Abstract
Exposure of cell membranes to an electromagnetic field (EMF) in the millimeter wave band (30–300 GHz) can produce a variety of responses. Further, many of the vibrational modes in complex biomolecules fall in the 1–100 GHz range. In addition to fundamental scientific interest, this may have applications in the development of diagnostic and therapeutic medical applications. In the present work, lipid vesicles of different size were used to study the effects of exposure to radiation at 52–72 GHz, with incident power densities (IPD) of 0.0035–0.010 mW/cm2, on the chemical-physical properties of cell membranes. Large unilamellar vesicles (LUVs) were used to study the effect of the radiation on the physical stability of vesicles by dynamic light scattering. An inhibition of the aging processes (Ostwald ripening), which usually occur in these vesicles because of their thermodynamic instability, resulted. Giant unilamellar vesicles (GUVs) were used to study the effect of the radiation on membrane water permeability under osmotic stress by phase contrast microscopy. In this case, a decrease in the water membrane permeability of the irradiated samples was observed. We advance the hypothesis that both the above effects may be explained in terms of a change of the polarization states of water induced by the radiation, which causes a partial dehydration of the membrane and consequently a greater packing density (increased membrane rigidity).
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References
Pakhomov, A.G., Akyel, Y., Pakhomova, O.N., Stuck, B.E., Murphy, M.R.: Current state and implications of research on biological effects of millimeter waves: a review of the literature. Bioelectromagnetics 19, 393–413 (1998)
Ramundo-Orlando, A.: Effects of millimeter waves radiation on cell membrane—a brief review. J. Infrared Milli. Terahz. Waves 31, 1400–1411 (2010)
Zhadobov, M., Chahat, N., Sauleau, R., Le Quement, C., Le Drean, Y.: Millimeter-wave interactions with the human body: state of knowledge and recent advances. Int. J. Microw. Wirel. Technol. 3, 237–247 (2011)
Pakhomov, A.G., Mathur, S.P., Doyle, J., Stuck, B.E., Kiel, J.L., Murphy, M.R.: Comparative effects of extremely high power microwave pulses and a brief CW irradiation on pacemaker function in isolated frog heart slices. Bioelectromagnetics 21, 245–54 (2000)
Rojavin, M.A., Radzievsky, A.A., Cowan, A., Ziskin, M.C.: Pain relief caused by millimeter waves in mice: results of cold water tail flick tests. Int. J. Radiat. Biol. 76, 575–579 (2000)
Radzievsky, A.A., Gordiienko, O.V., Szabo, I., Alekseev, S.I., Ziskin, M.C.: Millimeter wave-induced suppression of B16 F10 melanoma growth in mice: involvement of endogenous opioids. Bioelectromagnetics 25, 466–73 (2004)
Globus, T.R. Woolard, D.L., Khromova, T., Crowe, T.W., Bykhovskaia, M., Gelmont, B.L., Hesler, J., Samuels, A.C.: THz-spectroscopy of biological molecules. J. Biol. Phys. 29, 89–100 (2003)
Beneduci, A.: Which is the effective time scale of the fast Debye relaxation process in water? J. Mol. Liq. 138, 55–60 (2008)
Beneduci, A., Chidichimo, G.: Open-ended waveguide measurement and numerical simulation of the reflectivity of Petri dish supported skin cell monolayers in the mm-wave range. J. Infrared Milli. Terahz. Waves 33, 529–547 (2012)
Ellison, W.J.: Permittivity of pure water, at standard atmospheric pressure, over the frequency range 0.25 THz and the temperature range 0–100 °C. J. Phys. Chem. Ref. Data 36, 1–18 (2007)
Ronne, C., Keiding, S.R.: Low-frequency spectroscopy of liquid water using THz.time domain spectroscopy. J. Mol. Liq. 101, 199–218 (2002)
Jepsen, P.U., Merbold, H.: Terahertz reflection spectroscopy of aqueous NaCl and LiCl solutions. J. Infrared Milli. Terahz. Waves 31, 430–440 (2010)
Cifra, M., Fields, J.Z., Farhadi, A.: Electromagnetic cellular interactions. Prog. Biophys. Mol. Biol. 105, 223–246 (2011)
ICNIRP: Guidelines for limiting exposure to time varying electric, magnetic, and electromagnetic fields (up to 300 GHz). Health Phys. 74, 494–522 (1998)
IEEE: IEEE standard for safety levels with respect to human exposure to radio frequency electromagnetic fields, 3 kHz to 300 GHz. C95-1 (2005)
Zhadobov, M., Sauleau, R., Le Drean, Y., Alekseev, S.I., Ziskin, M.C.: Numerical and experimental millimeter-wave dosimetry for in vitro experiments. IEEE Trans. Microw. Theory Tech. 56, 2998–3007 (2008)
Ramundo-Orlando, A., Longo, G., Cappelli, M., Girasole, M., Tarricone, L., Beneduci, A., Massa, R.: The response of giant phospholipid vesicles to millimeter waves radiation. Biochim. Biophys. Acta 1788, 1497–1507 (2009)
