Configuration of the C(20) Epimer of 7,8-Dihydrobatrachotoxinin A (x-ray crystallography/frog/venom/phyllobates/cardioactive steroid)
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1 Proc. Nat. Acad. Sci. USA Vol. 69, No. 10, pp , October 1972 Configuration of the C(20) Epimer of 7,8-Dihydrobatrachotoxinin A (x-ray crystallography/frog/venom/phyllobates/cardioactive steroid) ISABELLA L. KARLE Laboratory for the Structure of Matter, Naval Research Laboratory, Washington, D.C Communicated by Bernhard Witkop, August 8, 1972 ABSTRACT 7,8-Dihydrobatrachotoxinin A is an intermediate in the synthesis of batrachotoxin, the extremely potent venom from the Colombian frog Phyllobates aurotaenia. A crystal structure analysis by x-ray diffraction has confirmed that the intermediate is identical with the natural batrachotoxinin A except for the saturation of the C(7)-C(8) bond. There are seven asymmetric carbon atoms in the molecule. The cis A/B and C/D ring junctions cause the molecule to assume the characteristic shape of cardioactive steroids. A cage is formed from the A-ring, atom C(9), and the 0 atom that makes the ether linkage between C(3) and C(9). The brightly colored Colombian frog, Phyllobates aurotaenia, contains a potent venom in its skin that has been used as an arrow poison by the Choco Indians. The isolation and characterization (1-3) of this venom has shown that the most toxic component is a steroidal alkaloid, batrachotoxin (Fig. 1A). The nature of the structural formula and the stereoconfiguration were revealed by an x-ray diffraction analysis of a minute single crystal of the p-bromobenzoate derivative of batrachotoxinin A (1, 3) (Fig. 1B), and the absolute configuration was established (4) by the anomalous scattering of the Br atom. Batrachotoxin has become a most valuable research tool. It selectively increases the permeability of electrogenic membranes to sodium ions. As a consequence, it blocks neuromuscular transmission, causes muscle contracture, and depolarizes heart Purkinje fibers (5). The difficulty in obtaining batrachotoxin from its natural source made a synthesis imperative. A total synthesis has been realized (6). During the progress of the synthesis, at the stage when 7,8-dihydrobatrachotoxinin A (Fig. 1C) was prepared, it was deemed advisable to confirm the structure TABLE 1. Formula Molecular weight Color Habit Size Space group a b c V z Density (calculated) Radiation No. of independent reflections Cell parameters and other physical data C25Hs9NO Colorless Prismatic on b 0.17 X 0.60 X 0.17 mm P21212, d A d A t A g/cm3 CuKa^ A 2179 of C by an x-ray diffraction analysis before proceeding with the time-consuming task of removing two hydrogen atoms in order to form the double bond at C(7)-C(8). The dihydro compound that was used for the structure analysis is a diastereoisomer of the natural product, i.e., it has the O-C(20), rather than the a-c(20), configuration. EXPERIMENTAL Intensity data were collected with Ni-filtered Cu radiation on a four-circle automatic diffractometer by the 0-20 scan NO OO C A a 0 Cx S -C C FIG. 1. (A) batrachotoxin; (B) bromobenzoate derivative of batrachotoxinin A; (C) C(20) epimer of 7,8-dihydrobatrachotoxinin A. 2932
