Noninvasive detection of neural progenitor cells in living brains by MRI

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1652-1662

  Liu, Christina H ^a,b   Ren, Jia Q ^a   You, Zerong ^a   Yang, Jinsheng ^a   Liu, Charng Ming ^a   Uppal, Ritika ^a,c   Liu, Philip K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c GE HEALTHCARE   (United Kingdom)

Author keywords

Angiogenesis; Drug delivery; Pericyte; Pharmacokinetics

Indexed keywords

ALPHA ACTIN; DNA; MESSENGER RNA; NESTIN; PHOSPHOROTHIOIC ACID; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; DRUG DISTRIBUTION; GENETIC TRANSCRIPTION; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; PERICYTE; PRIORITY JOURNAL; PROTEIN DETERMINATION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; BRAIN ISCHEMIA; CAROTID ARTERIES; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MAGNETIC RESONANCE IMAGING; MALE; METAL NANOPARTICLES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; OLIGODEOXYRIBONUCLEOTIDES; PERICYTES;

MUS; MUS MUSCULUS;

EID: 84860912958     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-199547     Document Type: Article

References (38)

1. Liu, C. H., You, Z., Ren, J. Q., Kim, Y. R., Eikermann-Haerter, K., and Liu, P. K. (2008) Noninvasive delivery of gene targeting probes to live brains for transcription MRI. FASEB J. 22, 193-203
2. Alliot, F., Rutin, J., Leenan, P. J., and Pessac, B. (1999) Pericytes and periendothelial cells of brain parenchyma vessels co-express aminopeptidase N, aminopeptidase A, and nestin. J. Neurosci. Res. 58, 367-378 (Pubitemid 29508570)
3. Abrahams, J. M., Lenart, C. J., and Tobias, M. E. (2009) Temporal variation of induction neurogenesis in a rat model of transient middle cerebral artery occlusion. Neurol. Res. 31, 528-533
4. Dore-Duffy, P., Katychev, A., Wang, X., and Van Buren, E. (2006) CNS microvascular pericytes exhibit multipotential stem cell activity. J. Cereb. Blood Flow Metab. 26, 613-624
5. Kokovay, E., Li, L., and Cunningham, L. A. (2006) Angiogenic recruitment of pericytes from bone marrow after stroke. J. Cereb. Blood Flow Metab. 26, 545-555
6. Rodriguez-Baeza, A., Reina-De La Torre, F., Ortega-Sanchez, M., and Sahuquillo-Barris, J. (1998) Perivascular structures in corrosion casts of the human central nervous system: a confocal laser and scanning electron microscope study. Anat. Rec. 252, 176-184 (Pubitemid 28440902)
7. Hughes, S., and Chan-Ling, T. (2004) Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest. Ophthalmol. Vis. Sci. 45, 2795-2806 (Pubitemid 38998879)
8. Bergers, G., and Song, S. (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro. Oncol. 7, 452-464 (Pubitemid 41555617)
9. Liu, C. H., Ren, J. Q., Yang, J., Liu, C. M., Mandeville, J. B., Rosen, B. R., Bhide, P. G., Yanagawa, Y., and Liu, P. K. (2009) DNA-based MRI probes for specific detection of chronic exposure to amphetamine in living brains. J. Neurosci. 29, 10663-10670
10. Minamishima, S., Bougaki, M., Sips, P. Y., Yu, J. D., Minamishima, Y. A., Elrod, J. W., Lefer, D. J., Bloch, K. D., and Ichinose F (2009) Hydrogen sulfide improves survival after cardiac arrest and cardiopulmonary resuscitation via a nitric oxide synthase 3-dependent mechanism in mice. Circulation 120, 888-896
