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The dynamics of magnetic nanoparticles exposed to non-heating alternating magnetic field in biochemical applications: theoretical study

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Abstract

In the past decade, magneto-nanomechanical approach to biochemical systems stimulation has been studied intensively. This method involves macromolecule structure local deformation via mechanical actuation of functionalized magnetic nanoparticles (f-MNPs) by non-heating low frequency (LF) alternating magnetic field (AMF). Specificity at cellular or molecular level and spatial locality in nanometer scale are its key advantages as compared to magnetic fluid hyperthermia. However, current experimental studies have weak theoretical basis. Several models of magneto-nanomechanical actuation of macromolecules and cells in non-heating uniform LF AMF are presented in the article. Single core-shell spherical, rod-like, and Janus MNPs, as well as dimers consisting of two f-MNPs with macromolecules immobilized on their surfaces are considered. AMF-induced rotational oscillations of MNPs can affect properties and functioning of macromolecules or cellular membranes attached to them via periodic deformations in nanometer scale. This could be widely used in therapy, in particular for targeted drug delivery, controlled drug release, and cancer cell killing. An aggregate composed of MNPs can affect associated macromolecules by force up to several hundreds of piconewton in the case of MNPs of tens of nanometers in diameter and LF AMF below 1 T. AMF parameters and MNP design requirements for effective in vitro and in vivo magneto-nanomechanical treatment are presented.

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Abbreviations

f-MNP:

Functionalized magnetic nanoparticle

LF:

Low frequency

AMF:

Alternating magnetic field

MRI:

Magnetic resonance imaging

RF MH:

Radiofrequency magnetic hyperthermia

MMA:

Magneto-mechanical actuation

MM:

Macromolecule

SAR:

Specific absorption rate

References

  • Ansari C, Tikhomirov GA, Hong SH, Falconer RA, Loadman PM, Gill JH, Castaneda R, Hazard FK, Tong L, Lenkov OD, Felsher DW, Rao J, Daldrup-Link HE (2014) Development of novel tumor-targeted theranostic nanoparticles activated by membrane-type matrix metalloproteinases for combined cancer magnetic resonance imaging and therapy. Small 10:566–575. doi:10.1002/smll.201301456

    Article  Google Scholar 

  • Arruebo M, Fernández-Pacheco R, Ibarra MR, Santamaría J (2007) Magnetic nanoparticles for drug delivery. Nano Today 2:22–32. doi:10.1016/S1748-0132(07)70084-1

    Article  Google Scholar 

  • Asin L, Ibarra MR, Tres A, Goya GF (2012) Controlled cell death by magnetic hyperthermia: effects of exposure time, field amplitude, and nanoparticle concentration. Pharm Res 29:1319–1327. doi:10.1007/s11095-012-0710-z

    Article  Google Scholar 

  • Betzer O, Ankri R, Motiei M, Popovtzer R (2015) Theranostic approach for cancer treatment: multifunctional gold nanorods for optical imaging and photothermal therapy. J Nanomater. doi:10.1155/2015/646713

    Google Scholar 

  • Blanco E, Shen H, Ferrari M (2015) Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol 33:941–951. doi:10.1038/nbt.3330

    Article  Google Scholar 

  • Buzug TM, Borgert J (2012) Magnetic particle imaging. A novel SPIO nanoparticle imaging technique. Springer-Verlag

  • Canfarotta F, Piletsky SA (2014) Engineered magnetic nanoparticles for biomedical applications. Advanced healthcare materials 3:160–175. doi:10.1002/adhm.201300141

    Article  Google Scholar 

  • Carrey J, Mehdaoui B, Respaud M (2011) Simple models for dynamic hysteresis loop calculations of magnetic single-domain nanoparticles: application to magnetic hyperthermia optimization. J Appl Phys 109:083921. doi:10.1063/1.3551582

    Article  Google Scholar 

  • Cho MH, Lee EJ, Son M, Lee JH, Yoo D, Kim J et al (2012) A magnetic switch for the control of cell death signalling in in vitro and in vivo systems. Nat Mater 11:1038–1043. doi:10.1038/nmat3430

    Article  Google Scholar 

  • Choi DS, Hopkins X, Kringel R, Park J, Jeon IT, Kim YK (2012) Magnetically driven spinning nanowires as effective materials for eradicating living cells. J Appl Phys 111:07B329. doi:10.1063/1.3678437

