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The application of super paramagnetic iron oxide-labeled mesenchymal stem cells in cell-based therapy

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Abstract

Mesenchymal stem cell (MSC)-based therapy has great potential for tissue regeneration. However, being able to monitor the in vivo behavior of implanted MSCs and understand the fate of these cells is necessary for further development of successful therapies and requires an effective, non-invasive and non-toxic technique for cell tracking. Super paramagnetic iron oxide (SPIO) is an idea label and tracer of MSCs. MRI can be used to follow SPIO-labeled MSCs and has been proposed as a gold standard for monitoring the in vivo biodistribution and migration of implanted SPIO-labeled MSCs. This review discusses the biological effects of SPIO labeling on MSCs and the therapeutic applications of local or systemic delivery of these labeled cells.

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References

  1. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147

    Article  PubMed  CAS  Google Scholar 

  2. Toma C, Pittenger MF, Cahill KS, Byrne BJ, Kessler PD (2002) Human mesenchymal stem cells differentiate to a cardiomyocyte phenotype in the adult murine heart. Circulation 105:93–98

    Article  PubMed  Google Scholar 

  3. Janssens S, Dubois C, Bogaert J et al (2006) Autologous bone marrow-derived stem-cell transfer in patients with ST-segment elevation myocardial infarction: double-blind, randomised controlled trial. Lancet 367:113–121

    Article  PubMed  Google Scholar 

  4. Wollert KC, Meyer GP, Lotz J et al (2004) Intracoronary autologous bone-marrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet 364:141–148

    Article  PubMed  Google Scholar 

  5. Stamm C, Westphal B, Kleine HD et al (2003) Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361:45–46

    Article  PubMed  Google Scholar 

  6. Kaminski A, Steinhoff G (2008) Current status of intramyocardial bone marrow stem cell transplantation. Semin Thorac Cardiovasc Surg 20:119–125

    Article  PubMed  Google Scholar 

  7. Roobrouck VD, Ulloa-Montoya F, Verfaillie CM (2008) Self-renewal and differentiation capacity of young and aged stem cells. Exp Cell Res 314:1937–1944

    Article  PubMed  CAS  Google Scholar 

  8. Abdallah BM, Kassem M (2008) Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther 15:109–116

    Article  PubMed  CAS  Google Scholar 

  9. Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568–584

    Article  PubMed  CAS  Google Scholar 

  10. Tsai CP, Hung Y, Chou YH et al (2008) High-contrast paramagnetic fluorescent mesoporous silica nanorods as a multifunctional cell-imaging probe. Small 4:186–191

    Article  PubMed  CAS  Google Scholar 

  11. Chavakis E, Urbich C, Dimmeler S (2008) Homing and engraftment of progenitor cells: a prerequisite for cell therapy. J Mol Cell Cardiol 45:514–522

    Article  PubMed  CAS  Google Scholar 

  12. Singh JP (2009) Enabling technologies for homing and engraftment of cells for therapeutic applications. JACC Cardiovasc Interv 2:803–804

    Article  PubMed  Google Scholar 

  13. Niemeyer M, Oostendorp RA, Kremer M et al (2010) Non-invasive tracking of human haemopoietic CD34(+) stem cells in vivo in immunodeficient mice by using magnetic resonance imaging. Eur Radiol 20:2184–2193

    Article  PubMed  Google Scholar 

  14. Wilhelm C, Bal L, Smirnov P et al (2007) Magnetic control of vascular network formation with magnetically labeled endothelial progenitor cells. Biomaterials 28:3797–3806

    Article  PubMed  CAS  Google Scholar 

  15. Phanapavudhikul P, Shen S, Ng WK, Tan RB (2008) Formulation of Fe3O4/acrylate co-polymer nanocomposites as potential drug carriers. Drug Deliv 15:177–183

    Article  PubMed  CAS  Google Scholar 

  16. Jing XH, Yang L, Duan XJ et al (2008) In vivo MR imaging tracking of magnetic iron oxide nanoparticle labeled, engineered, autologous bone marrow mesenchymal stem cells following intra-articular injection. Joint Bone Spine 75:432–438

    Article  PubMed  Google Scholar 

  17. Latorre M, Rinaldi C (2009) Applications of magnetic nanoparticles in medicine: magnetic fluid hyperthermia. P R Health Sci J 28:227–238

