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In vivo visualization and ex vivo quantification of murine breast cancer cells in the mouse brain using MRI cell tracking and electron paramagnetic resonance.

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Danhier, Pierre [UCL] Magat, Julie [UCL] Levêque, Philippe [UCL] De Preter, Géraldine [UCL] Porporato, Paolo [UCL] Bouzin, Caroline [UCL] Jordan, Bénédicte [UCL] Demeur, Gladys [UCL] Haufroid, Vincent [UCL] Feron, Olivier [UCL] Sonveaux, Pierre [UCL] Gallez, Bernard [UCL]

Cell tracking could be useful to elucidate fundamental processes of cancer biology such as metastasis. The aim of this study was to visualize, using MRI, and to quantify, using electron paramagnetic resonance (EPR), the entrapment of murine breast cancer cells labeled with superparamagnetic iron oxide particles (SPIOs) in the mouse brain after intracardiac injection. For this purpose, luciferase-expressing murine 4 T1-luc breast cancer cells were labeled with fluorescent Molday ION Rhodamine B SPIOs. Following intracardiac injection, SPIO-labeled 4 T1-luc cells were imaged using multiple gradient-echo sequences. Ex vivo iron oxide quantification in the mouse brain was performed using EPR (9 GHz). The long-term fate of 4 T1-luc cells after injection was characterized using bioluminescence imaging (BLI), brain MRI and immunofluorescence. We observed hypointense spots due to SPIO-labeled cells in the mouse brain 4 h after injection on T2 *-weighted images. Histology studies showed that SPIO-labeled cancer cells were localized within blood vessels shortly after delivery. Ex vivo quantification of SPIOs showed that less than 1% of the injected cells were taken up by the mouse brain after injection. MRI experiments did not reveal the development of macrometastases in the mouse brain several days after injection, but immunofluorescence studies demonstrated that these cells found in the brain established micrometastases. Concerning the metastatic patterns of 4 T1-luc cells, an EPR biodistribution study demonstrated that SPIO-labeled 4 T1-luc cells were also entrapped in the lungs of mice after intracardiac injection. BLI performed 6 days after injection of 4 T1-luc cells showed that this cell line formed macrometastases in the lungs and in the bones. Conclusively, EPR and MRI were found to be complementary for cell tracking applications. MRI cell tracking at 11.7 T allowed sensitive detection of isolated SPIO-labeled cells in the mouse brain, whereas EPR allowed the assessment of the number of SPIO-labeled cells in organs shortly after injection. Copyright © 2015 John Wiley & Sons, Ltd.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2015
Language Anglais
Journal information "NMR in Biomedicine" - Vol. 28, no. 3, p. 367-375 (2015)
Peer reviewed yes
Publisher JohnWiley & Sons Ltd. ((United Kingdom) Chichester)
issn 0952-3480
e-issn 1099-1492
Publication status Publié
Affiliations UCL - SSS/IREC/FATH - Pôle de Pharmacologie et thérapeutique
UCL - SSS/IREC/LTAP - Louvain Centre for Toxicology and Applied Pharmacology
UCL - SSS/LDRI - Louvain Drug Research Institute
UCL - (SLuc) Service de biochimie médicale
UCL - (SLuc) Service de médecine nucléaire
