Quantitative evaluation of MRI-based tracking of ferritin-labeled endogenous neural stem cell progeny in rodent brain

NeuroImage

Volumn 62, Issue 1, 2012, Pages 367-380

  Vande Velde, Greetje ^a,b   Raman Rangarajan, Janaki ^b,c   Vreys, Ruth ^d   Guglielmetti, Caroline ^d   Dresselaers, Tom ^a,b   Verhoye, Marleen ^d   Van der Linden, Annemie ^d   Debyser, Zeger ^e   Baekelandt, Veerle ^f   Maes, Frederik ^b,c   Himmelreich, Uwe ^a,b  

^a DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

^b KU Leuven   (Belgium)

^c UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^d UNIVERSITY OF ANTWERP   (Belgium)

^e DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^f UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Bias field correction; Cell tracking; Endogenous neurogenesis; Ferritin; Image processing; Neural stem cells; Reporter gene

Indexed keywords

FERRITIN; IRON OXIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL DIVISION; CELL MIGRATION; CELL TRACKING; CONTROLLED STUDY; DILUTION; EX VIVO STUDY; FEMALE; IMAGE ANALYSIS; IN VIVO STUDY; MOUSE; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; PRIORITY JOURNAL; PROGENY; QUANTITATIVE ANALYSIS; REPORTER GENE; SENSITIVITY ANALYSIS; STEM CELL;

ANIMALS; CELL TRACKING; CONTRAST MEDIA; FEMALE; FERRITINS; IMAGE ENHANCEMENT; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED C57BL; NEURONS; OLFACTORY BULB; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; STAINING AND LABELING; STEM CELLS;

EID: 84861640008     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.04.040     Document Type: Article

References (54)

