In vivo monitoring of adult neurogenesis in health and disease

Frontiers in Neuroscience

Volumn , Issue MAY, 2011, Pages

  Couillard Despres, Sebastien ^a   Vreys, Ruth ^b   Aigner, Ludwig ^a   Van der Linden, Annemie ^b  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Bioluminescence; Fluorescence; MPIO; MRI; MRS; Neurogenesis; Optical imaging; PET

Indexed keywords

DOUBLECORTIN; FERRITIN; GREEN FLUORESCENT PROTEIN; IRON OXIDE;

BIOLUMINESCENCE; CELL LABELING; CELL MIGRATION; CELLULAR DISTRIBUTION; FLUORESCENCE IMAGING; HUMAN; IN VIVO STUDY; IRON STORAGE; MONITORING; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTICAL TOMOGRAPHY; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; RADIOFREQUENCY; REPORTER GENE; REVIEW;

EID: 84857645293     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2011.00067     Document Type: Review

References (91)

1. Altman, J., and Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319-335.
2. Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., and Lindvall, O. (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8, 963-970.
3. Ben-Hur, T., van Heeswijk, R. B., Einstein, O., Aharonowiz, M., Xue, R., Frost, E. E., Mori, S., Reubinoff, B. E., and Bulte, J. W. M. (2007). Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn. Reson. Med. 57, 164-171.
4. Bulte, J. W., Brooks, R. A., Moskowitz, B. M., Bryant, L. H. Jr., and Frank, J. A. (1999). Relaxometry and magnetometry of the MR contrast agent MION-46L. Magn. Reson. Med. 42, 379-384.
5. Bulte, J. W., Duncan, I. D., and Frank, J. A. (2002). In vivo magnetic resonance tracking of magnetically labeled cells after transplantation. J. Cereb. Blood Flow Metab. 22, 899-907.
6. Bulte, J. W., and Kraitchman, D. L. (2004). Monitoring cell therapy using iron oxide MR contrast agents. Curr. Pharm. Biotechnol. 5, 567-584.
7. Cameron, H. A., Woolley, C. S., McEwen, B. S., and Gould, E. (1993). Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience 56, 337-344.
8. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A., and Lledo, P. M. (2003). Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518.
9. Cohen, B., Dafni, H., Meir, G., Harmelin, A., and Neeman, M. (2005). Ferritin as an endogenous MRI reporter for noninvasive imaging of gene expression in C6 glioma tumors. Neoplasia 7, 109-117.
10. Cohen, M. E., Muja, N., Fainstein, N., Bulte, J. W. M., and Ben-Hur, T. (2010). Conserved fate and function of ferumoxides-labeled neural precursor cells in vitro and in vivo. J. Neurosci. Res. 88, 936-944.
11. Conover, J. C., and Allen, R. L. (2002). The subventricular zone: new molecular and cellular developments. Cell. Mol. Life Sci. 59, 2128-2135.
12. Couillard-Despres, S., Finkl, R., Winner, B., Ploetz, S., Wiedermann, D., Aigner, R., Bogdahn, U., Winkler, J., Hoehn, M., and Aigner, L. (2008a). In vivo optical imaging of neurogenesis: watching new neurons in the intact brain. Mol. Imaging 7, 28-34.
13. Couillard-Despres, S., Quehl, E., Altendorfer, K., Karl, C., Ploetz, S., Bogdahn, U., Winkler, J., and Aigner, L. (2008b). Human in vitro reporter model of neuronal development and early differentiation processes. BMC Neurosci. 9, 31. doi: 10.1186/1471-2202-9-31
14. Couillard-Despres, S., Winner, B., Karl, C., Lindemann, G., Schmid, P., Aigner, R., Laemke, J., Bogdahn, U., Winkler, J., Bischofberger, J., and Aigner, L. (2006). Targeted transgene expression in neuronal precursors: watching young neurons in the old brain. Eur. J. Neurosci. 24, 1535-1545.
15. Couillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H. G., and Aigner, L. (2005). Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21, 1-14.
16. Crabbe, A., Vandeputte, C., Dresselaers, T., Sacido, A. A., Verdugo, J. M. G., Eyckmans, J., Luyten, F. P., Van Laere, K., Verfaillie, C. M., and Himmelreich, U. (2010). Effects of MRI contrast agents on the stem cell phenotype. Cell Transplant. 19, 919-936.
