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A thallium-205 NMR study of the thallium(I)-vafinomycin complex in the solid state
JOURNAL
OF MAGNETIC
RESONANCE
‘%%,217-219
(1981)
A Thallium-205 NMR Study of the Thallium(I)-Valinomycin Complex in the Solid State As part of a program initiated to study ion transport across biological membranes mediated by antibiotics, we recently reported the results of cation-antibiotic interactions in solution using Tl-205 NMR spectroscopy (I -4). It was found that the resonance frequency of the Tl+-205 ion, complexed by the antibiotic, is a good “fingerprint” for the type(s) of functional groups used by the antibiotic molecule ts bind the cation. Since biological membranes possess some solid-state characteristics, it was of interest to begin an investigation of the solid-state Tl+-antibiotic complexes, again using Tl-205 NMR, to try to gain a better understanding of the nature of the complex in a membrane. We report here the first results of this solid-state work, namely, the results pertaining to the Tl+-valinomycin complex. Valinomycin is well known for its ability to enhance the potassium ion permeability of membranes. X-Ray crystallography of the solid K+-valinomycin complex (4-8) and a number of investigations of the complex in solution (9-18) have shown that the structure of the complex is virtually the same in the two states. Thallium is an excellent NMR probe for studies of the role of potassium ions in biological systems since potassium has no isotope which can easily be monitored by NMR. The ionic radii of K+ and Tl+ are similar and the chemical properties of the two ions are sufficiently alike for Tl+ to replace K+ in a number of enzymes. It is also important to note that the K+ and Tl+ complexes with valinomycin in solution have nearly identical structures (10). The Tl+-valinomycin complex was prepared in the manner previously described ( I). The solid-state Tl-205 spectra of the complex were obtained with a modified Etruker HFX-90 NMR spectrometer (BO = 2.114 T), described elsewhere (19), that has a Nicolet Explorer III digital oscilloscope interfaced to the Nicolet computer. The details of the interface of the oscilloscope, which functions as a transient recorder to the computer, will be published separately. All spectra were obtained from the solid-state complex placed in a melting point capillary tube inserted into a standard 5-mm NMR tube containing a ‘H lock compound. The spectra were obtained under conditions of no ‘H dipolar decoupling or magica.ngle spinning. Figure 1 shows the absorption and power solid-state Tl-205 spectra obtained for the Tl+-valinomycin complex at 30°C. The spectra have the general appearance of an axially symmetric powder pattern. This is to be expected since the X-ray crystallographic analysis (5) of the K+ complex indicates that the K+ ion is coordinated octahedrally by six carbonyl oxygen atoms with the anion positioned along the symmetry axis. It has been suggested (8) that valinomycin is actually an ion-pair transport agent. Since the symmetry axis of the system is through the center of the macrocycle cavity, the cL tensor component may be associated with carbonyl oxygen inter217 0022-2364181/070217-03$02.00/O Copyright 0 1981 by Academic Press, Inc.. All rights of reproduction in any form reserved
218
COMMUNICATIONS
FIG.
1. Absorption
and power spectra of TI-valinomycin
complex.
action with the Tl+ ion. Because the power spectrum shows characteristic singularities at the eigenvalues of the chemical shift tensor (20), it was used to obtain the resonance frequencies. The resonance frequency of this chemical shift component ((TV = 51,884,700 Hz) is at a lower frequency than the ml1tensor component (a,, = 51,892,400 Hz). The u,, component is possibly related to an axial distortion of the carbonyl oxygen binding resulting from weak ion pairing with the anion. This is consistent with the fact that the Tl-205 resonance frequency of TlClO, is 51,895,719 Hz at 30°C. Previously, we reported a value for the chemical shift anisotropy of the Tl+-valinomycin complex based upon calculations made from Tl-205 spin-lattice relaxation time data obtained from solution spectra (2). The chemical shift anisotropy of approximately 7700 Hz obtained from the power spectrum is much smaller than that predicted from T, data. It might be argued that the solid-state spectrum does not show chemical shift anisotropy but two forms of the Tl+valinomycin complex with a chemical shift difference of about 4000 Hz! If this were the case, and we have no evidence for it, the chemical shift anisotropy would be even smaller and the predicted value more in error. ACKNOWLEDGMENT We wish to acknowledge the National Science Foundation for support through Grant PCM-7827037. REFERENCES I. J. F. HINTON AND R. W. BRIGGS, .I. Magn. Reson. 32, 155 (1978). 2. R. W. BRJ~GS AND J. F. HINTON, J. Magn. Reson. 33,363 (1979). 3. R. W. BRIGGS AND J. F. HINTON, Biochemistry 17, 5576 (1978).
219
COMMUNICATIONS 4. !i.
