Abstract
Superparamagnetic iron oxide nanoparticles are used in a rapidly expanding number of research and practical applications in biotechnology and biomedicine. Recent developments in iron oxide nanoparticle design and understanding of nanoparticle membrane interactions have led to applications in magnetically triggered, liposome delivery vehicles with controlled structure. Here we study the effect of external physical stimuli—such as millimeter wave radiation—on the induced movement of giant lipid vesicles in suspension containing or not containing iron oxide maghemite (γ-Fe2O3) nanoparticles (MNPs). To increase our understanding of this phenomenon, we used a new microscope image-based analysis to reveal millimeter wave (MMW)-induced effects on the movement of the vesicles. We found that in the lipid vesicles not containing MNPs, an exposure to MMW induced collective reorientation of vesicle motion occurring at the onset of MMW switch “on.” Instead, no marked changes in the movements of lipid vesicles containing MNPs were observed at the onset of first MMW switch on, but, importantly, by examining the course followed; once the vesicles are already irradiated, a directional motion of vesicles was induced. The latter vesicles were characterized by a planar motion, absence of gravitational effects, and having trajectories spanning a range of deflection angles narrower than vesicles not containing MNPs. An explanation for this observed delayed response could be attributed to the possible interaction of MNPs with components of lipid membrane that, influencing, e.g., phospholipids density and membrane stiffening, ultimately leads to change vesicle movement.
Similar content being viewed by others
References
Woodle MC, Newman MS, Cohen JA. Sterically stabilized liposomes: physical and biological properties. J Drug Target. 1994;2(5):397–403. https://doi.org/10.3109/10611869408996815.
Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science. 2004;303(5665):1818–22. https://doi.org/10.1126/science.1095833.
Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov. 2005;4(2):145–60. https://doi.org/10.1038/nrd1632.
Kagan D, Laocharoensuk R, Zimmerman M, Clawson C, Balasubramanian S, Kong D, et al. Rapid delivery of drug carriers propelled and navigated by catalytic nanoshuttles. Small. 2010;6(23):2741–7. https://doi.org/10.1002/smll.201001257.
MacDonald M, Spalding G, Dholakia K. Microfluidic sorting in an optical lattice. Nature. 2003;426(6965):421–4. https://doi.org/10.1038/nature02144.
Zhou R, Wang C. Acoustic bubble enhanced pinched flow fractionation for microparticle separation. J Micromech Microeng. 2015;25(8):084005. https://doi.org/10.1088/0960-1317/25/8/084005.
Baylis JR, Chan KY, Kastrup CJ. Halting hemorrhage with self-propelling particles and local drug delivery. Thromb Res. 2016;141(Suppl 2):S36–9.
Tabatabaei SN, Duchemin S, Girouard H, Martel S. Towards MR-navigable nanorobotic carriers for drug delivery into the brain. IEEE Int Conf Robot Autom. 2012;14:727–32.
Dimova R, Riske KA, Aranda S, Bezlyepkina N, Knorr RL, Lipowsky R. Giant vesicles in electric fields. Soft Matter. 2007;3(7):817–27.
Dimova R, Bezlyepkina N, Jordö MD, Knorr RL, Riske KA, Staykova M, et al. Vesicles in electric fields: some novel aspects of membrane behavior. Soft Matter. 2009;5(17):3201–12. https://doi.org/10.1039/b901963d.
Kolahdouz EM, Salac D. Dynamics of three-dimensional vesicles in dc electric fields. Phys Rev E. 2015;92(1):012302. https://doi.org/10.1103/PhysRevE.92.012302.
Salipante PF, Vlahovska PM. Vesicle deformation in DC electric pulses. Soft Matter. 2014;10:3386–93.
Salac D. Vesicles in magnetic fields. Soft Condensed Matter. 2016; arXiv:1608.05587v1.
Alavi M, Karimi N, Safaei M. Application of various types of liposomes in drug delivery systems. Adv Pharm Bull. 2017;7(1):3–9. https://doi.org/10.15171/apb.2017.002.
Bulbake U, Doppalapudi S, Kommineni N, Khan W. Liposomal formulations in clinical use: an updated review. Pharmaceutics. 2017;9(2) https://doi.org/10.3390/pharmaceutics9020012.
Dai M, Wu C, Fang HM, Li L, Yan JB, Zeng DL, et al. Thermo-responsive magnetic liposomes for hyperthermia-triggered local drug delivery. J Microencapsul. 2017;34(4):408–15. https://doi.org/10.1080/02652048.2017.1339738.
Jain A, Tiwari A, Verma A, Jain SK. Ultrasound-based triggered drug delivery to tumors. Drug Deliv Transl Res. 2018;8(1):150–64. https://doi.org/10.1007/s13346-017-0448-6.
Nappini S, Al Kayal T, Berti D, Nord Èn B, Baglioni P. Magnetically triggered release from giant unilamellar vesicles: visualization by means of confocal microscopy. J Phys Chem Lett. 2011;2(7):713–8. https://doi.org/10.1021/jz2000936.
