Magnetic nanoparticle-based approaches to locally target therapy and enhance tissue regeneration in vivo

Nanomedicine

Volumn 7, Issue 9, 2012, Pages 1425-1442

  Sensenig, Richard ^a   Sapir, Yulia ^b   MacDonald, Cristin ^c   Cohen, Smadar ^b   Polyak, Boris ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c DREXEL UNIVERSITY   (United States)

Author keywords

cell therapy; drug delivery; forced transport; magnetic cell seeding; magnetic cell stimulation; magnetic targeting; patterned cell assemblies; superparamagnetic nanoparticles; time varied magnetic field; tissue engineering

Indexed keywords

MAGNETIC NANOPARTICLE; TISSUE SCAFFOLD;

CELL STIMULATION; DRUG PENETRATION; DRUG TARGETING; IN VIVO STUDY; MAGNETIC FIELD; MEDICAL TECHNOLOGY; PRIORITY JOURNAL; REVIEW; TISSUE REGENERATION;

ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; MAGNETICS; MAGNETITE NANOPARTICLES; NANOMEDICINE; REGENERATIVE MEDICINE; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84866640090     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.12.109     Document Type: Review

References (133)

1. Colombo M, Carregal-Romero S, Casula MF et al. Biological applications of magnetic nanoparticles. Chem. Soc. Rev. 41(11), 4306-4334 (2012).
2. Krishnan KM. Biomedical nanomagnetics: a spin through possibilities in imaging, diagnostics, and therapy. IEEE Trans. Magn. 46(7), 2523-2558 (2010).
3. Laurent S, Dutz S, Hafeli UO, Mahmoudi M. Magnetic fluid hyperthermia: focus on superparamagnetic iron oxide nanoparticles. Adv. Colloid Interface Sci. 166(1-2), 8-23 (2011).
4. Laurent S, Forge D, Port M et al. Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem. Rev. 108(6), 2064-2110 (2008).
5. Mahmoudi M, Sant S, Wang B, Laurent S, Sen T. Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. Adv. Drug Deliv. Rev. 63(1-2), 24-46 (2011).
6. Pankhurst QA, Thanh NTK, Jones SK, Dobson J. Progress in applications of magnetic nanoparticles in biomedicine. J. Phys. D. Appl. Phys. 42, 224001 (2009).
7. Polyak B, Friedman G. Magnetic targeting for site-specific drug delivery: applications and clinical potential. Expert Opin. Drug Deliv. 6(1), 53-70 (2009).
8. Wankhede M, Bouras A, Kaluzova M, Hadjipanayis CG. Magnetic nanoparticles: an emerging technology for malignant brain tumor imaging and therapy. Expert Rev. Clin. Pharm. 5(2), 173-186 (2012).
9. Alexiou C, Schmid RJ, Jurgons R et al. Targeting cancer cells: magnetic nanoparticles as drug carriers. Eur. Biophys. J. 35(5), 446-450 (2006).
10. Lubbe AS, Alexiou C, Bergemann C. Clinical applications of magnetic drug targeting. J. Surg. Res. 95(2), 200-206 (2001).
11. Chorny M, Fishbein I, Yellen BB et al. Targeting stents with local delivery of paclitaxel-loaded magnetic nanoparticles using uniform fields. Proc. Natl Acad. Sci. USA 107(18), 8346-8351 (2010).
12. Pislaru SV, Harbuzariu A, Agarwal G et al. Magnetic forces enable rapid endothelialization of synthetic vascular grafts. Circulation 114(Suppl. 1), I314-I318 (2006).
13. 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).
14. 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).
15. Yellen BB, Forbes ZG, Halverson DS et al. Targeted drug delivery to magnetic implants for therapeutic applications. J. Magn. Magn. Mater. 293(1), 647-654 (2005).
16. Mccall AA, Swan EE, Borenstein JT, Sewell WF, Kujawa SG, Mckenna MJ. Drug delivery for treatment of inner ear disease: current state of knowledge. Ear Hearing 31(2), 156-165 (2010).
17. Goycoolea MV, Lundman L. Round window membrane. Structure function and permeability: a review. Microsc. Res. Tech. 36(3), 201-211 (1997).
18. Gao X, Wang Y, Chen K, Grady BP, Dormer KJ, Kopke RD. Magnetic assisted transport of PLGA nanoparticles through a human round window membrane model. J. Nanotechnol. Eng. Med. 1(3), 031010-031016 (2010).
