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3-Carboline of Animal Origin: Isolation and Chemical Characterization from the Skin of the African Rhacophorid Frog, Kassina Senegalensis

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3-Carboline of Animal Origin: Isolation and Chemical Characterization from the Skin of the African Rhacophorid Frog, Kassina Senegalensis Biomedical Research 3 (2) 232-234, I982 Trypargine, a new tetrahydro-|3-carboline of animal origin: Isolation and chemical characterization from the skin of the African rhacophorid frog, Kassina senegalensis TOSHIFUMI AKIZAWAI, KAZUO YAMAZAKI1, TADASHI YASUHARA2, TERUMI NAKAJIMA2, MARISA ROSEGHINI3, GUILIANA FALCONIERI ERSPAMER3 and VITTORIO ERSPAMER3 Ilnstitute of Pharmaceutical Sciences, Hiroshima University, School of Medicine, Hiroshima 734, Zlnstitute for Medical and Dental Engineering, Tokyo Medical and Dental University, Tokyo 101, Japan, and 3Depart- ment of Pharmacology, University of Rome, Rome 00100, Italy ABSTRACT A new tetrahydro-,8-carboline derivative, trypargine [l-(3’guanidinopropyl)-1, 2, 3, 4-tetrahydro-,6’-carboline] was isolated from methanol extracts of the skin of the African rhacophorid frog, Kassina senegafensis. Its structure was deduced by chemi- cal and spectrometric studies with “C-NMR and FD-Mass spectrometry and con- firmed by chemical synthesis. Intravenous administration (l0 mg/kg) of trypargine to mice caused death by respiratory failure and paralysis. The amphibian skin contains many active sub- an alumina column which was eluted with de- stances with interesting pharmacological prop- scending concentrations of ethanol as described erties. These substances include bufadienolides previously (12), Sakaguchi positive material in the toad, batracotoxin, pumiliotoxin and emerged in non-adsorbed and in 90% ethanol histrionicotoxin in the arrow poison frogs, tetro- eluates. This material was further purified by dotoxin in Zetek’s frog (13) and many other gel filtration on Sephadex G-25 followed by ion- active amines and polypeptides (5, 8). exchange chromatography on an SP-Sephadex In the present study, we isolated a new tetra- column which was eluted successively with hydro-ii-carboline derivative, trypargine, from ammonium formate buffer (pH 6.8) in a linear the skin extracts of the African rhacophorid gradient from 0.01 M to 0.5 M and at a constant frog, Kassfna senegalensis. The trypargine, concentration of 1.0 M. The purified com- which contains a guanidino group, was exten- pound thus obtained was crystallized in hydro- sively purified by gelfiltration and ion-exchange chloride form to white needles (mp 211-213°C). chromatography and the chemical structure was The compound showed an Rf of 0.68 and 0.45 elucidated by 13C-NMR and FD-mass spectro- on HPTLC (Merck) with solvent systems of n- metry. butanol/pyridine/acetic acid/water (4: 1: 1: 1) The skins (665 g, £10.55 g/frog) of Kassina and iso-propanol/methyl acetate/28% ammonia senegalensis, collected in Kenya and South (9: 7: 4), respectively. In addition to a positive Africa during the period 1971-1974, were used Sakaguchi reaction, the compound exhibited in this study. The skins were removed from the positive reaction in Dragendorf and Ehrlich frogs immediately after killing and extracted tests, but the reaction of the compound was twice with a volume of methanol 5 times the negative in Pauly, ninhydrin and fiuorescamine weight of the tissue. The methanol extracts tests. An acid hydrolysate of the compound contained kassinin, a biologically active dode- contained no free amino acids. It showed capeptide amide structurally related to substance UV‘,”,,‘§§“ nm (log 6): 222 (4.54), 272 (3.88), 279 P (1). During the purification of kassinin with (3.83) and 289 (3.74), suggesting the presence of TRYPARGINE 233 Table 1 13C-NMR Chemical Shifts (5 flom Inrernai TMS) of Trypar- gine, 1,2,3,4»Tetrahydroharman and Argimlue 8 M 1,2,3,4-Teifflhydr0- m Trypargine harmane Arginine 20-0(q) (~CHs) 18.5(t) a’ 22.6(t) 24.5(t) b’ 24.8(t) 29.3(t) c’ 28.4(t) 41.2(t) cl’ 41.5(t) 42.l(t) 43.1(t] 53.5(d) 49.1( , 55.3(d) (oi Cl-I) 107.0(3) 107.8(s) 112.4(d) 1 16.6(d] i19.6(d) 118.41 120.6(8) 119.41 123.5(1) ’ 121.91 :69‘ 9:’.0), \--/ '"::>¢'—.:—.::>-rm~3o__ 128.3(s_, 129.6(s) m’ 137.31§l@§§§1'==§Q;.33 137.2(5) n’ 137.5(3) o3-we:3~>r‘—--:1-ono-1:1:mo l57.6(s) 0’ 157.7(3) 175.5(s) (COOH) Letters in parentheses indicate the multiplicity. s, singlet; d, doublet; t, triplet; q, quartet the indole ring in the molecule. HCOO“) supported this conclusion. 