UCL - SSS/IREC - Institut de recherche expérimentale et clinique
Links
  1. Kircher Moritz F., Gambhir Sanjiv S., Grimm Jan, Noninvasive cell-tracking methods, 10.1038/nrclinonc.2011.141
  2. Cohen Batya, Dafni Hagit, Meir Gila, Harmelin Alon, Neeman Michal, Ferritin as an Endogenous MRI Reporter for Noninvasive Imaging of Gene Expression in C6 Glioma Tumors, 10.1593/neo.04436
  3. Iordanova Bistra, Ahrens Eric T., In vivo magnetic resonance imaging of ferritin-based reporter visualizes native neuroblast migration, 10.1016/j.neuroimage.2011.08.068
  4. Vande Velde Greetje, Raman Rangarajan Janaki, Vreys Ruth, Guglielmetti Caroline, Dresselaers Tom, Verhoye Marleen, Van der Linden Annemie, Debyser Zeger, Baekelandt Veerle, Maes Frederik, Himmelreich Uwe, Quantitative evaluation of MRI-based tracking of ferritin-labeled endogenous neural stem cell progeny in rodent brain, 10.1016/j.neuroimage.2012.04.040
  5. Bulte Jeff W. M., Kraitchman Dara L., Iron oxide MR contrast agents for molecular and cellular imaging, 10.1002/nbm.924
  6. Smirnov P., Gazeau F., Beloeil J.-C., Doan B.T., Wilhelm C., Gillet B., Single-cell detection by gradient echo 9.4 T MRI: a parametric study, 10.1002/cmmi.104
  7. Foster-Gareau Paula, Heyn Chris, Alejski Andrew, Rutt Brian K., Imaging single mammalian cells with a 1.5 T clinical MRI scanner, 10.1002/mrm.10417
  8. Langley Jason, Liu Wei, Jordan E. Kay, Frank J. A., Zhao Qun, Quantification of SPIO nanoparticles in vivo using the finite perturber method : Quantification of SPIO Nanoparticles, 10.1002/mrm.22727
  9. Kotek Gyula, van Tiel Sandra T., Wielopolski Piotr A., Houston Gavin C., Krestin Gabriel P., Bernsen Monique R., Cell quantification: evolution of compartmentalization and distribution of iron-oxide particles and labeled cells : Evolution in distribution of labeling iron-oxide particles, 10.1002/cmmi.481
  10. Girard O. M., Ramirez R., McCarty S., Mattrey R. F., Toward absolute quantification of iron oxide nanoparticles as well as cell internalized fraction using multiparametric MRI : IONP QUANTIFICATION USING MULTIPARAMETRIC MRI, 10.1002/cmmi.1467
  11. Rad Ali M., Arbab Ali S., Iskander A.S.M., Jiang Quan, Soltanian-Zadeh Hamid, Quantification of superparamagnetic iron oxide (SPIO)-labeled cells using MRI, 10.1002/jmri.20978
  12. Liu Wei, Frank Joseph A., Detection and quantification of magnetically labeled cells by cellular MRI, 10.1016/j.ejrad.2008.09.021
  13. van Buul Gerben M., Kotek Gyula, Wielopolski Piotr A., Farrell Eric, Bos P. Koen, Weinans Harrie, Grohnert Anja U., Jahr Holger, Verhaar Jan A. N., Krestin Gabriel P., van Osch Gerjo J. V. M., Bernsen Monique R., Clinically Translatable Cell Tracking and Quantification by MRI in Cartilage Repair Using Superparamagnetic Iron Oxides, 10.1371/journal.pone.0017001
  14. Chertok Beata, Cole Adam J., David Allan E., Yang Victor C., Comparison of Electron Spin Resonance Spectroscopy and Inductively-Coupled Plasma Optical Emission Spectroscopy for Biodistribution Analysis of Iron-Oxide Nanoparticles, 10.1021/mp900161h