11. Liu, C. H., You, Z., Liu, C. M., Kim, Y. R., Whalen, M. J., Rosen, B. R., and Liu, P. K. (2009) Diffusion-weighted magnetic resonance imaging reversal by gene knockdown of matrix metalloproteinase-9 activities in live animal brains. J. Neurosci. 29, 3508-3617
12. Liu, P. K., Hsu, C. Y., Dizdaroglu M, Floyd, R. A., Kow, Y. W., Karakaya A, Rabow, L. E., and Cui, J. K. (1996) Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. J. Neurosci. 16, 6795-6806 (Pubitemid 26359363)
13. Huang, D., Shenoy, A., Cui, J., Huang, W., and Liu, P. K. (2000) In situ detection of AP sites and DNA strand breaks bearing 3′-phosphate termini in ischemic mouse brain. FASEB J. 14, 407-417 (Pubitemid 30086078)
14. Yoshioka, H., Niizuma, K., Katsu, M., Okami, N., Sakata, H., Kim, G. S., Narasimhan, P., and Chan, P. H. (2010) NADPH oxidase mediates striatal neuronal injury after transient global cerebral ischemia. J. Cereb. Blood Flow Metab. 31, 868 - 880
15. Minamishima, S., Kida, K., Tokuda, K., Wang, H., Sips, P. Y., Kosugi, S., Mandeville, J. B., Buys, E. S., Brouckaert, P., Liu, P. K., Liu, C. H., Bloch, K. D., and Ichinose, F. (2011) Inhaled nitric oxide improves outcomes after successful cardiopulmonary resuscitation in mice. Circulation 124, 1645-1653
16. Liu, C. H., Kim, Y. R., Ren, J. Q., Eichler, F., Rosen, B. R., and Liu, P. K. (2007) Imaging cerebral gene transcripts in live animals. J. Neurosci. 27, 713-722 (Pubitemid 46143775)
17. Liu, C. H., Huang, S., Kim, Y. R., Rosen, B. R., and Liu, P. K. (2007) Forebrain ischemia-reperfusion simulating cardiac arrest in mice induces edema and DNA fragmentation in the brain. Mol. Imaging 6, 156-170 (Pubitemid 47152703)
18. Liu, C. H., Huang, S., Cui, J., Kim, Y. R., Farrar, C. T., Moskowitz, M. A., Rosen, B. R., and Liu, P. K. (2007) MR contrast probes that trace gene transcripts for cerebral ischemia in live animals. FASEB J. 21, 3004-3015 (Pubitemid 47372766)
19. Boxerman, J. L., Hamberg, L. M., Rosen, B. R., and Weisskoff, R. M. (1995) MR contrast due to intravascular magnetic susceptibility perturbations. Magn. Reson. Med. 34, 555-566
20. Fitzgerald, M. L., Xavier, R., Haley, K. J., Welti, R., Goss, J. L., Brown, C. E., Zhuang, D. Z., Bell, S. A., Lu, N., McKee, M., Seed, B., and Freeman, M. W. (2007) ABCA3 inactivation in mice causes respiratory failure, loss of pulmonary surfactant, and depletion of lung phosphatidylglycerol. J. Lipid Res. 48, 621- 632
21. Cobbs, C.S., Chen, J., Greenberg, D. A., and Graham, S. H. (1998) Vascular endothelial growth factor expression in transient focal cerebral ischemia in the rat. Neurosci Lett. 249, 79 - 82
22. Zhang, Z. G., Zhang, L., Jiang, Q., Zhang, R., Davies, K., Powers, C., Bruggen, N., and Chopp M. (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J. Clin. Invest. 106, 829-838
23. Greenberg, D.A. (1998) Angiogenesis and stroke. Drug News Perspect. 11, 265-270
24. Fischer, A. J., Scott, M. A., Zelinka, C., and Sherwood, P. (2010) A novel type of glial cell in the retina is stimulated by insulin-like growth factor 1 and may exacerbate damage to neurons and Müller glia. Glia 58, 633-649
25. Tagawa, A., Mezzacasa, A., Hayer, A., Longatti, A., Pelkmans, L., and Helenius, A. (2005) Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J. Cell Biol. 170, 769-779 (Pubitemid 41242109)
