [2,7,8]. risk of The PA toxicity mixtures of in PA-producing a sample is to plants assign mostly to all ofdepends them the on samethe absolutepotency PA as the concentration most toxic but congeners also on (namely,the plants’ lasiocarpine PA composition, or riddelliine), as the toxic resulting potential in a ofclear individual risk over-estimation PAs and their [9 ,N10-oxides]. widely differs [4,7]. The structural features deter- miningRecently, the toxic Merz potencies and Schrenkof PAs have suggested been extensively assigning studied interim and relative reviewed potency [2,4,9]. (iREP) factorsPA-containing to PA congeners plants of certaincommonly structural grow in features pastures [9]. and In brief, agricultural this approach fields, isresulting based on instructural occasional considerations cross-contamination together of with crops acute and toxicity agricultural data produce from rodents, [1,3,4]. cytotoxicity As PAs occur data asin mixtures mammalian of dozens cell cultures of various and PA genotoxicity congeners, data the risk in Drosophila, arising from obtained simultaneous for a expo- limited surenumber to different of PAs. congeners The iREP has factors to be range evalua fromted [9,10]. 1.0 for Although the most the toxic genotoxic PAs to potency 0.01 for of the differentleast toxic congeners congeners may [9]. vary The substantially limited available by severalin vivo ordersand in of vitro magnitude,toxicity datathe current indicate approach to assess the risk of PA mixtures in a sample is to assign to all of them the same potency as the most toxic congeners (namely, lasiocarpine or riddelliine), resulting in a clear risk over-estimation [9,10]. Recently, Merz and Schrenk suggested assigning interim relative potency (iREP) fac- tors to PA congeners of certain structural features [9]. In brief, this approach is based on structural considerations together with acute toxicity data from rodents, cytotoxicity data Molecules 2021, 26, 689 3 of 12 that cyclic PA di-esters and 7S-open-chained PA di-esters (compounds 10–16 in Figure1) are markedly more toxic than 7R-open-chained di-esters followed by 7S PA mono-esters (compounds 1–9)[3,9,10]. Heliotropium species are PA-producing weeds, widely distributed in the Mediter- ranean region, that have been implicated with lethal PA intoxications in livestock and humans [11–18]. In Israel, 14 different Heliotropium species have been reported, with H. europaeum, H. rotundifolium and H. suaveolens being frequently found in pastures [19–21]. During February 2014, a herd of 73 replacement mixed breed beef cattle (15–18 months old) from the Galilee region of Israel were fed for six weeks a total mixed ration containing hay contaminated with 15% Heliotropium europaeum, resulting in a mortality rate of 33% over a period of 63 days [17].
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