    PubMed  Google Scholar 

  18. Saldanha KJ, Doan RP, Ainslie KM, Desai TA, Majumdar S (2011) Micrometer-sized iron oxide particle labeling of mesenchymal stem cells for magnetic resonance imaging-based monitoring of cartilage tissue engineering. Magn Reson Imaging 29:40–49

    Article  PubMed  CAS  Google Scholar 

  19. Hill JM, Dick AJ, Raman VK et al (2003) Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 108:1009–1014

    Article  PubMed  Google Scholar 

  20. Tanimoto A, Kuribayashi S (2006) Application of superparamagnetic iron oxide to imaging of hepatocellular carcinoma. Eur J Radiol 58:200–216

    Article  PubMed  Google Scholar 

  21. Weissleder R, Stark DD, Engelstad BL et al (1989) Superparamagnetic iron oxide: pharmacokinetics and toxicity. AJR Am J Roentgenol 152:167–173

    PubMed  CAS  Google Scholar 

  22. Park B-H, Jung J-C, Lee G-H et al (2008) Comparison of labeling efficiency of different magnetic nanoparticles into stem cell. Colloids Surf A 14:145–149

    Article  CAS  Google Scholar 

  23. Zeng G, Wang G, Guan F et al (2011) Human amniotic membrane-derived mesenchymal stem cells labeled with superparamagnetic iron oxide nanoparticles: the effect on neuron-like differentiation in vitro. Mol Cell Biochem 357:331–341

    Article  PubMed  CAS  Google Scholar 

  24. Balakumaran A, Pawelczyk E, Ren J et al (2010) Superparamagnetic iron oxide nanoparticles labeling of bone marrow stromal (mesenchymal) cells does not affect their “stemness”. PLoS One 5:e11462

    Article  PubMed  CAS  Google Scholar 

  25. Heymer A, Haddad D, Weber M et al (2008) Iron oxide labelling of human mesenchymal stem cells in collagen hydrogels for articular cartilage repair. Biomaterials 29:1473–1483

    Article  PubMed  CAS  Google Scholar 

  26. Kostura L, Kraitchman DL, Mackay AM, Pittenger MF, Bulte JW (2004) Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 17:513–517

    Article  PubMed  Google Scholar 

  27. Arbab AS, Yocum GT, Kalish H et al (2004) Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 104:1217–1223

    Article  PubMed  CAS  Google Scholar 

  28. Schafer R, Bantleon R, Kehlbach R et al (2010) Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol 11:22

    Article  PubMed  CAS  Google Scholar 

  29. Kraitchman DL, Tatsumi M, Gilson WD et al (2005) Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 112:1451–1461

    Article  PubMed  Google Scholar 

  30. Ito A, Hibino E, Honda H et al (2004) A new methodology of mesenchymal stem cell expansion using magnetic nanoparticles. Biochem Eng J 20:119–125

    Article  CAS  Google Scholar 

  31. He G, Zhang H, Wei H et al (2007) In vivo imaging of bone marrow mesenchymal stem cells transplanted into myocardium using magnetic resonance imaging: a novel method to trace the transplanted cells. Int J Cardiol 114:4–10

    Article  PubMed  Google Scholar 

  32. Terrovitis JV, Bulte JW, Sarvananthan S et al (2006) Magnetic resonance imaging of ferumoxide-labeled mesenchymal stem cells seeded on collagen scaffolds-relevance to tissue engineering. Tissue Eng 12:2765–2775

    Article  PubMed  CAS  Google Scholar 

  33. van Buul GM, Kotek G, Wielopolski PA et al (2011) Clinically translatable cell tracking and quantification by MRI in cartilage repair using superparamagnetic iron oxides. PLoS One 6:e17001

    Article  PubMed  CAS  Google Scholar 

  34. Sun JH, Zhang YL, Qian SP et al (2012) Assessment of biological characteristics of mesenchymal stem cells labeled with superparamagnetic iron oxide particles in vitro. Mol Med Report 5:317–320

    PubMed  CAS  Google Scholar 

  35. Huang DM, Hsiao JK, Chen YC (2009) The promotion of human mesenchymal stem cell proliferation by superparamagnetic iron oxide nanoparticles. Biomaterials 30:3645–3651

    Article  PubMed  CAS  Google Scholar 

  36. Chang YK, Liu YP, Ho JH, Hsu SC, Lee OK (2012) Amine-surface-modified superparamagnetic iron oxide nanoparticles interfere with differentiation of human mesenchymal stem cells. J Orthop Res 30:1499–1506