17. Curtis, M. A., Penney, E. B., Pearson, A. G., van Roon-Mom, W. M., Butterworth, N. J., Dragunow, M., Connor, B., and Faull, R. L. (2003). Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc. Natl. Acad. Sci. U.S.A. 100, 9023-9027.
18. Curtis, M. A., Penney, E. B., Pearson, J., Dragunow, M., Connor, B., and Faull, R. L. (2005). The distribution of progenitor cells in the subependymal layer of the lateral ventricle in the normal and Huntington's disease human brain. Neuroscience 132, 777-788.
19. Deliolanis, N. C., Kasmieh, R., Wurdinger, T., Tannous, B. A., Shah, K., and Ntziachristos, V. (2008). Performance of the red-shifted fluorescent proteins in deep-tissue molecular imaging applications. J. Biomed. Opt. 13, 044008.
20. Dong, Z., Dreher, W., Leibfritz, D., and Peterson, B. S. (2009). Challenges of using MR spectroscopy to detect neural progenitor cells in vivo. AJNR Am. J. Neuroradiol. 30, 1096-1101.
21. Donovan, M. H., Yazdani, U., Norris, R. D., Games, D., German, D. C., and Eisch, A. J. (2006). Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J. Comp. Neurol. 495, 70-83.
22. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., and Gage, F. H. (1998). Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
23. Frank, J. A., Anderson, S. A., Kalsih, H., Jordan, E. K., Lewis, B. K., Yocum, G. T., and Arbab, A. S. (2004). Methods for magnetically labeling stem and other cells for detection by in vivo magnetic resonance imaging. Cytotherapy 6, 621-625.
24. Friedman, S. D. (2008). Comment on "magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain." Science 321, 640.
25. Fuhrmann, M., Mitteregger, G., Kretzschmar, H., and Herms, J. (2007). Dendritic pathology in prion disease starts at the synaptic spine. J. Neurosci. 27, 6224-6233.
26. Garofalakis, A., Zacharakis, G., Meyer, H., Economou, E. N., Mamalaki, C., Papamatheakis, J., Kioussis, D., Ntziachristos, V., and Ripoll, J. (2007). Three-dimensional in vivo imaging of green fluorescent protein-expressing T cells in mice with noncontact fluorescence molecular tomography. Mol. Imaging 6, 96-107.
27. Gass, A., Niendorf, T., and Hirsch, J. G. (2001). Acute and chronic changes of the apparent diffusion coefficient in neurological disorders-biophysical mechanisms and possible underlying histopathology. J. Neurol. Sci. 186(Suppl. 1), S15-S23.
28. Genove, G., DeMarco, U., Xu, H., Goins, W. F., and Ahrens, E. T. (2005). A new transgene reporter for in vivo magnetic resonance imaging. Nat. Med. 11, 450-454.
29. Gil, J. M., Mohapel, P., Araujo, I. M., Popovic, N., Li, J. Y., Brundin, P., and Petersen, A. (2005). Reduced hippocampal neurogenesis in R6/2 transgenic Huntington's disease mice. Neurobiol. Dis. 20, 744-751.
30. Goldhawk, D. E., Lemaire, C., McCreary, C. R., McGirr, R., Dhanvantari, S., Thompson, R. T., Figueredo, R., Koropatnick, J., Foster, P., and Prato, F. S. (2009). Magnetic resonance imaging of cells overexpressing MagA, an endogenous contrast agent for live cell imaging. Mol. Imaging 8, 129-139.
31. Gossuin, Y., Muller, R. N., and Gillis, P. (2004). Relaxation induced by ferritin: a better understanding for an improved MRI iron quantification. NMR Biomed. 17, 427-432.
32. Haughey, N. J., Nath, A., Chan, S. L., Borchard, A. C., Rao, M. S., and Mattson, M. P. (2002). Disruption of neurogenesis by amyloid beta-peptide, and perturbed neural progenitor cell homeostasis, in models of Alzheimer's disease. J. Neurochem. 83, 1509-1524.
33. Heim, R., Prasher, D. C., and Tsien, R. Y. (1994). Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. U.S.A. 91, 12501-12504.
34. Hoch, J. C., Maciejewski, M. W., and Gryk, M. R. (2008). Comment on "magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain." Science 321, 640.
