Advanced cell therapies: Targeting, tracking and actuation of cells with magnetic particles

Regenerative Medicine

Volumn 10, Issue 6, 2015, Pages 757-772

  Connell, John J ^a   Patrick, P Stephen ^a   Yu, Yichao ^a   Lythgoe, Mark F ^a   Kalber, Tammy L ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

cell tracking; magnetic actuation; magnetic targeting; MRI; regenerative medicine; SPION

Indexed keywords

FERUCARBOTRAN; FERUMOXYTOL; IRON OXIDE; MAGNETIC NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; CALCIUM; CALCIUM CHANNEL; DEXTRAN; FERRIC ION; FERRIC OXIDE; GLUCOSE BLOOD LEVEL; GREEN FLUORESCENT PROTEIN; INSULIN; MAGNETITE NANOPARTICLE; METAL NANOPARTICLE;

AMYOTROPHIC LATERAL SCLEROSIS; CELL LABELING; CELL MIGRATION; CELL THERAPY; CELL TRACKING; CELLULAR DISTRIBUTION; CONTRAST ENHANCEMENT; DENDRITIC CELL; GENE THERAPY; GENETIC TRANSFECTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; MAGNET; MAGNETIC FIELD; MECHANOTRANSDUCTION; MESENCHYMAL STEM CELL TRANSPLANTATION; MULTIPLE SCLEROSIS; NEURAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SPINAL CORD INJURY; THERMAL STIMULATION; TOXICITY TESTING; ANIMAL; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; GLUCOSE BLOOD LEVEL; MAGNETISM; MOUSE; PROCEDURES; REPRODUCIBILITY; STEM CELL; TRANSGENE; TRENDS;

ANIMALS; BLOOD GLUCOSE; CALCIUM; CALCIUM CHANNELS; DEXTRANS; FERRIC COMPOUNDS; GREEN FLUORESCENT PROTEINS; HUMANS; INSULIN; MAGNETIC RESONANCE IMAGING; MAGNETICS; MAGNETITE NANOPARTICLES; METAL NANOPARTICLES; MICE; MICROSCOPY, CONFOCAL; REGENERATIVE MEDICINE; REPRODUCIBILITY OF RESULTS; STEM CELLS; TRANSGENES;

EID: 84946743212     PISSN: 17460751     EISSN: 1746076X     Source Type: Journal    
DOI: 10.2217/rme.15.36     Document Type: Review

References (112)

