Contributions and future perspectives on the use of magnetic nanoparticles as diagnostic and therapeutic tools in the field of regenerative medicine

The current limitations of regenerative medicine strategies may be overcome through the use of magnetic nanoparticles (MNPs), a class of nanomaterial typically composed of magnetic elements that can be manipulated under the influence of an external magnetic field. Cell engineering approaches following the internalization of these MNPs by cells and/or the incorporation of these nanosystems within 3D constructs (scaffolds or hydrogels) may constitute a new attractive approach to achieve a magnetically responsive system enabling remote control over tissue-engineered constructs in an in vivo scenario. Moreover, the incorporation of bioactive factors within these MNPs also enables a targeted and smart delivery of biomolecules to specific regions and/or triggering specific cell responses upon external magnetic stimulation. Certainly, one of the most attractive properties of MNPs is their ability to be used as theranostic tools for regenerative medicine applications, enabling live monitoring and tracking of the system while simultaneously acting as a therapeutic stimulation.

[1]  David J. Mooney,et al.  Active scaffolds for on-demand drug and cell delivery , 2010, Proceedings of the National Academy of Sciences.

[2]  Heng Huang,et al.  Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. , 2010, Nature nanotechnology.

[3]  G. Gurtner,et al.  Pulsed Electromagnetic Fields Accelerate Normal and Diabetic Wound Healing by Increasing Endogenous FGF-2 Release , 2008, Plastic and reconstructive surgery.

[4]  M. Cima,et al.  Implantable magnetic relaxation sensors measure cumulative exposure to cardiac biomarkers , 2011, Nature Biotechnology.

[5]  E Wintermantel,et al.  Vascular tissue engineering with magnetic nanoparticles: seeing deeper , 2007, Journal of tissue engineering and regenerative medicine.

[6]  A Tampieri,et al.  A novel route in bone tissue engineering: magnetic biomimetic scaffolds. , 2010, Acta biomaterialia.

[7]  Takeshi Kobayashi,et al.  Cancer hyperthermia using magnetic nanoparticles , 2011, Biotechnology journal.

[8]  G. Cuniberti,et al.  Multifunctional magnetic mesoporous bioactive glass scaffolds with a hierarchical pore structure. , 2011, Acta biomaterialia.

[9]  P. Chu,et al.  Magnetic, fluorescent, and thermo-responsive Fe(3)O(4)/rare earth incorporated poly(St-NIPAM) core-shell colloidal nanoparticles in multimodal optical/magnetic resonance imaging probes. , 2013, Biomaterials.

[10]  Nicola Lopomo,et al.  A new approach to scaffold fixation by magnetic forces: Application to large osteochondral defects. , 2012, Medical Engineering and Physics.

[11]  F. Pezzetti,et al.  Effects of Pulsed Electromagnetic Fields on Human Articular Chondrocyte Proliferation , 2001, Connective tissue research.

[12]  G. Lucignani,et al.  Labeling Protocols for In Vivo Tracking of Human Skeletal Muscle Cells (HSkMCs) by Magnetic Resonance and Bioluminescence Imaging , 2012, Molecular Imaging and Biology.

[13]  Jochen Ringe,et al.  Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. , 2012, Biomaterials.

[14]  M. Markov,et al.  Expanding Use of Pulsed Electromagnetic Field Therapies , 2007, Electromagnetic biology and medicine.

[15]  Dar-Ming Lai,et al.  Magnetic nanoparticle labeling of mesenchymal stem cells without transfection agent: Cellular behavior and capability of detection with clinical 1.5 T magnetic resonance at the single cell level , 2007, Magnetic resonance in medicine.

[16]  R. Reis,et al.  Enhancement of osteogenic differentiation of human adipose derived stem cells by the controlled release of platelet lysates from hybrid scaffolds produced by supercritical fluid foaming. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[17]  Feng Xu,et al.  Three‐Dimensional Magnetic Assembly of Microscale Hydrogels , 2011, Advanced materials.

[18]  M. Dahaba,et al.  Effect of pulsed electromagnetic field on healing of mandibular fracture: a preliminary clinical study. , 2011, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[19]  A. Fioravanti,et al.  Biochemical and morphological study of human articular chondrocytes cultivated in the presence of pulsed signal therapy , 2002, Annals of the rheumatic diseases.

[20]  Paul R. Chalker,et al.  Thermal stability of neodymium aluminates high-κ dielectric deposited by liquid injection MOCVD using single-source heterometallic alkoxide precursors , 2012 .

