Detection and quantification of magnetically labeled cells by cellular MRI

European Journal of Radiology

Volumn 70, Issue 2, 2009, Pages 258-264

  Liu, Wei ^a,b   Frank, Joseph A ^b  

^a PHILIPS RESEARCH LABORATORIES   (Netherlands)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Cell labeling; Gadolinium; MRI; Perfluorocarbon; SPIO nanoparticles

Indexed keywords

CELL LABELING; INTRAVENOUS INJECTIONS; LABELED CELLS; MRI; MRI CONTRAST AGENTS; PARAMAGNETIC CONTRASTS; PERFLUOROCARBON; PERFLUOROCARBONS; PRACTICAL ISSUES; SPIO NANOPARTICLES; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES; TARGET TISSUES;

GADOLINIUM; INDUCTIVELY COUPLED PLASMA; IRON OXIDES; LABELING; MEDICAL IMAGING; NANOPARTICLES; SUPERPARAMAGNETISM;

CELL MEMBRANES;

CHELATING AGENT; CLATHRIN; CONTRAST MEDIUM; CRYSTALLIN; FLUOROCARBON; GADOLINIUM; IRON OXIDE; MAGNETITE; NANOPARTICLE; SUPERPARAMAGNETIC IRON OXIDE;

CELL LABELING; CELL THERAPY; CRYSTAL STRUCTURE; ENDOCYTOSIS; FLUORINE NUCLEAR MAGNETIC RESONANCE; MAGNETIC FIELD; NUCLEAR MAGNETIC RESONANCE IMAGING; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; REVIEW; SIGNAL NOISE RATIO; SIGNAL PROCESSING;

CELLS, CULTURED; CONTRAST MEDIA; IMAGE ENHANCEMENT; MAGNETIC RESONANCE IMAGING; MAGNETICS; STAINING AND LABELING;

EID: 67349114615     PISSN: 0720048X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejrad.2008.09.021     Document Type: Review

References (85)