R. W. BRIGGS, F. A. ETZKORN, AND K. NEUPERT-LAVES AND M. DOBLER,
6. I. KARLE, .I. Am. Chem. Sot. W, 4379 (1975). ?. G. D. SMITH, W. L. DUAX, D. A. LANGS, G. T. DETITTA, 8.
AND C. M. WEEKS, J. Am. Chem. M. PINKERTON, L. K. STEINRAUF,
(1980).
J. F. HINTON,J. Magn. Reson. 37, 523 He/v. Chim. Acta 58, 432 (1975). J. W.
EDMONDS,
D.
C.
ROHRER,
(1975).
Sot.
97, 7242
AND
P. DAWKINS,
Biochem.
Biophys.
Res.
Commun.
35,
J. Biochem.
78,
512 (1969). 9. Yu. A. OVCHINNIKOV 10. V. F. BYSTROV, Yu.
AND V. T. IVANOV, Tetrahedron D. GAVILOV, V. T. IVANOV, ANDTU.
30,
1871 (1974).
A. OVCHINNIKOV,&I~.
63 (1977). II.
J. D.
GLICKSON,
S. L. GORDON,
T. P. PITNER,
D. G. AGRESTI,
AND
R. WALTER,
Biochemistry
15, 5721 (1976). B. C. PRESSMAN, J. Biol. Chem. 244, 502 (1969). Biochemistry 12, 486 (1973). G. DAVIS AND D. C. TOSTESON, Biochemistry 14, 3962 (1975). J. PATEL, Biochemistry 12, 496 (1973). C. FEDARKO, J. Magn. Reson. 12, 30 (1973). H. HAYNES, B. C. PRESSMAN, AND A. KOWALSKY, Biochemistry 10, 852 (1971). G. DAVIS, Biochem. Biophys. Res. Commun. 63, 786 (1975). F. HINTON AND R. W. BRIGGS, J. Magn. Reson. 19, 393 (1975). RABER, G. BRUNGER, AND M. MEHRING, Chem. Phys. Lett. 23, 400 (1973).
12. IS.
D. H. HAYNES, A. KOWALSKY, D. J. PATEI. AND A. E. TONELLI,
14. 15.
D. D. M.
16. 17. D. 18. D. 19. J. 20.
H.
AND
J. F. HINTON K. R. METZ
F. S. Department of Chemistry (University of Arkansas Fayetteville, Arkansas 72701 Received January 20, 1981; revised March 16, 1981
MILLETT
OF MAGNETIC
RESONANCE
‘%%,217-219
(1981)
A Thallium-205 NMR Study of the Thallium(I)-Valinomycin Complex in the Solid State As part of a program initiated to study ion transport across biological membranes mediated by antibiotics, we recently reported the results of cation-antibiotic interactions in solution using Tl-205 NMR spectroscopy (I -4). It was found that the resonance frequency of the Tl+-205 ion, complexed by the antibiotic, is a good “fingerprint” for the type(s) of functional groups used by the antibiotic molecule ts bind the cation. Since biological membranes possess some solid-state characteristics, it was of interest to begin an investigation of the solid-state Tl+-antibiotic complexes, again using Tl-205 NMR, to try to gain a better understanding of the nature of the complex in a membrane. We report here the first results of this solid-state work, namely, the results pertaining to the Tl+-valinomycin complex. Valinomycin is well known for its ability to enhance the potassium ion permeability of membranes. X-Ray crystallography of the solid K+-valinomycin complex (4-8) and a number of investigations of the complex in solution (9-18) have shown that the structure of the complex is virtually the same in the two states. Thallium is an excellent NMR probe for studies of the role of potassium ions in biological systems since potassium has no isotope which can easily be monitored by NMR. The ionic radii of K+ and Tl+ are similar and the chemical properties of the two ions are sufficiently alike for Tl+ to replace K+ in a number of enzymes. It is also important to note that the K+ and Tl+ complexes with valinomycin in solution have nearly identical structures (10). The Tl+-valinomycin complex was prepared in the manner previously described ( I). The solid-state Tl-205 spectra of the complex were obtained with a modified Etruker HFX-90 NMR spectrometer (BO = 2.114 T), described elsewhere (19), that has a Nicolet Explorer III digital oscilloscope interfaced to the Nicolet computer. The details of the interface of the oscilloscope, which functions as a transient recorder to the computer, will be published separately. All spectra were obtained from the solid-state complex placed in a melting point capillary tube inserted into a standard 5-mm NMR tube containing a ‘H lock compound. The spectra were obtained under conditions of no ‘H dipolar decoupling or magica.ngle spinning. Figure 1 shows the absorption and power solid-state Tl-205 spectra obtained for the Tl+-valinomycin complex at 30°C. The spectra have the general appearance of an axially symmetric powder pattern. This is to be expected since the X-ray crystallographic analysis (5) of the K+ complex indicates that the K+ ion is coordinated octahedrally by six carbonyl oxygen atoms with the anion positioned along the symmetry axis. It has been suggested (8) that valinomycin is actually an ion-pair transport agent. Since the symmetry axis of the system is through the center of the macrocycle cavity, the cL tensor component may be associated with carbonyl oxygen inter217 0022-2364181/070217-03$02.00/O Copyright 0 1981 by Academic Press, Inc.. All rights of reproduction in any form reserved
218
COMMUNICATIONS
FIG.
