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Nonviral Locally Injected Magnetic Vectors for in Vivo Gene Delivery: a Review of Studies on Magnetofection

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Nonviral Locally Injected Magnetic Vectors for in Vivo Gene Delivery: a Review of Studies on Magnetofection nanomaterials Review Nonviral Locally Injected Magnetic Vectors for In Vivo Gene Delivery: A Review of Studies on Magnetofection Artem A. Sizikov 1, Marianna V. Kharlamova 1 , Maxim P. Nikitin 1,2, Petr I. Nikitin 3,* and Eugene L. Kolychev 1,* 1 Moscow Institute of Physics and Technology, 141701 Dolgoprudny, Russia; [email protected] (A.A.S.); [email protected] (M.V.K.); [email protected] (M.P.N.) 2 Sirius University of Science and Technology, 354340 Sochi, Russia 3 Prokhorov General Physics Institute of the Russian Academy of Sciences, 117942 Moscow, Russia * Correspondence: [email protected] (P.I.N.); [email protected] (E.L.K.) Abstract: Magnetic nanoparticles have been widely used in nanobiomedicine for diagnostics and the treatment of diseases, and as carriers for various drugs. The unique magnetic properties of “magnetic” drugs allow their delivery in a targeted tumor or tissue upon application of a magnetic field. The approach of combining magnetic drug targeting and gene delivery is called magnetofection, and it is very promising. This method is simple and efficient for the delivery of genetic material to cells using magnetic nanoparticles controlled by an external magnetic field. However, magnetofection in vivo has been studied insufficiently both for local and systemic routes of magnetic vector injection, and the relevant data available in the literature are often merely descriptive and contradictory. In this review, we collected and systematized the data on the efficiency of the local injections of magnetic nanoparticles that carry genetic information upon application of external magnetic fields. We also Citation: Sizikov, A.A.; Kharlamova, investigated the efficiency of magnetofection in vivo, depending on the structure and coverage of M.V.; Nikitin, M.P.; Nikitin, P.I.; magnetic vectors. The perspectives of the development of the method were also considered. Kolychev, E.L. Nonviral Locally Injected Magnetic Vectors for In Vivo Keywords: magnetofection; magnetic nanoparticles; gene delivery Gene Delivery: A Review of Studies on Magnetofection. Nanomaterials 2021, 11, 1078. https://doi.org/ 10.3390/nano11051078 1. Introduction Magnetic nanoparticles (MNPs) have been extensively used for various in vitro ap- Academic Editor: Eleonore Fröhlich plications, and their unique abilities to respond to magnetic fields make them especially attractive for in vivo theranostics [1–6]. In vivo magnetofection, i.e., the delivery of genetic Received: 25 March 2021 material with magnetic particles controlled by an external magnetic field, is a promising Accepted: 19 April 2021 Published: 22 April 2021 approach to significantly boost the efficiency of gene therapy. In gene therapy, a disease or cellular neoplasm can be treated by delivering the genetic material to specific cells in order, Publisher’s Note: MDPI stays neutral for instance, to increase the expression of specific genes or to reduce the production of a with regard to jurisdictional claims in desired protein [7,8]. It is obvious that the direct delivery of nucleic acids to the targeted published maps and institutional affil- cells is the limiting factor of such a therapy [9–11]; therefore, the choice of a reliable and iations. effective viral or nonviral vector [12–14] for delivery is very important. Commonly used viral vectors based on adenoviruses, lentiviruses, and adeno-associated viruses [15–18] are excellent carriers, but they suffer from a number of serious disadvantages, such as immunogenicity and carcinogenicity [19,20]. Nonviral vectors are safer; they include poly- plexes based on cationic or neutral biodegradable polymers, lipoplexes (cationic liposomes Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. and niosomes), complexes of deoxyribonucleic acid (DNA) with dendrimers or peptides This article is an open access article by themselves [21,22], as well as combinations of all the above-mentioned vectors with distributed under the terms and magnetic particles [23,24]. In this case, magnetic particles themselves can be used for tumor conditions of the Creative Commons therapy, for the targeted drug delivery to a selected part of the body, or for the magnetic Attribution (CC BY) license (https:// separation of cells [25–28]. creativecommons.org/licenses/by/ As stated above, complexes based on magnetic particles and nucleic acids have multi- 4.0/). modal properties; therefore, in addition to the direct gene delivery using such complexes, Nanomaterials 2021, 11, 1078. https://doi.org/10.3390/nano11051078 https://www.mdpi.com/journal/nanomaterials Nanomaterials 2021, 11, x 2 of 18 Nanomaterials 2021, 11, 