Magnetic resonance imaging and fluorescence labeling of clinical-grade mesenchymal stem cells without impacting their phenotype: Study in a rat model of stroke

Stem Cells Translational Medicine

Volumn 1, Issue 4, 2012, Pages 333-340

  Detante, Olivier ^a,b,c   Valable, Samuel ^a,b   De Fraipont, Florence ^b,d,e   Grillon, Emmanuelle ^a,b   Barbier, Emmanuel Luc ^a,b   Moisan, Anaïck ^a,b   Arnaud, Josiane ^b,f   Moriscot, Christine ^b,d,g   Segebarth, Christoph ^a,b   Hommel, Marc ^b,h   Remy, Chantal ^a,b   Richard, Marie Jeanne ^b,d,e,g  

^a Institut National de Santé et de Recherche Médicale   (France)

^b UNIV GRENOBLE ALPES   (France)

^c Unité Neurovasculaire Pôle Psychiatrie Neurologie   (France)

^d Unité de Biochimie des Cancers et Biothérapies   (France)

^e Biochimie Hormonale et Nutritionnelle   (France)

^f Unité Mixte de Thérapie Cellulaire et Tissulaire   (France)

^g GRENOBLE UNIVERSITY HOSPITAL   (France)

^h INSTITUT ALBERT BONNIOT   (France)

Author keywords

Cell culture; Cell migration; In vivo tracking; Mesenchymal stem cells

Indexed keywords

5' NUCLEOTIDASE; ENDOGLIN; FLUORESCENT DYE; IRON; SUPERPARAMAGNETIC IRON OXIDE; THY 1 ANTIGEN; FERRIC ION; FERRIC OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BONE MARROW; CELL DAMAGE; CELL DIFFERENTIATION; CELL LABELING; CELL TRACKING; CELL VIABILITY; CEREBROVASCULAR ACCIDENT; CLINICAL TRIAL (TOPIC); CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; FOLLOW UP; HISTOLOGY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NONHUMAN; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; RAT; SCORING SYSTEM; ANIMAL; CLINICAL TRIAL; DISEASE MODEL; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; METABOLISM; METHODOLOGY; PATHOLOGY; SPRAGUE DAWLEY RAT; XENOGRAFT;

ANIMALS; DISEASE MODELS, ANIMAL; FERRIC COMPOUNDS; FLUORESCENT DYES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; MICROSCOPY, FLUORESCENCE; RATS; RATS, SPRAGUE-DAWLEY; STROKE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84871862916     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2011-0043     Document Type: Article

References (62)