    Article  PubMed  CAS  Google Scholar 

  37. Hinds KA, Hill JM, Shapiro EM et al (2003) Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood 102:867–872

    Article  PubMed  CAS  Google Scholar 

  38. Frank JA, Miller BR, Arbab AS et al (2003) Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228:480–487

    Article  PubMed  Google Scholar 

  39. Arbab AS, Bashaw LA, Miller BR et al (2003) Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229:838–846

    Article  PubMed  Google Scholar 

  40. Hori J, Deie M, Kobayashi T, Yasunaga Y, Kawamata S, Ochi M (2011) Articular cartilage repair using an intra-articular magnet and synovium-derived cells. J Orthop Res 29:531–538

    Article  PubMed  Google Scholar 

  41. Farrell E, Wielopolski P, Pavljasevic P et al (2008) Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun 369:1076–1081

    Article  PubMed  CAS  Google Scholar 

  42. Schafer R, Kehlbach R, Muller M et al (2009) Labeling of human mesenchymal stromal cells with superparamagnetic iron oxide leads to a decrease in migration capacity and colony formation ability. Cytotherapy 11:68–78

    Article  PubMed  CAS  Google Scholar 

  43. Schafer R, Ayturan M, Bantleon R et al (2008) 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 17:923–941

    Article  PubMed  Google Scholar 

  44. Andreas K, Georgieva R, Ladwig M et al (2012) Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. Biomaterials 33:4515–4525

    Article  PubMed  CAS  Google Scholar 

  45. Chen YC, Hsiao JK, Liu HM et al (2010) The inhibitory effect of superparamagnetic iron oxide nanoparticle (Ferucarbotran) on osteogenic differentiation and its signaling mechanism in human mesenchymal stem cells. Toxicol Appl Pharmacol 245:272–279

    Article  PubMed  CAS  Google Scholar 

  46. Arbab AS, Yocum GT, Rad AM et al (2005) Labeling of cells with ferumoxides–protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR Biomed 18:553–559

    Article  PubMed  CAS  Google Scholar 

  47. Wang L, Deng J, Wang J et al (2009) Superparamagnetic iron oxide does not affect the viability and function of adipose-derived stem cells, and superparamagnetic iron oxide-enhanced magnetic resonance imaging identifies viable cells. Magn Reson Imaging 27:108–119

    Article  PubMed  CAS  Google Scholar 

  48. Yang CY, Hsiao JK, Tai MF et al (2011) Direct labeling of hMSC with SPIO: the long-term influence on toxicity, chondrogenic differentiation capacity, and intracellular distribution. Mol Imaging Biol 13:443–451

    Article  PubMed  Google Scholar 

  49. Nishida K, Tanaka N, Nakanishi K et al (2006) Magnetic targeting of bone marrow stromal cells into spinal cord: through cerebrospinal fluid. Neuroreport 17:1269–1272

    Article  PubMed  Google Scholar 

  50. Reddy AM, Kwak BK, Shim HJ et al (2009) Functional characterization of mesenchymal stem cells labeled with a novel PVP-coated superparamagnetic iron oxide. Contrast Media Mol Imaging 4:118–126

    Article  PubMed  CAS  Google Scholar 

  51. Saha S, Yang XB, Tanner S, Curran S, Wood D, Kirkham J (2012) The effects of iron oxide incorporation on the chondrogenic potential of three human cell types. J Tissue Eng Regen Med. doi:10.1002/term.544

  52. Henning TD, Sutton EJ, Kim A et al (2009) The influence of ferucarbotran on the chondrogenesis of human mesenchymal stem cells. Contrast Media Mol Imaging 4:165–173

    Article  PubMed  CAS  Google Scholar 

  53. Nejadnik H, Henning TD, Castaneda RT et al (2012) Somatic differentiation and MR imaging of magnetically labeled human embryonic stem cells. Cell Transplant. doi:10.3727/096368912X653156

  54. Watson DJ, Walton RM, Magnitsky SG, Bulte JW, Poptani H, Wolfe JH (2006) Structure-specific patterns of neural stem cell engraftment after transplantation in the adult mouse brain. Hum Gene Ther 17:693–704