1. Fischbach MA, Bluestone JA, Lim WA. Cell-based therapeutics: the next pillar of medicine. Sci. Transl. Med. 5(179), 179ps177 (2013).
2. Heathman TR, Nienow AW, Mccall MJ, Coopman K, Kara B, Hewitt CJ. The translation of cell-based therapies: clinical landscape and manufacturing challenges. Regen. Med. 10(1), 49-64 (2015).
3. Consigny PM, Silverberg DA, Vitali NJ. Use of endothelial cells containing superparamagnetic microspheres to improve endothelial cell delivery to arterial surfaces after angioplasty. J. Vasc. Interv. Radiol. 10(2 Pt 1), 155-163 (1999).
4. Arbab AS, Jordan EK, Wilson LB, Yocum GT, Lewis BK, Frank JA. In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum. Gene Ther. 15(4), 351-360 (2004).
5. Riegler J, Wells JA, Kyrtatos PG, Price AN, Pankhurst QA, Lythgoe MF. Targeted magnetic delivery and tracking of cells using a magnetic resonance imaging system. Biomaterials 31(20), 5366-5371 (2010).
6. Riegler J, Liew A, Hynes SO et al. Superparamagnetic iron oxide nanoparticle targeting of MSCs in vascular injury. Biomaterials 34(8), 1987-1994 (2013).
7. Riegler J, Allain B, Cook RJ, Lythgoe MF, Pankhurst QA. Magnetically assisted delivery of cells using a magnetic resonance imaging system. J. Phys. D Appl. Phys. 44(5), 055001 (2011).
8. Kyrtatos PG, Lehtolainen P, Junemann-Ramirez M et al. Magnetic tagging increases delivery of circulating progenitors in vascular injury. JACC Cardiovasc. Interv. 2(8), 794-802 (2009).
9. Sasaki H, Tanaka N, Nakanishi K et al. Therapeutic effects with magnetic targeting of bone marrow stromal cells in a rat spinal cord injury model. Spine 36(12), 933-938 (2011).
10. Cheng K, Malliaras K, Li TS et al. Magnetic enhancement of cell retention, engraftment, and functional benefit after intracoronary delivery of cardiac-derived stem cells in a rat model of ischemia/reperfusion. Cell Transplant. 21(6), 1121-1135 (2012).
11. Song M, Kim YJ, Kim YH, Roh J, Kim SU, Yoon BW. Using a neodymium magnet to target delivery of ferumoxide-labeled human neural stem cells in a rat model of focal cerebral ischemia. Hum. Gene Ther. 21(5), 603-610 (2010).
12. Yanai A, Hafeli UO, Metcalfe AL et al. Focused magnetic stem cell targeting to the retina using superparamagnetic iron oxide nanoparticles. Cell Transplant. 21(6), 1137-1148 (2012).
13. Cheng K, Li TS, Malliaras K, Davis DR, Zhang Y, Marban E. Magnetic targeting enhances engraftment and functional benefit of iron-labeled cardiosphere-derived cells in myocardial infarction. Circ. Res. 106(10), 1570-1581 (2010).
14. Vandergriff AC, Hensley TM, Henry ET et al. Magnetic targeting of cardiosphere-derived stem cells with ferumoxytol nanoparticles for treating rats with myocardial infarction. Biomaterials 35(30), 8528-8539 (2014).
15. Oshima S, Kamei N, Nakasa T, Yasunaga Y, Ochi M. Enhancement of muscle repair using human mesenchymal stem cells with a magnetic targeting system in a subchronic muscle injury model. J. Orthop. Sci. 19(3), 478-488 (2014).
16. Kobayashi T, Ochi M, Yanada S et al. Augmentation of degenerated human cartilage in vitro using magnetically labeled mesenchymal stem cells and an external magnetic device. Arthroscopy 25(12), 1435-1441 (2009).
17. Hofmann A, Wenzel D, Becher UM et al. Combined targeting of lentiviral vectors and positioning of transduced cells by magnetic nanoparticles. Proc. Natl Acad. Sci. USA 106(1), 44-49 (2009).
18. Bulte JW, Duncan ID, Frank JA. In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J. Cereb. Blood Flow Metab. 22(8), 899-907 (2002).
19. Frank JA, Zywicke H, Jordan EK et al. Magnetic intracellular labeling of mammalian cells by combining (FDA-approved) superparamagnetic iron oxide MR contrast agents and commonly used transfection agents. Acad. Radiol. 9(Suppl. 2), S484-S487 (2002).
20. Yeh TC, Zhang W, Ildstad ST, Ho C. In vivo dynamic MRI tracking of rat T-cells labeled with superparamagnetic ironoxide particles. Magn. Reson. Med. 33(2), 200-208 (1995).