    Article  Google Scholar 

  • Cihoric N, Tsikkinis A, van Rhoon G, Crezee H, Aebersold DM, Bodis S et al (2015) Hyperthermia-related clinical trials on cancer treatment within the ClinicalTrials.gov registry. Int J Hyperther 31:609–614. doi:10.3109/02656736.2015.1040471

    Article  Google Scholar 

  • Contreras MF, Sougrat R, Zaher A, Ravasi T, Kosel J (2015) Non-chemotoxic induction of cancer cell death using magnetic nanowires. Int J Nanomedicine 10:2141. doi:10.2147/IJN.S77081

    Article  Google Scholar 

  • Creixell M, Bohorquez AC, Torres-Lugo M, Rinaldi C (2011) EGFR-targeted magnetic nanoparticle heaters kill cancer cells without a perceptible temperature rise. ACS Nano 5:7124–7129. doi:10.1021/nn201822b

    Article  Google Scholar 

  • de Vries AH, Krenn BE, van Driel R, Subramaniam V, Kanger JS (2007) Direct observation of nanomechanical properties of chromatin in living cells. Nano Lett 7:1424–1427. doi:10.1021/nl070603+

    Article  Google Scholar 

  • Deatsch AE, Evans BA (2014) Heating efficiency in magnetic nanoparticle hyperthermia. J Magn Magn Mater 354:163–172. doi:10.1016/j.jmmm.2013.11.006

    Article  Google Scholar 

  • Demeric U, Khademhosseini A, Langer R, Blander J (2013) Microfluidic Technologies for Human Health. World Scientific, Singapore

    Google Scholar 

  • Dobson J, Cartmell SH, Keramane A, El Haj AJ (2006) Principles and design of a novel magnetic force mechanical conditioning bioreactor for tissue engineering, stem cell conditioning, and dynamic in vitro screening. IEEE T Nanobiosci 5(3):173–177. doi:10.1109/tnb.2006.880823

    Article  Google Scholar 

  • Dobson J (2008) Remote control of cellular behaviour with magnetic nanoparticles. Nat Nanotechnol 3:139–143. doi:10.1038/nnano.2008.39

    Article  Google Scholar 

  • Dutz S, Hergt R (2013) Magnetic nanoparticle heating and heat transfer on a microscale: basic principles, realities and physical limitations of hyperthermia for tumour therapy. Int J Hyperther 29:790–800. doi:10.3109/02656736.2013.822993

    Article  Google Scholar 

  • Dutz S, Hergt R (2014) Magnetic particle hyperthermia—a promising tumour therapy? Nanotechnology 25:452001. doi:10.1088/0957-4484/25/45/452001

    Article  Google Scholar 

  • Gao N, Wang H, Yang EH (2010) An experimental study on ferromagnetic nickel nanowires functionalized with antibodies for cell separation. Nanotechnology 21:105107. doi:10.1088/0957-4484/21/10/105107

    Article  Google Scholar 

  • Garcia J, Tang T, Louie AY (2015) Nanoparticle-based multimodal PET/MRI probes. Nanomedicine 10:1343–1359. doi:10.2217/nnm.14.224

    Article  Google Scholar 

  • Gilchrist RK, Medal R, Shorey WD, Hanselman RC, Parrott JC, Taylor CB (1957) Selective inductive heating of lymph nodes. Ann Surg 146:596

    Article  Google Scholar 

  • Gleich B, Weizenecker J (2005) Tomographic imaging using the nonlinear response of magnetic particles. Nature 435:1114–1217. doi:10.1038/nature03808

    Article  Google Scholar 

  • Gleich B (2014) Principles and applications of magnetic particle imaging. Springer Vieweg

  • Golovin YI, Gribanovskii SL, Golovin DY, Klyachko NL, Kabanov AV (2014) Single-domain magnetic nanoparticles in an alternating magnetic field as mediators of local deformation of the surrounding macromolecules. Phys Solid State 56:1342–1351

    Article  Google Scholar 

  • Golovin YI, Gribanovsky SL, Golovin DY, Klyachko NL, Majouga AG, Master АM, Sokolsky M, Kabanov AV (2015) Towards nanomedicines of the future: remote magneto-mechanical actuation of nanomedicines by alternating magnetic fields. J Control Release 219:43–60. doi:10.1016/j.jconrel.2015.09.038