19. Mondalek Fadee G, Zhang Yuan Y, Kropp B et al. The permeability of SPION over an artificial three-layer membrane is enhanced by external magnetic field. J. Nanobiotechnol. 4, 4 (2006).
20. Dormer KJ, Awasthi V, Galbraith W, Kopke RD, Chen K, Wassel R. Magnetically-targeted, technetium 99m-labeled nanoparticles to the inner ear. J. Biomed. Nanotechnol. 4(2), 174-184 (2008).
21. Chakeres DW, De Vocht F. Static magnetic field effects on human subjects related to magnetic resonance imaging systems. Prog. Biophys. Mol. Biol. 87(2-3), 255-265 (2005).
22. Schenck JF. Physical interactions of static magnetic fields with living tissues. Prog. Biophys. Mol. Biol. 87(2-3), 185-204 (2005).
23. Shapiro B, Dormer K, Rutel IB. A two-magnet system to push therapeutic nanoparticles. AIP Conf. Proc. 1311(1), 77-88 (2010).
24. Brightman M. Ultrastructure of brain endothelium. In: Physiology and Pharmacology of the Blood-Brain Barrier. Bradbury MWB (Ed.). Springer-Verlag, Berlin, Germany, 1-22 (1992).
25. Lo EH, Singhal AB, Torchilin VP, Abbott NJ. Drug delivery to damaged brain. Brain Res. Brain Res. Rev. 38(1-2), 140-148 (2001).
26. Garcia-Garcia E, Andrieux K, Gil S, Couvreur P. Colloidal carriers and blood-brain barrier (BBB) translocation: a way to deliver drugs to the brain? Int. J. Pharm. 298(2), 274-292 (2005).
27. Schlageter KE, Molnar P, Lapin GD, Groothuis DR. Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties. Microvasc. Res. 58(3), 312-328 (1999).
28. Vajkoczy P, Menger MD. Vascular microenvironment in gliomas. Cancer Treat. Res. 117, 249-262 (2004).
29. Hassan EE, Gallo JM. Targeting anticancer drugs to the brain. I: Enhanced brain delivery of oxantrazole following administration in magnetic cationic microspheres. J. Drug Target. 1(1), 7-14 (1993).
30. Pulfer SK, Gallo JM. Enhanced brain tumor selectivity of cationic magnetic polysaccharide microspheres. J. Drug Target. 6(3), 215-227 (1998).
31. Pulfer SK, Ciccotto SL, Gallo JM. Distribution of small magnetic particles in brain tumor-bearing rats. J. Neurooncol. 41(2), 99-105 (1999).
32. Chertok B, David AE, Huang Y, Yang VC. Glioma selectivity of magnetically targeted nanoparticles: a role of abnormal tumor hydrodynamics. J. Control. Release 122(3), 315-323 (2007).
33. Chertok B, Moffat BA, David AE et al. Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors. Biomaterials 29(4), 487-496 (2008).
34. Chorny M, Fishbein I, Forbes S, Alferiev I. Magnetic nanoparticles for targeted vascular delivery. IUBMB Life 63(8), 613-620 (2011).
35. Roiron C, Sanchez P, Bouzamondo A, Lechat P, Montalescot G. Drug eluting stents: an updated meta-analysis of randomised controlled trials. Heart 92(5), 641-649 (2006).
36. Gulati R, Jevremovic D, Witt TA et al. Modulation of the vascular response to injury by autologous blood-derived outgrowth endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 287(2), H512-H517 (2004).
37. 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).
38. 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).
39. 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).
40. Barnes AL, Wassel RA, Mondalek F, Che K, Dormer KJ, Kopke RD. Magnetic characterization of superparamagnetic nanoparticles pulled through model membranes. BioMag. Res. Technol. 5(1), 1-10 (2007).
41. Kalambur VS, Han B, Hammer BE, Shield TW, Bischof JC. In vitro characterization of movement, heating and visualization of magnetic nanoparticles for biomedical applications. Nanotechnology 16, 1221-1233 (2005).
42. Kuhn SJ, Hallahan DE, Giorgio TD. Characterization of superparamagnetic nanoparticle interactions with extracellular matrix in an in vitro system. Ann. Biomed. Eng. 34(1), 51-58 (2006).
43. Kuhn SJ, Finch SK, Hallahan DE, Giorgio TD. Proteolytic surface functionalization enhances in vitro magnetic nanoparticle mobility through extracellular matrix. Nano Lett. 6(2), 306-312 (2006).
