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Batrachotoxin Alkaloids from Passerine Birds: a Second Toxic Bird Genus (Ifrita Kowaldi) from New Guinea

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Batrachotoxin Alkaloids from Passerine Birds: a Second Toxic Bird Genus (Ifrita Kowaldi) from New Guinea Batrachotoxin alkaloids from passerine birds: A second toxic bird genus (Ifrita kowaldi) from New Guinea J. P. Dumbacher*†, T. F. Spande‡, and J. W. Daly‡ *Molecular Genetics Laboratory, National Zoological Park, Smithsonian Institution, 3001 Connecticut Avenue NW, Washington, DC 20008; and ‡Laboratory of Bioorganic Chemistry, Room 1A-15, Building 8, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892-0820 Contributed by J. W. Daly, July 24, 2000 Batrachotoxins, including many congeners not previously de- scribed, were detected, and relative amounts were measured by using HPLC-mass spectrometry, in five species of New Guinean birds of the genus Pitohui as well as a species of a second toxic bird genus, Ifrita kowaldi. The alkaloids, identified in feathers and skin, were batrachotoxinin-A cis-crotonate (1), an allylically rearranged 16-acetate (2), which can form from 1 by sigmatropic rearrange- ment under basic conditions, batrachotoxinin-A and an isomer (3 -and 3a, respectively), batrachotoxin (4), batrachotoxinin-A 3؅ hydroxypentanoate (5), homobatrachotoxin (6), and mono- and dihydroxylated derivatives of homobatrachotoxin. The highest levels of batrachotoxins were generally present in the contour feathers of belly, breast, or legs in Pitohui dichrous, Pitohui kirho- cephalus, and Ifrita kowaldi. Lesser amounts are found in head, back, tail, and wing feathers. Batrachotoxin (4) and homobatra- chotoxin (6) were found only in feathers and not in skin. The levels of batrachotoxins varied widely for different populations of Pito- hui and Ifrita, a result compatible with the hypothesis that these birds are sequestering toxins from a dietary source. omobatrachotoxin (6) was reported in 1992 to occur in the Hskins and feathers of three passerine bird species in the genus Pitohui (family Pachycephalidae) endemic to New Guinea and considered toxic by New Guineans (1). No defensive toxin had been previously isolated and identified from avian skin or feathers. Homobatrachotoxin is a member of a group of neu- rotoxic steroidal alkaloids, collectively called batrachotoxins, that stabilize the open form of voltage-gated sodium channels in nerve and muscle membranes (2). Previously, batrachotoxins Fig. 1. Batrachotoxins found in feathers and͞or skins of New Guinean ͞ ϭ ϩ were known only from the skins of five neotropical frog species passerine birds. The protonated parent ion (m z [molecular ion 1]) and major fragment ion in chemical ionization mass spectrometry (CIMS) is indi- in the genus Phyllobates (family Dendrobatidae). Batrachotoxins cated in brackets for each structure. occur at high levels in three species of the true poison-dart frogs of western Colombia (Phyllobates terribilis, Phyllobates bicolor, and Phyllobates aurotaenia), while being present only at trace We have now examined feather and skin extracts of Pitohui levels in the two Central American species (Phyllobates vittatus birds by using HPLC-CIMS and have discovered several other and Phyllobates lugubris) (3). In the frogs, batrachotoxin (4), batrachotoxin alkaloids (Fig. 1). Additionally, we examined skin homobatrachotoxin (6), and batrachotoxinin-A (BTX-A; 3) are and feathers from 11 specimens of an unrelated passerine the major alkaloids (for structures, see Fig. 1). Poison-dart frogs, species, Ifrita kowaldi, which New Guineans also report as toxic when raised in captivity, lack batrachotoxins (4) and thus appear (8, 9). In some Ifrita specimens we detected high levels of 6, lesser in the wild to obtain their skin alkaloids from some source, levels of 4, as well as most of the other batrachotoxin alkaloids probably a dietary arthropod. Dendrobatid frogs, when raised in now found in the Pitohui birds. captivity, readily accumulate alkaloids, including BTX-A (3) The amounts and relative proportions of batrachotoxins var- ied widely among different populations of Pitohui and Ifrita, from an alkaloid-containing diet, unchanged into their skin (5, some specimens having none detectable. Such results are com- 6), lending support to such a dietary hypothesis. Previous studies of Pitohui birds by using direct-probe mass spectrometry and TLC with a sensitive colorimetric reagent Abbreviations: CIMS, chemical ionization mass spectrometry; BTX-A, batrachotoxinin-A. revealed only the presence of homobatrachotoxin (6) and, in See commentary on page 12948. 