    Article  PubMed  CAS  Google Scholar 

  55. Hoehn M, Kustermann E, Blunk J et al (2002) Monitoring of implanted stem cell migration in vivo: a highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proc Natl Acad Sci USA 99:16267–16272

    Article  PubMed  CAS  Google Scholar 

  56. Arbab AS, Yocum GT, Wilson LB et al (2004) Comparison of transfection agents in forming complexes with ferumoxides, cell labeling efficiency, and cellular viability. Mol Imaging 3:24–32

    Article  PubMed  CAS  Google Scholar 

  57. Arbab AS, Bashaw LA, Miller BR, Jordan EK, Bulte JW, Frank JA (2003) Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation 76:1123–1130

    Article  PubMed  CAS  Google Scholar 

  58. Mailander V, Lorenz MR, Holzapfel V et al (2008) Carboxylated superparamagnetic iron oxide particles label cells intracellularly without transfection agents. Mol Imaging Biol 10:138–146

    Article  PubMed  Google Scholar 

  59. Hsiao JK, Tai MF, Chu HH et al (2007) 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. Magn Reson Med 58:717–724

    Article  PubMed  CAS  Google Scholar 

  60. Metz S, Bonaterra G, Rudelius M et al (2004) Capacity of human monocytes to phagocytose approved iron oxide MR contrast agents in vitro. Eur Radiol 14:1851–1858

    Article  PubMed  Google Scholar 

  61. Daldrup-Link HE, Meier R, Rudelius M et al (2005) In vivo tracking of genetically engineered, anti-HER2/neu directed natural killer cells to HER2/neu positive mammary tumors with magnetic resonance imaging. Eur Radiol 15:4–13

    Article  PubMed  Google Scholar 

  62. Simon GH, von Vopelius-Feldt J, Fu Y et al (2006) Ultrasmall supraparamagnetic iron oxide-enhanced magnetic resonance imaging of antigen-induced arthritis: a comparative study between SHU 555 C, ferumoxtran-10, and ferumoxytol. Invest Radiol 41:45–51

    Article  PubMed  Google Scholar 

  63. Boutry S, Brunin S, Mahieu I, Laurent S, Vander Elst L, Muller RN (2008) Magnetic labeling of non-phagocytic adherent cells with iron oxide nanoparticles: a comprehensive study. Contrast Media Mol Imaging 3:223–232

    Article  PubMed  CAS  Google Scholar 

  64. Henning TD, Wendland MF, Golovko D et al (2009) Relaxation effects of ferucarbotran-labeled mesenchymal stem cells at 1.5T and 3T: discrimination of viable from lysed cells. Magn Reson Med 62:325–332

    Article  PubMed  CAS  Google Scholar 

  65. Zhou YF, Sae-Lim V, Chou AM, Hutmacher DW, Lim TM (2006) Does seeding density affect in vitro mineral nodules formation in novel composite scaffolds? J Biomed Mater Res A 78:183–193

    PubMed  CAS  Google Scholar 

  66. Wilson CE, Dhert WJ, Van Blitterswijk CA, Verbout AJ, De Bruijn JD (2002) Evaluating 3D bone tissue engineered constructs with different seeding densities using the alamarBlue assay and the effect on in vivo bone formation. J Mater Sci Mater Med 13:1265–1269

    Article  PubMed  CAS  Google Scholar 

  67. Carrier RL, Papadaki M, Rupnick M et al (1999) Cardiac tissue engineering: cell seeding, cultivation parameters, and tissue construct characterization. Biotechnol Bioeng 64:580–589

    Article  PubMed  CAS  Google Scholar 

  68. Vunjak-Novakovic G, Radisic M (2004) Cell seeding of polymer scaffolds. Methods Mol Biol 238:131–146

    PubMed  CAS  Google Scholar 

  69. Shimizu K, Ito A, Honda H (2006) Enhanced cell-seeding into 3D porous scaffolds by use of magnetite nanoparticles. J Biomed Mater Res B Appl Biomater 77:265–272

    PubMed  Google Scholar 

  70. Corot C, Robert P, Idee JM, Port M (2006) Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 58:1471–1504

    Article  PubMed  CAS  Google Scholar 

  71. Shimizu K, Ito A, Honda H (2007) Mag-seeding of rat bone marrow stromal cells into porous hydroxyapatite scaffolds for bone tissue engineering. J Biosci Bioeng 104:171–177

