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

Molecular Biology Reports

Volumn 40, Issue 3, 2013, Pages 2733-2740

  Qi, Yiying ^a   Feng, Gang ^a   Huang, Zhongming ^a   Yan, Weiqi ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Label; Magnetic resonance imaging (MRI); Mesenchymal stem cells (MSCs); Super paramagnetic iron oxide (SPIO); Target

Indexed keywords

COLLAGEN GEL; FERUCARBOTRAN; GELATIN SPONGE; LIPOSOME; MAGNETIC NANOPARTICLE; RECOMBINANT BONE MORPHOGENETIC PROTEIN 2; SUPERPARAMAGNETIC IRON OXIDE; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; BONE DEFECT; CELL DIFFERENTIATION; CELL LABELING; CELL SEEDING; CELL TRACKING; CELL VIABILITY; CHONDROGENESIS; CHONDROPATHY; HEART INFARCTION; HEMATOPOIETIC STEM CELL; HUMAN; MAGNETIC FIELD; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES CONCERNING CELLS; SPINAL CORD INJURY; TISSUE REGENERATION;

ANIMALS; CELL CULTURE TECHNIQUES; CELL TRACKING; CELL- AND TISSUE-BASED THERAPY; FERRIC COMPOUNDS; HUMANS; MAGNETIC FIELDS; MAGNETITE NANOPARTICLES; MESENCHYMAL STROMAL CELLS; STAINING AND LABELING;

EID: 84878403427     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-012-2364-7     Document Type: Article

References (103)

1. Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147
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
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
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
5. Stamm C, Westphal B, Kleine HD et al (2003) Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet 361:45-46
6. Kaminski A, Steinhoff G (2008) Current status of intramyocardial bone marrow stem cell transplantation. Semin Thorac Cardiovasc Surg 20:119-125
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
8. Abdallah BM, Kassem M (2008) Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther 15:109-116
9. Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36:568-584
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
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
12. Singh JP (2009) Enabling technologies for homing and engraftment of cells for therapeutic applications. JACC Cardiovasc Interv 2:803-804
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
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
15. 4/acrylate co-polymer nanocomposites as potential drug carriers. Drug Deliv 15:177-183
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
17. Latorre M, Rinaldi C (2009) Applications of magnetic nanoparticles in medicine: magnetic fluid hyperthermia. P R Health Sci J 28:227-238
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
19. Hill JM, Dick AJ, Raman VK et al (2003) Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 108:1009-1014
20. Tanimoto A, Kuribayashi S (2006) Application of superparamagnetic iron oxide to imaging of hepatocellular carcinoma. Eur J Radiol 58:200-216
21. Weissleder R, Stark DD, Engelstad BL et al (1989) Superparamagnetic iron oxide: pharmacokinetics and toxicity. AJR Am J Roentgenol 152:167-173
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
68. Vunjak-Novakovic G, Radisic M (2004) Cell seeding of polymer scaffolds. Methods Mol Biol 238:131-146
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
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
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
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
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
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
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
76. Bulte JW, Kraitchman DL (2004) Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 17:484-499
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
78. Unger EC (2003) How can superparamagnetic iron oxides be used to monitor disease and treatment? Radiology 229:615-616
79. Thorek DL, Chen AK, Czupryna J, Tsourkas A (2006) Superparamagnetic iron oxide nanoparticle probes for molecular imaging. Ann Biomed Eng 34:23-38
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
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
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
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
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
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
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
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
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
89. Qi Y, Feng G, Yan W (2012) Mesenchymal stem cell-based treatment for cartilage defects in osteoarthritis. Mol Biol Rep 39:5683-5689
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
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
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
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
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
95. Lubbe AS, Alexiou C, Bergemann C (2001) Clinical applications of magnetic drug targeting. J Surg Res 95:200-206
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
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
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
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
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
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
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
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