2 Proc. Nat. Acad. Sci. USA 69 (1972) 7,8-Dihydrobatrachotoxinin A Configuration 2933 Atom C(1) C(2) ;(3) C(4) C0) C(6) C(7) C(l) Q9) C C(13) 0(;t4) ( 134 ) t;(15) C(16) C(17) C(18) C (19) 0(20) ; (21) 0(22) C(23) 0(24) C(25) N (2) e(3) e(4) x , 6981 O, i 0,242 0,4173 O. 704 O,3777 0,4862 0, 5292 O O, ,3534 0, , , 673 0, ,3121 0,3337 0, , , ,7063 0,1659 0,6706 0Q5472 0,5756 0, , 2121 TABLE 2. y 0, , ,3521 0,3867 0, , , , 2057,2415 0,2785, 35,7 0, , O, , I , Q 4747,s ,3554 0, 2661 Fractional coordinates* and thermal parameterst oll ,3!507 0,4588 O95n O ,.3278 O Q4399 O, ,1404 O, , O 151I O,4906-0, , O0,939 O ,1080 0,2084 OQ O,O , ,064 6, ,1l ,86 6,24 5,82 5,29 6,32 6,35 3,69 6,12 7,Q9 4,32 4,188 5,31 3,95 3,76 3,39 3,70 3,85 3,16 3,09 5 I O 9 5, ,72 3,1.6 2,*8 3,01 2,76 2,53 3,36 3,44 3,36 3,57 5,54 2,20 4,82 3,79 3,24 4, 67 3,142 3,46 3,11 3, , ,54 3,36 3,35 4,34 3,39 3,"5 5,64 4, ,*6 5,72 5,64 5,42 4,36 2,65 3,40 5,26 6,9j 3,43 4,96 4,71 3,56 3,86 6,25 6,12 6,90 7,20 5, ,21 4,02 1,72 0,56 -of45-0,10 0,5 1,07 0,56 0,70 0,33 0,30 0,37 0,30 0,72 0,49-0,14 0,67-0,53 1,12-2,33S 2,72-0,82-2,t22 1,11 1,27-1,e96 e55-1,,46-0,99-1,*07-103,03 0,18 0, O 0,02 0,04 0, , e, 27-0,t 0, O t 5 2,71 0, O00 0,29 't50-1,31, -1, ,,48-1, ,02 0, ,62 0,72-0,03 1,08 0,63 0,05 1,08-1,,21 1,12-1,,89-0,58-0,18 * The standard deviations are near for each coordinate for the carbon atoms and for the oxygen atoms. t The thermal parameters are expressed in the form T = exp -l/4(bllh2a*2 + B22k2b*2 + B3312c*2 + 2Bi2hka*b* + 2Bl3hla*c* + 2B23klb*c*)]. 0,65 FIG. 2. (Top) Stereodiagram of the synthetic C(20) epimer of 7,8-dihydrobatrachotoxinin A. The smaller circles represent H atoms and the blackened bond represents a double bond. The figure was drawn from experimentally determined coordinates by means of a computer, from a program prepared by Johnson (11). (Bottom) Stereodiagram of natural batrachotoxinin A (1, 3).
3 2934 Chemistry: Karle Proc. Nat. Acad. Sci. USA 69 (1972) TABLE 3. Torsional angles* Atoms A B C D Degrees ring A -3 10, 1, 2, 3 is 2, 3, 4 2,.3, 4, 5 4, 5, 10 (boat) 4, 5, 10, 1 K 5 10, 1, /13, 14, 8, 9 14, 8, 9, 11 8, 9, 11, 12 ring C 9 11, 12, 13 (chair) 12, 13, 14 k 12, 13, 14, , 1, 2, 3 1, 2, 3, 0(2) ring A1 2, 3, 0(2), 9 3, 0(2), 9, 10 (boat) 0(2), 9, 10, 1 k 9, 10, 1, , 14, 15, 16 14, 15, 16, 17 ring D 15, 16, 17, 13 16, 17, 13, 14 (envelope) 17, 13, 14, , 5, 4, 3 5, 4, 3, 0(2) 4, 3, 0(2), 9 ring A2 3, 9, 10 0(2), (boat) 0(2), 9, 10, 5 9, 10, 5, 4 10, 5, 6, 7 5, 6, 7, 8 6, 7, 8, 9 ring B 7, 8, 9, 10 (chair) 8, 9, 10, 5 9, 10, 5, ring E (twist chair) 13, 14, 0(4), 14, 0(4), 23, 0(4), 23, 22, 23, 22, N, 22, N, 18, N. 18, 13, 18, 13, 14, N (4) * The torsional angle ABCD about the bond BC is defined as: technique, with a (a2)-20(al) scan over 20 at a rate of 20/min. The background was counted for 10 sec at either end of the scan. The data were corrected for Lorentz and polarization factors and placed on an absolute scale by means of a K-curve, and normalized structure factor magnitudes El, as well as structure factor magnitudes IFl, were derived. Cell parameters and other physical data are listed in Table 1. Phases for the structure factors were determined directly from the observed intensities by means of the symbolic addition procedure (7). In the initial steps, this procedure depends upon the relationship [1 (8), 4hiki h + 4Oh2k2, 4'hi+h2, ki+k2, where 10hnknln is the phase of the reflection with indices hnkln. This relation is used with those reflections having the largest JEl magnitudes. In the present structure determination, the relatively small errors in the values of the phases as obtained from [1] were not random, but accrued in one direction in the stepwise application of [1]. As a result, the maxima in a sharpened electron-density function (E-map) (9), computed with the phases as obtained with the symbolic