35. Hoehn, M., Kustermann, E., Blunk, J., Wiedermann, D., Trapp, T., Wecker, S., Focking, M., Arnold, H., Hescheler, J., Fleischmann, B. K., Schwindt, W., and Buhrle, C. (2002). 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. U.S.A. 99, 16267-16272.
36. Hoglinger, G. U., Rizk, P., Muriel, M. P., Duyckaerts, C., Oertel, W. H., Caille, I., and Hirsch, E. C. (2004). Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 7, 726-735.
37. Jansen, J. F., Gearhart, J. D., and Bulte, J. W. (2008). Comment on "Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain." Science 321, 640.
38. Jendelova, P., Herynek, V., DeCroos, J., Glogarova, K., Andersson, B., Hajek, M., and Sykova, E. (2003). Imaging the fate of implanted bone marrow stromal cells labeled with superparamagnetic nanoparticles. Magn. Reson. Med. 50, 767-776.
39. Jin, K., Minami, M., Lan, J. Q., Mao, X. O., Batteur, S., Simon, R. P., and Greenberg, D. A. (2001). Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. U.S.A. 98, 4710-4715.
40. Kandasamy, M., Couillard-Despres, S., Raber, K. A., Stephan, M., Lehner, B., Winner, B., Kohl, Z., Rivera, F. J., Nguyen, H. P., Riess, O., Bogdahn, U., Winkler, J., von Horsten, S., and Aigner, L. (2010). Stem cell quiescence in the hippocampal neurogenic niche is associated with elevated transforming growth factor-beta signaling in an animal model of Huntington disease. J. Neuropathol. Exp. Neurol. 69, 717-728.
41. Karl, C., Couillard-Despres, S., Prang, P., Munding, M., Kilb, W., Brigadski, T., Plotz, S., Mages, W., Luhmann, H., Winkler, J., Bogdahn, U., and Aigner, L. (2005). Neuronal precursor-specific activity of a human doublecortin regulatory sequence. J. Neurochem. 92, 264-282.
42. Kaur, D., Rajagopalan, S., and Andersen, J. K. (2009). Chronic expression of H-ferritin in dopaminergic midbrain neurons results in an age-related expansion of the labile iron pool and subsequent neurodegeneration: implications for Parkinson's disease. Brain Res. 1297, 17-22.
43. Kaur, D., Rajagopalan, S., Chinta, S., Kumar, J., Di Monte, D., Cherny, R. A., and Andersen, J. K. (2007). Chronic ferritin expression within murine dopaminergic midbrain neurons results in a progressive age-related neurodegeneration. Brain Res. 1140, 188-194.
44. Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M., and Gage, F. H. (2003). Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130, 391-399.
45. Kohl, Z., Kandasamy, M., Winner, B., Aigner, R., Gross, C., Couillard-Despres, S., Bogdahn, U., Aigner, L., and Winkler, J. (2007). Physical activity fails to rescue hippocampal neurogenesis deficits in the R6/2 mouse model of Huntington's disease. Brain Res. 1155, 24-33.
46. Kustermann, E., Himmelreich, U., Kandal, K., Geelen, T., Ketkar, A., Wiedermann, D., Strecker, C., Esser, J., Arnhold, S., and Hoehn, M. (2008). Efficient stem cell labeling for MRI studies. Contrast Media Mol. Imaging 3, 27-37.
47. Ladewig, J., Koch, P., Endl, E., Meiners, B., Opitz, T., Couillard-Despres, S., Aigner, L., and Brustle, O. (2008). Lineage selection of functional and cryopreservable human embryonic stem cell-derived neurons. Stem Cells 26, 1705-1712.
48. Lazic, S. E., Grote, H., Armstrong, R. J., Blakemore, C., Hannan, A. J., van Dellen, A., and Barker, R. A. (2004). Decreased hippocampal cell proliferation in R6/1 Huntington's mice. Neuroreport 15, 811-813.
49. Le Bihan, D., Breton, E., Lallemand, D., Grenier, P., Cabanis, E., and Laval-Jeantet, M. (1986). MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161, 401-407.
50. Lee, K. H., Byun, S. S., Paik, J. Y., Lee, S. Y., Song, S. H., Choe, Y. S., and Kim, B. T. (2003). Cell uptake and tissue distribution of radioiodine labelled d-luciferin: implications for luciferase based gene imaging. Nucl. Med. Commun. 24, 1003-1009.
51. Liu, J., Solway, K., Messing, R. O., and Sharp, F. R. (1998). Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils. J. Neurosci. 18, 7768-7778.
