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Electromagnetic field (EMF) effects on channel activity of nanopore OmpF protein

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Abstract

In this study, the effects of nonionizing electromagnetic fields (EMF; 925 MHz) on the OmpF porin channel have been characterized at the single-channel level. Channel activity was recorded in real time by the voltage clamp method. Our results showed an increase in the frequency of channel gating and voltage sensitivity. The effects of EMF lasted for several milliseconds after the field source was terminated. However, the conductance levels of channels did not change significantly. Thermal effects of EMF on single-channel properties are a possible cause, based on theoretical evaluation of results that were comparable to those seen in conventional experiments at different temperatures. We conclude that EMF affects both the dynamics and conformation of the channel, either directly by affecting critical amino acid side-chain arrangement, or indirectly, via the electrolyte or the lipid membrane.

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References

  • Acar GO, Yener HM, Savrun FK, Kalkan T, Bayrak I, Enver O (2009) Thermal effects of mobile phones on facial nerves and surrounding soft tissue. Laryngoscope 119:559–562

    Google Scholar 

  • Adair R (2002) Vibrational resonances in biological systems at microwave frequencies. Biophys J 82:1147–1152

    Article  PubMed  CAS  Google Scholar 

  • Adair RK (2003) Biophysical limits on athermal effects of RF and microwave. Bioelectromagnetics 24:39–48

    Article  PubMed  Google Scholar 

  • Adey WR (1993) Biological effects of electromagnetic fields. J Cell Biochem 51:410–416

    PubMed  CAS  Google Scholar 

  • Barnes FS (2007) Biological effects of magnetic and electromagnetic fields. Springer, London

    Google Scholar 

  • Bohr H, Bohr J (2000) Microwave-enhanced folding and denaturation of globular proteins. Phys Rev E Sat Phys Plasmas Fluids Relat Interdiscip Topics 61(4):4310–4314

    CAS  Google Scholar 

  • Cain CA (2005) Biological effects of oscillating electric fields: roles of voltage sensitive ion channels. Bioelectromagnetics 2(1):23–32

    Article  Google Scholar 

  • Chiang H, Shao BJ (1989) The effects of microwaves on the immune system in mice. Electromagn Biol Med 8:1–10

    Article  Google Scholar 

  • d’Inzeo G, Bernardi P, Eusebi F, Grassi F, Tamburello C, Zani BM (1988) Microwave effects on acetylcholine-induced channels in cultured chick myotubes. Bioelectromagnetics 9(4):363–372

    Article  PubMed  Google Scholar 

  • de Pomerai D, Daniells C, David H, Allan J, Duce I, Mutwakil M, Thomas D, Sewell P, Tattersall J, Jones D, Candido P (2000) Non-thermal heat-shock response to microwaves. Nature 405:417–418

    Article  PubMed  Google Scholar 

  • de Pomerai DI, Smith B, Dawe A, North K, Smith T, Archer DB, Duce IR, Jones D, Candido EP (2003) Microwave radiation can alter protein conformation without bulk heating. FEBS Lett 22;543(1–3):93–97

    Google Scholar 

  • Dutta SK, Das K, Ghosh B, Blackman CF (1992) Dose dependence of acetylcholinesterase activity in neuroblastoma cells exposed to modulated radio-frequency electromagnetic radiation. Bioelectromagnetics 13:317–322

    Article  PubMed  CAS  Google Scholar 

  • Farmer LE, Oman H (1991) Effects of DC and AC electric and magnetic fields on people and animals. IEEE 6:26–29

    Google Scholar 

  • Foster KR (2000) Thermal and non thermal mechanisms of interaction of radio frequency energy with biological systems. IEEE Trans Plasma Sci 28:15–23

    Article  Google Scholar 

  • Foster KR, Glaser R (2007) Thermal mechanisms of interaction of radiofrequency energy with biological systems with relevance to exposure guidelines. Health Phys 92(6):609–620

    Article  PubMed  CAS  Google Scholar 

  • Gaber MH, Abd El Halim N, Khalil WA (2005) Effect of microwave radiation on the biophysical properties of liposomes. Bioelectromagnetics 26:194–200

    Article  PubMed  CAS  Google Scholar 

  • Galvanovskis J, Sandblom J (1997) Amplification of electromagnetic signals by ion channels. Biophy J 73:3056–3065

    Article  CAS  Google Scholar 

  • Gandhi CR, Ross DH (1989) Microwave induced stimulation of 32Pi-incorporation into phosphoinositides of rat brain synaptosomes. Radiat Environ Biophys 28:223–234

    Article  PubMed  CAS  Google Scholar 

  • Garavito RM, Rosenbusch JP (1986) Isolation and crystallization of bacterial porin. Methods Enzymol 125:309–328