44. Mondalek FG, Zhang YY, Kropp B et al. The permeability of SPION over an artificial three-layer membrane is enhanced by external magnetic field. J. Nanobiotechnol. 4(4), 1-9 (2006).
45. Rotariu O, Udrea LE, Strachan NJC, Badescu V. The guidance of magnetic colloids in simulated tissues for targeted drug delivery. J. Optoelect. Adv. Mat. 9(4), 942-945 (2007).
46. Crick FHC, Hughes AFW. The physical properties of cytoplasm: a study by means of the magnetic particle method. Exp. Cell. Res. 1, 37-80 (1950).
47. Dobson J. Remote control of cellular behaviour with magnetic nanoparticles. Nat. Nanotechnol. 3(3), 139-143 (2008).
48. Macdonald C, Friedman G, Alamia J, Barbee K, Polyak B. Time-varied magnetic field enhances transport of magnetic nanoparticles in viscous gel. Nanomedicine (Lond.) 5(1), 65-76 (2010).
49. Guillotin B, Guillemot F. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 29(4), 183-190 (2011).
50. Sachlos E, Czernuszka JT. Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. Eur. Cell. Mater. 5, 29-39; discussion 39-40 (2003).
51. Ikada Y. Challenges in tissue engineering. J. R. Soc. Interface 3(10), 589-601 (2006).
52. Howard D, Buttery LD, Shakesheff KM, Roberts SJ. Tissue engineering: strategies, stem cells and scaffolds. J. Anat. 213(1), 66-72 (2008).
53. Lee K, Silva EA, Mooney DJ. Growth factor delivery-based tissue engineering: general approaches and a review of recent developments. J. R. Soc. Interface 8(55), 153-170 (2011).
54. Patel ZS, Young S, Tabata Y, Jansen JA, Wong MEK, Mikos AG. Dual delivery of an angiogenic and an osteogenic growth factor for bone regeneration in a critical size defect model. Bone 43(5), 931-940 (2008).
55. Perets A, Baruch Y, Weisbuch F, Shoshany G, Neufeld G, Cohen S. Enhancing the vascularization of three-dimensional porous alginate scaffolds by incorporating controlled release basic fibroblast growth factor microspheres. J. Biomed. Mat. Res. Part A 65(4), 489-497 (2003).
56. Tayalia P, Mooney DJ. Controlled growth factor delivery for tissue engineering. Adv. Mater. 21(32-33), 3269-3285 (2009).
57. Wei GB, Jin QM, Giannobile WV, Ma PX. Nano-fibrous scaffold for controlled delivery of recombinant human PDGF-BB. J. Control. Release 112(1), 103-110 (2006).
58. Kempen DHR, Lu LC, Heijink A et al. Effect of local sequential VEGF and BMP-2 delivery on ectopic and orthotopic bone regeneration. Biomaterials 30(14), 2816-2825 (2009).
59. Freeman I, Cohen S. The influence of the sequential delivery of angiogenic factors from affinity-binding alginate scaffolds on vascularization. Biomaterials 30(11), 2122-2131 (2009).
60. Freeman I, Kedem A, Cohen S. The effect of sulfation of alginate hydrogels on the specific binding and controlled release of heparin-binding proteins. Biomaterials 29(22), 3260-3268 (2008).
61. Zhang SF, Uludag H. Nanoparticulate systems for growth factor delivery. Pharm. Res. 26(7), 1561-1580 (2009).
62. Bock N, Riminucci A, Dionigi C et al. A novel route in bone tissue engineering: magnetic biomimetic scaffolds. Acta Biomater. 6(3), 786-796 (2010).
63. Hu SH, Liu TY, Tsai CH, Chen SY. Preparation and characterization of magnetic ferroscaffolds for tissue engineering. J. Magn. Magn. Mater. 310(2), 2871-2873 (2007).
64. Zhao XH, Kim J, Cezar CA et al. Active scaffolds for on-demand drug and cell delivery. Proc. Natl Acad. Sci. USA 108(1), 67-72 (2011).
65. Timko BP, Dvir T, Kohane DS. Remotely triggerable drug delivery systems. Adv. Mat. 22(44), 4925-4943 (2010).
66. Ward MA, Georgiou TK. Thermoresponsive polymers for biomedical applications. Polymers 3(3), 1215-1242 (2011).
67. Hiergeist R, Andra W, Buske N et al. Application of magnetite ferrofluids for hyperthermia. J. Magn. Magn. Mater. 201, 420-422 (1999).
