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Characterization of Biophysical and Metabolic Properties of Cells Labeled with Superparamagnetic Iron Oxide Nanoparticles and Transfection Agent for Cellular MR Imaging¹

¹ From the Experimental Neuroimaging Section, Laboratory of Diagnostic Radiology Research, National Institutes of Health, 10 Center Dr, Rm B1N256, Bethesda, MD 20892. Received September 23, 2002; revision requested December 3; final revision received February 14, 2003; accepted March 12. Address correspondence to A.S.A. (e-mail: saali@cc.nih.gov).

View larger version (147K): [in a new window]   Figure 1. Photomicrophraphs of diaminobenzide-enhanced Prussian blue-stained labeled HeLa (A) and mesenchymal stem (B) cells and nonlabeled HeLa (C) and mesenchymal stem (D) cells. Note the abundant iron particles in the cytoplasm of the cells (brown dots). Approximately 100% of the cells showed uptake of iron particles. The cells were counterstained with nuclear fast red and photographed at a magnification of x20.

View larger version (50K): [in a new window]   Figure 2. A, B, Graphs show results of analysis of apoptotic and dead cells in samples of control (ie, nonlabeled) HeLa (A) and mesenchymal stem (B) cells, conducted with fluorescent-activated cell sorting. C, D, Graphs show results of analysis of apoptotic and dead cells in samples of ferumoxides-PLL complex-labeled HeLa (C) and mesenchymal stem (D) cells, conducted with fluorescent-activated cell sorting. Dead cells show double fluorescence (induced by both propidium iodide and annexin V), and apoptotic cells show single fluorescence (induced by annexin V). On each graph, the fluorescent activity in the right lower quadrant is due to apoptotic cells, and the fluorescent activity in the right upper quadrant is due to dead cells. There is no significant increase in the number of apoptotic or dead labeled HeLa cells, even after 24 days, as compared with the number of apoptotic or dead control HeLa cells.

View larger version (144K): [in a new window]   Figure 3. Photomicrophraphs of diaminobenzide-enhanced Prussian blue-stained HeLa cells show the rapid disappearance of stainable iron particles (brown dots) from the fast growing cells. Findings at day 0 (A), day 7 (B), day 14 (C), and day 21 (D) after labeling with the ferumoxides-PLL complex are shown. The doubling time of the cells was 2.6 days. By five to eight divisions (ie, 14-21 days), no detectable iron particles are observed in the cells. The cells were counterstained with nuclear fast red and photographed at a magnification of x20.

View larger version (53K): [in a new window]   Figure 4. Graphs show values of MR imaging signal intensity at different sequences (A), 1/T2 relaxation rate with different echo times (ie, tau values) (B), iron concentration in the cells (C), and iron concentration in the media (D) for HeLa cells. The signal intensity, 1/T2 relaxation rate, and iron concentration are indicative of the rapid clearance of iron from the cells. The iron seen in the media at day 7 indicates that there was some iron release either during cell division or due to exocytosis. In A, GRE = gradient-echo MR imaging, PDWI = proton-density-weighted imaging, T1WI = T1-weighted MR imaging, T2WI = T2-weighted MR imaging. In B, Tau 1 = echo time of 1,000 msec, Tau 3 = echo time of 3,000 msec, Tau 5 = echo time of 5,000 msec. In C, # = significant differences (P < .05) from values at other time points except day 0. In C and D, * = significant differences (P < .001) from values at other time points.

View larger version (136K): [in a new window]   Figure 5. Photomicrophraphs of Prussian blue-stained mesenchymal stem cells show the retention of stainable (Prussian blue) iron particles (blue to dark-blue dots) in the confluent growth-inhibited cells. Findings at day 0 (A), day 13 (B), day 27 (C), and day 44 (D) after labeling with the ferumoxides-PLL complex are shown. The cells were counterstained with nuclear fast red and photographed at a magnification of x20.

View larger version (40K): [in a new window]   Figure 6. Graphs show values of 1/T2 relaxation rate (A), intracellular iron concentration (B), and iron concentration in the media (C) of mesenchymal stem cells at different time points. Note the nonsignificant decreases in 1/T2 relaxation rate and iron concentration in the cells, even after 44 days of labeling. In A, Tau 1 = echo time of 1,000 msec, Tau 3 = echo time of 3,000 msec, Tau 5 = echo time of 5,000 msec. In C, * = significant differences (P < .01) from values at other time points except day 21, # = significant difference (P < .05) from the values for the media of nonlabeled cells.