1. Arbab A.S., and Frank J.A. Cellular MRI and its role in stem cell therapy. Regenerative Med 3 (2008) 199-215
2. Arbab A.S., Liu W., and Frank J.A. Cellular magnetic resonance imaging: current status and future prospects. Expert Rev Med Devices 3 (2006) 427-439
3. Bulte J.W., Arbab A.S., Douglas T., et al. Preparation of magnetically labeled cells for cell tracking by magnetic resonance imaging. Methods Enzymol 386 (2004) 275-299
4. Bulte J.W., and Kraitchman D.L. Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 17 (2004) 484-499
5. Modo M., Hoehn M., and Bulte J.W. Cellular MR imaging. Mol Imaging 4 (2005) 143-164
6. Heyn C., Ronald J.A., Ramadan S.S., et al. In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn Reson Med 56 (2006) 1001-1010
7. Walczak P., Zhang J., Gilad A.A., et al. Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 39 (2008) 1569-1574
8. Kim J.K., Kucharczyk W., and Henkelman R.M. Cavernous hemangiomas: dipolar susceptibility artifacts at MR imaging. Radiology 187 (1993) 735-741
9. Yablonskiy D.A., and Haacke E.M. Theory of NMR signal behavior in magnetically inhomogeneous tissues: the static dephasing regime. Magn Reson Med 32 (1994) 749-763
10. Arbab A.S., Jordan E.K., Wilson L.B., et al. In vivo trafficking and targeted delivery of magnetically labeled stem cells. Hum Gene Ther 15 (2004) 351-360
11. Frank J.A., Miller B.R., Arbab A.S., et al. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 228 (2003) 480-487
12. Frank J.A., Zywicke H., Jordan E.K., 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 (2002) S484-S487
13. Anderson S.A., Lee K.K., and Frank J.A. Gadolinium-fullerenol as a paramagnetic contrast agent for cellular imaging. Invest Radiol 41 (2006) 332-338
14. Crich S.G., Biancone L., Cantaluppi V., et al. Improved route for the visualization of stem cells labeled with a Gd-/Eu-Chelate as dual (MRI and fluorescence) agent. Magn Reson Med 51 (2004) 938-944
15. Daldrup-Link H.E., Rudelius M., Metz S., et al. Cell tracking with gadophrin-2: a bifunctional contrast agent for MR imaging, optical imaging, and fluorescence microscopy. Eur J Nucl Med Mol Imaging 31 (2004) 1312-1321
16. Giesel F.L., Stroick M., Griebe M., et al. Gadofluorine m uptake in stem cells as a new magnetic resonance imaging tracking method: an in vitro and in vivo study. Invest Radiol 41 (2006) 868-873
17. Himmelreich U., Aime S., Hieronymus T., et al. A responsive MRI contrast agent to monitor functional cell status. NeuroImage 32 (2006) 1142-1149
18. Modo M., Cash D., Mellodew K., et al. Tracking transplanted stem cell migration using bifunctional, contrast agent-enhanced, magnetic resonance imaging. NeuroImage 17 (2002) 803-811
19. Su W., Mishra R., Pfeuffer J., et al. Synthesis and cellular uptake of a MR contrast agent coupled to an antisense peptide nucleic acid-cell-penetrating peptide conjugate. Magn Reson Med 2 (2007) 42-49
20. Ahrens E.T., Flores R.H.X., et al. In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 23 (2005) 983-987
21. 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J 21 (2007) 1647-1654
22. Srinivas M., Morel P.A., Ernst L.A., et al. Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn Reson Med 58 (2007) 725-734
23. Aime S., Barge A., Cabella C., et al. Targeting cells with MR imaging probes based on paramagnetic Gd(III) chelates. Curr Pharm Biotechnol 5 (2004) 509-518
24. Conner S.D., and Schmid S.L. Regulated portals of entry into the cell. Nature 422 (2003) 37-44
25. Frankline R.J.M., Blaschuk K.L., Bearchell M.C., et al. Magnetic resonance imaging of transplanted oligodendrocyte precursors in the rat brain. Neuroreport 10 (1999) 3961-3965
26. Ho C., and Hitchens T.K. A non-invasive approach to detecting organ rejection by MRI: monitoring the accumulation of immune cells at the transplanted organ. Curr Pharm Biotechnol 5 (2004) 551-566
27. Moore A., Weissleder R., and Bogdanov A.J. Uptake of dextran-coated monocrystalline iron oxides in tumor cells and macrophages. Magn Reson Med 7 (1997) 1140-1145
28. Sipe J.C., Filippi M., Martino G., et al. Method for intracellular magnetic labeling of human mononuclear cells using approved iron contrast agents. Magn Reson Med 17 (1999) 1521-1523
29. Billotey C., Wilhelm C., Devaud M., et al. Cell internalization of anionic maghemite nanoparticles: quantitative effect on magnetic resonance imaging. Magn Reson Med 49 (2003) 646-654
30. Fleige G., Nolte C., Synowitz M., et al. Magnetic labeling of activated microglia in experimental gliomas. Neoplasia 3 (2001) 489-499
31. Fleige G., Seeberger F., Laux D., et al. In vitro characterization of two different ultrasmall iron oxide particles for magnetic resonance cell tracking. Invest Radiol 37 (2002) 482-488