Beneduci, A., Filippelli, L., Cosentino, K., Calabrese, M.L., Massa, R., Chidichimo, G.: Microwave-induced shift of the main phase transition in phosphatidylcholine membranes. Bioelectrochemistry 84, 18–24 (2012)
Armengol, X., Estelrich, J.: Physical stability of different liposome compositions obtained by extrusion method. J. Microencapsul. 12, 525–535 (1995)
Madani, E.W., Kaler, H.: Aging and stability of vesicular dispersions. Langmuir 6, 125–132 (1990)
Zhdanov, V.P., Kasemo, B.: Lipid-diffusion-limited kinetics of vesicle growth. Langmuir 16, 7352–7354 (2000)
Olsson, U., Wennerström, H.: On the ripening of vesicle dispersions. J. Phys. Chem. B 106, 5135–5138 (2002)
Oglęcka, K., Sanborn, J., Parikh A.N., Kraut R.S.: Osmotic gradients induce bio-reminiscent morphological transformations in giant unilamellar vesicles. Front Physiol. 3, 1–11 (2012)
Raphael, R., Waugh, R.: Accelerated interleaflet transport of phosphatidylcholine molecules in membranes under deformation. Biophys. J. 71, 1374–1388 (1996)
Dimova, R., Riske, K.A., Aranda, S., Bezlyepkina, N., Knorr, R.L., Lipowsky, R.: Giant vesicles in electric fields. Soft Matter 3, 817–827 (2007)
Dimova, R., Bezlyepkina, N., Jordo, M.D., Knorr, R.L., Riske, K.A., Staykova, M., Vlahovska, P.M., Yamamoto, T., Yang, P., Lipowsky, R.: Vesicles in electric fields: some novel aspects of membrane behavior. Soft Matter 5, 3201–3212 (2009)
Hope, M.J., Bally, M.B., Webb, G., Cullis, P.R.: Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta 812, 55–65 (1985)
Mayer, L.D., Hope, M.J., Cullis, P.R.: Vesicle of various sizes produced by a rapid extrusion procedure. Biochem. Biophys. Acta 858, 161–168 (1986)
Huster, D., Jin, A.J., Arnold, K., Gawrisch, K.: Water permeability of polyunsaturated lipid membranes measured by 17O NMR. Biophys. J. 73, 855–64 (1997)
MacDonald, R.C., et al.: Small-volume extrusion apparatus for preparation of large, unilamellar vesicles. Biochim. Biophys. Acta 1061, 297–303 (1991)
Angelova, M.I.: Liposome electroformation. In: Luisi, P.L., Walde, P. (eds.) Giant Vesicles. Perspectives in Supramolecular Chemistry, vol. 6, pp. 27–36. Wiley, Chichester (2000)
Bucher, P., Fischer, A., Luisi, P.L., Oberholzer, T., Walde, P.: Giant vesicles as biochemical compartments: the use of microinjection techniques. Langmuir 14, 2712–2721 (1998)
Lande, M.B., Donovan, J.M., Zeidel, M.L. The relationship between membrane fluidity and permeabilities to water, solutes, ammonia, and protons. J. Gen. Physiol. 106, 67–84 (1995)
Walde, P.: Preparation of vesicles (liposomes). In: Nalwa, H. S. (ed.) Encyclopedia of Nanoscience and Nanotechnology, vol. 9, pp. 43–79. American Scientific Publishers, Los Angeles (2004)
Cantor, R.S.: Lipid composition and the lateral pressure profile in bilayers. Biophys. J. 76, 2625–2639 (1999)
Zhadobov, M., et al.: Interactions between 60-GHz millimeter waves and artificial biological membranes: dependence on radiation parameters. Microw. Theory Tech. IEEE Trans. 54, 2534–2542 (2006)
Koenig, B.W., Strey, H.H., Gawrisch, K.: Membrane lateral compressibility determined by NMR and X-ray diffraction: effect of acyl chain polyunsaturation. Biophys. J. 73, 1954–1966 (1997)
Faure, C., Bonakdar, L., Dufourc, E.J.: Determination of DMPC hydration in the L(alpha) and L(beta’) phases by 2H solid state NMR of D2O. FEBS Lett. 405, 263–266 (1997)
Moazezi, Z., Hojjati, S.M.M., Ayrapetyan, S.: Low-intensity millimeter wave as a potential tool in treatment of diabetic sensorymotor polyneuropathy. Int. Dent. Med. Disord. 1, 50–55 (2008)
Alekseev, S.I., Ziskin, M.C.: Distortion of MMW absorption in biological media due to presence of thermocouples and other objects. IEEE Trans. Biomed. Eng. 48, 1013–1019 (2000)
Khizhnyak, E.P., Ziskin, M.C.: Temperature oscillations in liquid media caused by continuous (nonmodulated) millimeter wavelength electromagnetic irradiation. Bioelectromagnetics 17, 223–229 (1996)
Acknowledgements
K.C. would like to thank Prof. Peter Walde (ETH, Zurich) for very helpful discussions of the experiments and his support of this work. K.C. acknowledges the financial support from Regione Calabria and Università della Calabria, Italy.
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Cosentino, K., Beneduci, A., Ramundo-Orlando, A. et al. The influence of millimeter waves on the physical properties of large and giant unilamellar vesicles. J Biol Phys 39, 395–410 (2013). https://doi.org/10.1007/s10867-012-9296-2
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DOI: https://doi.org/10.1007/s10867-012-9296-2