Electrostatically stabilized magnetic nanoparticles - An optimized protocol to label murinet cells for in vivo MRI

Frontiers in Neurology

Volumn DEC, Issue , 2011, Pages

  Wuerfel, Eva ^a,b   Smyth, Maureen ^a   Millward, Jason M ^a   Schellenberger, Eyk ^a   Glumm, Jana ^a   Prozorovski, Timour ^a,c   Aktas, Orhan ^a,c   Schulze Topphoff, Ulf ^a,d   Schnorr, Jörg ^a   Wagner, Susanne ^a   Taupitz, Matthias ^a   Infante Duarte, Carmen ^a   Wuerfel, Jens ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF LÜBECK   (Germany)

^c Department of Orthopedic Surgery   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell labeling; EAE; Magnetic nanoparticles; Magnetic resonance imaging; Protamine; T cell

Indexed keywords

EID: 84865848267     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2011.00072     Document Type: Article

References (42)

1. Aktas, O., Smorodchenko, A., Brocke, S., Infante-Duarte, C., Schulze Top-phoff, U., Vogt, J., Prozorovski, T., Meier, S., Osmanova, V., Pohl, E., Bechmann, I., Nitsch, R., and Zipp, F. (2005). Neuronal damage in autoimmune neuroinflammation mediated by the death ligand TRAIL. Neuron 46, 421-432.
2. Anderson, S. A., Lee, K. K., and Frank, J. A. (2006). Gadolinium-fullerenol as a paramagnetic contrast agent for cellular imaging. Invest. Radiol. 41, 332-338.
3. Anderson, S. A., Shukaliak-Quandt, J., Jordan, E. K., Arbab, A. S., Martin, R., Mcfarland, H., and Frank, J. A. (2004). Magnetic resonance imaging of labeled T-cells in a mouse model of multiple sclerosis. Ann. Neurol. 55, 654-659.
4. Arbab, A. S., Liu, W., and Frank, J. A. (2006). Cellular magnetic resonance imaging: current status and future prospects. Expert Rev. Med. Devices 3, 427-439.
5. Arbab, A. S., Yocum, G. T., Kalish, H., Jordan, E. K., Anderson, S. A., Khakoo, A. Y., Read, E. J., and Frank, J. A. (2004). Efficient magnetic cell labeling with prota-mine sulfate complexed to ferumox-ides for cellular MRI. Blood 104, 1217-1223.
6. Arbab, A. S., Yocum, G. T., Rad, A. M., Khakoo, A. Y., Fellowes, V., Read, E. J., and Frank, J. A. (2005). Labeling of cells with ferumoxides-protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchy-mal stem cells. NMR Biomed. 18, 553-559.
7. Berger, C., Rausch, M., Schmidt, P., and Rudin, M. (2006). Feasibility and limits of magnetically labeling primary cultured rat T cells with fer-umoxides coupled with commonly used transfection agents. Mol. Imaging 5, 93-104.
8. Billotey, C., Aspord, C., Beuf, O., Piag-gio, E., Gazeau, F., Janier, M. F., and Thivolet, C. (2005). T-cell homing to the pancreas in autoimmune mouse models of diabetes: in vivo MR imaging. Radiology 236, 579-587.
9. Daldrup-Link, H. E., Meier, R., Rudelius, M., Piontek, G., Piert, M., Metz, S., Settles, M., Uherek, C., Wels, W., Schlegel, J., and Rummeny, E. J. (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.
10. Djeha, A., and Brock, J. H. (1992). Uptake and intracellular handling of iron from transferrin and iron chelates by mitogen stimulated mouse lymphocytes. Biochim. Bio-phys. Acta 1133, 147-152.
11. Dodd, C. H., Hsu, H. C., Chu, W. J., Yang, P., Zhang, H. G., Mountz, J. D. Jr., Zinn, K., Forder, J., Josephson, L., Weissleder, R., Mountz, J. M., and Mountz, J. D. (2001). Normal T-cell response and in vivo magnetic resonance imaging of T cells loaded with HIV transactivator-peptide-derived superparamagnetic nanoparticles. J. Immunol. Methods 256, 89-105.