Ramundo-Orlando A, Longo G, Cappelli M, Girasole M, Tarricone L, Beneduci A, et al. The response of giant phospholipid vesicles to millimeter waves radiation. Biochim Biophys Acta. 2009;1788(7):1497–507. https://doi.org/10.1016/j.bbamem.2009.04.006.
Rojavin MA, Ziskin MC. Medical application of millimetre waves. QJM. 1998;91(1):57–66.
Usichenko TI, Edinger H, Gizhko VV, Lehmann C, Wendt M, Feyerherd F. Low-intensity electromagnetic millimeter waves for pain therapy. Evidence-based complementary and alternative medicine. eCAM. 2006;3(2):201–7. https://doi.org/10.1093/ecam/nel012.
Partyla T, Hacker H, Edinger H, Leutzow B, Lange J, Usichenko T. Remote effects of electromagnetic millimeter waves on experimentally induced cold pain: a double-blinded crossover investigation in healthy volunteers. Anesth Analg. 2017;124(3):980–5. https://doi.org/10.1213/ANE.0000000000001657.
Vecchia P, Matthes R, Ziegelberger G, Lin J, Saunders R, Swerdlow A. Exposure to high frequency electromagnetic fields, biological effects and health consequences (100 kHz-300 GHz). International Commission on Non-Ionizing Radiation Protection; 2009.
Ramundo-Orlando A. Effects of millimeter waves radiation on cell membrane—a brief review. J Infrared Millimeter Terahertz Waves. 2010;31(12):1400–11. https://doi.org/10.1007/s10762-010-9731-z.
Albini M, Dinarelli S, Pennella F, Romeo S, Zampetti E, Girasole M, et al. Induced movements of giant vesicles by millimeter wave radiation. Biochim Biophys Acta. 2014;1838(7):1710–8. https://doi.org/10.1016/j.bbamem.2014.03.021.
Angelakeris M. Magnetic nanoparticles: a multifunctional vehicle for modern theranostics. Biochim Biophys Acta. 2017;1861(6):1642–51. https://doi.org/10.1016/j.bbagen.2017.02.022.
Estelrich J, Escribano E, Queralt J, Busquets MA. Iron oxide nanoparticles for magnetically-guided and magnetically-responsive drug delivery. Int J Mol Sci. 2015;16(4):8070–101. https://doi.org/10.3390/ijms16048070.
Shirmardi Shaghasemi B, Virk MM, Reimhult E. Optimization of magneto-thermally controlled release kinetics by tuning of magnetoliposome composition and structure. Sci Rep. 2017;7(1):7474. https://doi.org/10.1038/s41598-017-06980-9.
Preiss MR, Bothun GD. Stimuli-responsive liposome-nanoparticle assemblies. Expert Opin Drug Deliv. 2011;8(8):1025–40. https://doi.org/10.1517/17425247.2011.584868.
Kuster N, Schonborn F. Recommended minimal requirements and development guidelines for exposure setups of bio-experiments addressing the health risk concern of wireless communications. Bioelectromagnetics. 2000;21(7):508–14.
Pautot S, Frisken BJ, Weitz DA. Production of unilamellar vesicles using an inverted emulsion. Langmuir. 2003;19(7):2870–9. https://doi.org/10.1021/la026100v.
Carrara P, Stano P, Luisi PL. Giant vesicles “colonies”: a model for primitive cell communities. Chembiochem. 2012;13(10):1497–502. https://doi.org/10.1002/cbic.201200133.
Saywell LG, Cunningham BB. Determination of Iron: colorimetric o-phenanthroline method. Ind Eng Chem Anal Ed. 1937;9(2):67–9. https://doi.org/10.1021/ac50106a005.
Zhao JX. Numerical dosimetry for cells under millimetre-wave irradiation using Petri dish exposure set-ups. Phys Med Biol. 2005;50(14):3405–21. https://doi.org/10.1088/0031-9155/50/14/015.
Mally M, Majhenc J, Svetina S, Zeks B. The response of giant phospholipid vesicles to pore-forming peptide melittin. Biochim Biophys Acta. 2007;1768(5):1179–89. https://doi.org/10.1016/j.bbamem.2007.02.015.
Riske KA, Dimova R. Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophys J. 2005;88(2):1143–55. https://doi.org/10.1529/biophysj.104.050310.
Hough PVC. Method and means for recognizing complex pattern. US Patent No3069654. 1962.
Chiba M, Miyazaki M, Ishiwata S. Quantitative analysis of the lamellarity of giant liposomes prepared by the inverted emulsion method. Biophys J. 2014;107(2):346–54. https://doi.org/10.1016/j.bpj.2014.05.039.
Bonnaud C, Monnier CA, Demurtas D, Jud C, Vanhecke D, Montet X, et al. Insertion of nanoparticle clusters into vesicle bilayers. ACS Nano. 2014;8(4):3451–60. https://doi.org/10.1021/nn406349z.
Giardini PA, Fletcher DA, Theriot JA. Compression forces generated by actin comet tails on lipid vesicles. Proc Natl Acad Sci U S A. 2003;100(11):6493–8. https://doi.org/10.1073/pnas.1031670100.