32. Weissleder R., Cheng H.C., Bogdanov A., et al. Magnetically labeled cells can be detected by MR imaging. J Magn Reson Imaging 7 (1997) 258-263
33. Jendelova P., Herynek V., DeCroos J., et al. Imaging the fate of implanted bone marrow stromal cells labeled with superparamagnetic nanoparticles. Magn Reson Med 50 (2003) 767-776
34. Jendelova P., Herynek V., Urdzikova L., et al. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J Neurosci Res 76 (2004) 232-243
35. Jirak D., Kriz J., Herynek V., et al. MRI of transplanted pancreatic islets. Magn Reson Med 52 (2004) 1228-1233
36. Walczak P., Kedziorek D.A., Gilad A.A., et al. Instant MR labeling of stem cells using magnetoelectroporation. Magn Reson Med 54 (2005) 769-774
37. Plank C., Scherer F., Schillinger U., et al. Magnetofection: enhancing and targeting gene delivery with superparamagnetic nanoparticles and magnetic fields. J Liposome Res 13 (2003) 29-32
38. 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 (2002) 102-109
39. Bulte J.W., Douglas T., Witwer B., et al. Magnetodendrimers allow endosomal magnetic labeling and in vivo tracking of stem cells. Nat Biotechnol 19 (2001) 1141-1147
40. Josephson L., Tung C.-H., Moore A., et al. High-efficiency intracellular magnetic labeling with novel superparamagnetic-Tat peptide conjugates. Bioconjugate Chem 10 (1999) 186-191
41. Mills P.H., and Ahrens E.T. Theoretical MRI contrast model for exogenous T2 agents. Magn Reson Med 57 (2007) 442-447
42. Kim D., Hong K.S., and Song J. The present status of cell tracking methods in animal models using magnetic resonance imaging technology. Mol Cells 23 (2007) 132-137
43. Bulte J.W., Zhang S., van Gelderen P., et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc Natl Acad Sci USA 96 (1999) 15256-15261
44. Turetschek K., Huber S., Floyd E., et al. MR imaging characterization of microvessels in experimental breast tumors by using a particulate contrast agent with histopathologic correlation. Radiology 218 (2001) 562-569
45. Turetschek K., Roberts T.P., Floyd E., et al. Tumor microvascular characterization using ultrasmall superparamagnetic iron oxide particles (USPIO) in an experimental breast cancer model. J Magn Reson Imaging 13 (2001) 882-888
46. Bowen C.V., Zhang X., Saab G., et al. Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med 48 (2002) 52-61
47. Heyn C., Bowen C.V., Rutt B.K., et al. Detection threshold of single SPIO-labeled cells with FIESTA. Magn Reson Med 53 (2005) 312-320
48. Lebel R.M., Menon R.S., and Bowen C.V. Relaxometry model of strong dipolar perturbers for balanced-SSFP: application to quantification of SPIO loaded cells. Magn Reson Med 55 (2006) 583-591
49. Anderson S.A., Glod J., Arbab A.S., et al. Noninvasive MR imaging of magnetically labeled stem cells to directly identify neovasculature in a glioma model. Blood 105 (2005) 420-425
50. Himmelreich U., Weber R., Ramos-Cabrer P., et al. Improved stem cell MR detectability in animal models by modification of the inhalation gas. Mol Imaging 4 (2005) 104-109
51. Mills P.H., Wu Y.-J., Ho C., et al. Sensitive and automated detection of iron-oxide-labeled cells using phase image cross-correlation analysis. Magn Reson Imaging 26 (2008) 618-628
52. Cunningham C.H., Arai T., Yang P.C., et al. Positive contrast magnetic resonance imaging of cells labeled with magnetic nanoparticles. Magn Reson Med 53 (2005) 999-1005
53. Dahnke H., Liu W., Frank J.A., et al. Opitmal positive contrast of labeled cells via conventional 3D imaging. Proc Int Soc Magn Reson Med 14 (2006) 361
54. Mani V., Briley-Saebo K.C., Itskovich V.V., et al. Gradient echo acquisition for superparamagnetic particles with positive contrast (GRASP): sequence characterization in membrane and glass superparamagnetic iron oxide phantoms at 1.5 T and 3 T. Magn Reson Med 55 (2006) 126-135
55. Seppenwoolde J.H., Viergever M.A., and Bakker C.J. Passive tracking exploiting local signal conservation: the white marker phenomenon. Magn Reson Med 50 (2003) 784-790
56. Stuber M., Gilson W.D., Schaer M., et al. Positive contrast visualization of iron oxide-labeled stem cells using inversion-recovery with ON-resonant water suppression (IRON). Magn Reson Med 58 (2007) 1072-1077
57. Zurkiya O., and Hu X. Off-resonance saturation as a means of generating contrast with superparamagnetic nanoparticles. Magn Reson Med 56 (2006) 726-732
58. Farrar C.T., Dai G., Novikov M., et al. Impact of field strength and iron oxide nanoparticle concentration on the linearity and diagnostic accuracy of off-resonance imaging. NMR Biomed 21 (2007) 453-463