1. Bliss T, Guzman R, Daadi M et al. Cell transplantation therapy for stroke. Stroke 2007;38:817-826.
2. Lindvall O, Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 2006;441:1094-1096.
3. Jiang Y, Jahagirdar BN, Reinhardt RL et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418: 41-49. Erratum in: Nature 2007;447:879-880.
4. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
5. Li Y, Chen J, Chen XG et al. Human marrow stromal cell therapy for stroke in rat: Neurotrophins and functional recovery. Neurology 2002;59:514-523.
6. Plumas J, Chaperot L, Richard MJ et al. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 2005;19:1597-1604.
7. Bang OY, Lee JS, Lee PH et al. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 2005;57:874-882.
8. Lee JS, Hong JM, Moon GJ et al. A longterm follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. STEM CELLS 2010; 28:1099-1106.
9. Chamberlain G, Fox J, Ashton B et al. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. STEM CELLS 2007;25:2739-2749.
10. Krampera M, Marconi S, Pasini A et al. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 2007;40:382-390.
11. Woodbury D, Schwarz EJ, Prockop DJ et al. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000;61:364-370.
12. Borlongan CV, Lind JG, Dillon-Carter O et al. Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats. Brain Res 2004;1010:108-116.
13. Chen J, Li Y, Wang L et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001;32:1005-1011.
14. Chen J, Li Y, Wang L et al. Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 2001;189:49-57.
15. Chen J, Li Y, Katakowski M et al. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 2003;73:778-786.
16. Liu Z, Li Y, Qu R et al. Axonal sprouting into the denervated spinal cord and synaptic and postsynaptic protein expression in the spinal cord after transplantation of bone marrow stromal cell in stroke rats. Brain Res 2007; 1149:172-180.
17. Onda T, Honmou O, Harada K et al. Therapeutic benefits by human mesenchymal stem cells (hMSCs) and Ang-1 gene-modified hMSCs after cerebral ischemia. J Cereb Blood Flow Metab 2008;28:329-340.
18. Shen LH, Li Y, Chen J et al. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 2007;27:6-13.
19. Shen LH, Li Y, Chen J et al. One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke 2007;38:2150-2156.
20. Allers C, Sierralta WD, Neubauer S et al. Dynamic of distribution of human bone marrow-derived mesenchymal stem cells after transplantation into adult unconditioned mice. Transplantation 2004;78:503-508.
21. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003;108:863-868.
22. Bindslev L, Haack-Sorensen M, Bisgaard K et al. Labelling of human mesenchymal stem cells with indium-111 for SPECT imaging: Effect on cell proliferation and differentiation. Eur J Nucl Med Mol Imaging 2006;33:1171-1177.
23. Correa PL, Mesquita CT, Felix RM et al. Assessment of intra-arterial injected autologous bone marrow mononuclear cell distribution by radioactive labeling in acute ischemic stroke. Clin Nucl Med 2007;32:839-841.
24. de Haro J, Zurita M, Ayllon L et al. Detection of 111In-oxine-labeled bone marrow stromal cells after intravenous or intralesional administration in chronic paraplegic rats. Neurosci Lett 2005;377:7-11.
25. Detante O, Moisan A, Dimastromatteo J et al. Intravenous administration of 99mTcHMPAO-labeled human mesenchymal stem cells after stroke: In vivo imaging and biodistribution. Cell Transplant 2009;18:1369-1379.
26. Gao J, Dennis JE, Muzic RF et al. The dynamic in vivo distribution of bone marrow-derived mesenchymal stem cells after infusion. Cells Tissues Organs 2001;169:12-20.
27. Kraitchman DL, Tatsumi M, Gilson WD et al. Dynamic imaging of allogeneic mesenchymal stem cells trafficking to myocardial infarction. Circulation 2005;112:1451-1461.
28. Brenner W, Aicher A, Eckey T et al. 111Inlabeled CD34 hematopoietic progenitor cells in a rat myocardial infarction model. J Nucl Med 2004;45:512-518.
29. Arbab AS, Pandit SD, Anderson SA et al. Magnetic resonance imaging and confocal microscopy studies of magnetically labeled endothelial progenitor cells trafficking to sites of tumor angiogenesis. STEM CELLS 2006;24:671-678.
30. Bulte JWM, Kraitchman DL. Iron oxide MR contrast agents for molecular and cellular imaging. NMr Biomed 2004;17:484-499.
31. Hinds KA, Hill JM, Shapiro EM et al. Highly efficient endosomal labeling of progenitor and stem cells with large magnetic particles allows magnetic resonance imaging of single cells. Blood 2003;102:867-872.
32. Hauger O, Frost EE, van Heeswijk R et al. MR evaluation of the glomerular homing of magnetically labeled mesenchymal stem cells in a rat model of nephropathy. Radiology 2006; 238:200-210.
