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Identification of Cyclopropylacetyl-(R)-Carnitine, a Unique Chemical Marker of the Fatally Toxic Mushroom Russula Subnigricans

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Identification of Cyclopropylacetyl-(R)-Carnitine, a Unique Chemical Marker of the Fatally Toxic Mushroom Russula Subnigricans 602 Chem. Pharm. Bull. 64, 602–608 (2016) Vol. 64, No. 6 Regular Article Identification of Cyclopropylacetyl-(R)-carnitine, a Unique Chemical Marker of the Fatally Toxic Mushroom Russula subnigricans Masanori Matsuura, Suguru Kato, Yoko Saikawa, Masaya Nakata, and Kimiko Hashimoto* Department of Applied Chemistry, Faculty of Science and Technology, Keio University; 3–14–1 Hiyoshi, Kohoku-ku, Yokohama 223–8522, Japan. Received December 20, 2015; accepted March 17, 2016 A toxic mushroom, Russula subnigricans, causes fatal poisoning by mistaken ingestion. In spite of the potent bioactivity, the responsible toxin had not been identified for about 50 years since its first documenta- tion. Recently, we isolated an unstable toxin and determined the structure. The slow elucidation was partly due to the instability of the toxin and also due to misidentification of R. subnigricans for similar mushrooms. To discriminate genuine Russula subnigricans from similar unidentified Russula species, we searched for a unique chemical marker contained in the mushroom. Cyclopropylacetyl-(R)-carnitine specific to R. subnigri- cans was identified as a novel compound whose 1H-NMR signals appearing in the upfield region were easily recognizable among the complicated signals of the crude extract. Key words cyclopropylacetyl-(R)-carnitine; cycloprop-2-ene carboxylic acid; russuphelin G; mushroom poisoning; Russula subnigricans; Russulaceae Mushroom poisonings attributable to the Russulaceae cause of accidental poisonings. The three representative Rus- mushroom Russula subnigricans were first documented in sula species identified to date in Japan are R. subnigricans, R. 1954 in Japan.1) In the past 50 years, the following seven nigricans, and R. densifolia; the latter two are considered to poisonings have occurred: [deaths/cases (year, place where be edible after cooking. The most useful characteristic feature poisoning occurred)] unknown/unknown (1954, Kyoto); 2/4 to discriminate R. subnigricans from the other two species is (1958, Osaka); 1/3 (1958, Osaka); 0/2 (1970, Toyama); 2/2 the color change that occurs after scratching fruiting body. All (2005, Aichi); 1/1 (2006, Miyazaki); 1/3 (2007, Osaka). In three species have whitish flesh that are tinged reddish brown addition, nine individuals in Taiwan were identified with on scratching. After that, the colors of R. nigricans and R. symptoms of R. subnigricans poisoning in 1998.2) Typical densifolia turn black, whereas the color of R. subnigricans is symptoms following ingestion of R. subnigricans are vomiting persistent. However, classifying these species based on only and diarrhea, which first appear approximately 30 min after this color change is difficult and unreliable. Although discrim- ingestion, followed by stiff shoulders, back ache, and bloody ination of R. subnigricans from R. densifolia is rather easy, as urine that is reddish-brown in color due to high levels of the latter has crowded gills compared to the former, the clas- myoglobin, not hemoglobin. Myoglobin is an oxygen-binding sification of Russula species becomes more complicated due to protein pigment of striated muscles, such as skeletal and car- the existence of several similar unclassified species in addition diac muscles, and is discharged following the breakdown of to the three aforementioned Russula species. Unclassified Rus- myocells, a condition termed rhabdomyolysis. In severe cases sula spp. have distant gills and fruiting bodies that undergo of R. subnigricans poisoning, further symptoms develop, in- color changes similar to those of R. subnigricans. cluding speech impediment, chronic convulsion, contraction Here, to discriminate genuine R. subnigricans from similar of pupils, loss of consciousness, and weakening of the heart, unclassified Russula species, we searched for a compound that resulting in death.3) could serve as a unique chemical marker. In spite of the strong toxicity of R. subnigricans, the re- sponsible toxin remained unknown until recently, when we Results and Discussion isolated and identified a small, unstable compound, cycloprop- Prior to our identification of cycloprop-2-ene carboxylic 2-ene carboxylic acid (1; Fig. 1), as the fatal toxin of this acid as the compound responsible for R. subnigricans toxic- mushroom.4) The toxicity of this compound was demonstrated ity,4) several candidate molecules had been reported. Using on administration to mice, which displayed severe rhabdo- fruiting bodies collected in Miyagi Prefecture, Japan, 3-hy- myolysis. It appears that the difficulty in identifying this droxybaikiain (2),5) russuphelins A–F (3A–F),6,7) and a related compound as the responsible toxin was due in part to its in- compound, russuphelol,8) were isolated (Fig. 1). Among these stability; concentration of solutions of this toxin by drying, a compounds, russuphelins A–D showed cytotoxic acitivity. To common technique in chemical separation and isolation steps, confirm