    Article  PubMed  CAS  Google Scholar 

  72. Laschke MW, Harder Y, Amon M et al (2006) Angiogenesis in tissue engineering: breathing life into constructed tissue substitutes. Tissue Eng 12:2093–2104

    Article  PubMed  CAS  Google Scholar 

  73. Matsuo T, Sugita T, Kubo T, Yasunaga Y, Ochi M, Murakami T (2003) Injectable magnetic liposomes as a novel carrier of recombinant human BMP-2 for bone formation in a rat bone-defect model. J Biomed Mater Res A 66:747–754

    Article  PubMed  CAS  Google Scholar 

  74. Tanaka H, Sugita T, Yasunaga Y et al (2005) Efficiency of magnetic liposomal transforming growth factor-beta 1 in the repair of articular cartilage defects in a rabbit model. J Biomed Mater Res A 73:255–263

    PubMed  Google Scholar 

  75. Motoyama M, Deie M, Kanaya A et al (2010) In vitro cartilage formation using TGF-beta-immobilized magnetic beads and mesenchymal stem cell-magnetic bead complexes under magnetic field conditions. J Biomed Mater Res A 92:196–204

    PubMed  Google Scholar 

  76. Bulte JW, Kraitchman DL (2004) Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 17:484–499

    Article  PubMed  CAS  Google Scholar 

  77. Bulte JW, Duncan ID, Frank JA (2002) In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J Cereb Blood Flow Metab 22:899–907

    Article  PubMed  Google Scholar 

  78. Unger EC (2003) How can superparamagnetic iron oxides be used to monitor disease and treatment? Radiology 229:615–616

    Article  PubMed  Google Scholar 

  79. Thorek DL, Chen AK, Czupryna J, Tsourkas A (2006) Superparamagnetic iron oxide nanoparticle probes for molecular imaging. Ann Biomed Eng 34:23–38

    Article  PubMed  Google Scholar 

  80. Lalande C, Miraux S, Derkaoui SM et al (2011) Magnetic resonance imaging tracking of human adipose derived stromal cells within three-dimensional scaffolds for bone tissue engineering. Eur Cell Mater 21:341–354

    PubMed  CAS  Google Scholar 

  81. Ko IK, Song HT, Cho EJ, Lee ES, Huh YM, Suh JS (2007) In vivo MR imaging of tissue-engineered human mesenchymal stem cells transplanted to mouse: a preliminary study. Ann Biomed Eng 35:101–108

    Article  PubMed  Google Scholar 

  82. Lee JH, Jung MJ, Hwang YH et al (2012) Heparin-coated superparamagnetic iron oxide for in vivo MR imaging of human MSCs. Biomaterials 33:4861–4871

    Article  PubMed  CAS  Google Scholar 

  83. Yang K, Xiang P, Zhang C et al (2011) Magnetic resonance evaluation of transplanted mesenchymal stem cells after myocardial infarction in swine. Can J Cardiol 27:818–825

    Article  PubMed  Google Scholar 

  84. Hu SL, Zhang JQ, Hu X et al (2009) In vitro labeling of human umbilical cord mesenchymal stem cells with superparamagnetic iron oxide nanoparticles. J Cell Biochem 108:529–535

    Article  PubMed  CAS  Google Scholar 

  85. Hu SL, Lu PG, Zhang LJ et al (2012) In vivo magnetic resonance imaging tracking of SPIO-labeled human umbilical cord mesenchymal stem cells. J Cell Biochem 113:1005–1012

    Article  PubMed  CAS  Google Scholar 

  86. Nishimori M, Deie M, Kanaya A, Exham H, Adachi N, Ochi M (2006) Repair of chronic osteochondral defects in the rat. A bone marrow-stimulating procedure enhanced by cultured allogenic bone marrow mesenchymal stromal cells. J Bone Joint Surg Br 88:1236–1244

    Article  PubMed  CAS  Google Scholar 

  87. Agung M, Ochi M, Yanada S et al (2006) Mobilization of bone marrow-derived mesenchymal stem cells into the injured tissues after intraarticular injection and their contribution to tissue regeneration. Knee Surg Sports Traumatol Arthrosc 14:1307–1314

    Article  PubMed  Google Scholar 

  88. Kobayashi T, Ochi M, Yanada S et al (2008) A novel cell delivery system using magnetically labeled mesenchymal stem cells and an external magnetic device for clinical cartilage repair. Arthroscopy 24:69–76