12. Fleige, G., Seeberger, F., Laux, D., Kresse, M., Taupitz, M., Pilgrimm, H., and Zimmer, C. (2002). In vitro characterization of two different ultrasmall iron oxide particles for magnetic resonance cell tracking. Invest. Radiol. 37, 482-488.
13. Focke, A., Schwarz, S., Foerschler, A., Scheibe, J., Milosevic, J., Zimmer, C., and Schwarz, J. (2008). Labeling of human neural precursor cells using ferromagnetic nanoparticles. Magn. Reson. Med. 60, 1321-1328.
14. Frank, J. A., Miller, B. R., Arbab, A. S., Zywicke, H. A., Jordan, E. K., Lewis, B. K., Bryant, L. H. Jr., and Bulte, J. W. (2003). Clinically applicable labeling of mammalian and stem cells by combining superparamag-netic iron oxides and transfection agents. Radiology 228, 480-487.
15. Hendrix, S., and Nitsch, R. (2007). The role of T helper cells in neuroprotec-tion and regeneration. J. Neuroim-munol. 184, 100-112.
16. Heymer, A., Haddad, D., Weber, M., Gbureck, U., Jakob, P. M., Eulert, J., and Noth, U. (2008). Iron oxide labeling of human mesenchymal stem cells in collagen hydrogels for articular cartilage repair. Biomateri-als 29, 1473-1483.
17. Hu, D. E., Kettunen, M. I., and Brindle, K. M. (2005). Monitoring T-lymphocyte trafficking in tumors undergoing immune rejection. Magn. Reson. Med. 54, 1473-1479.
18. Infante-Duarte, C., Horton, H. F., Byrne, M. C., and Kamradt, T. (2000). Microbial lipopeptides induces the production of IL-17 in Th cells. J. Immunol. 165, 6107-6115.
19. Kircher, M. F.,Allport,J. R., Graves, E. E., Love, V., Josephson, L., Lichtman, A. H., and Weissleder, R. (2003). In vivo high resolution three-dimensional imaging of antigen-specific cyto-toxic T-lymphocyte trafficking to tumors. Cancer Res. 63, 6838-6846.
20. Lewin, M., Carlesso, N., Tung, C. H., Tang, X. W., Cory, D., Scadden, D. T., and Weissleder, R. (2000). Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol. 18, 410-414.
21. Liu, W., and Frank, J. A. (2008). Detection and quantification of magnetically labeled cells by cellular MRI. Eur. J. Radiol. 70, 258-264.
22. Modo, M., Hoehn, M., and Bulte, J. W. (2005). Cellular MR imaging. Mol. Imaging 4, 143-164.
23. Perl, D. P., and Good, P. F. (1992). Comparative techniques for determining cellular iron distribution in brain tissues. Ann. Neurol. 32(Suppl.), S76-S81.
24. Pirko, I., Johnson, A., Ciric, B., Gamez, J., Macura, S. I., Pease, L. R., and Rodriguez, M. (2004). In vivo magnetic resonance imaging of immune cells in the central nervous system with superparamagnetic antibodies. FASEB J. 18, 179-182.
25. Raine, C. S., Cannella, B., Duijvestijn, A. M., and Cross, A. H. (1990). Homing to central nervous system vascu-lature by antigen-specific lymphocytes. II. Lymphocyte/endothelial cell adhesion during the initial stages of autoimmune demyelination. Lab. Invest. 63, 476-489.
26. Reynolds, F., Weissleder, R., and Joseph-son, L. (2005). Protamine as an efficient membrane-translocating peptide. Bioconjug. Chem. 16, 1240-1245.
27. Rogers, W. J., Meyer, C. H., and Kramer, C. M. (2006). Technology insight: in vivo cell tracking by use of MRI. Nat. Clin. Pract. Cardiovasc. Med. 3, 554-562.
