Abstract
Stem cells transplantation is a promising therapy for numerous diseases where transplanted cells repair or replace damaged host tissue. While their efficacy and optimal delivery is under intense investigation, there lies a pivotal question seeking the whereabouts of the cells after transplantation. Imaging techniques have emerged in recent years, both to enable monitoring of stem cell location in patients and to improve the reliability of animal experimentation. Magnetic resonance imaging (MRI) allows tracking of stem cells tagged with magnetic nanoparticle labels prior to transplantation, but is restricted by the inability of stem cells to incorporate sufficient label. This review addresses the optimisation of stem cell tagging with iron oxide particles to improve MR tracking, alternative cell labelling techniques using gene transfer, and the translational applications of cellular imaging.
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Abbreviations
- MRI:
-
magnetic resonance imaging
- ESC:
-
embryonic stem cells
- MSC:
-
mesenchymal stem cells
- Gd-DTPA:
-
gadolinium diethylenetriaminopentaacetic acid
- SPIO:
-
superparamagnetic iron oxide particles
- USPIO:
-
ultrasmall SPIO
- MION:
-
monocrystalline iron oxide nanocompound
- VSOP:
-
very small superparamagnetic iron oxide particles
- AMNP:
-
anionic magnetic nanoparticle
- IV:
-
intravenously
- CLIO:
-
cross-linked iron oxide particles
- Ab:
-
antibody
- MGIO:
-
microgel iron oxide particles
- EPC:
-
endothelial progenitor cells
- PLL:
-
poly-L-lysine
- Tf:
-
transferrin
- TfR:
-
transferrin receptor
- NSC:
-
neural stem cells
- DC:
-
dendritic cells
- CGMP:
-
clinical grade manufacturing practice
- BrdU:
-
5-bromo-2-deoxyuridine
- BBZ:
-
bis benzamide
- SDR:
-
static dephasing regime
References
Ahrens, E. T., Feili-Hariri, M., Xu, H., Genove, G. & Morel, P. A. 2003. Receptor-mediated endocytosis of iron-oxide particles provides efficient labeling of dendritic cells for in vivo MR imaging. Magnetic Resonance in Medicine, 49, 1006–1013.
Aigner, F., Pallwein, L., Mitterberger, M., Pinggera, G. M., Mikuz, G., Horninger, W. & Frauscher, F. 2009. Contrast-enhanced ultrasonography using cadence-contrast pulse sequencing technology for targeted biopsy of the prostate. BJU International, 103, 458–463.
Anderson, S. A., Glod, J., Arbab, A. S., Noel, M., Ashari, P., Fine, H. A. & Frank, J. A. 2005. Noninvasive MR imaging of magnetically labeled stem cells to directly identify neovasculature in a glioma model. Blood, 105, 420–5.
Arbab, A. S., Bashaw, L. A., Miller, B. R., Jordan, E. K., Bulte, J. W. & Frank, J. A. 2003a. Intracytoplasmic tagging of cells with ferumoxides and transfection agent for cellular magnetic resonance imaging after cell transplantation: methods and techniques. Transplantation, 76, 1123–1130.
Arbab, A. S., Bashaw, L. A., Miller, B. R., Jordan, E. K., Lewis, B. K., Kalish, H. & Frank, J. A. 2003b. 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.
Arbab, A. S. & Frank, J. A. 2008. Cellular MRI and its role in stem cell therapy. Regen Med, 3, 199–215.
Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J. & Frank, J. A. 2004a. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood, 104, 1217–1223.
Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J. & Frank, J. A. 2004b. Feridex-protamine sulfate labeling does not alter differentiation of mesenchymal stem cells. Blood, 104, 3412–3413.
Balakumaran, A., Pawelczyk, E., Ren, J., Sworder, B., Chaudhry, A., Sabatino, M., Stroncek, D., Frank, J. A. & Robey, P. G. 2010. Superparamagnetic Iron Oxide Nanoparticles Labeling of Bone Marrow Stromal (Mesenchymal) Cells Does Not Affect Their “Stemness”. PLoS One, 5, e11462.
Bang, O. Y., Lee, J. S., Lee, P. H. & Lee, G. 2005. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol, 57, 874–82.
Bazylinski, D. A. & Frankel, R. B. 2004. Magnetosome formation in prokaryotes. Nat Rev Microbiol, 2, 217–30.
Bendszus, M., Kleinschnitz, C. & Stoll, G. 2007. Iron-Enhanced MRI in Ischemic Stroke: Intravascular Trapping Versus Cellular Inflammation. Stroke, 38, e12.
Bennett, K. M., Shapiro, E. M., Sotak, C. H. & Koretsky, A. P. 2008. Controlled Aggregation of Ferritin to Modulate MRI Relaxivity. Biophys. J., 95, 342–351.