[21]  Peter van Gelderen,et al.  Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells , 2001, Nature Biotechnology.

[22]  H. Hamann,et al.  Polymer mediated self-assembly of magnetic nanoparticles. , 2002, Journal of the American Chemical Society.

[23]  E. Schemitsch,et al.  The science of electrical stimulation therapy for fracture healing , 2009, Indian Journal of Orthopaedics.

[24]  Smadar Cohen,et al.  The promotion of in vitro vessel-like organization of endothelial cells in magnetically responsive alginate scaffolds. , 2012, Biomaterials.

[25]  Hirokazu Akiyama,et al.  Genetically engineered angiogenic cell sheets using magnetic force-based gene delivery and tissue fabrication techniques. , 2010, Biomaterials.

[26]  C. Wilhelm,et al.  Use of Magnetic Forces to Promote Stem Cell Aggregation During Differentiation, and Cartilage Tissue Modeling , 2013, Advanced materials.

[27]  Savas Tasoglu,et al.  Paramagnetic Levitational Assembly of Hydrogels , 2013, Advanced materials.

[28]  K. Varani,et al.  Functional tissue engineering in articular cartilage repair: is there a role for electromagnetic biophysical stimulation? , 2013, Tissue engineering. Part B, Reviews.

[29]  H. S. Azevedo,et al.  Synthesis and functionalization of superparamagnetic poly-ɛ-caprolactone microparticles for the selective isolation of subpopulations of human adipose-derived stem cells , 2011, Journal of The Royal Society Interface.

[30]  Christopher S. Chen,et al.  Magnetic microposts as an approach to apply forces to living cells , 2007, Proceedings of the National Academy of Sciences.

[31]  Ali Yilmaz,et al.  Imaging of myocardial infarction using ultrasmall superparamagnetic iron oxide nanoparticles: a human study using a multi-parametric cardiovascular magnetic resonance imaging approach. , 2013, European heart journal.

[32]  L. Sedel,et al.  Current trends in the enhancement of fracture healing. , 2001, The Journal of bone and joint surgery. British volume.

[33]  Tal Dvir,et al.  Tissue engineering on the nanoscale: lessons from the heart. , 2013, Current opinion in biotechnology.

[34]  Christian Binek,et al.  Magnetic nanoparticles: recent advances in synthesis, self-assembly and applications , 2011 .

[35]  Gaudenz Danuser,et al.  Scale integration: the structure and dynamics of macromolecular assemblies, cells and tissues. , 2012, Current opinion in cell biology.

[36]  J. Dobson,et al.  Magnetic targeting of mechanosensors in bone cells for tissue engineering applications. , 2007, Journal of biomechanics.

[37]  D. Gemmati,et al.  Proteoglycan synthesis in bovine articular cartilage explants exposed to different low-frequency low-energy pulsed electromagnetic fields. , 2007, Osteoarthritis and cartilage.

[38]  Seong Deok Kong,et al.  In situ tissue engineering using magnetically guided three-dimensional cell patterning. , 2012, Tissue engineering. Part C, Methods.

[39]  G. Arendash.  Transcranial electromagnetic treatment against Alzheimer's disease: why it has the potential to trump Alzheimer's disease drug development. , 2012, Journal of Alzheimer's disease : JAD.

[40]  Antonios G Mikos,et al.  Design of a flow perfusion bioreactor system for bone tissue-engineering applications. , 2003, Tissue engineering.

[41]  F. Štěpánek,et al.  Investigation of radiofrequency induced release kinetics from magnetic hollow silica microspheres , 2012 .

[42]  Haeshin Lee,et al.  In vivo tracking of mesechymal stem cells using fluorescent nanoparticles in an osteochondral repair model. , 2012, Molecular therapy : the journal of the American Society of Gene Therapy.

[43]  David H. Miller,et al.  Assessment of disease activity in multiple sclerosis phenotypes with combined gadolinium- and superparamagnetic iron oxide-enhanced MR imaging. , 2012, Radiology.

[44]  Liping Tang,et al.  Magnetic Nanoparticles to Enhance Cell Seeding and Distribution in Tissue Engineering Scaffolds , 2008, 2008 8th IEEE Conference on Nanotechnology.

[45]  T. Webster,et al.  Eradicating Antibiotic‐Resistant Biofilms with Silver‐Conjugated Superparamagnetic Iron Oxide Nanoparticles , 2013, Advanced healthcare materials.