addition procedure, corresponded to the atoms of a large fragment of the molecule; however, the fragment was incorrectly placed in the unit cell with respect to the symmetry elements. The shift to the correct position (x , y 0.15, - z 0.15) - was obtained from the application of a translation function (10) on the knownfragment ofthe molecule. Least-squares refinement of the coordinates and thermal parameters, initially isotropic then anisotropic, was followed by a calculation of a difference map. The 39 strongest peaks in the difference map corresponded to the positions of the 39 hydrogen atoms. Further least-squares refinement was performed with anisotropic thermal parameters for the carbon, nitrogen, and oxygen atoms and with the coordinates and thermal factors for all the hydrogen atoms included as constant parameters. The thermal factors for the hydrogen atoms were chosen to be equal to those of the carbon or oxygen atom to which the hydrogen atom is attached. The final agreement factor between observed and calculated structure factors was 6.4%. RESULTS The results of the x-ray analysis confirmed that the synthetic product is the C(20) epimer of 7,8-dihydrobatrachotoxinin
4 Proc. Nat. Acad. Sci. USA 69 (1972) 7,8-Dihydrobatrachotoxinin A Configuration 2935 G(2) 0(3) 0(I) G(3) 0(2) 0(9) 0(8) 0(9) C(l) G(10 0(5) G0O) C(12) G(13) 004) '0(13) 0(4) G(14) 0(8) 0(14) 0(4) 0(2) C(O1) C(OO C(9) C(19) C(18) C(17) C(13) G(15) FIG. 3. Bond lengths and angles in the C(20) epimer of 7,8-dihydrobatrachotoxinin A. The standard deviations are of the order of A for the bond lengths and 0.4 for the bond angles. A. The molecule is shown in the stereodiagram in Fig. 2, which was drawn by computer (11) from the experimentally determined coordinates listed in Table 2. For comparison, the molecule of batrachotoxinin A (1, 3) is also shown in Fig. 2. Aside from the difference in the conformation of the B ringhalf-chair in batrachotoxinin A due to the double bond between C(7) and C(8) and chair in 7,8-dihydrobatrachotoxinin A-the geometry of the two molecules is remarkably similar. In 7,8-dihydrobatrachotoxinin A, the A/B and C/D ring junctions are cis; ring A is forced into the boat conformation by the ether bridge between C(3) and C(9); rings B and C are in the chair conformation; ring D is in the,8-envelope conformation with C(14) 0.41 X out of the plane of the other four atoms; and the heterocyclic seven-membered ring E is in a twisted boat conformation with atoms 0(4), C(14), C(13), and C(18) near one plane to within i 0.17 A, atoms C(18), N, C(14), and 0(4) near another plane to within X, and atoms N, C(22), and C(23) in a third plane. The dihedral angles in ring E are 125 between the first and second planes and 124 between the second and third planes. The torsional angles about each bond contained within a ring are listed in Table 3. These angles are a measure of the deviation of a ring from an idealized boat, chair, or envelope conformation. The C atom of the methoxy moiety is trans to the C(4) atom. In both compounds, the methyl group on the N atom is equatorial with respect to the seven-membered ring. Bond lengths and angles are illustrated in Fig. 3. The standard deviations calculated from the least-squares agreement to the experimental data are of the order of for C-C bonds, A for C-0 bonds, and 0.40 for the angles. In the elucidation of the structure of batrachotoxinin A, the standard deviations for the bond lengths were of the order of 0.05 A. This relatively large value obtains because only 830 