    Article  PubMed  CAS  Google Scholar 

  • Goodman EM, B Greenebaum, Marron MT (1995) Effects of electromagnetic fields on molecules and cells. Int Rev Cytol 158:279–338

    Article  PubMed  CAS  Google Scholar 

  • Grigoriev PA, Pashovkin TV (2006) Molecular mechanisms of microwave interactions with model ion channels. J Biol Phys Chem 6(4):163–165

    Article  CAS  Google Scholar 

  • Hille B (1984) Ionic channels of excitable membranes. Sinauer, Sunderland

    Google Scholar 

  • Illinger KH (1981) Biological effects of nonionizing radiation. American Chemical Society Symposium Series no. 157. ACS, Washington DC

    Google Scholar 

  • Lakey JH, Pattus F (1989) The voltage-dependent activity of Escherichia coli porins in different planar bilayer reconstitutions. Eur J Biochem 186(30):3–308

    Google Scholar 

  • Liburdy RP (1992) The influence of oscillating electromagnetic fields on membrane structure and function. In: Norden B, Ramel C (eds) Interaction mechanisms of low-level electromagnetic fields in living systems. Oxford University Press, Oxford

    Google Scholar 

  • Lindstrom T, Oksendal B, Ubøe J, Zhang T (1995) Stability properties of stochastic partial differential equations. Stoch Anal Appl 13:177–204

    Article  Google Scholar 

  • Mancinelli F, Caraglia M, Abbruzzese A, d’Ambrosio G, Massa R, Bismuto E (2004) Non-thermal effects of electromagnetic fields at mobile phone frequency on the refolding of intracellular protein:myglobin. J Cell Biochem 93:188–196

    Article  PubMed  CAS  Google Scholar 

  • Montal M, Mueller P (1972) Formation of bimolecular membrane from lipid monolayers and a study of their electrical properties. Proc Natl Acad Sci USA 69(12):3561–3566

    Article  Google Scholar 

  • Munoz S, Sebastian JL, Sancho M, Miranda JM (2004) Transmembrane voltage induced on altered erythrocyte shapes exposed to RF fields. Bioelectromagnetics 25(8):631–633

    Article  PubMed  CAS  Google Scholar 

  • Nonner W, Eisenberg B (2000) Electrodiffusion in ionic channels of biological membranes. J Mol Liq 87:149–162

    Article  CAS  Google Scholar 

  • Norden B, Ramel C (1992) Interaction mechanisms of low-level electromagnetic fields in living systems. Oxford University Press, Oxford

    Google Scholar 

  • Porcelli M, Cacciapuoti GC, Fusco S, Massa R, d’Ambrosio G, Bertoldo C, De Rosa M, Zppia V (1997) Non-thermal effects of microwaves on proteins: thermophilic enzymes as model system. FEBS Lett 402:102–106

    Article  PubMed  CAS  Google Scholar 

  • Richard HW, Funk T, Monsees K (2006) Effects of electromagnetic fields on cells: physiological and therapeutical approaches and molecular mechanisms of interaction. Cells Tissues Organs 182:59–78

    Article  Google Scholar 

  • Sandblom J, Thenander S (1991) The effect of microwave radiation on the stability and formation of gramicidin-a channels in lipid bilayer membranes. Bioelectromagnetics 12:9–20

    Article  PubMed  CAS  Google Scholar 

  • Sharp KA, Honig B (1990) Electrostatic interactions in macromolecules: theory and applications. Annu Rev Biophys Biophys Chem 19:301–332

    Article  PubMed  CAS  Google Scholar 

  • Stavroulakis P (2003) Biological effects of electromagnetic fields. Springer, Berlin

    Google Scholar 

  • Tyazhelov VV, Alekseev SI, Grigor’ev PA (1978) Changes in the conductivity of alamethicin modified phospholipid membranes upon exposure to a high frequency electromagnetic field. Biofizika 23:732–733

    CAS  Google Scholar 

  • Weissenborn R, Diederichs K, Welte W, Mareta G, Gisler T (2005) Non-thermal microwave effects on protein dynamics? An X-ray diffraction study on tetragonal lysozyme crystals. Acta Crystallogr D 61:163–172

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors appreciate the assistance of Eng Saeed Farsi for designing the antenna and simulating the EMF in the Faraday cage and chamber. We would also like to thank Dr. Edward Lea, University of East Anglia, and Dr. Edwin Thrower, Yale University, for their critical revision of the manuscript. The financial support of the University of Tehran is greatly appreciated.

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Correspondence to H. Mobasheri.

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Mohammadzadeh, M., Mobasheri, H. & Arazm, F. Electromagnetic field (EMF) effects on channel activity of nanopore OmpF protein. Eur Biophys J 38, 1069–1078 (2009). https://doi.org/10.1007/s00249-009-0511-4

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  • DOI: https://doi.org/10.1007/s00249-009-0511-4

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