33. Ittrich H, Lange C, Togel F et al. In vivo magnetic resonance imaging of iron oxide-labeled, arterially-injected mesenchymal stem cells in kidneys of rats with acute ischemic kid-ney injury: Detection and monitoring at 3T. J Magn Reson Imaging 2007;25:1179-1191.
34. Hill JM, Dick AJ, Raman VK et al. Serial cardiac magnetic resonance imaging of injected mesenchymal stem cells. Circulation 2003;108:1009-1014.
35. Kraitchman DL, Heldman AW, Atalar E et al. In vivo magnetic resonance imaging of mesenchymal stem cells in myocardial infarction. Circulation 2003;107:2290-2293.
36. Bulte JW, 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 1999;96:15256-15261.
37. Bulte JWM, Duncan ID, Frank JA. In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J Cereb Blood Flow Metab 2002;22:899-907.
38. 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 2002;99: 16267-16272.
39. Jendelová P, Herynek V, DeCroos J et al. Imaging the fate of implanted bone marrow stromal cells labeled with superparamagnetic nanoparticles. Magn Reson Med 2003;50:767-776.
40. Shyu W-C, Chen C-P, Lin S-Z et al. Efficient tracking of non-iron-labeled mesenchymal stem cells with serial MRI in chronic stroke rats. Stroke 2007;38:367-374.
41. Shapiro EM, Skrtic S, Sharer K et al. MRI detection of single particles for cellular imaging. Proc Natl Acad Sci USA 2004;101:10901-10906.
42. Valable S, Barbier EL, Bernaudin M et al. In vivo MRI tracking of exogenous monocytes/macrophages targeting brain tumors in a rat model of glioma. Neuroimage 2007;37(suppl 1):S47-S58.
43. Lewin M, Carlesso N, Tung CH et al. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat Biotechnol 2000;18:410-414.
44. Arbab AS, Yocum GT, Kalish H et al. Efficient magnetic cell labeling with protamine sulfate complexed to ferumoxides for cellular MRI. Blood 2004;104:1217-1223.
45. Arbab AS, Yocum GT, Rad AM et al. Labeling of cells with ferumoxides-protamine sulfate complexes does not inhibit function or differentiation capacity of hematopoietic or mesenchymal stem cells. NMR Biomed 2005; 18:553-559.
46. Kostura L, Kraitchman DL, Mackay AM et al. Feridex labeling of mesenchymal stem cells inhibits chondrogenesis but not adipogenesis or osteogenesis. NMR Biomed 2004;17:513-517.
47. Walczak P, Zhang J, Gilad AA et al. Dualmodality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 2008;39:1569-1574.
48. Farrell E, Wielopolski P, Pavljasevic P et al. Effects of iron oxide incorporation for long term cell tracking on MSC differentiation in vitro and in vivo. Biochem Biophys Res Commun 2008;369:1076-1081.
49. Hsiao J-K, Tai M-F, Chu H-H et al. Magnetic nanoparticle labeling of mesenchymal stem cells without transfection agent: Cellular behavior and capability of detection with clinical 1.5 T magnetic resonance at the single cell level. Magn Reson Med 2007;58:717-724.
50. Moriscot C, de Fraipont F, Richard M-J et al. Human bone marrow mesenchymal stem cells can express insulin and key transcription factors of the endocrine pancreas developmental pathway upon genetic and/or microenvironmental manipulation in vitro. STEM CELLS 2005;23:594-603.
51. Grillon E, Provent P, Montigon O et al. Blood-brain barrier permeability to manganese and to Gd-DOTA in a rat model of transient cerebral ischaemia. NMR Biomed 2008; 21:427-436.
52. Longa EZ, Weinstein PR, Carlson S et al. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989;20: 84-91.
53. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press, 1998.
54. Kim D, Chun B-G, Kim Y-K et al. In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant 2008;16: 1007-1012.
55. Heyn C, Ronald JA, Mackenzie LT et al. In vivo magnetic resonance imaging of single cells in mouse brain with optical validation. Magn Reson Med 2006;55:23-29.
56. Shapiro EM, Sharer K, Skrtic S et al. In vivo detection of single cells by MRI. Magn Reson Med 2006;55:242-249.
57. Nohroudi K, Arnhold S, Berhorn T et al. In vivo MRI stem cell tracking requires balancing of detection limit and cell viability. Cell Transplant 2010;19:431-441.
58. Crabbe A, Vandeputte C, Dresselaers T et al. Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant 2010;19:919-936.
59. Danchuk S, Ylostalo JH, Hossain F et al. Human multipotent stromal cells attenuate lipopolysaccharide-induced acute lung injury in mice via secretion of tumor necrosis factor--induced protein 6. Stem Cell Res Ther 2011;2:27.
60. Naqvi S, Samim M, Abdin M et al. Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int J Nanomedicine 2010;16:983-989.
61. Corot C, Robert P, Idée JM et al. Recent advances in iron oxide nanocrystal technology for medical imaging. Adv Drug Deliv Rev 2006; 58:1471-1504.
62. Cengelli F, Maysinger D, Tschudi-Monnet F et al. Interaction of functionalized superparamagnetic iron oxide nanoparticles with brain structures. J Pharmacol Exp Ther 2006;318: 108-116.