Berry, C. C., Charles, S., Wells, S., Dalby, M. J. & Curtis, A. S. 2004. The influence of transferrin stabilised magnetic nanoparticles on human dermal fibroblasts in culture. International Journal of Pharmaceutics, 269, 211–225.
Bowen, C. V., Zhang, X., Saab, G., Gareau, P. J. & Rutt, B. K. 2002. Application of the static dephasing regime theory to superparamagnetic iron-oxide loaded cells. Magn Reson Med, 48, 52–61.
Bulte, J. W. & Kraitchman, D. L. 2004. Monitoring cell therapy using iron oxide MR contrast agents. Curr Pharm Biotechnol, 5, 567–584.
Bulte, J. W., Kraitchman, D. L., Mackay, A. M., Pittenger, M. F., Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J. & Frank, J. A. 2004. Chondrogenic differentiation of mesenchymal stem cells is inhibited after magnetic labeling with ferumoxides. Blood, 104, 3410–3413.
Burns, T. C., Ortiz-Gonzalez, X. R., Gutierrez-Perez, M., Keene, C. D., Sharda, R., Demorest, Z. L., Jiang, Y., Nelson-Holte, M., Soriano, M. & Nakagawa, Y. 2006. Thymidine Analogs Are Transferred from Prelabeled Donor to Host Cells in the Central Nervous System After Transplantation: A Word of Caution. Stem Cells, 24, 1121–1127.
Callera, F. & De Melo, C. M. 2007. Magnetic Resonance Tracking of Magnetically Labeled Autologous Bone Marrow CD34+ Cells Transplanted into the Spinal Cord via Lumbar Puncture Technique in Patients with Chronic Spinal Cord Injury: CD34+ Cells’ Migration into the Injured Site. Stem Cells and Development, 16, 461–466.
Cao, F., Lin, S., Xie, X., Ray, P., Patel, M., Zhang, X., Drukker, M., Dylla, S. J., Connolly, A. J. & Chen, X. 2006. In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation, 113, 1005–14.
Carr, D. H., Brown, J., Bydder, G. M., Steiner, R. E., Weinmann, H. J., Speck, U., Hall, A. S. & Young, I. R. 1984. Gadolinium-DTPA as a contrast agent in MRI: initial clinical experience in 20 patients. American Journal of Roentgenology, 143, 215–224.
Chen, A., Siow, B., Blamire, A. M., Lako, M. & Clowry, G. J. 2010. Transplantation of magnetically labeled mesenchymal stem cells in a model of perinatal brain injury. Stem Cell Research, 5, 255–266.
Cohen, B., Dafni, H., Meir, G., Harmelin, A. & Neeman, M. 2005. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia, 7, 109–17.
Cohen, B., Ziv, K., Plaks, V., Israely, T., Kalchenko, V., Harmelin, A., Benjamin, L. E. & Neeman, M. 2007. MRI detection of transcriptional regulation of gene expression in transgenic mice. Nat Med, 13, 498–503.
Coyne, T. M., Marcus, A. J., Woodbury, D. & Black, I. B. 2006. Marrow stromal cells transplanted to the adult brain are rejected by an inflammatory response and transfer donor labels to host neurons and glia. Stem Cells, 24, 2483–92.
Cozzi, A., Corsi, B., Levi, S., Santambrogio, P., Albertini, A. & Arosio, P. 2000. Overexpression of Wild Type and Mutated Human Ferritin H-chain in HeLa Cells IN VIVO ROLE OF FERRITIN FERROXIDASE ACTIVITY. Journal of Biological Chemistry, 275, 25122–25129.
Dahnke, H. & Schaeffter, T. 2005. Limits of detection of SPIO at 3.0 T using T2 relaxometry. Magn Reson Med, 53, 1202–6.
Daldrup-Link, H. E., Rudelius, M., Oostendorp, R. A., Jacobs, V. R., Simon, G. H., Gooding, C. & Rummeny, E. J. 2005. Comparison of iron oxide labeling properties of hematopoietic progenitor cells from umbilical cord blood and from peripheral blood for subsequent in vivo tracking in a xenotransplant mouse model XXX1. Academic Radiology, 12, 502–510.
Daldrup-Link, H. E., Rudelius, M., Oostendorp, R. A., Settles, M., Piontek, G., Metz, S., Rosenbrock, H., Keller, U., Heinzmann, U. & Rummeny, E. J. 2003. Targeting of hematopoietic progenitor cells with MR contrast agents. Radiology, 228, 760–7.
De Vries, I., Lesterhuis, W. J., Barentsz, J. O., Verdijk, P., Van, K. J., Boerman, O. C., Oyen, W. J., Bonenkamp, J. J., Boezeman, J. B. & Adema, G. J. 2005. Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol, 23, 1407–1413.
Deans, A. E., Wadghiri, Y. Z., Bernas, L. M., Yu, X., Rutt, B. K. & Turnbull, D. H. 2006. Cellular MRI contrast via coexpression of transferrin receptor and ferritin. Magn Reson Med, 56, 51–9.