21. Huang Z, Shen Y, Sun A et al. Magnetic targeting enhances retrograde cell retention in a rat model of myocardial infarction. Stem Cell Res. Ther. 4(6), 149 (2013).
22. Cheng K, Shen D, Hensley MT et al. Magnetic antibodylinked nanomatchmakers for therapeutic cell targeting. Nat. Commun. 5, 4880 (2014).
23. Huang Z, Shen Y, Pei N et al. The effect of nonuniform magnetic targeting of intracoronary-delivering mesenchymal stem cells on coronary embolisation. Biomaterials 34(38), 9905-9916 (2013).
24. Thorek DL, Tsourkas A. Size, charge and concentration dependent uptake of iron oxide particles by non-phagocytic cells. Biomaterials 29(26), 3583-3590 (2008).
25. Kolosnjaj-Tabi J, Wilhelm C, Clement O, Gazeau F. Cell labeling with magnetic nanoparticles: opportunity for magnetic cell imaging and cell manipulation. J. Nanobiotechnology 11(Suppl. 1), S7 (2013).
26. Foged C, Brodin B, Frokjaer S, Sundblad A. Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model. Int. J. Pharm. 298(2), 315-322 (2005).
27. Zauner W, Farrow NA, Haines AM. In vitro uptake of polystyrene microspheres: effect of particle size, cell line and cell density. J. Control. Release 71(1), 39-51 (2001).
28. Pislaru SV, Harbuzariu A, Gulati R et al. Magnetically targeted endothelial cell localization in stented vessels. J. Am. Coll. Cardiol. 48(9), 1839-1845 (2006).
29. Gupta AK, Gupta M. Cytotoxicity suppression and cellular uptake enhancement of surface modified magnetic nanoparticles. Biomaterials 26(13), 1565-1573 (2005).
30. Lewinski N, Colvin V, Drezek R. Cytotoxicity of nanoparticles. Small 4(1), 26-49 (2008).
31. Ordidge KL, Gregori M, Kalber TL, Lythgoe MF, Janes SM, Giangreco A. Coupled cellular therapy and magnetic targeting for airway regeneration. Biochem. Soc. Trans. 42(3), 657-661 (2014).
32. Voinov MA, Sosa Pagan JO, Morrison E, Smirnova TI, Smirnov AI. Surface-mediated production of hydroxyl radicals as a mechanism of iron oxide nanoparticle biotoxicity. J. Am. Chem. Soc. 133(1), 35-41 (2011).
33. Imlay JA, Chin SM, Linn S. Toxic DNA damage by hydrogen peroxide through the fenton reaction in vivo and in vitro. Science 240(4852), 640-642 (1988).
34. Petri-Fink A, Chastellain M, Juillerat-Jeanneret L, Ferrari A, Hofmann H. Development of functionalized superparamagnetic iron oxide nanoparticles for interaction with human cancer cells. Biomaterials 26(15), 2685-2694 (2005).
35. Tengood JE, Alferiev IS, Zhang K, Fishbein I, Levy RJ, Chorny M. Real-time analysis of composite magnetic nanoparticle disassembly in vascular cells and biomimetic media. Proc. Natl Acad. Sci. USA 111(11), 4245-4250 (2014).
36. Schafer R, Ayturan M, Bantleon R et al. The use of clinically approved small particles of iron oxide (SPIO) for labeling of mesenchymal stem cells aggravates clinical symptoms in experimental autoimmune encephalomyelitis and influences their in vivo distribution. Cell Transplant. 17(8), 923-941 (2008).
37. Loebinger MR, Kyrtatos PG, Turmaine M et al. Magnetic resonance imaging of mesenchymal stem cells homing to pulmonary metastases using biocompatible magnetic nanoparticles. Cancer Res. 69(23), 8862-8867 (2009).
38. Bulte JW. In vivo MRI cell tracking: clinical studies. AJR Am. J. Roentgenol. 193(2), 314-325 (2009).
39. Richards JM, Shaw CA, Lang NN et al. In vivo mononuclear cell tracking using superparamagnetic particles of iron oxide: feasibility and safety in humans. Circ. Cardiovasc. Imaging 5(4), 509-517 (2012).
40. Nishida K, Tanaka N, Nakanishi K et al. Magnetic targeting of bone marrow stromal cells into spinal cord: through cerebrospinal fluid. Neuroreport 17(12), 1269-1272 (2006).
41. Kodama A, Kamei N, Kamei G et al. In vivo bioluminescence imaging of transplanted bone marrow mesenchymal stromal cells using a magnetic delivery system in a rat fracture model. J. Bone Joint Surg. Br. 94(7), 998-1006 (2012).
42. Shen Y, Liu X, Huang Z et al. Comparison of magnetic intensities for mesenchymal stem cell targeting therapy on ischemic myocardial repair: high magnetic intensity improves cell retention but has no additional functional benefit. Cell Transplant. doi:10. 3727/096368914X685302 (2014) (Epub ahead of print).