1078 2 of 17 As stated above, complexes based on magnetic particles and nucleic acids have multimodal properties; therefore, in addition to the direct gene delivery using such itcomplexes, is possible it to is carry possible out theto carry magnetically out the magnetically controlled accumulation controlled accumulation and release of and parti- re- cleslease [29 of– 31particles], particle [29 tracking–31], particle by magnetic trackingresonance by magnetic imaging resonance (MRI) imaging [32–36], (MRI) the imaging [32–36], ofthe tumors imaging [37 ,of38 tumors], and magnetic [37,38], and particle magnetic quantification particle quantification (MPQ) studies (MPQ) [32,39– studies41], as well [32,39 as– magnetofection41], as well as magnetofection [9,42,43]. The term [9,42,43] “magnetofection”. The term “magnetofection” refers to the use refers of a magnetic to the use field of a andmagnetic magnetic field particles and magnetic to improve particles the to efficiency improve of the gene efficiency delivery of [ 44gene–47 ].delivery The principle [44–47]. ofThe the principle method of is clear:the method the magnetic is clear: fieldthe magne promotestic field the promotes accumulation the accumulation and retention and of magneticretention particlesof magnetic in the particles area of in its the application area of its (a application schematic conception(a schematic of conception magnetofec- of tionmagnetofection is shown in Figureis shown1). Comparedin Figure 1). to Compared conventional to transfectionconventional based transfection on polymers based or on lipids,polymers magnetofection or lipids, magnetofection benefits from benefits a number from of obviousa number advantages, of obvious suchadvantages, as a higher such efficiencyas a higher and, efficiency consequently, and, consequently, a lower required a lower dose required of nucleic dose acid, of shorter nucleic delivery acid, shorter time, anddelivery the ability time, and to transfect the ability locally to transfect and in alocally limited and area in a [9 limited,48–50]. area As for[9,48 the–50] comparison. As for the ofcomparison advantages of andadvantages disadvantages and disadvantages of MNPs among of MNPs other among inorganic other nanoparticles inorganic nanopar- (gold nanoparticles,ticles (gold nanoparticles, silica nanoparticles, silica nanoparticles, quantum dots, quantum etc.) for indots, vivo etc.)gene for delivery, in vivo theregene arede- severallivery, comprehensivethere are several reviews comprehensive with detailed reviews tables with [8 ,detailed26,51]. tables [8,26,51]. FigureFigure 1. 1.Principle Principle ofof magnetofectionmagnetofection inin cellcell culture.culture. Polyelectrolyte-coatedPolyelectrolyte-coatedmagnetic magnetic nanoparticles nanoparticles areare mixedmixed withwith nakednaked nucleic acids acids or or synthetic synthetic or or viral viral nucleic nucleic acid acid vectors vectors in insalt salt containing containing a a buffer. The particles associate with the nucleic acids and vectors by electrostatic interaction and/or buffer. The particles associate with the nucleic acids and vectors by electrostatic interaction and/or salt-induced colloid aggregation. The mixtures are added to cells in culture. The cell culture plate is salt-induced colloid aggregation. The mixtures are added to cells in culture. The cell culture plate positioned on a magnetic plate during 5–30 min of incubation. The magnetic plate consists of 96 isindividual positioned neodymium on a magnetic–iron plate–boron during magnets 5–30 inserted min of in incubation. drill holes Thein an magnetic acrylic glass plate or consists PVC of 96(polyvinyl individual chloride) neodymium–iron–boron plate in a strictly alternating magnets inserted polarization. in drill The holes magnetic in an field acrylic rapidly glass sedi- or PVC (polyvinylments vectors chloride) on the plate cells in to a be strictly transfected/transduced. alternating polarization. The result The magnetic is rapid kinetics field rapidly and sediments vectorshigh-efficiency on the cells nucleic to be acid transfected/transduced. delivery. Adapted with The permission result is from rapid [52] kinetics. Copyright and high-efficiency Elsevier, 2005. nucleic acid delivery. Adapted with permission from [52]. Copyright Elsevier, 2005. All these properties are especially relevant when carrying out in vivo magnetofec- tion.All There these are properties a number are of especiallyreviews in relevant the literature when carryingthat are dedicated out in vivo tomagnetofection. various aspects Thereof the arenonviral a number delivery of reviews of genetic in theinformation, literature such that areas the dedicated properties to variousand characteristics aspects of theof vectors nonviral for delivery in vitro of magnetofection genetic information, [9,47,52 such–57] as, thethe propertiesmechanism and and characteristics
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