Di Marco, M., Sadun, C., Port, M., Guilbert, I., Couvreur, P. & Dubernet, C. 2007. Physicochemical characterization of ultrasmall superparamagnetic iron oxide particles (USPIO) for biomedical application as MRI contrast agents. Int J Nanomedicine, 2, 609–622.
Fleige, G., Seeberger, F., Laux, D., Kresse, M., Taupitz, M., Pilgrimm, H. & Zimmer, C. 2002. In vitro characterization of two different ultrasmall iron oxide particles for magnetic resonance cell tracking. Invest Radiol, 37, 482–8.
Fontaine, R., Viscogliosi, N., Semmaoui, H., B, F., Lemieux, F., T, M. A., Michaud, J. B., B, P., Cadorette, J. & Pepin, C. M. 2007. Digital signal processing applied to crystal identification in Positron Emission Tomography dedicated to small animals. Nuclear Inst. and Methods in Physics Research, A, 571, 385–388.
Frank, J. A., Miller, B. R., Arbab, A. S., Zywicke, H. A., Jordan, E. K., Lewis, B. K., Bryant, L. H. & Bulte, J. W. 2003. Clinically Applicable Labeling of Mammalian and Stem Cells by Combining Superparamagnetic Iron Oxides and Transfection Agents. Radiology, 228, 480–487.
Gafni, Y., Turgeman, G., Liebergal, M., Pelled, G., Gazit, Z. & Gazit, D. 2004. Stem cells as vehicles for orthopedic gene therapy. Gene Ther, 11, 417–26.
Gao, F., Kar, S., Zhang, J., Qiu, B., Walczak, P., Larabi, M., Xue, R., Frost, E., Qian, Z. & Bulte, J. W. 2007. MRI of intravenously injected bone marrow cells homing to the site of injured arteries. NMR Biomed, 20, 673–81.
Ghosh, P., Hawrylak, N., Broadus, J., Greenough, W. T. & Lauterbur, P. C. Year. NMR imaging of transplanted iron oxide-labelled cells in the rat brain. In, 1990. 1193.
Gilad, A. A., Van Laarhoven, H. W. M., Mcmahon, M. T., Walczak, P., Heerschap, A., Neeman, M., Van Zijl, P. C. M. & Bulte, J. W. M. 2009. Feasibility of concurrent dual contrast enhancement using CEST contrast agents and superparamagnetic iron oxide particles. Magnetic Resonance in Medicine, 61, 970–974.
Gonzalez-Lara, L., Xu, X., Hofstetrova, K., Pniak, A., Chen, Y., Mcfadden, C., Martinez-Santiesteban, F., Rutt, B., Brown, A. & Foster, P. 2010. The Use of Cellular Magnetic Resonance Imaging to Track the Fate of Iron-Labeled Multipotent Stromal Cells after Direct Transplantation in a Mouse Model of Spinal Cord Injury. Molecular Imaging and Biology, 1–10.
Gossuin, Y., Roch, A., Muller, R. N. & Gillis, P. 2000. Relaxation induced by ferritin and ferritin-like magnetic particles: The role of proton exchange. Magnetic Resonance in Medicine, 43, 237–243.
Grabill, C., Silva, A. C., Smith, S. S., Koretsky, A. P. & Rouault, T. A. 2003. MRI detection of ferritin iron overload and associated neuronal pathology in iron regulatory protein-2 knockout mice. Brain Research, 971, 95–106.
Guzman, R., Uchida, N., Bliss, T. M., He, D., Christopherson, K. K., Stellwagen, D., Capela, A., Greve, J., Malenka, R. C., Moseley, M. E., Palmer, T. D. & Steinberg, G. K. 2007. Long-term monitoring of transplanted human neural stem cells in developmental and pathological contexts with MRI. Proc Natl Acad Sci USA, 104, 10211–6.
Harrison, P. M. & Arosio, P. 1996. The ferritins: molecular properties, iron storage function and cellular regulation. BBA-Bioenergetics, 1275, 161–203.
Harush-Frenkel, O., Debotton, N., Benita, S. & Altschuler, Y. 2007. Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochemical and Biophysical Research Communications, 353, 26–32.
Heyn, C., Bowen, C. V., Rutt, B. K. & Foster, P. J. 2005. Detection threshold of single SPIO-labeled cells with FIESTA. Magn Reson Med, 53, 312–20.
Heyn, C., Ronald, J. A., Mackenzie, L. T., Macdonald, I. C., Chambers, A. F., Rutt, B. K. & Foster, P. J. 2006. In Vivo Magnetic Resonance Imaging of Single Cells in Mouse Brain with Optical Validation. Magn Reson Med, 55, 23.