59. Posse S. Direct imaging of magnetic field gradients by group spin-echo selection. Magn Reson Med 25 (1992) 12-29
60. Reichenbach J.R., Venkatesan R., Yablonskiy D.A., et al. Theory and application of static field inhomogeneity effects in gradient-echo imaging. J Magn Reson Imaging 7 (1997) 266-279
61. Bakker C.J., Seppenwoolde J.H., and Vincken K.L. Dephased MRI Magn Reson Med 55 (2006) 92-97
62. Liu W., Dahnke H., Jordan E.K., et al. In vivo MRI using positive-contrast techniques in detection of cells labeled with superparamagnetic iron oxide nanoparticles. NMR Biomed 21 (2007) 242-250
63. De Vries I.J., Lesterhuis W.J., Barentsz J.O., et al. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 23 (2005) 1407-1413
64. Verdijk P., Scheenen T.W., Lesterhuis W.J., et al. Sensitivity of magnetic resonance imaging of dendritic cells for in vivo tracking of cellular cancer vaccines. Int J Cancer 120 (2007) 978-984
65. Hoehn M., Kustermann E., Blunk J., et al. 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 (2002) 16267-16272
66. Magnitsky S., Watson D.J., Walton R.M., et al. In vivo and ex vivo MRI detection of localized and disseminated neural stem cell grafts in the mouse brain. NeuroImage 26 (2005) 744-754
67. Dahnke H., and Schaeffter T. Limits of detection of SPIO at 3.0 T using T2 relaxometry. Magn Reson Med 53 (2005) 1202-1206
68. Kircher M.F., Allport J.R., Graves E.E., et al. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res 63 (2003) 6838-6846
69. Foster-Gareau P., Heyn C., Alejski A., et al. Imaging single mammalian cells with a 1.5 T clinical MRI scanner. Magn Reson Med 49 (2003) 968-971
70. Bulte J.W., Miller G.F., Vymazal J., et al. Hepatic hemosiderosis in non-human primates: quantification of liver iron using different field strengths. Magn Reson Imaging 37 (1997) 530-536
71. Rad A.M., Arbab A.S., Iskander A.S., et al. Quantification of superparamagnetic iron oxide (SPIO)-labeled cells using MRI. J Magn Reson Imaging 26 (2007) 366-374
72. Bos C., Delmas Y., Desmouliere A., et al. In vivo MR imaging of intravascularly injected magnetically labeled mesenchymal stem cells in rat kidney and liver. Radiology 233 (2004) 781-789
73. Politi L.S., Bacigaluppi M., Brambilla E., et al. Magnetic-resonance-based tracking and quantification of intravenously injected neural stem cell accumulation in the brains of mice with experimental multiple sclerosis. Stem Cells 25 (2007) 2583-2592
74. Young I.R., Cox I.J., Bryant D.J., et al. The benefits of increasing spatial resolution as a means of reducing artifacts due to field inhomogeneities. Magn Reson Imaging 6 (1988) 585-590
75. Frahm J., Merboldt K.D., and Hanicke W. Direct FLASH MR imaging of magnetic field inhomogeneities by gradient compensation. Magn Reson Med 6 (1988) 474-480
76. Kuhlpeter R., Dahnke H., Matuszewski L., et al. R2 and R2* mapping for sensing cell-bound superparamagnetic nanoparticles: in vitro and murine in vivo testing. Radiology 245 (2007) 449-457
77. Walczak P., Kedziorek D.A., Gilad A.A., et al. Applicability and limitations of MR tracking of neural stem cells with asymmetric cell division and rapid turnover: the case of the Shiverer dysmyelinated mouse brain. Magn Reson Imaging 58 (2007) 261-269
78. Terrovitis J., Stuber M., Youssef A., et al. Magnetic resonance imaging overestimates ferumoxide-labeled stem cell survival after transplantation in the heart. Circulation 117 (2008) 1555-1562
79. Pawelczyk E., Arbab A.S., Chaudhry A., et al. In vitro model of Brdu or iron oxide nanoparticle uptake by activated macrophages from labeled stem cells: implications for cellular therapy. Stem Cells 26 (2008) 1366-1375
80. Mikawa M., Kato H., Okumura M., et al. Paramagnetic water-soluble metallofullerenes having the highest relaxivity for MRI contrast agents. Bioconjugate Chem 12 (2001) 510-514
81. Brekke C., Morgan S.C., Lowe A.S., et al. The in vitro effects of a bimodal contrast agent on cellular functions and relaxometry. NMR Biomed 20 (2007) 77-89
82. Aime S., Dastru W., Crich S.G., et al. Innovative magnetic resonance imaging diagnostic agents based on paramagnetic Gd(III) complexes. Biopolymers 66 (2002) 419-428
83. Daldrup-Link H.E., Rudelius M., Oostendorp R.A., et al. Targeting of hematopoietic progenitor cells with MR contrast agents. Radiology 228 (2003) 760-767
84. Granot D., Addadi Y., Kalchenko V., et al. In vivo imaging of the systemic recruitment of fibroblasts to the angiogenic rim of ovarian carcinoma tumors. Cancer Res 67 (2007) 9180-9189
85. Haacke E.M., Xu Y., Cheng Y.C., et al. Susceptibility weighted imaging (SWI). Magn Reson Imaging 52 (2004) 612-618