1478
Langmuir 2000, 16, 1478-1480
Magnetoresponse in Electrical Properties of Black Lipid Membranes Sumio Ozeki,*,† Hutoshi Kurashima,† Mamiko Miyanaga,‡ and Chie Nozawa‡ Department of Chemistry, Faculty of Science, Shinshu University, 3-1-1 Asahi, Matsumoto, Nagano 390-8621, Japan, and Department of Chemistry, Faculty of Science, Chiba University, 1-33 Yayoi-cho, Inage-ku, Chiba 263-8522, Japan Received September 14, 1999. In Final Form: December 6, 1999 The membrane potential and resistance of black lipid membranes (BLM), comprising didodecyl phosphite or dipalmitoylphosphatidylcholine, markedly changed up to -50% and 4%, respectively, due to steady magnetic fields in the region of 0.2 T. The magnetic-field effects on the electrical properties seem to occur not via the Lorentz force on the ion flux but via the cooperative orientation of lipid molecules. Thus, the addition of molecules having different magnetic anisotropy to a BLM modified the magnetoresponses of the membrane. These examples demonstrate that relatively low magnetic fields may regulate the electrical properties of lipid membranes.
The effects of magnetic fields on living organisms have been investigated from many points of view, such as the structural changes of organisms,1-8 catalytic activities,9-11 and material transport.12,13 Biological cells contain many components and elementary processes for molecular syntheses, mass transport, and metabolism. Therefore, the results reported concerning the magnetic responses of such complex biological systems may often be obscure or contradictory. To elucidate the magnetic effects on biosystems, those on each elementary process should be examined. For this purpose, an artificial lipid bimolecular membrane, the so-called black lipid membrane (BLM), may be used as a model for biomembranes, although a thermodynamical BLM must be too simple. Here, we present the great effects of relatively low, steady magnetic fields (MF, 1010 Ω) were stored in a personal computer. BLM-forming solutions were prepared by mixing 20 ppm of DP or DPPC with (3 + 2) octane-dodecane. The general features in the magnetic response (∆f ≡ ∆fH - f0, where f is |Ψ| or R, and the subscripts 0 and H mean H ) 0 and H, respectively) are its reversibility, the maximum response (∆fmax) at around 0.2 T (H ) Hc), and the reverse response at H > 0.4 T, as shown in Figure 1. Ψ for DPPC membranes changed by ca. 2 mV, even at 0.025 T. The reproducibility of the trends in the magnetic response was fairly good (e.g., Figure 1B), besides some differences in their absolute values from run to run. The changing rate (100∆f/f0) in Ψ and R reached more than -50 and 4% (13 mV and 20 MΩ) at 0.2 T and 20 and -2% at 0.45 T. These magnetic responses seem to be notably large from the viewpoint that, for example, the magnetic field theoretically required to produce a 10% reduction in the conduction of a nerve impulse was roughly 24 T.16 We assume that MFs should modify the apparent fixed charge density (σ) of the membrane, besides how magnetic fields affect σ, e.g., a modification of the distribution of small ions around the headgroups and/or in the membrane and inherent charge-bearing ability of headgroups. To discuss qualitatively from the viewpoint of σ, a theory17 for a thick membrane was applied to our systems because, in our knowledge, no theory exists for a BLM. The features in the experimental magnetic responses of Ψ and R for DP membranes seem to be consistent with the theory (eqs 11 and 13 in ref 17): For σ (10-3 mol/dm3) ) 6.4 at H ) 0, 4.3 at H ) Hc, and 7.4 at H ) 0.45 T, Ψ (mV), R (MΩ) are estimated to be -20, 520; -10, 546; and -24, 503, respectively. The changing rates in Ψ and R from the estimated values are -50 and 5% at Hc and 20 and -1.9% at 0.45 T, respectively, which are consistent with the experimental rates of -50 and 4% at Hc and 20 and -2% at 0.45 T. Thus, the σ values may be used as a measure for an effective fixed charge density of the BLM. Figure 2A shows that the estimated σ changed with MF through a minimum (σmin) at around 0.2 T. When a magnetic field was parallel to the lipid membrane, i.e., perpendicular to the direction of ion flow, little magnetic effect was observed, suggesting that an ion flow would be not directly affected by the Lorentz force. Thus, the change in σ due to magnetic fields may be brought about by the molecular orientation, which leads to changes in the molecular density (area per molecule) at the membrane surface. Since the magnetic orientational energy of a diamagnetic lipid domain containing N molecules (volume Nv), whose long molecular axis is at an angle φ to H, is given by -(H2/2)(χ⊥ + ∆χ cos2 φ)Nv, lipid molecules in a domain may cooperatively align in the direction of the averaged φ according to the thermal energy.7 If H is large enough, the long molecular axis tends to align in a direction perpendicular to H (φ ) π/2) because of the negative diamagnetic anisotropy (∆χ ) ∆χ| - ∆χ⊥, where ∆χ| and ∆χ⊥ are the magnetic susceptibility parallel and perpendicular to H). Under 1 T and 298 K, significant orientational effects are expected when N is on the order of 107 for ∆χ ∼ -1 × 10-6 (for lipids), at which point the magnetic orientational energy is comparable to the thermal energy if other energies associated with orientational changes, such as a surface energy, an intermolecular interaction energy, and an elastic energy for (16) Wisco, J. P. Jr.; J. P. Barach, J. P. IEEE Trans. Biomed. Eng. 1980, BME-27, 722. (17) Ueda, T.; Kamo, N.; Ishida, N.; Kobatake, Y. J. Phys. Chem. 1972, 76, 2447.