Hill, J. M., Dick, A. J., Raman, V. K., Thompson, R. B., Yu, Z. X., Hinds, K. A., Pessanha, B. S., Guttman, M. A., Varney, T. R. & Martin, B. J. 2003. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation, 108, 1009.
Himmelreich, U., Weber, R., Ramos-Cabrer, P., Wegener, S., Kandal, K., Shapiro, E. M., Koretsky, A. P. & Hoehn, M. 2005. Improved stem cell MR detectability in animal models by modification of the inhalation gas. Mol Imaging, 4, 104–9.
Hoehn, M., Kustermann, E., Blunk, J., Wiedermann, D., Trapp, T., Wecker, S., Focking, M., Arnold, H., Hescheler, J. & Fleischmann, B. K. 2002. Monitoring of implanted stem cell migration in vivo: A highly resolved in vivo magnetic resonance imaging investigation of experimental stroke in rat. Proceedings of the National Academy of Sciences, 99, 16267–16272.
Horwitz, E. M., Prockop, D. J., Gordon, P. L., Koo, W. W., Fitzpatrick, L. A., Neel, M. D., Mccarville, M. E., Orchard, P. J., Pyeritz, R. E. & Brenner, M. K. 2001. Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood, 97, 1227–31.
Hunter, R. J. 1995. Foundations of colloid science, Oxford, Clarendon Press.
Jendelova, P., Herynek, V., Decroos, J., Glogarova, K., Andersson, B., Hajek, M. & Sykova, E. 2003. Imaging the fate of implanted bone marrow stromal cells labeled with superparamagnetic nanoparticles. Magn Reson Med, 50, 767–76.
Jung, C. W. 1995. Surface properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magnetic Resonance Imaging, 13, 675–691.
Jung, C. W. & Jacobs, P. 1995. Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: Ferumoxides, ferumoxtran, ferumoxsil. Magnetic Resonance Imaging, 13, 661–674.
Kadayakkara, D. K. K., Janjic, J. M., Pusateri, L. K., Young, W.-B. & Ahrens, E. T. 2010. In vivo observation of intracellular oximetry in perfluorocarbon-labeled glioma cells and chemotherapeutic response in the CNS using fluorine-19 MRI. Magnetic Resonance in Medicine, 64, 1252–1259.
Kawaguchi, H., Koiwai, N., Ohtsuka, Y., Miyamoto, M. & Sasakawa, S. 1986. Phagocytosis of latex particles by leucocytes. I. Dependence of phagocytosis on the size and surface potential of particles. Biomaterials, 7, 61–66.
Kim, H.-S. Year. Comparison of the Biological Properties of Human Mesenchymal Stem Cells Labeled with Different Iron Oxide Nanoparticles. In, 2008 Nice, France. Poster No. 1071
Kleinschnitz, C., Bendszus, M., Frank, M., Solymosi, L., Toyka, K. V. & Stoll, G. 2003. In Vivo Monitoring of Macrophage Infiltration in Experimental Ischemic Brain Lesions by Magnetic Resonance Imaging. Journal of Cerebral Blood Flow & Metabolism, 23, 1356–1361.
Kleinschnitz, C., Sch, A., N, I., Horn, T., Frank, M., Solymosi, L., Stoll, G. & Bendszus, M. 2005. In vivo detection of developing vessel occlusion in photothrombotic ischemic brain lesions in the rat by iron particle enhanced MRI. Journal of Cerebral Blood Flow & Metabolism, 25, 1548–1555
Ko, I. K., Song, H. T., Cho, E. J., Lee, E. S., Huh, Y. M. & Suh, J. S. 2007. In vivo MR imaging of tissue-engineered human mesenchymal stem cells transplanted to mouse: a preliminary study. Ann Biomed Eng, 35, 101–8.
Kooi, M. E., Cappendijk, V. C., Cleutjens, K., Kessels, A. G., Kitslaar, P., Borgers, M., Frederik, P. M., Daemen, M. & Van, E. J. 2003. Accumulation of Ultrasmall Superparamagnetic Particles of Iron Oxide in Human Atherosclerotic Plaques Can Be Detected by In Vivo Magnetic Resonance Imaging. Am Heart Assoc
Kostura, L., Kraitchman, D. L., Mackay, A. M., Pittenger, M. F. & Bulte, J. W. 2004. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR in Biomedicine, 17, 513–517.
Kraitchman, D. L., Heldman, A. W., Atalar, E., Amado, L. C., Martin, B. J., Pittenger, M. F., Hare, J. M. & Bulte, J. W. 2003. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation, 107, 2290–3.
Kraitchman, D. L., Tatsumi, M., Gilson, W. D., Ishimori, T., Kedziorek, D., Walczak, P., Segars, W. P., Chen, H. H., Fritzges, D. & Izbudak, I. 2005. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation, 112, 1451–61.
Lai, E. & Van Zanten, J. H. 2001. Monitoring DNA/Poly-l-Lysine Polyplex Formation with Time-Resolved Multiangle Laser Light Scattering. Biophysical Journal, 80, 864–873.