  15. Levy Michael, Luciani Nathalie, Alloyeau Damien, Elgrabli Dan, Deveaux Vanessa, Pechoux Christine, Chat Sophie, Wang Guillaume, Vats Nidhi, Gendron François, Factor Cécile, Lotersztajn Sophie, Luciani Alain, Wilhelm Claire, Gazeau Florence, Long term in vivo biotransformation of iron oxide nanoparticles, 10.1016/j.biomaterials.2011.02.031
  16. Serres S., Soto M. S., Hamilton A., McAteer M. A., Carbonell W. S., Robson M. D., Ansorge O., Khrapitchev A., Bristow C., Balathasan L., Weissensteiner T., Anthony D. C., Choudhury R. P., Muschel R. J., Sibson N. R., Molecular MRI enables early and sensitive detection of brain metastases, 10.1073/pnas.1117412109
  17. Carbonell W. Shawn, Ansorge Olaf, Sibson Nicola, Muschel Ruth, The Vascular Basement Membrane as “Soil” in Brain Metastasis, 10.1371/journal.pone.0005857
  18. Danhier P., De Preter G., Boutry S., Mahieu I., Leveque P., Magat J., Haufroid V., Sonveaux P., Bouzin C., Feron O., Muller R. N., Jordan B. F., Gallez B., Electron paramagnetic resonance as a sensitive tool to assess the iron oxide content in cells for MRI cell labeling studies : EPR AS A TOOL TO MEASURE IRON OXIDE IN CELLS, 10.1002/cmmi.497
  19. McFadden C., Mallett C. L., Foster P. J., Labeling of multiple cell lines using a new iron oxide agent for cell tracking by MRI : CELL LABELING FOR MRI WITH MOLDAY ION-RHODAMINE B, 10.1002/cmmi.456
  20. Radermacher Kim A., Beghein Nelson, Boutry Sebastien, Laurent Sophie, Elst Luce Vander, Muller Robert N., Jordan Benedicte F., Gallez Bernard, In Vivo Detection of Inflammation Using Pegylated Iron Oxide Particles Targeted at E-Selectin : A Multimodal Approach Using MR Imaging and EPR Spectroscopy, 10.1097/rli.0b013e3181a49639
  21. Radermacher K. A., Boutry S., Laurent S., Elst L. Vander, Mahieu I., Bouzin C., Magat J., Gregoire V., Feron O., Muller R. N., Jordan B. F., Gallez B., Iron oxide particles covered with hexapeptides targeted at phosphatidylserine as MR biomarkers of tumor cell death, 10.1002/cmmi.382
  22. Radermacher K. A., Magat J., Bouzin C., Laurent S., Dresselaers T., Himmelreich U., Boutry S., Mahieu I., Vander Elst L., Feron O., Muller R. N, Jordan B. F., Gallez B., Multimodal assessment of early tumor response to chemotherapy: comparison between diffusion-weighted MRI, 1H-MR spectroscopy of choline and USPIO particles targeted at cell death : EARLY ASSESSMENT OF TUMOR RESPONSE TO CHEMOTHERAPY, 10.1002/nbm.1765
  23. IANNONE ANNA, FEDERICO MASSIMO, TOMAS ALDO, MAGIN RICHARD L., CASASCO ANDREA, CALLIGARO ALBERTO, VANNINI VANIO, Detection and Quantitation in Rat Tissues of the Superparamagnetic Magnetic Resonance Contrast Agent Dextran Magnetite as Demonstrated by Electron Spin Resonance Spectroscopy : , 10.1097/00004424-199206000-00010
  24. Danhier Pierre, De Preter Géraldine, Magat Julie, Godechal Quentin, Porporato Paolo E., Jordan Bénédicte F., Feron Olivier, Sonveaux Pierre, Gallez Bernard, Multimodal cell tracking of a spontaneous metastasis model: comparison between MRI, electron paramagnetic resonance and bioluminescence : CELL TRACKING OF METASTASIS, 10.1002/cmmi.1553
  25. Syková Eva, Jendelová Pavla, Herynek Vít, Magnetic Resonance Imaging of Stem Cell Migration, Methods in Molecular Biology (2011) ISBN:9781617791444 p.79-90, 10.1007/978-1-61779-145-1_5