43. Chaudeurge A, Wilhelm C, Chen-Tournoux A et al. Can magnetic targeting of magnetically labeled circulating cells optimize intramyocardial cell retention? Cell Transplant. 21(4), 679-691 (2012).
44. Wilhelm C, Bal L, Smirnov P et al. Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28(26), 3797-3806 (2007).
45. Polyak B, Fishbein I, Chorny M et al. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc. Natl Acad. Sci. USA 105(2), 698-703 (2008).
46. Vanecek V, Zablotskii V, Forostyak S et al. Highly efficient magnetic targeting of mesenchymal stem cells in spinal cord injury. Int. J. Nanomedicine 7, 3719-3730 (2012).
47. Kang HJ, Kim JY, Lee HJ et al. Magnetic bionanoparticle enhances homing of endothelial progenitor cells in mouse hindlimb ischemia. Korean Circ. J. 42(6), 390-396 (2012).
48. Cheng L, Wang C, Ma X et al. Multifunctional upconversion nanoparticles for dual-modal imaging-guided stem cell therapy under remote magnetic control. Adv. Funct. Mater. 23(3), 272-280 (2013).
49. Landazuri N, Tong S, Suo J et al. Magnetic targeting of human mesenchymal stem cells with internalized superparamagnetic iron oxide nanoparticles. Small 9(23), 4017-4026 (2013).
50. Carenza E, Barcelo V, Morancho A et al. In vitro angiogenic performance and in vivo brain targeting of magnetized endothelial progenitor cells for neurorepair therapies. Nanomedicine 10(1), 225-234 (2014).
51. Tran LA, M. H-R, Berlin AN et al. The use of gadoliniumcarbon nanostructures to magnetically enhance stem cell retention for cellular cardiomyoplasty. Biomaterials 35(2), 720-726 (2014).
52. Kobayashi T, Ochi M, Yanada S et al. A novel cell delivery system using magnetically labeled mesenchymal stem cells and an external magnetic device for clinical cartilage repair. Arthroscopy 24(1), 69-76 (2008).
53. Riegler J, Lau KD, Garcia-Prieto A et al. Magnetic cell delivery for peripheral arterial disease: a theoretical framework. Med. Phys. 38(7), 3932-3943 (2011).
54. Tateishi-Yuyama E, Matsubara H, Murohara T et al. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial. Lancet 360(9331), 427-435 (2002).
55. Prochazka V, Gumulec J, Jaluvka F et al. Cell therapy, a new standard in management of chronic critical limb ischemia and foot ulcer. Cell Transplant. 19(11), 1413-1424 (2010).
56. Wei X, Yang X, Han ZP, Qu FF, Shao L, Shi YF. Mesenchymal stem cells: a new trend for cell therapy. Acta Pharmacol. Sin. 34(6), 747-754 (2013).
57. Bulte JW, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed. 17(7), 484-499 (2004).
58. Vuu K, Xie J, Mcdonald MA et al. Gadolinium-rhodamine nanoparticles for cell labeling and tracking via magnetic resonance and optical imaging. Bioconjug. Chem. 16(4), 995-999 (2005).
59. Crich SG, Biancone L, Cantaluppi V et al. Improved route for the visualization of stem cells labeled with a Gd-/Euchelate as dual (MRI and fluorescence) agent. Magn. Reson. Med. 51(5), 938-944 (2004).
60. Rudelius M, Daldrup-Link HE, Heinzmann U et al. Highly efficient paramagnetic labelling of embryonic and neuronal stem cells. Eur. J. Nucl. Med. Mol. Imaging 30(7), 1038-1044 (2003).
61. Modo M, Cash D, Mellodew K et al. Tracking transplanted stem cell migration using bifunctional, contrast agentenhanced, magnetic resonance imaging. Neuroimage 17(2), 803-811 (2002).
62. Ahrens ET, Helfer BM, O'hanlon CF, Schirda C. Clinical cell therapy imaging using a perfluorocarbon tracer and fluorine-19 MRI. Magn. Reson. Med. 72(6), 1696-1701 (2014).
63. De Vries IJ, Lesterhuis WJ, Barentsz JO et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat. Biotechnol. 23(11), 1407-1413 (2005).
64. Franklin RJ, Blaschuk KL, Bearchell MC et al. Magnetic resonance imaging of transplanted oligodendrocyte precursors in the rat brain. Neuroreport 10(18), 3961-3965 (1999).
65. Cromer Berman SM, Walczak P, Bulte JW. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 3(4), 343-355 (2011).