Lee, E. S., Bou-Gharios, G., Seppanen, E., Khosrotehrani, K. & Fisk, N. M. 2010a. Fetal Stem Cell Microchimerism: Natural Born Healers or Killers? Molecular Human Reproduction, [Epub ahead of print].
Lee, E. S., Chan, J., Shuter, B., Tan, L. G., Chong, M. S. K., Ramachandra, D. L., Dawe, G. S., Ding, J., Teoh, S. H., Beuf, O., Briguet, A., Tam, K. C., Choolani, M. & Wang, S.-C. 2009. Microgel Iron Oxide Nanoparticles For Tracking Human Fetal Mesenchymal Stem Cells Through Magnetic Resonance Imaging. Stem Cells, 27, 1921–1931.
Lee, E. S., Shuter, B., Chan, J., Chong, M. S. K., Ding, J., Teoh, S.-H., Beuf, O., Briguet, A., Tam, K. C., Choolani, M. & Wang, S.-C. 2010b. The use of microgel iron oxide nanoparticles in studies of magnetic resonance relaxation and endothelial progenitor cell labelling. Biomaterials, 31, 3296–3306.
Lee, H., Lee, E., Kim, K., Jang, N. K., Jeong, Y. Y. & Jon, S. 2006. Antibiofouling polymer-coated superparamagnetic iron oxide nanoparticles as potential magnetic resonance contrast agents for in vivo cancer imaging. J Am Chem Soc, 128, 7383–9.
Lewin, M., Carlesso, N., Tung, C. H., Tang, X. W., Cory, D., Scadden, D. T. & Weissleder, R. 2000. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nature biotechnology, 18, 410–414.
Liu, G., Molas, M., Grossmann, G. A., Pasumarthy, M., Perales, J. C., Cooper, M. J. & Hanson, R. W. 2001. Biological Properties of Poly-l-lysine-DNA Complexes Generated by Cooperative Binding of the Polycation. Journal of Biological Chemistry, 276, 34379–34387.
Mailander, V., Lorenz, M. R., Holzapfel, V., Musyanovych, A., Fuchs, K., Wiesneth, M., Walther, P., Landfester, K. & Schrezenmeier, H. 2008. Carboxylated Superparamagnetic Iron Oxide Particles Label Cells Intracellularly Without Transfection Agents. Molecular Imaging and Biology, 10, 138–146.
Matuszewski, L., Persigehl, T., Wall, A., Schwindt, W., Tombach, B., Fobker, M., Poremba, C., Ebert, W., Heindel, W. & Bremer, C. 2005. Cell Tagging with Clinically Approved Iron Oxides: Feasibility and Effect of Lipofection, Particle Size, and Surface Coating on Labeling Efficiency. Radiology, 235, 155–161.
Mendonca, D. M. & Lauterbur, P. C. 1986. Ferromagnetic particles as contrast agents for magnetic resonance imaging of liver and spleen. Magnetic resonance in medicine: official journal of the Society of Magnetic Resonance in Medicine/Society of Magnetic Resonance in Medicine, 3, 328–330.
Metz, S., Bonaterra, G., Rudelius, M., Settles, M., Rummeny, E. J. & Daldrup-Link, H. E. 2004. Capacity of human monocytes to phagocytose approved iron oxide MR contrast agents in vitro. Eur Radiol, 14, 1851–8.
Meyer, G. P., Wollert, K. C., Lotz, J., Steffens, J., Lippolt, P., Fichtner, S., Hecker, H., Schaefer, A., Arseniev, L., Hertenstein, B., Ganser, A. & Drexler, H. 2006. Intracoronary Bone Marrow Cell Transfer After Myocardial Infarction: Eighteen Months’ Follow-Up Data From the Randomized, Controlled BOOST (BOne marrOw transfer to enhance ST-elevation infarct regeneration) Trial. Circulation, 113, 1287–1294.
Mills, P. H., Wu, Y. J., Ho, C. & Ahrens, E. T. 2008. Sensitive and automated detection of iron-oxide-labeled cells using phase image cross-correlation analysis. Magnetic Resonance Imaging
Modo, M., Cash, D., Mellodew, K., Williams, S. C., Fraser, S. E., Meade, T. J., Price, J. & Hodges, H. 2002. Tracking transplanted stem cell migration using bifunctional, contrast agent-enhanced, magnetic resonance imaging. Neuroimage, 17, 803–11.
Montet-Abou, K., Montet, X., Weissleder, R. & Josephson, L. 2007. Cell internalization of magnetic nanoparticles using transfection agents. Mol Imaging, 6, 1–9.
Moore, A., Josephson, L., Bhorade, R. M., Basilion, J. P. & Weissleder, R. 2001. Human transferrin receptor gene as a marker gene for MR imaging. Radiology, 221, 244–50.