    Article  PubMed  Google Scholar 

  89. Qi Y, Feng G, Yan W (2012) Mesenchymal stem cell-based treatment for cartilage defects in osteoarthritis. Mol Biol Rep 39:5683–5689

    Article  PubMed  CAS  Google Scholar 

  90. Oshima S, Ishikawa M, Mochizuki Y, Kobayashi T, Yasunaga Y, Ochi M (2010) Enhancement of bone formation in an experimental bony defect using ferumoxide-labelled mesenchymal stromal cells and a magnetic targeting system. J Bone Joint Surg Br 92:1606–1613

    Article  PubMed  CAS  Google Scholar 

  91. Daldrup-Link HE, Rudelius M, Piontek G et al (2005) Migration of iron oxide-labeled human hematopoietic progenitor cells in a mouse model: in vivo monitoring with 1.5-T MR imaging equipment. Radiology 234:197–205

    Article  PubMed  Google Scholar 

  92. Amsalem Y, Mardor Y, Feinberg MS et al (2007) Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116:I38–I45

    Article  PubMed  CAS  Google Scholar 

  93. Pawelczyk E, Jordan EK, Balakumaran A et al (2009) In vivo transfer of intracellular labels from locally implanted bone marrow stromal cells to resident tissue macrophages. PLoS One 4:e6712

    Article  PubMed  CAS  Google Scholar 

  94. Kyrtatos PG, Lehtolainen P, Junemann-Ramirez M et al (2009) Magnetic tagging increases delivery of circulating progenitors in vascular injury. JACC Cardiovasc Interv 2:794–802

    Article  PubMed  Google Scholar 

  95. Lubbe AS, Alexiou C, Bergemann C (2001) Clinical applications of magnetic drug targeting. J Surg Res 95:200–206

    Article  PubMed  CAS  Google Scholar 

  96. Pislaru SV, Harbuzariu A, Gulati R et al (2006) Magnetically targeted endothelial cell localization in stented vessels. J Am Coll Cardiol 48:1839–1845

    Article  PubMed  CAS  Google Scholar 

  97. Polyak B, Fishbein I, Chorny M et al (2008) High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc Natl Acad Sci USA 105:698–703

    Article  PubMed  CAS  Google Scholar 

  98. Arbab AS, Jordan EK, Wilson LB, Yocum GT, Lewis BK, Frank JA (2004) In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum Gene Ther 15:351–360

    Article  PubMed  CAS  Google Scholar 

  99. Chen H, Kaminski MD, Pytel P, Macdonald L, Rosengart AJ (2008) Capture of magnetic carriers within large arteries using external magnetic fields. J Drug Target 16:262–268

    Article  PubMed  CAS  Google Scholar 

  100. Galanzha EI, Shashkov EV, Kelly T, Kim JW, Yang L, Zharov VP (2009) In vivo magnetic enrichment and multiplex photoacoustic detection of circulating tumour cells. Nat Nanotechnol 4:855–860

    Article  PubMed  CAS  Google Scholar 

  101. Sugioka T, Ochi M, Yasunaga Y, Adachi N, Yanada S (2008) Accumulation of magnetically labeled rat mesenchymal stem cells using an external magnetic force, and their potential for bone regeneration. J Biomed Mater Res A 85:597–604

    PubMed  Google Scholar 

  102. Yanai A, Hafeli UO, Metcalfe AL et al (2012) Focused magnetic stem cell targeting to the retina using superparamagnetic iron oxide nanoparticles. Cell Transplant 21(6):1137–1148

    Article  PubMed  Google Scholar 

  103. Riegler J, Wells JA, Kyrtatos PG, Price AN, Pankhurst QA, Lythgoe MF (2010) Targeted magnetic delivery and tracking of cells using a magnetic resonance imaging system. Biomaterials 31:5366–5371

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The project was supported by the Science Technology Program of Zhejiang Province (2008C13025); the Natural Science Foundation of China (81071259, 81271356) and the Natural Science Grants of Zhejiang Province (Y2090283, LZ12H16002).

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All authors have no conflicts of interest.

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Correspondence to Weiqi Yan.

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Qi, Y., Feng, G., Huang, Z. et al. The application of super paramagnetic iron oxide-labeled mesenchymal stem cells in cell-based therapy. Mol Biol Rep 40, 2733–2740 (2013). https://doi.org/10.1007/s11033-012-2364-7

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