  26. Ślawska-Waniewska A., Mosiniewicz-Szablewska E., Nedelko N., Gałązka-Friedman J., Friedman A., Magnetic studies of iron-entities in human tissues, 10.1016/j.jmmm.2003.12.843
  27. Walczak P., Kedziorek D.A., Gilad A.A., Barnett B.P., Bulte J.W.M., 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, 10.1002/mrm.21280
  28. Weissleder R, Stark DD, Engelstad BL, Bacon BR, Compton CC, White DL, Jacobs P, Lewis J, Superparamagnetic iron oxide: pharmacokinetics and toxicity, 10.2214/ajr.152.1.167
  29. Arbab Ali S., Wilson Lindsey B., Ashari Parwana, Jordan Elaine K., Lewis Bobbi K., Frank Joseph A., A model of lysosomal metabolism of dextran coated superparamagnetic iron oxide (SPIO) nanoparticles: implications for cellular magnetic resonance imaging, 10.1002/nbm.970
  30. Song Ho-Taek, Jordan Elaine K, Lewis Bobbi K, Liu Wei, Ganjei Justin, Klaunberg Brenda, Despres Daryl, Palmieri Diane, Frank Joseph A, Rat model of metastatic breast cancer monitored by MRI at 3 tesla and bioluminescence imaging with histological correlation, 10.1186/1479-5876-7-88
  31. Addicott Benjamin, Willman Melissa, Rodriguez Jose, Padgett Kyle, Han Dongmei, Berman Dora, Hare Joshua M., Kenyon Norma Sue, Mesenchymal stem cell labeling and in vitro MR characterization at 1.5 T of new SPIO contrast agent: Molday ION Rhodamine-B™, 10.1002/cmmi.396
  32. Shen, Int. J. Nanomedicine, 8, 4593 (2013)
  33. Balathasan Lukxmi, Beech John S., Muschel Ruth J., Ultrasonography-Guided Intracardiac Injection, 10.1016/j.ajpath.2013.03.003
  34. Heyn Chris, Ronald John A., Ramadan Soha S., Snir Jonatan A., Barry Andrea M., MacKenzie Lisa T., Mikulis David J., Palmieri Diane, Bronder Julie L., Steeg Patricia S., Yoneda Toshiyuki, MacDonald Ian C., Chambers Ann F., Rutt Brian K., Foster Paula J., In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain, 10.1002/mrm.21029
  35. Perera Mevan, Ribot Emeline J., Percy Dean B., McFadden Catherine, Simedrea Carmen, Palmieri Diane, Chambers Ann F., Foster Paula J., In Vivo Magnetic Resonance Imaging for Investigating the Development and Distribution of Experimental Brain Metastases due to Breast Cancer, 10.1593/tlo.12109
  36. Barbee, Am. J. Physiol., 263, R728 (1992)
  37. Terrovitis J., Stuber M., Youssef A., Preece S., Leppo M., Kizana E., Schar M., Gerstenblith G., Weiss R. G., Marban E., Abraham M. R., Magnetic Resonance Imaging Overestimates Ferumoxide-Labeled Stem Cell Survival After Transplantation in the Heart, 10.1161/circulationaha.107.732073
  38. Townson J. L., Ramadan S. S., Simedrea C., Rutt B. K., MacDonald I. C., Foster P. J., Chambers A. F., Three-Dimensional Imaging and Quantification of Both Solitary Cells and Metastases in Whole Mouse Liver by Magnetic Resonance Imaging, 10.1158/0008-5472.can-09-1496
  39. Cromer Berman Stacey M., Walczak Piotr, Bulte Jeff W.M., Tracking stem cells using magnetic nanoparticles, 10.1002/wnan.140
Bibliographic reference Danhier, Pierre ; Magat, Julie ; Levêque, Philippe ; De Preter, Géraldine ; Porporato, Paolo ; et. al. In vivo visualization and ex vivo quantification of murine breast cancer cells in the mouse brain using MRI cell tracking and electron paramagnetic resonance.. In: NMR in Biomedicine, Vol. 28, no. 3, p. 367-375 (2015)
Permanent URL http://hdl.handle.net/2078.1/155353