Moore, A., Weissleder, R. & Bogdanov, A. 1997. Uptake of Dextran-Coated Monocrystalline Iron Oxides in Tumor Cells and Macrophages. Journal of Magnetic Resonance Imaging, 7, 1140–1145.
Nath, N., Hyun, J., Ma, H. & Chilkoti, A. 2004. Surface engineering strategies for control of protein and cell interactions. Surface Science, 570, 98–110.
Nelson, G. N., Roh, J. D., Mirensky, T. L., Wang, Y., Yi, T., Tellides, G., Pober, J. S., Shkarin, P., Shapiro, E. M., Saltzman, W. M., Papademetris, X., Fahmy, T. M. & Breuer, C. K. 2008. Initial evaluation of the use of USPIO cell labeling and noninvasive MR monitoring of human tissue-engineered vascular grafts in vivo. FASEB J., 22, 3888–3895.
Neri, M., Maderna, C., Cavazzin, C., Deidda-Vigoriti, V., Politi, L. S., Scotti, G., Marzola, P., Sbarbati, A., Vescovi, A. L. & Gritti, A. 2008. Efficient In Vitro Labeling of Human Neural Precursor Cells with Superparamagnetic Iron Oxide Particles: Relevance for In Vivo Cell Tracking. Stem Cells, 26, 505–516.
Nguyen Huu, S., Oster, M., Uzan, S., Chareyre, F., Aractingi, S. & Khosrotehrani, K. 2007. Maternal neoangiogenesis during pregnancy partly derives from fetal endothelial progenitor cells. Proceedings of the National Academy of Sciences, 104, 1871–1876.
Nohroudi, K. A., S.; Berhorn, T.; Addicks, K.; Hoehn, M.; Himmelreich, U. 2010. In Vivo MRI Stem Cell Tracking Requires Balancing of Detection Limit and Cell Viability. Cell Transplantation, 19, 431–441
Norman, A. B., Thomas, S. R., Pratt, R. G., Lu, S. Y. & Norgren, R. B. 1992. Magnetic resonance imaging of neural transplants in rat brain using a superparamagnetic contrast agent. Brain Res, 594, 279–83.
Park, S. J., Leslie, R. W., Huh, S., Kagan, H., Honscheid, K., Burdette, D., Chesi, E., Lacasta, C., Llosa, G. & Mikuz, M. 2007. A prototype of very high-resolution small animal PET scanner using silicon pad detectors. Nuclear Inst. and Methods in Physics Research, A, 570, 543–555.
Pawelczyk, E., Arbab, A. S., Pandit, S., Hu, E. & Frank, J. A. 2006. Expression of transferrin receptor and ferritin following ferumoxides–protamine sulfate labeling of cells: implications for cellular magnetic resonance imaging. NMR in Biomedicine, 19, 581–592.
Phinney, D. G. & Prockop, D. J. 2007. Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair – current views. Stem Cells, 25, 2896–902.
Pintaske, J., Muller-Bierl, B. & Schick, F. 2006. Geometry and extension of signal voids in MR images induced by aggregations of magnetically labelled cells. Phys Med Biol, 51, 4707–4718.
Pratten, M. K. & Lloyd, J. B. 1986. Pinocytosis and phagocytosis: the effect of size of a particulate substrate on its mode of capture by rat peritoneal macrophages cultured in vitro. Biochim Biophys Acta, 881, 307–13.
Qiu, B., Gao, F., Walczak, P., Zhang, J., Kar, S., Bulte, J. W. & Yang, X. 2007. In vivo MR imaging of bone marrow cells trafficking to atherosclerotic plaques. J Magn Reson Imaging, 26, 339–43.
Raynal, I., Prigent, P., Peyramaure, S., Najid, A., Rebuzzi, C. & Corot, C. 2004. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles: mechanisms and comparison of ferumoxides and ferumoxtran-10. Invest Radiol, 39, 56–63.
Reimer, P. & Balzer, T. 2003. Ferucarbotran (Resovist): a new clinically approved RES-specific contrast agent for contrast-enhanced MRI of the liver: properties, clinical development, and applications. European Radiology, 13, 1266–1276.
Reimer, P., Rummeny, E. J., Daldrup, H. E., Balzer, T., Tombach, B., Berns, T. & Peters, P. E. 1995. Clinical results with Resovist: a phase 2 clinical trial. Radiology, 195, 489–96.
Rejman, J., Oberle, V., Zuhorn, I. S. & Hoekstra, D. 2004. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J, 377, 159–69.
Rogers, W. J. & Basu, P. 2005. Factors regulating macrophage endocytosis of nanoparticles: implications for targeted magnetic resonance plaque imaging. Atherosclerosis, 178, 67–73.
Roser, M., Fischer, D. & Kissel, T. 1998. Surface-modified biodegradable albumin nano-and microspheres. II: effect of surface charges on in vitro phagocytosis and biodistribution in rats. European Journal of Pharmaceutics and Biopharmaceutics, 46, 255–263.