68. Mornet S, Vasseur S, Grasset F et al. Magnetic nanoparticle design for medical applications. Prog. Solid State Chem. 34(2-4), 237-247 (2006).
69. Brule S, Levy M, Wilhelm C et al. Doxorubicin release triggered by alginate embedded magnetic nanoheaters: a combined therapy. Adv. Mater. 23(6), 787-790 (2011).
70. Liu TY, Hu SH, Liu DM, Chen SY, Chen IW. Biomedical nanoparticle carriers with combined thermal and magnetic responses. Nano Today 4(1), 52-65 (2009).
71. Derfus AM, Von Maltzahn G, Harris TJ et al. Remotely triggered release from magnetic nanoparticles. Adv. Mat. 19(22), 3932-3936 (2007).
72. Hoare T, Santamaria J, Goya GF et al. A magnetically triggered composite membrane for on-demand drug delivery. Nano Lett. 9(10), 3651-3657 (2009).
73. Akhyari P, Fedak PW, Weisel RD et al. Mechanical stretch regimen enhances the formation of bioengineered autologous cardiac muscle grafts. Circulation 106(12 Suppl. 1), I137-I142 (2002).
74. Zimmermann WH, Schneiderbanger K, Schubert P et al. Tissue engineering of a differentiated cardiac muscle construct. Circ. Res. 90(2), 223-230 (2002).
75. Radisic M, Park H, Shing H et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc. Natl Acad. Sci. USA 101(52), 18129-18134 (2004).
76. Radisic M, Yang L, Boublik J et al. Medium perfusion enables engineering of compact and contractile cardiac tissue. Am. J. Physiol. Heart Circ. Physiol. 286(2), H507-H516 (2004).
77. Dvir T, Levy O, Shachar M, Granot Y, Cohen S. Activation of the ERK1/2 cascade via pulsatile interstitial fluid flow promotes cardiac tissue assembly. Tissue Eng. 13(9), 2185-2193 (2007).
78. Carver SE, Heath CA. Semi-continuous perfusion system for delivering intermittent physiological pressure to regenerating cartilage. Tissue Eng. 5(1), 1-11 (1999).
79. Guldberg RE. Consideration of mechanical factors. Ann. NY Acad. Sci. 961, 312-314 (2002).
80. Roberts SR, Knight MM, Lee DA, Bader DL. Mechanical compression influences intracellular Ca2+ signaling in chondrocytes seeded in agarose constructs. J. Appl. Physiol. 90(4), 1385-1391 (2001).
81. Wu X, Davis MJ. Characterization of stretch-activated cation current in coronary smooth muscle cells. Am. J. Physiol. Heart Circ. Physiol. 280(4), H1751-H1761 (2001).
82. Naruse K, Yamada T, Sokabe M. Involvement of SA channels in orienting response of cultured endothelial cells to cyclic stretch. Am. J. Physiol. 274(5 Pt 2), H1532-H1538 (1998).
83. Kamkin A, Kiseleva I, Wagner KD et al. Characterization of stretch-activated ion currents in isolated atrial myocytes from human hearts. Pflugers. Arch. Eur. J. Physiol. 446(3), 339-346 (2003).
84. Frank D, Kuhn C, Brors B et al. Gene expression pattern in biomechanically stretched cardiomyocytes: evidence for a stretch-specific gene program. Hypertension 51(2), 309-318 (2008).
85. Park SM, Liu G, Kubal A, Fury M, Cao L, Marx SO. Direct interaction between BKCa potassium channel and microtubule-associated protein 1A. FEBS Lett. 570(1-3), 143-148 (2004).
86. Bockenhauer D, Zilberberg N, Goldstein SA. KCNK2: reversible conversion of a hippocampal potassium leak into a voltage-dependent channel. Nat. Neurosci. 4(5), 486-491 (2001).
87. Lee HS, Millward-Sadler SJ, Wright MO, Nuki G, Salter DM. Integrin and mechanosensitive ion channel-dependent tyrosine phosphorylation of focal adhesion proteins and b-catenin in human articular chondrocytes after mechanical stimulation. J. Bone Miner. Res. 15(8), 1501-1509 (2000).
88. Paoletti P, Ascher P. Mechanosensitivity of NMDA receptors in cultured mouse central neurons. Neuron 13(3), 645-655 (1994).
89. 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).
90. Matthews BD, Overby DR, Mannix R, Ingber DE. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell. Sci. 119(Pt 3), 508-518 (2006).