4 some samples, traces of batrachotoxin ( ) (1, 7). The colorimet- †To whom reprint requests should be addressed. E-mail: [email protected]. ric assay using the modified Ehrlich reagent detects only batra- The publication costs of this article were defrayed in part by page charge payment. This chotoxins containing the pyrrole moiety—i.e., 4 and 6. Pharma- article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. cological assays suggested, however, that some extracts were §1734 solely to indicate this fact. slightly more toxic than homobatrachotoxin levels alone could Article published online before print: Proc. Natl. Acad. Sci. USA, 10.1073͞pnas.200346897. explain (7). Article and publication date are at www.pnas.org͞cgi͞doi͞10.1073͞pnas.200346897 12970–12975 ͉ PNAS ͉ November 21, 2000 ͉ vol. 97 ͉ no. 24 Downloaded by guest on September 27, 2021 patible with the hypothesis that these birds obtain batrachotoxin double bond) and mono- and dihydroxylated derivatives of 6 alkaloids from an environmental source and do not produce were commonly detected at trace to minor levels in feather them de novo. extracts (M ϩ H, m͞z 569 3 400; 585 3 416; 585 3 400; data not shown). In addition, a number of other minor alkaloids, some Materials and Methods undoubtedly artifacts, were characterized; their tentative struc- Field Collection and Preparation of Samples. Pitohui and Ifrita tures will be presented elsewhere. However, the methyl ketal (8) samples were collected from a variety of localities in Papua New of 1 was important in determining the crotonate stereochemistry Guinea (see footnote, Table 1). Ifrita is normally found at higher of 1 and is discussed below. It is probably an artifact of storage altitudes than Pitohui dichrous, so the two species were never of samples in methanol. collected at the same locality. Wet tissues were placed in glass vials with Teflon-lined lids in 95% (vol͞vol) or 100% ethanol, Characterization of BTX-A cis-Crotonate (1). Natural BTX-A (3) (40 and feathers were placed dry in Ziploc bags (S. C. Johnson & ␮gin5␮l of methanol) was converted to a C-20 crotonate with Son). Tissues were stored cold (4°C) whenever possible. Crude a 1:9 mixture of cis and trans-crotonic anhydride by treatment ethanol or methanol extracts were made from each sample. For with excess reagent at room temperature for 18 hr. It had on feather extracts, approximately 30–60 mg of feathers was ex- HPLC-CIMS, a mass spectrum, and retention time on coinjec- tracted with 2.0 ml of methanol in 3-ml vials with Teflon-lined tion identical to a new and often major batrachotoxin analog caps by vigorously shaking for a few minutes. The methanol and found in feathers or skin of Pitohui or Ifrita species that did not two additional 2-ml methanol washes were withdrawn and absorb UV at 260 nm and had a CIMS showing a m͞z 486 3 400 concentrated under a stream of nitrogen to approximately 50 ␮l. fragmentation. A synthetic 20S-epimer of BTX-A, dideuterated A 10-␮l aliquot corresponding to 6–12 mg of feathers was at C-22 (10), was crotonylated as above. The resulting 20S- injected onto the HPLC column as described below. Skin crotonate coeluted on HPLC-MS with 1 as did the starting samples, prepared in the field, were trimmed of feathers (some epimeric C-20 alcohols. The epimeric alcohol and ester pairs had feather stubs remained) and were extracted with 95% ethyl virtually identical mass spectra outside of the effect of the two alcohol. Typically samples representing about 50% of total skin deuterium atoms and thus under our conditions, HPLC-CIMS is from one bird were concentrated to 50 ␮l before analysis (data unable to distinguish C-20 epimers, either of the alcohols or not shown). crotonates. Since HPLC was also evidently not able to separate the 1:9 mixture of cis and trans crotonates expected from 3,we HPLC-MS Analysis. A Hewlett Packard (HP) model 1100 liquid could not establish the crotonate stereochemistry of 1.Inan chromatograph with variable wavelength detector set at 260 nm attempt to prove the structure of another new batrachotoxin, (long-wavelength absorption maximum of the pyrrole moiety of namely the methyl ketal (8)of1, we were able to observe a 1:9 4 and 6) was interfaced with a Finnigan LCQ mass spectrometer ratio of HPLC peaks, evidently isomers, of identical chemical operating in the atmospheric pressure chemical ionization ionization mass spectra (m͞z 500 3 414) resulting when an (APCI) mode. Under these conditions, the batrachotoxin alka- authentic sample of the methyl ketal (7)of3 was crotonylated (18 loids yield a protonated molecular ion and only losses of neutral hr, room temperature). The methyl ketal prepared from 1 moieties are observed (e.g., H2O, HOAc, crotonic acid, or (MeOH, p-toluenesulfonic acid, 4 hr) cochromatographed with substituted pyrrolecarboxylic acids. An HP Zorbax column the minor, leading peak of the mixture of crotonates resulting (SB-C18 column of 4.6 mm ϫ 23 cm, 5-␮m particle size) was used from 7, and consequently 1 has a cis-crotonate moiety. The ketal with a 0.5-ml͞min flow rate of 90:10 A:B 3 1:1 A:B over 30 min, crotonates on mild acid hydrolysis (3 hr, 0.1 M HCl) gave a single ϭ ϭ ͞ 3 where A 1% HOAc in H2O and B 1% HOAc in CH3CN. peak on HPLC with m z 486 400, proving that our HPLC HPLC-grade solvents were used. Typically 10-␮l injections were conditions cannot separate the cis and trans crotonates of 3.
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