52. Lois, C., and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
53. Ma, D. K., Bonaguidi, M. A., Ming, G. L., and Song, H. (2009). Adult neural stem cells in the mammalian central nervous system. Cell Res. 19, 672-682.
54. Magavi, S. S., Leavitt, B. R., and Macklis, J. D. (2000). Induction of neurogenesis in the neocortex of adult mice. Nature 405, 951-955.
55. Magnitsky, S., Watson, D. J., Walton, R. M., Pickup, S., Bulte, J. W., Wolfe, J. H., and Poptani, H. (2005). In vivo and ex vivo MRI detection of localized and disseminated neural stem cell grafts in the mouse brain. Neuroimage 26, 744-754.
56. Manganas, L. N., Zhang, X., Li, Y., Hazel, R. D., Smith, S. D., Wagshul, M. E., Henn, F., Benveniste, H., Djuric, P. M., Enikolopov, G., and Maletic-Savatic, M. (2007). Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318, 980-985.
57. Markakis, E. A., and Gage, F. H. (1999). Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J. Comp. Neurol. 406, 449-460.
58. Marxreiter, F., Nuber, S., Kandasamy, M., Klucken, J., Aigner, R., Burgmayer, R., Couillard-Despres, S., Riess, O., Winkler, J., and Winner, B. (2009). Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein. Eur. J. Neurosci. 29, 879-890.
59. Modo, M., Hoehn, M., and Bulte, J. W. (2005). Cellular MR imaging. Mol. Imaging 4, 143-164.
60. Nieman, B. J., Shyu, J. Y., Rodriguez, J. J., Garcia, A. D., Joyner, A. L., and Turnbull, D. H. (2010). In vivo MRI of neural cell migration dynamics in the mouse brain. Neuroimage 50, 456-464.
61. Norman, A. B., Thomas, S. R., Pratt, R. G., Lu, S. Y., and Norgren, R. B. (1992). Magnetic resonance imaging of neural transplants in rat brain using a superparamagnetic contrast agent. Brain Res. 594, 279-283.
62. Panizzo, R. A., Kyrtatos, P. G., Price, A. N., Gadian, D. G., Ferretti, P., and Lythgoe, M. F. (2009). In vivo magnetic resonance imaging of endogenous neuroblasts labelled with a ferumoxide-polycation complex. Neuroimage 44, 1239-1246.
63. Parent, J. M., Vexler, Z. S., Gong, C., Derugin, N., and Ferriero, D. M. (2002). Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann. Neurol. 52, 802-813.
64. Parent, J. M., Yu, T. W., Leibowitz, R. T., Geschwind, D. H., Sloviter, R. S., and Lowenstein, D. H. (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17, 3727-3738.
65. Pfeuffer, J., Tkac, I., Provencher, S. W., and Gruetter, R. (1999). Toward an in vivo neurochemical profile: quantification of 18 metabolites in short-echo-time (1)H NMR spectra of the rat brain. J. Magn. Reson. 141, 104-120.
66. Pichler, A., Prior, J. L., and Piwnica-Worms, D. (2004). Imaging reversal of multidrug resistance in living mice with bioluminescence: MDR1 P-glycoprotein transports coelenterazine. Proc. Natl. Acad. Sci. U.S.A. 101, 1702-1707.
67. Ramm, P., Couillard-Despres, S., Plotz, S., Rivera, F. J., Krampert, M., Lehner, B., Kremer, W., Bogdahn, U., Kalbitzer, H. R., and Aigner, L. (2009). A nuclear magnetic resonance biomarker for neural progenitor cells: is it all neurogenesis? Stem Cells 27, 420-423.
68. Reumers, V., Deroose, C. M., Krylyshkina, O., Nuyts, J., Geraerts, M., Mortelmans, L., Gijsbers, R., Van den Haute, C., Debyser, Z., and Baekelandt, V. (2008). Noninvasive and quantitative monitoring of adult neuronal stem cell migration in mouse brain using bioluminescence imaging. Stem Cells 26, 2382-2390.
69. Reynolds, B. A., and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
70. Rueger, M. A., Backes, H., Walberer, M., Neumaier, B., Ullrich, R., Simard, M. L., Emig, B., Fink, G. R., Hoehn, M., Graf, R., and Schroeter, M. (2010). Noninvasive imaging of endogenous neural stem cell mobilization in vivo using positron emission tomography. J. Neurosci. 30, 6454-6460.
71. Schafer, R. (2010). Labeling and imaging of stem cells - promises and concerns. Transfus. Med. Hemother. 37, 85-89.