1. Alvarez-Buylla A., Garcia-Verdugo J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 2002, 22:629-634.
2. Baekelandt V., Claeys A., Eggermont K., Lauwers E., De Strooper B., Nuttin B., Debyser Z. Characterization of lentiviral vector-mediated gene transfer in adult mouse brain. Hum. Gene Ther. 2002, 13:841-853.
3. Baekelandt V., Eggermont K., Michiels M., Nuttin B., Debyser Z. Optimized lentiviral vector production and purification procedure prevents immune response after transduction of mouse brain. Gene Ther. 2003, 10:1933-1940.
4. Bennett K.M., Shapiro E.M., Sotak C.H., Koretsky A.P. Controlled aggregation of ferritin to modulate MRI relaxivity. Biophys. J. 2008, 95:342-351.
5. Cohen B., Dafni H., Meir G., Harmelin A., Neeman M. Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 2005, 7:109-117.
6. Cohen B., Ziv K., Plaks V., Israely T., Kalchenko V., Harmelin A., Benjamin L.E., Neeman M. MRI detection of transcriptional regulation of gene expression in transgenic mice. Nat. Med. 2007, 13:498-503.
7. Consiglio A., Gritti A., Dolcetta D., Follenzi A., Bordignon C., Gage F.H., Vescovi A.L., Naldini L. Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:14835-14840.
8. Couillard-Despres S., Vreys R., Aigner L., Van der Linden A. In vivo monitoring of adult neurogenesis in health and disease. Front. Neurosci. 2011, 5:67.
9. Cozzi A., Corsi B., Levi S., Santambrogio P., Albertini A., Arosio P. Overexpression of wild type and mutated human ferritin H-chain in HeLa cells: in vivo role of ferritin ferroxidase activity. J. Biol. Chem. 2000, 275:25122-25129.
10. Deroose C.M., Reumers V., Gijsbers R., Bormans G., Debyser Z., Mortelmans L., Baekelandt V. Noninvasive monitoring of long-term lentiviral vector-mediated gene expression in rodent brain with bioluminescence imaging. Mol. Ther. 2006, 14:423-431.
11. Deroose C.M., Reumers V., Debyser Z., Baekelandt V. Seeing genes at work in the living brain with non-invasive molecular imaging. Curr. Gene Ther. 2009, 9:212-238.
12. Eriksson P.S., Perfilieva E., Bjork-Eriksson T., Alborn A.M., Nordborg C., Peterson D.A., Gage F.H. Neurogenesis in the adult human hippocampus. Nat. Med. 1998, 4:1313-1317.
13. Genove G., DeMarco U., Xu H., Goins W.F., Ahrens E.T. A new transgene reporter for in vivo magnetic resonance imaging. Nat. Med. 2005, 11:450-454.
14. Geraerts M., Michiels M., Baekelandt V., Debyser Z., Gijsbers R. Upscaling of lentiviral vector production by tangential flow filtration. J. Gene Med. 2005, 7:1299-1310.
15. Geraerts M., Eggermont K., Hernandez-Acosta P., Garcia-Verdugo J.M., Baekelandt V., Debyser Z. Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum. Gene Ther. 2006, 17:635-650.
16. Geraerts M., Krylyshkina O., Debyser Z., Baekelandt V. Concise review: therapeutic strategies for Parkinson disease based on the modulation of adult neurogenesis. Stem Cells 2007, 25:263-270.
17. Gilad A.A., Ziv K., McMahon M.T., van Zijl P.C., Neeman M., Bulte J.W. MRI reporter genes. J. Nucl. Med. 2008, 49:1905-1908.
18. Gossuin Y., Muller R.N., Gillis P. Relaxation induced by ferritin: a better understanding for an improved MRI iron quantification. NMR Biomed. 2004, 17:427-432.
19. Granot D., Scheinost D., Markakis E.A., Papademetris X., Shapiro E.M. Serial monitoring of endogenous neuroblast migration by cellular MRI. NeuroImage 2011, 57:817-824.
20. Harrison P.M., Arosio P. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Acta 1996, 1275:161-203.
21. Heyn C., Ronald J.A., Ramadan S.S., Snir J.A., Barry A.M., MacKenzie L.T., Mikulis D.J., Palmieri D., Bronder J.L., Steeg P.S., Yoneda T., MacDonald I.C., Chambers A.F., Rutt B.K., Foster P.J. In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn. Reson. Med. 2006, 56:1001-1010.
22. Himmelreich U., Dresselaers T. Cell labeling and tracking for experimental models using magnetic resonance imaging. Methods 2009, 48:112-124.
23. Hoehn M., Wiedermann D., Justicia C., Ramos-Cabrer P., Kruttwig K., Farr T., Himmelreich U. Cell tracking using magnetic resonance imaging. J. Physiol. 2007, 584:25-30.
24. Ibrahimi A., Vande Velde G., Reumers V., Toelen J., Thiry I., Vandeputte C., Vets S., Deroose C., Bormans G., Baekelandt V., Debyser Z., Gijsbers R. Highly efficient multicistronic lentiviral vectors with peptide 2A sequences. Hum. Gene Ther. 2009, 20:845-860.
25. Iordanova B., Ahrens E.T. In vivo magnetic resonance imaging of ferritin-based reporter visualizes native neuroblast migration. NeuroImage 2012, 59:1004-1012.
26. Justicia C., Himmelreich U., Ramos-Cabrer P., Sprenger C., Hoehn M. In vivo tracking of endogenous stem cells by MRI after intraparenchymal injection of iron oxide nanoparticles. Mol. Imaging 2005, 4:351-352.
27. Kraitchman D.L., Bulte J.W. Imaging of stem cells using MRI. Basic Res. Cardiol. 2008, 103:105-113.
28. Levi S., Yewdall S.J., Harrison P.M., Santambrogio P., Cozzi A., Rovida E., Albertini A., Arosio P. Evidence of H- and L-chains have co-operative roles in the iron-uptake mechanism of human ferritin. Biochem. J. 1992, 288(Pt 2):591-596.
29. Likar B., Viergever M.A., Pernus F. Retrospective correction of MR intensity inhomogeneity by information minimization. IEEE Trans. Med. Imaging 2001, 20:1398-1410.