the results of these experiments, we also collected R. promotes its polymerization. Polymerized cycloprop-2-ene subnigricans candidate in Miyagi Prefecture in a broadleaf carboxylic acid lacks toxicity. forest including the Japanese oak, Quercus serrata (one of In addition to inactivation, the long period required for the generally proposed host trees of R. subnigricans; Japanese the determination of cycloprop-2-ene carboxylic acid as the name: konara), and subjected fruiting bodies to methanol responsible toxin is attributable to difficulties discriminating extraction. According to a previous report,5) we isolated 3-hy- R. subnigricans from similar species, which is the primary droxybaikiain (2) from the aqueous layer of the methanol ex- * To whom correspondence should be addressed. e-mail: [email protected] © 2016 The Pharmaceutical Society of Japan Vol. 64, No. 6 (2016) Chem. Pharm. Bull. 603 Fig. 1. Chemical Structures Appeared in Text Fig. 2. Photos of Three Russula spp. Used in This Study (a) R. subnigricans collected in Kyoto, (b) Russula sp. collected in Miyagi, (c) Russula sp. collected in Saitama. tract, which partitioned between water (H2O) and ethyl acetate carboxylic acid (1), from the Kyoto specimen, but could not (EtOAc), while russuphelins A and D (3A, D)6,7) were isolated isolate the toxin in the other two R. subnigricans candi- from the organic layer. Thus, we confirmed that the Russula dates. Taken together, these results indicated that the Kyoto sp. collected in Miyagi Prefecture was the mushroom materi- specimen was genuine R. subnigricans, whereas the other two als previously analyzed and reported in refs. 5–8. Notably, in specimens collected in Miyagi and Saitama were not.4) Thus, addition to these compounds, we isolated a new russuphelin the existence of two unidentifiable mushroom species that congener which we named russuphelin G (3G). On compari- shared nearly identical features with R. subnigricans prompted son of the spectroscopic data (see Experimental) with those of us to search for a unique chemical marker among these three other russuphelins, the structure of 3G was determined to be a species. The photos of R. subnigricans and unidentified two demethyl congener of russuphelin E or F (3E, F). In addition, Russula spp. collected in Miyagi or Saitama are cited in the position of the methoxy group was determined by nuclear Fig. 2. Overhauser effect (NOE) analysis (see Experimental). Genuine R. subnigricans contains cycloprop-2-ene car- We also collected two additional R. subnigricans candidate boxylic acid (1), which could potentially serve as a chemical specimens in Kyoto and Saitama Prefectures for analysis, be- marker to distinguish the fatally toxic mushroom from other cause the first poisoning of R. subnigricans occurred in Kyoto, similar species by chemical analysis. However, as mentioned, and Saitama Prefecture is located between Miyagi and Kyoto toxic compound 1 is easily polymerized under concentrated Prefectures with respect to latitude. In Kyoto Prefecture, conditions, limiting the usefulness of this toxin as a unique mushrooms were collected in a chinquapin forest including marker of genuine R. subnigricans. We next compared the Castanopsis cuspidate (Japanese name: tsuburajii or kojii), 1H-NMR spectra of the crude water extracts of R. subni- whereas in Saitama Prefecture, mushrooms similar to those of gricans and the two unidentifiable species. In the 1H-NMR Miyagi Prefecture were collected in a broadleaf forest includ- spectrum of the R. subnigricans (Kyoto) extract, characteristic ing Quercus serrata, similar forest to that of Miyagi Prefec- signals of a cyclopropane unit were observed in the upfield ture. Our analysis revealed that neither of these two candidate region (0.15, 0.52 ppm). As this compound was not found in specimens contained either russuphelins or 3-hydroxybaikiain the 1H-NMR spectra of the extracts from the two examined (2). Among the three candidate R. subnigricans specimens species, we attempted to isolate the compound indicated by obtained from Miyagi, Kyoto, and Saitama Prefectures, only the 1H-NMR measurement. the Kyoto candidate exhibited fatal toxicity to mice on oral The fruiting bodies of genuine R. subnigricans were cut administration of the water extract. Following further separa- into small pieces (approximately 5 mm) and extracted with tion, we isolated the responsible lethal toxin, cycloprop-2-ene 0.3% acetic acid (AcOH). After filtration and dialysis, the 604 Chem. Pharm. Bull. Vol. 64, No. 6 (2016) Table 1. NMR Data of Cyclopropylacetyl-(R)-carnitine (4) 1H-NMR (300 MHz, D O) 13C-NMR (75 MHz, D O) Position 2 2 HMBC correlation HOD=4.79 DSSa)=−2.04 1 — 177.1 C2-Ha, Hb 2 a: 2.49 (1H, dd, J=8.0, 16.0 Hz) 40.9 C3-H, C4-Ha b: 2.63 (1H, dd, J=5.6, 16.0 Hz) 3 5.63 (1H, m) 67.5 C2-Ha, Hb, C4-Hb 4 a: 3.60 (1H, d, J=14.0 Hz) 68.9 C2-Ha, Hb, C3-H, NMe b: 3.86 (1H, dd, J=9.0, 14.0 Hz) NMe3 3.18 (9H, s) 54.5 C4-Ha, Hb 1′ — 175.6 C2′-Ha, Hb 2′ a: 2.27 (1H, dd, J=7.0, 16.0 Hz) 39.7 C4′-Ha, C5′-Ha b: 2.36 (1H, dd, J=7.4, 16.0 Hz) 3′ 0.98 (1H, m) 6.7 C4′-Ha, C5′-Ha, C2′-Ha, Hb 4′ a: 0.15 (1H, m) 4.2 C2′-Ha, Hb b: 0.52 (1H, m) 5′ a: 0.15 (1H, m) 4.4 C2′-Ha, Hb b: 0.52 (1H, m) a) DSS=sodium 2,2-dimethyl-2-silapentane-5-sulfonate.
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