[46]  Qing Ye,et al.  In situ labeling of immune cells with iron oxide particles: an approach to detect organ rejection by cellular MRI. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[47]  R. Reis,et al.  Controlled release strategies for bone, cartilage, and osteochondral engineering--Part II: challenges on the evolution from single to multiple bioactive factor delivery. , 2013, Tissue engineering. Part B, Reviews.

[48]  Alicia J El Haj,et al.  Controlled differentiation of human bone marrow stromal cells using magnetic nanoparticle technology. , 2010, Tissue engineering. Part A.

[49]  C. Ménager,et al.  Human Erythrocytes Covered with Magnetic Core–Shell Nanoparticles for Multimodal Imaging , 2013, Advanced healthcare materials.

[50]  L. Massari,et al.  Chondroprotective effects of pulsed electromagnetic fields on human cartilage explants , 2011, Bioelectromagnetics.

[51]  Jiyan Liu,et al.  Synthesis, preliminary structure-activity relationships, and in vitro biological evaluation of 6-aryl-3-amino-thieno[2,3-b]pyridine derivatives as potential anti-inflammatory agents. , 2013, Bioorganic & medicinal chemistry letters.

[52]  Orthopaedic applications of nanoparticle-based stem cell therapies , 2012, Stem Cell Research & Therapy.

[53]  S. Oldenburg,et al.  Silver nanoparticles do not influence stem cell differentiation but cause minimal toxicity. , 2012, Nanomedicine.

[54]  D. Holmes,et al.  Magnetizable Duplex Steel Stents Enable Endothelial Cell Capture , 2013, IEEE Transactions on Magnetics.

[55]  Damien Dauphinee,et al.  Pulsed radiofrequency electromagnetic field therapy: a potential novel treatment of plantar fasciitis. , 2012, The Journal of foot and ankle surgery : official publication of the American College of Foot and Ankle Surgeons.

[56]  Tian Jian Lu,et al.  Magnetic Hydrogels and Their Potential Biomedical Applications , 2013 .

[57]  B. Chalidis,et al.  Pulsed electromagnetic fields for the treatment of tibial delayed unions and nonunions. A prospective clinical study and review of the literature , 2012, Journal of Orthopaedic Surgery and Research.

[58]  S. Zaffagnini,et al.  Conservative treatment of spontaneous osteonecrosis of the knee in the early stage: pulsed electromagnetic fields therapy. , 2013, European journal of radiology.

[59]  Hiroyuki Honda,et al.  Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force. , 2005, Tissue engineering.

[60]  W. Graninger,et al.  Effect of pulsed electromagnetic fields on proteoglycan biosynthesis of articular cartilage is age dependent , 2005, Annals of the Rheumatic Diseases.

[61]  Jian-feng Dong,et al.  Anticancer effect and feasibility study of hyperthermia treatment of pancreatic cancer using magnetic nanoparticles. , 2011, Oncology reports.

[62]  D. Gemmati,et al.  Effects of Electromagnetic Fields on Proteoglycan Metabolism of Bovine Articular Cartilage Explants , 2003, Connective tissue research.

[63]  A. Pilla,et al.  Pulsed magnetic field therapy increases tensile strength in a rat Achilles' tendon repair model. , 2006, The Journal of hand surgery.

[64]  Thomas L. Smith,et al.  Microcirculatory effects of pulsed electromagnetic fields , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[65]  Melba Navarro,et al.  Nanotechnology in regenerative medicine: the materials side. , 2008, Trends in biotechnology.

[66]  Sungho Jin,et al.  Magnetic nanoparticles for theragnostics. , 2009, Advanced drug delivery reviews.

[67]  M. Kolonin,et al.  Adipose tissue engineering in three-dimensional levitation tissue culture system based on magnetic nanoparticles. , 2013, Tissue engineering. Part C, Methods.

[68]  中林 昭裕.  In vivo bioluminescence imaging of magnetically targeted bone marrow-derived mesenchymal stem cells in skeletal muscle injury model , 2013 .

[69]  Franco Rustichelli,et al.  Stem Cell Tracking by Nanotechnologies , 2010, International journal of molecular sciences.

[70]  Hiroyuki Honda,et al.  Enhanced cell-seeding into 3D porous scaffolds by use of magnetite nanoparticles. , 2006, Journal of biomedical materials research. Part B, Applied biomaterials.

[71]  A. J. Guiomar,et al.  Biofunctionalized magnetic hydrogel nanospheres of magnetite and κ-carrageenan , 2009, Nanotechnology.

[72]  Y. Mardor,et al.  Magnetic Scaffolds Enriched with Bioactive Nanoparticles for Tissue Engineering , 2012, Advanced healthcare materials.