30. Liu J., Cheng E.C., Long R.C., Yang S.H., Wang L., Cheng P.H., Yang J.J., Wu D., Mao H., Chan A.W. Noninvasive monitoring of embryonic stem cells in vivo with MRI transgene reporter. Tissue Eng. Part C Methods 2009, 15:739-747.
31. MacKenzie-Graham A., Lee E.F., Dinov I.D., Bota M., Shattuck D.W., Ruffins S., Yuan H., Konstantinidis F., Pitiot A., Ding Y., Hu G., Jacobs R.E., Toga A.W. A multimodal, multidimensional atlas of the C57BL/6J mouse brain. J. Anat. 2004, 204:93-102.
32. Maes F., Collignon A., Vandermeulen D., Marchal G., Suetens P. Multimodality image registration by maximization of mutual information. IEEE Trans. Med. Imaging 1997, 16:187-198.
33. Magnitsky S., Watson D.J., Walton R.M., Pickup S., Bulte J.W., Wolfe J.H., Poptani H. In vivo and ex vivo MRI detection of localized and disseminated neural stem cell grafts in the mouse brain. NeuroImage 2005, 26:744-754.
34. Massoud T.F., Gambhir S.S. Integrating noninvasive molecular imaging into molecular medicine: an evolving paradigm. Trends Mol. Med. 2007, 13:183-191.
35. Meier D.S., Guttmann C.R. Time-series analysis of MRI intensity patterns in multiple sclerosis. NeuroImage 2003, 20:1193-1209.
36. Mizuguchi H., Xu Z., Ishii-Watabe A., Uchida E., Hayakawa T. IRES-dependent second gene expression is significantly lower than cap-dependent first gene expression in a bicistronic vector. Mol. Ther. 2000, 1:376-382.
37. Modo M., Hoehn M., Bulte J.W. Cellular MR imaging. Mol. Imaging 2005, 4:143-164.
38. Naldini L., Blomer U., Gallay P., Ory D., Mulligan R., Gage F.H., Verma I.M., Trono D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996, 272:263-267.
39. Nieman B.J., Shyu J.Y., Rodriguez J.J., Garcia A.D., Joyner A.L., Turnbull D.H. In vivo MRI of neural cell migration dynamics in the mouse brain. NeuroImage 2010, 50:456-464.
40. Palmer T.D., Schwartz P.H., Taupin P., Kaspar B., Stein S.A., Gage F.H. Cell culture. Progenitor cells from human brain after death. Nature 2001, 411:42-43.
41. Panizzo R.A., Kyrtatos P.G., Price A.N., Gadian D.G., Ferretti P., Lythgoe M.F. In vivo magnetic resonance imaging of endogenous neuroblasts labelled with a ferumoxide-polycation complex. NeuroImage 2009, 44:1239-1246.
42. Reumers V., Deroose C.M., Krylyshkina O., Nuyts J., Geraerts M., Mortelmans L., Gijsbers R., Van den Haute C., Debyser Z., Baekelandt V. Noninvasive and quantitative monitoring of adult neuronal stem cell migration in mouse brain using bioluminescence imaging. Stem Cells 2008, 26:2382-2390.
43. Sanai N., Tramontin A.D., Quinones-Hinojosa A., Barbaro N.M., Gupta N., Kunwar S., Lawton M.T., McDermott M.W., Parsa A.T., Manuel-Garcia Verdugo J., Berger M.S., Alvarez-Buylla A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004, 427:740-744.
44. Shapiro E.M., Gonzalez-Perez O., Manuel Garcia-Verdugo J., Alvarez-Buylla A., Koretsky A.P. Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. NeuroImage 2006, 32:1150-1157.
45. Shapiro E.M., Sharer K., Skrtic S., Koretsky A.P. In vivo detection of single cells by MRI. Magn. Reson. Med. 2006, 55:242-249.
46. Sumner J.P., Shapiro E.M., Maric D., Conroy R., Koretsky A.P. In vivo labeling of adult neural progenitors for MRI with micron sized particles of iron oxide: quantification of labeled cell phenotype. NeuroImage 2009, 44:671-678.
47. Taupin P. Adult neurogenesis, neural stem cells and Alzheimer's disease: developments, limitations, problems and promises. Curr. Alzheimer Res. 2009, 6:461-470.
48. Vande Velde G., Baekelandt V., Dresselaers T., Himmelreich U. Magnetic resonance imaging and spectroscopy methods for molecular imaging. Q. J. Nucl. Med. Mol. Imaging 2009, 53:565-585.
49. Vande Velde G., Raman Rangarajan J., Toelen J., Dresselaers T., Ibrahimi A., Krylychkina O., Vreys R., Van der Linden A., Maes F., Debyser Z., Himmelreich U., Baekelandt V. Evaluation of the specificity and sensitivity of ferritin as an MRI reporter gene in mouse brain using lentiviral and adeno-associated viral vectors. Gene Ther. 2011, 18:594-605.
50. Vandenbosch R., Borgs L., Beukelaers P., Belachew S., Moonen G., Nguyen L., Malgrange B. Adult neurogenesis and the diseased brain. Curr. Med. Chem. 2009, 16:652-666.
51. Vreys R., Vande Velde G., Krylychkina O., Vellema M., Verhoye M., Timmermans J.P., Baekelandt V., Van der Linden A. MRI visualization of endogenous neural progenitor cell migration along the RMS in the adult mouse brain: validation of various MPIO labeling strategies. NeuroImage 2010, 49:2094-2103.
52. Vreys R., Soenen S.J., De Cuyper M., Van der Linden A. Background migration of USPIO/MLs is a major drawback for in situ labeling of endogenous neural progenitor cells. Contrast Media Mol. Imaging 2011, 6:1-6.
53. Wood J.C., Fassler J.D., Meade T. Mimicking liver iron overload using liposomal ferritin preparations. Magn. Reson. Med. 2004, 51:607-611.
54. Yang J., Liu J., Niu G., Chan K.C., Wang R., Liu Y., Wu E.X. In vivo MRI of endogenous stem/progenitor cell migration from subventricular zone in normal and injured developing brains. NeuroImage 2009, 48:319-328.