91. Hughes S, Dobson J, El Haj AJ. Magnetic targeting of mechanosensors in bone cells for tissue engineering applications. J. Biomech. 40(Suppl. 1), S96-S104 (2007).
92. 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.
93. Hughes S, McBain S, Dobson J, El Haj AJ. Selective activation of mechanosensitive ion channels using magnetic particles. J. R. Soc. Interface 5(25), 855-863 (2008).
94. Pickard M, Chari D. Enhancement of magnetic nanoparticle-mediated gene transfer to astrocytes by 'magnetofection': effects of static and oscillating fields. Nanomedicine (Lond.) 5(2), 217-232 (2010).
95. Mcbain SC, Griesenbach U, Xenariou S et al. Magnetic nanoparticles as gene delivery agents: enhanced transfection in the presence of oscillating magnet arrays. Nanotechnology 19(40), 405102 (2008).
96. Chorny M, Polyak B, Alferiev IS, Walsh K, Friedman G, Levy RJ. Magnetically driven plasmid DNA delivery with biodegradable polymeric nanoparticles. FASEB J. 21(10), 2510-2519 (2007).
97. Chorny M, Alferiev IS, Fishbein I et al. Formulation and in vitro characterization of composite biodegradable magnetic nanoparticles for magnetically guided cell delivery. Pharm. Res. 29(5), 1232-1241 (2012).
98. Macdonald C, Barbee K, Polyak B. Force dependent internalization of magnetic nanoparticles results in highly loaded endothelial cells for use as potential therapy delivery vectors. Pharm. Res. 29(5), 1270-1281 (2012).
99. Sapir Y, Cohen S, Friedman G, Polyak B. The promotion of in vitro vessel-like organization of endothelial cells in magnetically responsive alginate scaffolds. Biomaterials 33(16), 4100-4109 (2012).
100. Alsberg E, Feinstein E, Joy MP, Prentiss M, Ingber DE. Magnetically-guided self-assembly of fibrin matrices with ordered nano-scale structure for tissue engineering. Tissue Eng. 12, 3247-3256 (2006).
101. Takamatsu R, Oura H, Uchida T et al. Development of biodegradable scaffolds by leaching self-assembled magnetic sugar particles. Presented at: 20th Anniversary MHS 2009 and Micro-Nano Global COE-2009 International Symposium on Micro-NanoMechatronics and Human Science. Nagoya, Japan, 8-11 November 2009.
102. Uchida T, Oura H, Ikeda S, Arai F, Negoro M, Fukuda T. Fabrication of biodegradable scaffolds by use of self-assembled magnetic sugar particles as a casting template. Presented at: 2008 IEEE International Conference on Robotics and Automation, ICRA 2008, Pasadena, CA, USA, 19-23 May 2008.
103. Yuet KP, Hwang DK, Haghgooie R, Doyle PS. Multifunctional superparamagnetic janus particles. Langmuir 26(6), 4281-4287 (2010).
104. 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).
105. Wu Y, Jiang W, Wen XT et al. A novel calcium phosphate ceramic-magnetic nanoparticle composite as a potential bone substitute. Biomed. Mater. 5(1), 15001 (2010).
106. Wei Y, Zhang XH, Song Y et al. Magnetic biodegradable Fe(3)O(4)/CS/PVA nanofibrous membranes for bone regeneration. Biomed. Mater. 6(5), 055008 (2011).
107. Souza GR, Molina JR, Raphael RM et al. Three-dimensional tissue culture based on magnetic cell levitation. Nat. Nanotechnol. 5(4), 291-296 (2010).
108. Liu X, Kaminski MD, Riffle JS et al. Preparation and characterization of biodegradable magnetic carriers by single emulsion-solvent evaporation. J. Magn. Magn. Mater. 311(1), 84-87 (2007).
109. Demirbag B, Huri P, Kose G, Buyuksungur A, Hasirci V. Tissue engineering-to scaffold or not to scaffold. Bioessays 34(2), A3-A3 (2012).
110. Ito A, Takizawa Y, Honda H et al. Tissue engineering using magnetite nanoparticles and magnetic force: heterotypic layers of cocultured hepatocytes and endothelial cells.Tissue Eng. 10(5-6), 833-840 (2004).
111. Yamamoto Y, Ito A, Kato M et al. Preparation of artificial skeletal muscle tissues by a magnetic force-based tissue engineering technique. J. Biosci. Bioeng. 108(6), 538-543 (2009).