Husen P, Fidorra M, Hartel S, Bagatolli LA, Ipsen JH. A method for analysis of lipid vesicle domain structure from confocal image data. Eur Biophys J. 2012;41(2):161–75. https://doi.org/10.1007/s00249-011-0768-2.
Rey Suarez I, Leidy C, Tellez G, Gay G, Gonzalez-Mancera A. Slow sedimentation and deformability of charged lipid vesicles. PLoS One. 2013;8(7):e68309. https://doi.org/10.1371/journal.pone.0068309.
Pasenkiewicz-Gierula M, Baczynski K, Markiewicz M, Murzyn K. Computer modelling studies of the bilayer/water interface. Biochim Biophys Acta. 2016;1858(10):2305–21. https://doi.org/10.1016/j.bbamem.2016.01.024.
Chukova YP. Doubts about nonthermal effects of MM radiation have no scientific foundations. J Phys Conf Ser. 2011;329(1) https://doi.org/10.1088/1742-6596/329/1/012032.
Beneduci A, Bernstein E. Review on the mechanisms of interaction between millimeter waves and biological systems. Bioelectrochem Res Dev. 2008:35–80.
Chukova YP. Reasons of poor replicability of nonthermal bioeffects by millimeter waves. Bioelectrochem Bioenerg. 1999;48(2):349–53.
Vlahovska PM, Gracia RS, Aranda-Espinoza S, Dimova R. Electrohydrodynamic model of vesicle deformation in alternating electric fields. Biophys J. 2009;96(12):4789–803. https://doi.org/10.1016/j.bpj.2009.03.054.
Seiwert J, Vlahovska PM. Instability of a fluctuating membrane driven by an ac electric field. Phys Rev E Stat Nonlinear Soft Matter Phys. 2013;87(2):022713. https://doi.org/10.1103/PhysRevE.87.022713.
Monnier CA, Burnand D, Rothen-Rutishauser B, Lattuada M, Petri-Fink A. Magnetoliposomes: opportunities and challenges. Eur J Nanomed. 2014;6(4):201–15. https://doi.org/10.1515/ejnm-2014-0042.
Schulz M, Olubummo A, Binder WH. Beyond the lipid-bilayer: interaction of polymers and nanoparticles with membranes. Soft Matter. 2012;8(18):4849–64. https://doi.org/10.1039/c2sm06999g.
Man D, Olchawa R. Dynamics of surface of lipid membranes: theoretical considerations and the ESR experiment. Eur Biophys J. 2017;46(4):325–34. https://doi.org/10.1007/s00249-016-1172-8.
Darros-Barbosa R, Balaban MO, Teixeira AA. Temperature and concentration dependence of heat capacity of model aqueous solutions. Int J Food Prop. 2003;6(2):239–58. https://doi.org/10.1081/JFP-120017845.
Keblinski P, Cahill DG, Bodapati A, Sullivan CR, Taton TA. Limits of localized heating by electromagnetically excited nanoparticles. J Appl Phys. 2006;100(5) https://doi.org/10.1063/1.2335783.
Khizhnyak EP, Ziskin MC. Temperature oscillations in liquid media caused by continuous (nonmodulated) millimeter wavelength electromagnetic irradiation. Bioelectromagnetics. 1996;17(3):223–9. https://doi.org/10.1002/(SICI)1521-186X(1996)17:3<223::AID-BEM8>3.0.CO;2-5.
Schuderer J, Samaras T, Oesch W, Spät D, Kuster N. High peak SAR exposure unit with tight exposure and environmental control for in vitro experiments at 1800 MHz. IEEE Trans Microwave Theory Tech. 2004;52(8 II):2057–66. https://doi.org/10.1109/TMTT.2004.832009.
Zhao J. In vitro dosimetry and temperature evaluations of a typical millimeter-wave aperture-field exposure setup. IEEE Trans Microwave Theory Tech. 2012;60(11):3608–22. https://doi.org/10.1109/TMTT.2012.2213829.
IEEE standard for safety levels with respect to human exposure to radio frequency electromagnetic fields, 3 kHz to 300 GHz. IEEE Standard for Safety Levels with Respect to Human Exposure to Radio Frequency Electromagnetic Fields, 3 KHz to 300 GHz. 1992.
Fannin P, Relihan T, Charles S. Experimental and theoretical profiles of the frequency-dependent complex susceptibility of systems containing nanometer-sized magnetic particles. Phys Rev B Condens Matter Mater Phys. 1997;55(21):14423–8. https://doi.org/10.1103/PhysRevB.55.14423.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(PDF 239 kb)
Rights and permissions
About this article
Cite this article
Albini, M., Salvi, M., Altamura, E. et al. Movement of giant lipid vesicles induced by millimeter wave radiation change when they contain magnetic nanoparticles. Drug Deliv. and Transl. Res. 9, 131–143 (2019). https://doi.org/10.1007/s13346-018-0572-y
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13346-018-0572-y