    Article  Google Scholar 

  • Golovin YI, Klyachko NL, Golovin DY, Efremova MV, Samodurov AA, Sokolski-Papkov M, Kabanov AV (2013a) A new approach to the control of biochemical reactions in a magnetic nanosuspension using a low-frequency magnetic field. Tech Phys Lett 39:240–243. doi:10.1134/s106378501303005x

    Article  Google Scholar 

  • Golovin YI, Klyachko NL, Sokolsky-Papkov M, Kabanov AV (2013b) Single-domain magnetic nanoparticles as force generators for the nanomechanical control of biochemical reactions by low-frequency magnetic fields. Bull Russ Acad Sci Phys 77(11):1350–1359. doi:10.3103/s1062873813110130

    Article  Google Scholar 

  • Guo Q, He Y, Lu HP (2015) Interrogating the activities of conformational deformed enzyme by single-molecule fluorescence-magnetic tweezers microscopy. Proceedings of the National Academy of Sciences 112:13904–13909. doi: 10.1073/pnas.1506405112

  • Golovin YI, Golovin DY, Klyachko NL, Majouga AG, Kabanov AV (2017) Modeling drug release from functionalized magnetic nanoparticles actuated by non-heating low frequency magnetic field. J Nanopart Res. doi:10.1007/s11051-017-3754-5

  • Hauser AK, Wydra RJ, Stocke NA, Anderson KW, Hilt JZ (2015) Magnetic nanoparticles and nanocomposites for remote controlled therapies. J Control Release 219:76–94. doi:10.1016/j.jconrel.2015.09.039

    Article  Google Scholar 

  • Hergt R, Dutz S, Müller R, Zeisberger M (2006) Magnetic particle hyperthermia: nanoparticle magnetism and materials development for cancer therapy. J Phys-Condens Mat 18:S2919. doi:10.1088/0953-8984/18/38/S26

    Article  Google Scholar 

  • Hou Y, Yu J, Chu X (2016) Design of magnetic nanoparticles for MRI-based theranostics. In: Advances in nanotheranostics II. Springer Singapore. pp. 3–37

  • Hu B, Dobson J, El Haj AJ (2014) Control of smooth muscle α-actin (SMA) up-regulation in HBMSCs using remote magnetic particle mechano-activation. Nanomedicine: Nanotechnology, Biology and Medicine 10:45–55. doi:10.1016/j.nano.2013.06.014

    Google Scholar 

  • Hu SH, Gao X (2010) Nanocomposites with spatially separated functionalities for combined imaging and magnetolytic therapy. J Am Chem Soc 132:7234–7237. doi:10.1021/ja102489q

    Article  Google Scholar 

  • Huang J, Zhong X, Wang L, Yang L, Mao H (2012) Improving the magnetic resonance imaging contrast and detection methods with engineered magnetic nanoparticles. Theranostics 2:86–102. doi:10.7150/thno.4006

    Article  Google Scholar 

  • Kamalapuram SK, Kanwar RK, Roy K, Chaudhary R, Sehgal R, Kanwar JR (2016) Theranostic multimodular potential of zinc-doped ferrite-saturated metal-binding protein-loaded novel nanocapsules in cancers. Int J Nanomedicine 11:1349–1366. doi:10.2147/IJN.S95253

    Google Scholar 

  • Kanczler JM, Sur HS, Magnay J, Green D, Oreffo RO, Dobson JP, El Haj AJ (2010) Controlled differentiation of human bone marrow stromal cells using magnetic nanoparticle technology. Tissue Eng Pt A 16:3241–3250. doi:10.1089/ten.tea.2009.0638

    Article  Google Scholar 

  • Kheirolomoom A, Lai CY, Tam SM, Mahakian LM, Ingham ES, Watson KD, Ferrara KW (2013) Complete regression of local cancer using temperature-sensitive liposomes combined with ultrasound-mediated hyperthermia. J Control Release 172:266–273. doi:10.1016/j.jconrel.2013.08.019

    Article  Google Scholar 

  • Kim DH, Rozhkova EA, Ulasov IV, Bader SD, Rajh T, Lesniak MS, Novosad V (2010) Biofunctionalized magnetic-vortex microdiscs for targeted cancer-cell destruction. Nat Mater 9:165–171. doi:10.1038/nmat2591