112. Shimizu K, Ito A, Yoshida T, Yamada Y, Ueda M, Honda H. Bone tissue engineering with human mesenchymal stem cell sheets constructed using magnetite nanoparticles and magnetic force. J. Biomed. Mater. Res. B. Appl. Biomater. 82(2), 471-480 (2007).
113. Shimizu K, Ito A, Honda H. Mag-seeding of rat bone marrow stromal cells into porous hydroxyapatite scaffolds for bone tissue engineering. J. Biosci. Bioeng. 104(3), 171-177 (2007).
114. Ito A, Ino K, Shimizu K, Honda H, Kamihira M. Fabrication of 3D tissue-like structure using magnetite nanoparticles and magnetic force. Presented at: 2006 IEEE International Symposium on Micro-Nano Mechanical and Human Science, MHS. Nagoya, Japan, 5-8 November 2006.
115. Ito A, Hibino E, Kobayashi C et al. Construction and delivery of tissue-engineered human retinal pigment epithelial cell sheets, using magnetite nanoparticles and magnetic force. Tissue Eng. 11(3-4), 489-496 (2005).
116. 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).
117. Frasca G, Gazeau F, Wilhelm C. Formation of a three-dimensional multicellular assembly using magnetic patterning. Langmuir 25(4), 2348-2354 (2009).
118. Wilhelm C, Riviere C, Biais N. Magnetic control of dictyostelium aggregation. Phys. Rev. E. 75(4), 041906 (2007).
119. Lee WR, Oh KT, Park SY et al. Magnetic levitating polymeric nano/microparticular substrates for three-dimensional tumor cell culture. Colloid Surf. B-Biointerfaces 85(2), 379-384 (2011).
120. Lee WY, Cheng WY, Yeh YC et al. Magnetically directed self-assembly of electrospun superparamagnetic fibrous bundles to form three-dimensional tissues with a highly ordered architecture. Tissue Eng. Part C Methods 17(6), 651-661 (2011).
121. Xu F, Wu CA, Rengarajan V et al. Three-dimensional magnetic assembly of microscale hydrogels. Adv. Mater. 23(37), 4254-4260 (2011).
122. Fu CY, Lin CY, Chu WC, Chang HY. A simple cell patterning method using magnetic particle-containing photosensitive poly (ethylene glycol) hydrogel blocks: a technical note. Tissue Eng. Part C Methods. 17(8), 871-877 (2011).
123. Weinand C, Xu JW, Peretti GM, Bonassar LJ, Gill TJ. Conditions affecting cell seeding onto three-dimensional scaffolds for cellular-based biodegradable implants. J. Biomed. Mater. Res. Part B 91B(1), 80-87 (2009).
124. Zhao F, Ma T. Perfusion bioreactor system for human mesenchymal stem cell tissue engineering: dynamic cell seeding and construct development. Biotech. Bioeng. 91(4), 482-493 (2005).
125. Martin I, Wendt D, Heberer M. The role of bioreactors in tissue engineering. Trends Biotech. 22(2), 80-86 (2004).
126. Thevenot P, Sohaebuddin S, Poudyal N, Ping Liu J, Tang L. Magnetic nanoparticles to enhance cell seeding and distribution in tissue engineering scaffolds. Presented at: 2008 8th IEEE Conference on Nanotechnology, IEEE-NANO. Arlington, TX, USA, 18-21 August 2008.
127. Robert D, Fayol D, Le Visage C et al. Magnetic micro-manipulations to probe the local physical properties of porous scaffolds and to confine stem cells. Biomaterials 31(7), 1586-1595 (2010).
128. Shimizu K, Ito A, Honda H. Enhanced cell-seeding into 3D porous scaffolds by use of magnetite nanoparticles. J. Biomed. Mater. Res. Part B Appl. Biomater. 77, 265-272 (2006).
129. 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).
130. Mitragotri S. Transdermal drug delivery using low-frequency sonophoresis. BioMEMS Biomed. Nanotechnol. 3, 223-236 (2006).
131. Mitragotri S, Blankschtein D, Langer R. Ultrasound-mediated transdermal protein delivery. Science 269(5225), 850-853 (1995).
132. Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA. What the cell 'sees' in bionanoscience. J. Am. Chem. Soc. 132(16), 5761-5768 (2010).
133. Mahon E, Salvati A, Baldelli Bombelli F, Lynch I, Dawson KA. Designing the nanoparticle-biomolecule interface for 'targeting and therapeutic delivery'. J. Control. Release 161(2), 164-174 (2012).