72. Shaner, N. C., Campbell, R. E., Steinbach, P. A., Giepmans, B. N., Palmer, A. E., and Tsien, R. Y. (2004). Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22, 1567-1572.
73. Shapiro, E. M., Gonzalez-Perez, O., Garcia-Verdugo, J. M., Alvarez-Buylla, A., and Koretsky, A. P. (2006a). Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 32, 1150-1157.
74. Shapiro, E. M., Sharer, K., Skrtic, S., and Koretsky, A. P. (2006b). In vivo detection of single cells by MRI. Magn. Reson. Med. 55, 242-249.
75. Slotkin, J. R., Cahill, K. S., Tharin, S. A., and Shapiro, E. M. (2007). Cellular magnetic resonance imaging: nanometer and micrometer size particles for noninvasive cell localization. Neurotherapeutics 4, 428-433.
76. Stanfield, B. B., and Trice, J. E. (1988). Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp. Brain Res. 72, 399-406.
77. Sumner, J. P., Shapiro, E. M., Maric, D., Conroy, R., and Koretsky, A. P. (2009). In vivo labeling of adult neural progenitors for MRI with micron sized particles of iron oxide: quantification of labeled cell phenotype. Neuroimage 44, 671-678.
78. Toni, N., Laplagne, D. A., Zhao, C., Lombardi, G., Ribak, C. E., Gage, F. H., and Schinder, A. F. (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat. Neurosci. 11, 901-907.
79. van Praag, H., Shubert, T., Zhao, C., and Gage, F. H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680-8685.
80. 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., and Baekelandt, V. (2011). 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. [Epub ahead of print].
81. Vreys, R., Soenen, S. J., De, C. M., and Van der Linden, A. (2011). Background migration of USPIO/MLs is a major drawback for in situ labeling of endogenous neural progenitor cells. Contrast Media Mol. Imaging 6, 1-6.
82. Vreys, R., Vande Velde, G., Krylychkina, O., Vellema, M., Verhoye, M., Timmermans, J. P., Baekelandt, V., and Van der Linden, A. (2010). MRI visualization of endogenous neural progenitor cell migration along the RMS in the adult mouse brain: validation of various MPIO labeling strategies. Neuroimage 49, 2094-2103.
83. Wen, P. H., Hof, P. R., Chen, X., Gluck, K., Austin, G., Younkin, S. G., Younkin, L. H., DeGasperi, R., Gama Sosa, M. A., Robakis, N. K., Haroutunian, V., and Elder, G. A. (2004). The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp. Neurol. 188, 224-237.
84. Winner, B., Cooper-Kuhn, C. M., Aigner, R., Winkler, J., and Kuhn, H. G. (2002). Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci. 16, 1681-1689.
85. Winner, B., Lie, D. C., Rockenstein, E., Aigner, R., Aigner, L., Masliah, E., Kuhn, H. G., and Winkler, J. (2004). Human wild-type alpha-synuclein impairs neurogenesis. J. Neuropathol. Exp. Neurol. 63, 1155-1166.
86. Winner, B., Rockenstein, E., Lie, D. C., Aigner, R., Mante, M., Bogdahn, U., Couillard-Despres, S., Masliah, E., and Winkler, J. (2008). Mutant alpha-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol. Aging 29, 913-925.
87. Yamaguchi, M., Saito, H., Suzuki, M., and Mori, K. (2000). Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 11, 1991-1996.
88. Yang, J., Liu, J., Niu, G., Chan, K. C., Wang, R., Liu, Y., and Wu, E. X. (2009). In vivo MRI of endogenous stem/Progenitor cell migration from subventricular zone in normal and injured developing brains. Neuroimage 48, 319-328.
89. Zhang, R. L., Zhang, Z. G., Zhang, L., and Chopp, M. (2001). Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105, 33-41.
90. Zhao, H., Doyle, T. C., Wong, R. J., Cao, Y., Stevenson, D. K., Piwnica-Worms, D., and Contag, C. H. (2004). Characterization of coelenterazine analogs for measurements of Renilla luciferase activity in live cells and living animals. Mol. Imaging 3, 43-54.
91. Zurkiya, O., Chan, A. W., and Hu, X. (2008). MagA is sufficient for producing magnetic nanoparticles in mammalian cells, making it an MRI reporter. Magn. Reson. Med. 59, 1225-1231.