1. Absorption
and power spectra of TI-valinomycin
complex.
action with the Tl+ ion. Because the power spectrum shows characteristic singularities at the eigenvalues of the chemical shift tensor (20), it was used to obtain the resonance frequencies. The resonance frequency of this chemical shift component ((TV = 51,884,700 Hz) is at a lower frequency than the ml1tensor component (a,, = 51,892,400 Hz). The u,, component is possibly related to an axial distortion of the carbonyl oxygen binding resulting from weak ion pairing with the anion. This is consistent with the fact that the Tl-205 resonance frequency of TlClO, is 51,895,719 Hz at 30°C. Previously, we reported a value for the chemical shift anisotropy of the Tl+-valinomycin complex based upon calculations made from Tl-205 spin-lattice relaxation time data obtained from solution spectra (2). The chemical shift anisotropy of approximately 7700 Hz obtained from the power spectrum is much smaller than that predicted from T, data. It might be argued that the solid-state spectrum does not show chemical shift anisotropy but two forms of the Tl+valinomycin complex with a chemical shift difference of about 4000 Hz! If this were the case, and we have no evidence for it, the chemical shift anisotropy would be even smaller and the predicted value more in error. ACKNOWLEDGMENT We wish to acknowledge the National Science Foundation for support through Grant PCM-7827037. REFERENCES I. J. F. HINTON AND R. W. BRIGGS, .I. Magn. Reson. 32, 155 (1978). 2. R. W. BRJ~GS AND J. F. HINTON, J. Magn. Reson. 33,363 (1979). 3. R. W. BRIGGS AND J. F. HINTON, Biochemistry 17, 5576 (1978).
219
COMMUNICATIONS 4. !i.
R. W. BRIGGS, F. A. ETZKORN, AND K. NEUPERT-LAVES AND M. DOBLER,
6. I. KARLE, .I. Am. Chem. Sot. W, 4379 (1975). ?. G. D. SMITH, W. L. DUAX, D. A. LANGS, G. T. DETITTA, 8.
AND C. M. WEEKS, J. Am. Chem. M. PINKERTON, L. K. STEINRAUF,
(1980).
J. F. HINTON,J. Magn. Reson. 37, 523 He/v. Chim. Acta 58, 432 (1975). J. W.
EDMONDS,
D.
C.
ROHRER,
(1975).
Sot.
97, 7242
AND
P. DAWKINS,
Biochem.
Biophys.
Res.
Commun.
35,
J. Biochem.
78,
512 (1969). 9. Yu. A. OVCHINNIKOV 10. V. F. BYSTROV, Yu.
AND V. T. IVANOV, Tetrahedron D. GAVILOV, V. T. IVANOV, ANDTU.
30,
1871 (1974).
A. OVCHINNIKOV,&I~.
63 (1977). II.
J. D.
GLICKSON,
S. L. GORDON,
T. P. PITNER,
D. G. AGRESTI,
AND
R. WALTER,
Biochemistry
15, 5721 (1976). B. C. PRESSMAN, J. Biol. Chem. 244, 502 (1969). Biochemistry 12, 486 (1973). G. DAVIS AND D. C. TOSTESON, Biochemistry 14, 3962 (1975). J. PATEL, Biochemistry 12, 496 (1973). C. FEDARKO, J. Magn. Reson. 12, 30 (1973). H. HAYNES, B. C. PRESSMAN, AND A. KOWALSKY, Biochemistry 10, 852 (1971). G. DAVIS, Biochem. Biophys. Res. Commun. 63, 786 (1975). F. HINTON AND R. W. BRIGGS, J. Magn. Reson. 19, 393 (1975). RABER, G. BRUNGER, AND M. MEHRING, Chem. Phys. Lett. 23, 400 (1973).
12. IS.
D. H. HAYNES, A. KOWALSKY, D. J. PATEI. AND A. E. TONELLI,
14. 15.
D. D. M.
16. 17. D. 18. D. 19. J. 20.
H.
AND
J. F. HINTON K. R. METZ
F. S. Department of Chemistry (University of Arkansas Fayetteville, Arkansas 72701 Received January 20, 1981; revised March 16, 1981
MILLETT