    Article  Google Scholar 

  • Klyachko NL, Sokolsky-Papkov M, Pothayee N, Efremova MV, Gulin DA, Pothayee N, Kuznetsov AA, Majouga AG, Riffle JS, Golovin YI, Kabanov AV (2012) Changing the enzyme reaction rate in magnetic nanosuspensions by a non-heating magnetic field. Angew Chem Int Edit 51:12016–12019. doi:10.1002/anie.201205905

    Article  Google Scholar 

  • Kraff O, Fischer A, Nagel AM, Mönninghoff C, Ladd ME (2015) MRI at 7 tesla and above: demonstrated and potential capabilities. J Magn Reson Imaging 41:13–33. doi:10.1002/jmri.24573

    Article  Google Scholar 

  • Kuda-Wedagedara AN, Allen MJ (2014) Enhancing magnetic resonance imaging with contrast agents for ultra-high field strengths. Analyst 139:4401–4410. doi:10.1039/C4AN00990H

    Article  Google Scholar 

  • Kumar CSS (2009) Magnetic nanomaterials. Wiley-VCH, Weinheim

    Google Scholar 

  • Lee N, Yoo D, Ling D, Cho MH, Hyeon T, Cheon J (2015) Iron oxide based nanoparticles for multimodal imaging and magnetoresponsive therapy. Chem Rev 115:10637–10689. doi:10.1021/acs.chemrev.5b00112

    Article  Google Scholar 

  • Lin WS, Lin HM, Chen HH, Hwu YK, Chiou YJ (2013) Shape effects of iron nanowires on hyperthermia treatment. J Nanomater. doi:10.1155/2013/237439

    Google Scholar 

  • Luo S, Wang LF, Ding WJ, Wang H, Zhou JM, Jin HK et al (2014) Clinical trials of magnetic induction hyperthermia for treatment of tumours. OA Cancer 2:2

    Google Scholar 

  • Majouga A, Sokolsky-Papkov M, Kuznetsov A, Lebedev D, Efremova M, Beloglazkina E, Rudakovskaya PG, Veselov M, Zyk N, Golovin YI, Klyachko NL, Kabanov AV (2015) Enzyme-functionalized gold-coated magnetite nanoparticles as novel hybrid nanomaterials: synthesis, purification and control of enzyme function by low-frequency magnetic field. Colloid Surface B 125:104–109. doi:10.1016/j.colsurfb.2014.11.012

    Article  Google Scholar 

  • Mehdaoui B, Meffre A, Carrey J, Lachaize S, Lacroix LM, Gougeon M et al (2011) Optimal size of nanoparticles for magnetic hyperthermia: a combined theoretical and experimental study. Adv Funct Mater 21:4573–4581. doi:10.1002/adfm.201101243

    Article  Google Scholar 

  • Mody VV, Cox A, Shah S, Singh A, Bevins W, Parihar H (2014) Magnetic nanoparticle drug delivery systems for targeting tumor. Appl Nanosci 4:385–392. doi:10.1007/s13204-013-0216-y

    Article  Google Scholar 

  • Mura S, Nicolas J, Couvreur P (2013) Stimuli-responsive nanocarriers for drug delivery. Nat Mater 12:991–1003. doi:10.1038/nmat3776

    Article  Google Scholar 

  • Nappini S, Bonini M, Bombelli FB, Pineider F, Sangregorio C, Baglioni P, Nordèn B (2011) Controlled drug release under a low frequency magnetic field: effect of the citrate coating on magnetoliposomes stability. Soft Matter 7:1025–1037. doi:10.1039/C0SM00789G

    Article  Google Scholar 

  • Noy A (2008) Handbook of molecular force spectroscopy. Springer, New York

    Book  Google Scholar 

  • Oberhauser AF (2013) Single-molecule studies of proteins. Springer, New York

    Book  Google Scholar 

  • Panagiotopoulos N, Duschka RL, Ahlborg M, Bringout G, Debbeler C, Graeser M, Kaethner C, Lüdtke-Buzug K, Medimagh H, Stelzner J, Buzug TM, Barkhausen J, Vogt FM, Haegele J (2015) Magnetic particle imaging: current developments and future directions. Int J Nanomedicine 2015:3097–3114. doi:10.2147/IJN.S70488