[73]  R. Raphael,et al.  Assembly of a three-dimensional multitype bronchiole coculture model using magnetic levitation. , 2013, Tissue engineering. Part C, Methods.

[74]  Jeff W M Bulte,et al.  Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. , 2003, Radiology.

[75]  Yuhui Li,et al.  Techniques for fabrication and construction of three-dimensional scaffolds for tissue engineering , 2013, International journal of nanomedicine.

[76]  R. Reis,et al.  From nano- to macro-scale: nanotechnology approaches for spatially controlled delivery of bioactive factors for bone and cartilage engineering. , 2012, Nanomedicine.

[77]  Todd Hoare,et al.  Injectable superparamagnets: highly elastic and degradable poly(N-isopropylacrylamide)-superparamagnetic iron oxide nanoparticle (SPION) composite hydrogels. , 2013, Biomacromolecules.

[78]  A. E. Haj,et al.  Biocompatibility and toxicity of magnetic nanoparticles in regenerative medicine , 2012 .

[79]  B. S. Sekhon,et al.  Inorganic nanomedicine--part 1. , 2010, Nanomedicine : nanotechnology, biology, and medicine.

[80]  André R. Fajardo,et al.  Natural polymer-based magnetic hydrogels: Potential vectors for remote-controlled drug release. , 2012, Carbohydrate polymers.

[81]  Antonios G. Mikos,et al.  Fluid flow increases mineralized matrix deposition in 3D perfusion culture of marrow stromal osteoblasts in a dose-dependent manner , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[82]  San-Yuan Chen,et al.  Preparation and characterization of magnetic ferroscaffolds for tissue engineering , 2007 .

[83]  Hsuan-Liang Liu,et al.  Can low frequency electromagnetic field help cartilage tissue engineering? , 2009, Journal of biomedical materials research. Part A.

[84]  S. Martel,et al.  Co-encapsulation of magnetic nanoparticles and doxorubicin into biodegradable microcarriers for deep tissue targeting by vascular MRI navigation. , 2011, Biomaterials.

[85]  R. Reis,et al.  Controlled release strategies for bone, cartilage, and osteochondral engineering--Part I: recapitulation of native tissue healing and variables for the design of delivery systems. , 2013, Tissue engineering. Part B, Reviews.

[86]  Susann Müller,et al.  From multi-omics to basic structures of biological systems. , 2013, Current opinion in biotechnology.

[87]  K. Varani,et al.  Electromagnetic fields (EMFs) and adenosine receptors modulate prostaglandin E2 and cytokine release in human osteoarthritic synovial fibroblasts , 2012, Journal of cellular physiology.

[88]  E. Galliera,et al.  Low Frequency Pulsed Electromagnetic Field Affects Proliferation, Tissue-Specific Gene Expression, and Cytokines Release of Human Tendon Cells , 2013, Cell Biochemistry and Biophysics.

[89]  G. Whitesides,et al.  Fabrication and Manipulation of Ionotropic Hydrogels Crosslinked by Paramagnetic Ions. , 2007, Chemistry of materials : a publication of the American Chemical Society.

[90]  H. Honda,et al.  iPS cell sheets created by a novel magnetite tissue engineering method for reparative angiogenesis , 2013, Scientific Reports.

[91]  Hiroyuki Honda,et al.  Construction and harvest of multilayered keratinocyte sheets using magnetite nanoparticles and magnetic force. , 2004, Tissue engineering.

[92]  Piotr Walczak,et al.  Tracking stem cells using magnetic nanoparticles. , 2011, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[93]  B. Bonnemain,et al.  Superparamagnetic agents in magnetic resonance imaging: physicochemical characteristics and clinical applications. A review. , 1998, Journal of drug targeting.

[94]  James A Bankson,et al.  Three-dimensional tissue culture based on magnetic cell levitation. , 2010, Nature nanotechnology.

[95]  R. Reis,et al.  Chitosan–chondroitin sulphate nanoparticles for controlled delivery of platelet lysates in bone regenerative medicine , 2012, Journal of tissue engineering and regenerative medicine.

[96]  Charles P. Lin,et al.  Tracking mesenchymal stem cells with iron oxide nanoparticle loaded poly(lactide-co-glycolide) microparticles. , 2012, Nano letters.

[97]  Dino Di Carlo,et al.  Magnetic nanoparticle-mediated massively-parallel mechanical modulation of single-cell behavior , 2012, Nature Methods.