Ruehm, S. G., Corot, C., Vogt, P., Kolb, S. & Debatin, J. F. 2001. Magnetic Resonance Imaging of Atherosclerotic Plaque With Ultrasmall Superparamagnetic Particles of Iron Oxide in Hyperlipidemic Rabbits. Am Heart Assoc
Sadan, O., Shemesh, N., Barzilay, R., Bahat-Stromza, M., Melamed, E., Cohen, Y. & Offen, D. 2008. Migration of neurotrophic factors-secreting mesenchymal stem cells towards a quinolinic acid lesion as viewed by MRI. Stem Cells
Saini, S., Stark, D. D., Brady, T. J., Wittenberg, J. & Ferrucci, J. J. 1986. Dynamic spin-echo MRI of liver cancer using Gadolinium-DTPA: animal investigation. AJR Am J Roentgenol, 147, 357–62.
Saini, S., Stark, D. D., Hahn, P. F., Wittenberg, J., Brady, T. J. & Ferrucci, J. J. 1987. Ferrite particles: a superparamagnetic MR contrast agent for the reticuloendothelial system. Radiology, 162, 211–216.
Saleh, A., Schroeter, M., Jonkmanns, C., Hartung, H. P., Modder, U. & Jander, S. 2004. In vivo MRI of brain inflammation in human ischaemic stroke. Brain, 127, 1670.
Sharma, R., Saini, S., Ros, P. R., Hahn, P. F., Small, W. C., De, L. E., Stillman, A. E., Edelman, R. R., Runge, V. M. & Outwater, E. K. 1999. Safety profile of ultrasmall superparamagnetic iron oxide ferumoxtran-10: phase II clinical trial data. Journal of magnetic resonance imaging: JMRI, 9, 291.
Shen, T., Weissleder, R., Papisov, M., Bogdanov, J. A. & Brady, T. J. 1993. Monocrystalline iron oxide nanocompounds (MION): physicochemical properties. Magn Reson Med, 29, 599–604.
Song, M., Moon, W. K., Kim, Y., Lim, D., Song, I. C. & Yoon, B. W. 2007. Labeling efficacy of superparamagnetic iron oxide nanoparticles to human neural stem cells: comparison of ferumoxides, monocrystalline iron oxide, cross-linked iron oxide (CLIO)-NH2 and tat-CLIO. Korean J Radiol, 8, 365–71.
Stuckey, D. J., Carr, C. A., Martin-Rendon, E., Tyler, D. J., Willmott, C., Cassidy, P. J., Hale, S. J., Schneider, J. E., Tatton, L. & Harding, S. E. 2006. Iron Particles for Noninvasive Monitoring of Bone Marrow Stromal Cell Engraftment into, and Isolation of Viable Engrafted Donor Cells from, the Heart. Stem Cells, 24, 1968–1975.
Tabata, Y. & Ikada, Y. 1988. Effect of the size and surface charge of polymer microspheres on their phagocytosis by macrophage. Biomaterials, 9, 356–362.
Taupitz, M., Schnorr, J., Abramjuk, C., Wagner, S., Pilgrimm, H., Hunigen, H. & Hamm, B. 2000. New generation of monomer-stabilized very small superparamagnetic iron oxide particles (VSOP) as contrast medium for MR angiography: preclinical results in rats and rabbits. J Magn Reson Imaging, 12, 905–11.
Terrovitis, J. V., Bulte, J. W., Sarvananthan, S., Crowe, L. A., Sarathchandra, P., Batten, P., Sachlos, E., Chester, A. H., Czernuszka, J. T. & Firmin, D. N. 2006. Magnetic resonance imaging of ferumoxide-labeled mesenchymal stem cells seeded on collagen scaffolds-relevance to tissue engineering. Tissue Eng, 12, 2765–75.
Thorek, D. L. & Tsourkas, A. 2008. Size, charge and concentration dependent uptake of iron oxide particles by non-phagocytic cells. Biomaterials, 29, 3583–3590.
Toso, C., Vallee, J. P., Morel, P., Ris, F., Demuylder-Mischler, S., Lepetit-Coiffe, M., Marangon, N., Saudek, F., James Shapiro, A. M., Bosco, D. & Berney, T. 2008. Clinical Magnetic Resonance Imaging of Pancreatic Islet Grafts After Iron Nanoparticle Labeling. American Journal of Transplantation, 8, 701–706.
Van Den Bos, E. J., Baks, T., Moelker, A. D., Kerver, W., Van, G. R., Van, G. W., Duncker, D. J. & Wielopolski, P. A. 2006. Magnetic resonance imaging of haemorrhage within reperfused myocardial infarcts: possible interference with iron oxide-labelled cell tracking? Eur Heart J, 27, 1620–6.