66. Zhu J, Zhou L, Xingwu F. Tracking neural stem cells in patients with brain trauma. N. Engl. J. Med. 355(22), 2376-2378 (2006).
67. Karussis D, Karageorgiou C, Vaknin-Dembinsky A et al. Safety and immunological effects of mesenchymal stem cell transplant in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch. Neurol. 67(10), 1187-1194 (2010).
68. Callera F, De Melo CM. Magnetic resonance tracking of magnetically labeled autologous bone marrow CD34+ cells transplanted into the spinal cord via lumbar puncture technique in patients with chronic spinal cord injury: CD34+ cells' migration into the injured site. Stem Cells Dev. 16(3), 461-466 (2007).
69. Cunningham CH, Arai T, Yang PC, Mcconnell MV, Pauly JM, Conolly SM. Positive contrast magnetic resonance imaging of cells labeled with magnetic nanoparticles. Magn. Reson. Med. 53(5), 999-1005 (2005).
70. Robson MD, Gatehouse PD, Bydder M, Bydder GM. Magnetic resonance: an introduction to ultrashort TE (UTE) imaging. J. Comput. Assist. Tomogr. 27(6), 825-846 (2003).
71. Crowe LA, Ris F, Nielles-Vallespin S et al. A novel method for quantitative monitoring of transplanted islets of langerhans by positive contrast magnetic resonance imaging. Am. J. Transplant. 11(6), 1158-1168 (2011).
72. Li L, Jiang W, Luo K et al. Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking. Theranostics 3(8), 595-615 (2013).
73. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP. MRI detection of single particles for cellular imaging. Proc. Natl Acad. Sci. USA 101(30), 10901-10906 (2004).
74. Pawelczyk E, Arbab AS, Chaudhry A, Balakumaran A, Robey PG, Frank JA. In vitro model of bromodeoxyuridine or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: implications for cellular therapy. Stem Cells 26(5), 1366-1375 (2008).
75. Serganova I, Ponomarev V, Blasberg R. Human reporter genes: potential use in clinical studies. Nucl. Med. Biol. 34(7), 791-807 (2007).
76. Patrick PS, Hammersley J, Loizou L et al. Dual-modality gene reporter for in vivo imaging. Proc. Natl Acad. Sci. USA 111(1), 415-420 (2014).
77. Yaghoubi SS, Jensen MC, Satyamurthy N et al. Noninvasive detection of therapeutic cytolytic T cells with 18F-FHBG PET in a patient with glioma. Nat. Clin. Pract. Oncol. 6(1), 53-58 (2009).
78. Kircher MF, Gambhir SS, Grimm J. Noninvasive celltracking methods. Nat. Rev. Clin. Oncol. 8(11), 677-688 (2011).
79. Ingber DE. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20(7), 811-827 (2006).
80. Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10(1), 75-82 (2009).
81. Na S, Collin O, Chowdhury F et al. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl Acad. Sci. USA 105(18), 6626-6631 (2008).
82. Trappmann B, Gautrot JE, Connelly JT et al. Extracellularmatrix tethering regulates stem-cell fate. Nat. Mater. 11(7), 642-649 (2012).
83. Huebsch N, Arany PR, Mao AS et al. Harnessing tractionmediated manipulation of the cell/matrix interface to control stem-cell fate. Nat. Mater. 9(6), 518-526 (2010).
84. Hughes S, El Haj AJ, Dobson J. Magnetic micro-and nanoparticle mediated activation of mechanosensitive ion channels. Med. Eng. Phys. 27(9), 754-762 (2005).
85. Kasten A, Muller P, Bulnheim U et al. Mechanical integrin stress and magnetic forces induce biological responses in mesenchymal stem cells which depend on environmental factors. J. Cell. Biochem. 111(6), 1586-1597 (2010).
86. Muller P, Langenbach A, Kaminski A, Rychly J. Modulating the actin cytoskeleton affects mechanically induced signal transduction and differentiation in mesenchymal stem cells. PLoS ONE 8(7), e71283 (2013).
87. Yan YX, Gong YW, Guo Y et al. Mechanical strain regulates osteoblast proliferation through integrin-mediated erk activation. PLoS ONE 7(4), e35709 (2012).
88. Panseri S, Cunha C, D'alessandro T et al. Intrinsically superparamagnetic FE-hydroxyapatite nanoparticles positively influence osteoblast-like cell behaviour. J. Nanobiotechnology 10, 32 (2012).
89. Glogauer M, Ferrier J, Mcculloch CA. Magnetic fields applied to collagen-coated ferric oxide beads induce stretchactivated CA2+ flux in fibroblasts. Am. J. Physiol. 269(5 Pt 1), C1093-C1104 (1995).