reflections were observed from the extremely small crystal. The present structure determination of the dihydro compound yields more precise values for the bond lengths and angles. The average length for 19 saturated C-C ring bonds is A, the average length for three saturated C-N bonds is A, and the average length for eight C-0 bonds is A. These values are very close to those normally observed for saturated C-C, C-N, and C-0 linkages (12). The packing of the molecules in the unit cell is shown in Fig. 4. The packing is characterized by two parallel strands of molecules. Between the strands, all C... C intermolecular approaches are greater than 3.7 ix and all C... 0 approaches are greater than 3.6 X, except for 3.29.A between C(15)... 0(3') (the atoms are associated with molecules that are related by x, y, z and -x, 1/2 + y, 1/2 - z, respectively). Within each strand, the molecules are linked together into a continuous chain by the formation of a hydrogen bond between 0(3)H... 0(5') of length 2.77 I Atom 0(3) is the donor and 0 (5') the acceptor. A detail of the continuous chain, wherein the molecules are related by a screw axis parallel to the a direction, is shown in Fig. 5. FIG. 4. Packing of the molecules in the unit cell. Oxygen atoms are shaded. The axial directions are: a I, b, and c up from the plane of the paper.
5 2936 Chemistry: Karle Proc. Nat. Acad. Sci. USA 69 (1972) FIG. 5. A portion of the infinite chain formed by hydrogen bonding between O(5)H and 0(3). Oxygen atoms are shaded. The axial directions are: a A-, c t, and b up from the plane of the paper. Batrachotoxin and batrachotoxinin A are cardiotoxic materials. The geometry of these molecules bears a close resemblance to that of the cardioactive drugs digitoxigenin (18) and strophanthidin (14). Each of these materials has cis A/B and C/D ring junctions, which cause the steroidal moieties to assume a globular shape. The resemblance of the shape of dihydrobatrachotoxinin A to batrachotoxinin A, as well as to digitoxigenin and strophanthidin, suggests that the synthetic dihydro compound may also have cardioactive properties. I thank Dr. Bernhard Witkop of the National Institutes of Health for his cooperation in this project. 1. Tokuyama, T., Daly, J., Witkop, B., Karle, I. L, & Karle, J. (1968) J. Amer. Chem. Soc. 90, Tokuyama, T., Daly, J. W. & Witkop, B. (1969) J. Amer. Chem. Soc. 91, Karle, I. L. & Karle, J. (1969) Acta Crystallogr. Sect. B 25, Gilardi, R. D. (1970) Acta Crystallogr. Sect. B 26, Albuquerque, E. X., Daly, J. W. & Witkop, B. (1971) Science 172, Imhof,- R., Gdssinger, E., Graf, W., Berner, H., Berner- Fenz, L. & Wehrli, H., Helv. Chim. Acta, in press; see also Graf, W., Berner, H., Berner-Fenz, L., G6ssinger, E., Imhof, R. & Wehrli, H. (1970) Helv. Chim. Acta 53, ; G6ssinger, E., Graf, W., Imhof, R. & Wehrli, H. (1971) Helv. Chim. Acta 54, Karle, J. & Karle, I. L. (1966) Acta Crystallogr. 21, Karle, J. & Hauptman, H. (1950) Acta Crystallogr. 3, , Ineq Karle, I. L., Hauptman, H., Karle J. & Wing, A. B. (1958) Acta Crystallogr. 11, Karle, J. (1972) Acta Crystallogr. Sect. B 28, Johnson, C. K. (1965) ORTEP, ORNL-3794 (Oak Ridge National Laboratory, Oak Ridge, Tenn). 12. See e.g. (1962) International Tables for X-Ray Crystallography (The Kynoch Press, Birmingham, England), Vol. III, p Karle, I. L. & Karle, J. (1969) Acta Crystallogr. Sect. B 25, Flippen, J. L. & Gilardi, R. D. (1971) Abstract C-4 (American Crystallographic Association Meeting, Ames, Iowa).
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