Van Den Bos, E. J., Wagner, A., Mahrholdt, H., Thompson, R. B., Morimoto, Y., Sutton, B. S., Judd, R. M. & Taylor, D. A. 2003. Improved efficacy of stem cell labeling for magnetic resonance imaging studies by the use of cationic liposomes. Cell Transplant, 12, 743–56.
Von Zur Muhlen, C., Von, E. D., Bassler, N., Neudorfer, I., Steitz, B., Petri-Fink, A., Hofmann, H., Bode, C. & Peter, K. 2007. Superparamagnetic iron oxide binding and uptake as imaged by magnetic resonance is mediated by the integrin receptor Mac-1 (CD11b/CD18): implications on imaging of atherosclerotic plaques. Atherosclerosis, 193, 102–11.
Walczak, P., Kedziorek, D. A., Gilad, A. A., Lin, S. & Bulte, J. W. 2005. Instant MR labeling of stem cells using magnetoelectroporation. Magn Reson Med, 54, 769–774.
Walczak, P., Zhang, J., Gilad, A. A., Kedziorek, D. A., Ruiz-Cabello, J., Young, R. G., Pittenger, M. F., Van, Z. P., Huang, J. & Bulte, J. W. 2008. Dual-Modality Monitoring of Targeted Intraarterial Delivery of Mesenchymal Stem Cells After Transient Ischemia. Stroke, 39, 1569.
Wang, L., Neoh, K.-G., Kang, E.-T., Shuter, B. & Wang, S.-C. 2010. Biodegradable magnetic-fluorescent magnetite/poly(dl-lactic acid-co-[alpha],[beta]-malic acid) composite nanoparticles for stem cell labeling. Biomaterials, 31, 3502–3511.
Weissleder, R., Elizondo, G., Wittenberg, J., Lee, A. S., Josephson, L. & Brady, T. J. 1990a. Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology, 175, 494–8.
Weissleder, R., Moore, A., Mahmood, U., Bhorade, R., Benveniste, H., Chiocca, E. A. & Basilion, J. P. 2000. In vivo magnetic resonance imaging of transgene expression. Nature medicine, 6, 351.
Weissleder, R., Wittenberg, J., Rabito, C. A. & Bengele, H. H. 1990b. Ultrasmall Superparamagnetic Iron Oxide: Characterization of a New Class of Contrast Agents for MR Imaging’. Radiology, 175, 489–493.
Wiart, M., Davoust, N., Pialat, J. B., Desestret, V., Moucharaffie, S., Cho, T. H., Mutin, M., Langlois, J. B., Beuf, O. & Honnorat, J. 2007. MRI Monitoring of Neuroinflammation in Mouse Focal Ischemia. Stroke, 38, 131.
Wilhelm, C., Billotey, C., Roger, J., Pons, J. N., Bacri, J. C. & Gazeau, F. 2003. Intracellular uptake of anionic superparamagnetic nanoparticles as a function of their surface coating. Biomaterials, 24, 1001–1011.
Wilhelm, C. & Gazeau, F. 2008. Universal cell labelling with anionic magnetic nanoparticles. Biomaterials
Wu, H., Pal, D., O, S. J. & Tai, Y.-C. 2008. A Feasibility Study of a Prototype PET Insert Device to Convert a General-Purpose Animal PET Scanner to Higher Resolution. J Nucl Med, 49, 79–87.
Yeh, T. C., Zhang, W., Ildstad, S. T. & Ho, C. 1993. Intracellular labeling of T-cells with superparamagnetic contrast agents. Magn Reson Med, 30, 617–25.
Zhang, X., Bowen, C. V., Gareau, P. & Rutt, B. K. Year. Quantitative Analysis of SPIO and USPIO Uptake Rate by Macrophages: Effects of Particle Size, Concentration, and Labeling Time. In: Proc. Intl. Soc. Mag. Reson. Med, 2001. 880.
Zhu, J., Zhou, L. & Xingwu, F. G. 2006. Tracking Neural Stem Cells in Patients with Brain Trauma. New England Journal of Medicine, 355, 2376.
Ziener, C. H., Bauer, W. R. & Jakob, P. M. 2005. Transverse relaxation of cells labeled with magnetic nanoparticles. Magn Reson Med, 54, 702–6.
Zurkiya, O., Chan, A. W. S. & Hu, X. 2008. MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magnetic Resonance in Medicine, 59, 1225–1231.
Acknowledgements
EL was supported by project grants from Australian NHMRC, and JC received salary support from Singapore NMRC (CSA/012/2009). Appreciation is expressed to Debbie Ng for proofreading of the manuscript.
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Lee, E.S.M., Rutt, B.K., Fisk, N.M., Wang, SC., Chan, J. (2011). Magnetic Resonance Tracking of Stem Cells with Iron Oxide Particles. In: Prokop, A. (eds) Intracellular Delivery. Fundamental Biomedical Technologies, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1248-5_17
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