13C-NMR spectra of the compound (80 mg/ml The structure of trypargine (Fig. 1) was D20, 25°C, dioxane as an internal standard), as confirmed by chemical synthesis. Natural compared with those of harmane (4) and argi- trypargine was identified with (-—)trypargine nine (7), showed features indicative of a tetra- obtained by optical resolution of the synthetic hydro-,3-carboline derivative, 1-(3’-guanidino- racemate (10). propyl)-1,2,3,4-tetrahydro-)6-carboline (Table 1). Trypargine was considered to be a product of Color tests and FD-Mass spectrometry (m/e 272 a Pictet-Spenglar type reaction of tryptamine (MH)+, m/e 544(MI—l)%+, m/e 589(MH)%" - and an 00-ketoacid or aldehyde derived from trypargine i a as-'-... O/NH2 §<---.- §iUQ Z I2,0 --c ;:~ I °ea QLZCD ‘NH b 1, 2, 3, 4-tetrahydroharmane arginine .i I H2 I z ra ., Z’ 8' 7 J e HOOC\C,N 11$E/NH2 k’ fr, M..- \NH hi H b’ x Fig. 1 Trypargine, a new tetrahydro-,6’-carboline of animal origin. Isolation and chemical characterization from the skin of the African rhacophorid frog, Kasszlua senegalensis 234 T. AKIZAWA et al. arginine. A structurally similar compound with BUCKHOLTZ N. S. (1980) Neurobiology of tetra- antimicrobial activity (9), which may be derived hydro-,B-carboline. Life Sci. 27, 893-903 by condensation of histamine and one carbon CRABB T. A. (1978) Nuclear magnetic resonance unit (spinaceamine and N-methyl spinaceamine), of alkaloids. In Annual Reports on NMR Spectro- has been isolated from the skin extracts of the scopy (ed. WEBB G. H.) Academic Press, New York, p. 117 South American frog Leptodactylnspentadactylns ERSPAMER V. and MELCHIORRI P. (1980) Active labyrt'ntln'cus (6). Large amounts of trypargine polypeptides: from amphibian skin to gastro- or a related compound were also found in the intestinal tract and brain of mammals. Trends skin of Hylambates macnlatns, an African am- Plrarrnacol. Sci. 1, 391-395 phibian related to Kassina. Recent studies ERSPAMER V., ROSEGHINI M. and CEI J. M. (1964) disclosed the occurrence and in vivo formation of Indole and imidazole and phenylalkylamines in tetrahydro-fl-carboline derivative in mammalian the skin of thirteen Leptodactylns species. Bio- brain (2, 11), suggesting that tetrahydro-fi- cltem. Plzarmacol. 13, 1083-1093 carbolines may interact with some part of the JOHNSON L. F. and JANLOWSKY W. C. (1972) serotonergic neurotransmitter system (3). Carbon-13 NMR spectra, John Wiley and Sons, New York/London/Sydney/Tronto, p. 213 Intravenous administration of trypargine to NAKAJIMA T. (1981) Active peptides in am- mice (10 mg/kg, n~—7) caused death within 2 min phibian skin. Trends Plzarmacol. Sci. 2, 202-205 by respiratory failure and paralysis. A phar- PREUSSER H. J., HABERMEHL G., SABLOFSKI M. macological study on trypargine is in progress. and SCI-IMALL—I-IAURY D. (1975) Antimicrobial activity of alkaloids from amphibian venoms and Received for publication 7 October 198],‘ and in effects on the ultrastructure of yeast cells. revisedform 23 January 1982 Toxricon 13, 285-289 Snnvnzu M., Ismxawrx M., KOMODA Y. and NAKAJIMA T. (1982) Total synthesis of (—)trypar- REFERENCES gine. Chem. Pharm. Bull. 30, 909-914 SHOEMAKER D. W., CUMMINS J. T. and BIDDER 1. Anasrasr A., Monracuccm P., ERSPAMER V. and T. G. (1978) )6‘-Carbolines in rat arcuate nucleus. VIssER J. (1977) Amino acid composition and Neuroscience 3, 233-239 sequence of kassinin, a tachykinin dodecapeptide YASUHARA T, NAKAJIMA T., ERSPAMER G. F. and from the skin of the African frog Kassina sene- ERSPAMER V. (1981) New tachykinis, Gluz, Pro5- galensfs. Experientia 33, 857-858 kassinin (Hylambates-kassinin) and hylambatin 2. BAKER S. A., HARRISON R. E., Baown G. B. and in the skin of the African rhacophorid frog, CHRISTIAN S. T. (1979) Gaschromatographicl Hylanibates macnlatns. 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