Langmuir, Vol. 16, No. 4, 2000 1479
Figure 2. (A) Apparent fixed charge density σ of the BLM estimated from the Ψ values (Figure 1A) as a function of the magnetic field (H). σ changes with the magnetic field through a minimum (σmin) at Hc. (B) A possible model for the magnetic responses in the membrane potential and resistance is depicted schematically. Because the long axis of a lipid molecule tilts by an angle of φ to a magnetic field, the occupied molecular area at the membrane surface increases monotonically with φ, but the increase in the hydrocarbon/water interface leads to the critical tilt angle (φc) at Hc. A further increase in H induces a certain surface roughness to lead to an increase in σ.
membrane deformation, are neglected. It is possible that such a domain exists in a used BLM comprising 1012 molecules, as is known in insoluble monolayers.18 When a lipid molecule tilts under a MF, the occupied molecular area increases monotonically with φ, and thus σ would also decrease monotonically with MF. On the other hand, with increasing φ, the hydrocarbon/water interface at the membrane surface should increase and destabilize the tilted structure: The critical tilt angle (φc) must exist. Then, one possible way to increase σ or |Ψ| at higher MF than Hc would be to introduce membrane deformation in and out of a plain surface, which would lead to a reduction of the hydrocarbon/water interfacial energy and to relax the orientational defects (among domains having different orientation at φ), respectively. The former arises from a small displacement of the headgroups in the direction perpendicular to the surface, like a nematic liquid crystal; the latter, similar to the ripple structure, arises from undulation of a membrane due to high magnetic fields (probably larger than a few tesla, referring to the liposome case8). We found that DPPC liposomes, which were cooled from 318 to 303 K under a high magnetic field (11.7 T), showed a H NMR (500 MHz) pattern very similar to its ripple phase. From these considerations, a possible model for the magnetic responses under low magnetic fields is depicted schematically in Figure 2B. According to the model, a certain modification in the magnetic anisotropy of a membrane or domain would lead to changes in the magnetic responses of the electrical properties. The addition of cholesterol to a DP membrane (18) Kajiyama, T.; Zhang, L.; Uchida, M.; Oishi, Y.; Takahara, A. Langmuir 1993, 9, 760.
1480
Langmuir, Vol. 16, No. 4, 2000
Figure 3. Magnetoresponses in the membrane resistance of DP membranes containing cholesterol at 298 K. Cholesterol content (mol %): O, 0; 2, 25; 0,65.
shifted Hc to a lower MF along with an increase in the cholesterol content, as shown in Figure 3; on the other hand, undecyl calix arene (UCA) did not affect Hc. The large magnetic anisotropy of cholesterol assists the
Letters
magnetic orientation of DP molecules even under low magnetic fields; however, undecyl chains of UCA buried in a membrane (a headgroup having eight hydroxyl groups tend to be at the membrane surfaces) should have no influence on the magnetic orientation of the dodecyl chains of DP. Also, when aramethicin, a helical oligopeptide (∆χ > 0) which will align in parallel to a MF, was added to an aqueous phase of the cell during Ψ measurements, Ψ changed significantly only under a MF: ∆Ψ at 0.2 T was 20 times larger than that at no MF. These examples suggest that molecules having various magnetic anisotropies can regulate the magnetic response of the electrical processes in membrane systems. The great magnetic responses described here in the electrical properties are a remarkable example and seem to be the result of a cooperative molecular behavior. These results demonstrate that relatively low MFs might affect at least some elementary electrical processes in biosystems, such as synapse and receptor potentials having several tens of millivolts. Also, as is illustrated in the last examples, the magnetic regulation of the functions of artificial organized membranes, such as LB membranes, may be related to molecular devices and sensors. LA9912085