28. Shen, T., Weissleder, R., Papisov, M., Bogdanov, A. Jr., and Brady, T. J. (1993). Monocrystalline iron oxide nanocompounds (MION): physico-chemical properties. Magn. Reson. Med. 29, 599-604.
29. Smirnov, P., Poirier-Quinot, M., Wil-helm, C., Lavergne, E., Ginefri, J. C., Combadiere, B., Clement, O., Darrasse, L., and Gazeau, F. (2008). In vivo single cell detection of tumor-infiltrating lymphocytes with a clinical 1.5 Tesla MRI system. Magn. Reson. Med. 60, 1292-1297.
30. Stroh, A., Faber, C., Neuberger, T., Lorenz, P., Sieland, K., Jakob, P. M., Webb, A., Pilgrimm, H., Schober, R., Pohl, E. E., and Zimmer, C. (2005). In vivo detection limits of magnetically labeled embryonic stem cells in the rat brain using high-field (17.6 T) magnetic resonance imaging. Neuroimage 24, 635-645.
31. Stroh, A., Zimmer, C., Gutzeit, C., Jakstadt, M., Marschinke, F., Jung, T., Pilgrimm, H., and Grune, T. (2004). Iron oxide particles for molecular magnetic resonance imaging cause transient oxidative stress in rat macrophages. Free Radic. Biol. Med. 36, 976-984.
32. Stroh, A., Zimmer, C., Werner, N., Gertz, K., Weir, K., Kronenberg, G., Steinbrink, J., Mueller, S., Sieland, K., Dirnagl, U., Nickenig, G., and Endres, M. (2006). Tracking of systemically administered mononu-clear cells in the ischemic brain by high-field magnetic resonance imaging. Neuroimage 33, 886-897.
33. Suzuki, Y., Zhang, S., Kundu, P., Yeung, A. C., Robbins, R. C., and Yang, P. C. (2007). In vitro comparison of the biological effects of three transfec-tion methods for magnetically labeling mouse embryonic stem cells with ferumoxides. Magn. Reson. Med. 57, 1173-1179.
34. Thorek, D. L., and Tsourkas, A. (2008). Size, charge and concentration dependent uptake of iron oxide particles by non-phagocytic cells. Biomaterials 29, 3583-3590.
35. Vellinga, M. M., Oude Engberink, R. D., Seewann, A., Pouwels, P. J., Wat-tjes, M. P., van der Pol, S. M., Per-ing, C., Polman, C. H., de Vries, H. E., Geurts, J. J., and Barkhof, F. (2008). Pluriformity of inflammation in multiple sclerosis shown by ultra-small iron oxide particle enhancement. Brain 131, 800-807.
36. Walczak, P., Kedziorek, D. A., Gilad, A. A., Lin, S., and Bulte, J. W. (2005). Instant MR labeling of stem cells using magnetoelectro-poration. Magn. Reson. Med. 54, 769-774.
37. Weiner, H. L., and Frenkel, D. (2006). Immunology and immunotherapy of Alzheimer's disease. Nat. Rev. Immunol. 6, 404-416.
38. Wuerfel,E.,Infante-Duarte,C.,Glumm, R., and Wuerfel, J. T. (2010). Gad-ofluorine M-enhanced MRI shows involvement of circumventricular organs in neuroinflammation. J. Neuroinflammation 18, 70.
39. Wuerfel, J., Tysiak, E., Prozorovski, T., Smyth, M., Mueller, S., Schnorr, J., Taupitz, M., and Zipp, F. (2007). Mouse model mimics multiple sclerosis in the clinico-radiological paradox. Eur. J. Neurosci. 26, 190-198.
40. Yeh, T. C., Zhang, W., Ildstad, S. T., and Ho, C. (1995). In vivo dynamic MRI tracking of rat T-cells labeled with superparamagnetic iron-oxide particles. Magn. Reson. Med. 33, 200-208.
41. Zepp, J., Wu, L., and Li, X. (2011). IL-17 receptor signaling and T helper 17-mediated autoimmune demyeli-nating disease. Trends Immunol. 32, 232-239
42. Zipp, F., and Aktas, O. (2006). The brain as a target of inflammation: common pathways link inflammatory and neurodegenera-tive diseases. Trends Neurosci. 29, 518-527.