    Article  Google Scholar 

  • Pankhurst QA, Connolly J, Jones SK, Dobson JJ (2003) Applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys 36:R167. doi:10.1088/0022-3727/36/13/201

    Article  Google Scholar 

  • Puchner EM, Gaub HE (2012) Single-molecule mechanoenzymatics. Ann Rev Biophys 41:497–518. doi:10.1146/annurev-biophys-050511-102301

    Article  Google Scholar 

  • Reddy LH, Arias JL, Nicolas J, Couvreur P (2012) Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev 112:5818–5878. doi:10.1021/cr300068p

    Article  Google Scholar 

  • Reeves DB, Weaver JB (2014) Approaches for modeling magnetic nanoparticle dynamics. Crit Rev Biomed Eng 42(1):85–93

    Article  Google Scholar 

  • Rosensweig RE (2014) Ferrohydrodynamics. Dover Publications, Mineola, New York

    Google Scholar 

  • Shah RR, Davis TP, Glover AL, Nikles DE, Brazel CS (2015) Impact of magnetic field parameters and iron oxide nanoparticle properties on heat generation for use in magnetic hyperthermia. J Magn Magn Mater 387:96–106. doi:10.1016/j.jmmm.2015.03.085

    Article  Google Scholar 

  • Shin TH, Choi Y, Kim S, Cheon J (2015) Recent advances in magnetic nanoparticle-based multi-modal imaging. Chem Soc Rev 44:4501–4516. doi:10.1039/C4CS00345D

    Article  Google Scholar 

  • Singh A, Sahoo SK (2014) Magnetic nanoparticles: a novel platform for cancer theranostics. Drug Discov Today 19:474–481. doi:10.1016/j.drudis.2013.10.005

    Article  Google Scholar 

  • Suresh S (2007) Biomechanics and biophysics of cancer cells. Acta Biomater 55:3989–4014. doi:10.1016/j.actamat.2007.04.022

    Google Scholar 

  • Thanh NTK (2012) Magnetic nanoparticles. From fabrication to clinical application. CRC Press, Boca Raton

    Book  Google Scholar 

  • Valberg PA, Butler JP (1987) Magnetic particle motions within living cells. Physical theory and techniques. Biophys J 52:537. doi:10.1016/S0006-3495(87)83243-5

    Article  Google Scholar 

  • Walther A, Müller AHE (2013) Janus particles: synthesis, self-assembly, physical properties, and applications. Chem Rev 113:5194–5261. doi:10.1021/cr300089t

    Article  Google Scholar 

  • Ware MJ, Alexander JF, Summers HD, Godin B (2016) The importance of particle geometry in design of therapeutic and imaging nanovectors. In: Nanomedicine Springer New York. pp. 157–200

  • Wu W, Wu Z, Yu T, Jiang C, Kim WS (2016) Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mat 16:023501. doi:10.1088/1468-6996/16/2/023501

    Article  Google Scholar 

  • Yanagida T, Ishii Y (2009) Single molecule dynamics in life science. Wiley-VCH, Weinheim

    Google Scholar 

  • Zhang E, Kircher MF, Koch M, Eliasson L, Goldberg SN, Renström E (2014) Dynamic magnetic fields remote-control apoptosis via nanoparticle rotation. ACS Nano 8:3192–3201. doi:10.1021/nn406302j

    Article  Google Scholar 

  • Zhao Q, Wang L, Cheng R, Mao L, Arnold RD, Howerth EW, Chen ZG, Platt S (2012) Magnetic nanoparticle-based hyperthermia for head & neck cancer in mouse models. Theranostics 2:113–121. doi:10.7150/thno.3854

    Article  Google Scholar 

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Correspondence to Yuri I. Golovin.

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This work was supported by the Ministry of Education and Science of the Russian Federation (project no. K1-2014-022, development of the model) and Russian Science Foundation (project no. 14-13-00731, carrying out computer calculations).

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The authors declare that they have no conflict of interest.

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Based on the presentation at the 7th International Conference “Nanoparticles, Nanostructured coatings and microcontainers: technology, properties, applications.”

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Golovin, Y.I., Gribanovsky, S.L., Golovin, D.Y. et al. The dynamics of magnetic nanoparticles exposed to non-heating alternating magnetic field in biochemical applications: theoretical study. J Nanopart Res 19, 59 (2017). https://doi.org/10.1007/s11051-017-3753-6

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