90. Glogauer M, Ferrier J. A new method for application of force to cells via ferric oxide beads. Pflugers Arch. 435(2), 320-327 (1998).
91. Kanczler JM, Sura HS, Magnay J et al. Controlled differentiation of human bone marrow stromal cells using magnetic nanoparticle technology. Tissue Eng. Part A 16(10), 3241-3250 (2010).
92. Henstock JR, Rotherham M, Rashidi H, Shakesheff KM, El Haj AJ. Remotely activated mechanotransduction via magnetic nanoparticles promotes mineralization synergistically with bone morphogenetic protein 2: applications for injectable cell therapy. Stem Cells Transl. Med. 3(11), 1363-1374 (2014).
93. Hu B, Dobson J, El Haj AJ. Control of smooth muscle-actin (SMA) up-regulation in HBMSCs using remote magnetic particle mechano-activation. Nanomedicine 10(1), 45-55 (2014).
94. Stanley SA, Sauer J, Kane RS, Dordick JS, Friedman JM. Remote regulation of glucose homeostasis in mice using genetically encoded nanoparticles. Nat. Med. 21(1), 92-98 (2015).
95. Huang H, Delikanli S, Zeng H, Ferkey DM, Pralle A. Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. Nat. Nanotechnol. 5(8), 602-606 (2010).
96. Totonelli G, Maghsoudlou P, Garriboli M et al. A rat decellularized small bowel scaffold that preserves villus-crypt architecture for intestinal regeneration. Biomaterials 33(12), 3401-3410 (2012).
97. Hu C, Uchida T, Tercero C et al. Development of biodegradable scaffolds based on magnetically guided assembly of magnetic sugar particles. J. Biotechnol. 159(1-2), 90-98 (2012).
98. Perea H, Aigner J, Hopfner U, Wintermantel E. Direct magnetic tubular cell seeding: a novel approach for vascular tissue engineering. Cells Tissues Organs 183(3), 156-165 (2006).
99. Ishii M, Shibata R, Numaguchi Y et al. Enhanced angiogenesis by transplantation of mesenchymal stem cell sheet created by a novel magnetic tissue engineering method. Arterioscler. Thromb. Vasc. Biol. 31(10), 2210-2215 (2011).
100. Souza GR, Molina JR, Raphael RM et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol. 5(4), 291-296 (2010).
101. Gonzalez-Molina J, Riegler J, Southern P et al. Rapid magnetic cell delivery for large tubular bioengineered constructs. J. R. Soc. Interface 9(76), 3008-3016 (2012).
102. Corchero JL, Villaverde A. Biomedical applications of distally controlled magnetic nanoparticles. Trends Biotechnol. 27(8), 468-476 (2009).
103. Cartier N, Hacein-Bey-Abina S, Bartholomae CC et al. Hematopoietic stem cell gene therapy with a lentiviral vector in X-linked adrenoleukodystrophy. Science 326(5954), 818-823 (2009).
104. Aiuti A, Cattaneo F, Galimberti S et al. Gene therapy for immunodeficiency due to adenosine deaminase deficiency. N. Engl. J. Med. 360(5), 447-458 (2009).
105. Hanna J, Wernig M, Markoulaki S et al. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318(5858), 1920-1923 (2007).
106. Jooss K, Chirmule N. Immunity to adenovirus and adenoassociated viral vectors: implications for gene therapy. Gene Ther. 10(11), 955-963 (2003).
107. Bessis N, Garciacozar FJ, Boissier MC. Immune responses to gene therapy vectors: influence on vector function and effector mechanisms. Gene Ther. 11(Suppl. 1), S10-S17 (2004).
108. Mah C, Fraites TJ, Jr., Zolotukhin I et al. Improved method of recombinant AAV2 delivery for systemic targeted gene therapy. Mol. Ther. 6(1), 106-112 (2002).
109. Scherer F, Anton M, Schillinger U et al. Magnetofection: enhancing and targeting gene delivery by magnetic force in vitro and in vivo. Gene Ther. 9(2), 102-109 (2002).
110. Mcbain SC, Yiu HH, Dobson J. Magnetic nanoparticles for gene and drug delivery. Int. J. Nanomedicine 3(2), 169-180 (2008).
111. Pickard M, Chari D. Enhancement of magnetic nanoparticle-mediated gene transfer to astrocytes by 'magnetofection': effects of static and oscillating fields. Nanomedicine 5(2), 217-232 (2010).
112. Fouriki A, Dobson J. Oscillating magnet array-based nanomagnetic gene transfection of human mesenchymal stem cells. Nanomedicine 9(7), 989-997 (2014).