26. Pelkmans, L., Kartenbeck, J., and Helenius, A. (2001) Caveolar endocytosis of simian virus 40 reveals a new two-step vesiculartransport pathway to the ER. Nat. Cell Biol. 3, 473-483 (Pubitemid 32422083)
27. Lee, H. J., Boado, R. J., Braasch, D. A., Corey, D. R., and Pardridge, W. M. (2002) Imaging gene expression in the brain in vivo in a transgenic mouse model of Huntington's disease with an antisense radiopharmaceutical and drug-targeting technology. J. Nucl. Med. 43, 948-956 (Pubitemid 34747821)
28. Beltinger, C., Saragovi, H. U., Smith, R. M., LeSauteur, L., Shah, N., DeDionisio, L., Christensen, L., Raible, A., Jarett, L., and Gewirtz, A. M. (1995) Binding, uptake, and intracellular trafficking of phosphorothioate- modified oligodeoxynucleotides. J. Clin. Invest. 95, 1814-1823
29. Muldoon, L. L., Nilaver, G., Kroll, R. A., Pagel, M. A., Breakefield, X. O., Chiocca, E. A., Davidson, B. L., Weissleder, R., and Neuwelt, E. A. (1995) Comparison of intracerebral inoculation and osmotic blood-brain barrier disruption for delivery of adenovirus, herpesvirus, and iron oxide particles to normal rat brain. Am. J. Pathol. 147, 1840-1851
30. Shapiro, E. M., Skrtic, S., Sharer, K., Hill, J. M., Dunbar, C. E., and Koretsky, A. P. (2004) MRI detection of single particles for cellular imaging. Proc. Natl. Acad. Sci. U. S. A. 101, 10901-10906 (Pubitemid 38989558)
31. Cui, J., Holmes, E. H., and Liu, P. K. (1999) Oxidative damage to the c-fos gene and reduction of its transcription after focal cerebral ischemia. J. Neurochem. 73, 1164-1174 (Pubitemid 29395475)
32. Kalaria, R. N., Cohen, D. L., Premkumar, D. R., Nag S, La-Manna, J. C., and Lust, W. D. (1998) Vascular endothelial growth factor in Alzheimer's disease and experimental cerebral ischemia. Brain Res. Mol. Brain Res. 62, 101-105 (Pubitemid 29023185)
33. Ricaurte, G., Bryan, G., Strauss, L., Seiden, L., and Schuster C. (1985) Hallucinogenic amphetamine selectively destroys brain serotonin nerve terminals. Science 229, 986-988 (Pubitemid 16248493)
34. Malberg, J. E., and Seiden, L. S. (1998) Small changes in ambient temperature cause large changes in 3,4-methylenedioxymethamphetamine (MDMA)-induced serotonin neurotoxicity and core body temperature in the rat. J. Neurosci. 18, 5086-5094 (Pubitemid 28285417)
35. Fornai, F., Lenzi, P., Frenzilli, G., Gesi, M., Ferrucci, M., Lazzeri, G., Biagioni, F., Nigro, M., Falleni, A., Giusiani, M., Pellegrini, A., Blandini, F., Ruggieri, S., and Paparelli A. (2004) DNA damage and ubiquitinated neuronal inclusions in the substantia nigra and striatum of mice following MDMA (ecstasy). Psychopharmacology (Berl.) 173, 353-363 (Pubitemid 38703809)
36. Zhu, M., Bi, X., Jia, Q., and Shangguan S. The possible mechanism for impaired angiogenesis after transient focal ischemia in type 2 diabetic GK rats: different expressions of angiostatin and vascular endothelial growth factor. Biomed. Pharmacother. 64, 208-213
37. Krupinski, J., Font, A., Luque, A., Turu, M., and Slevin, M. (2008) Angiogenesis and inflammation in carotid atherosclerosis. Front. Biosci. 13, 6472-6482
38. Lee, J. H., Durand, R., Gradinaru, V., Zhang, F., Goshen, I., Kim, D. S., Fenno, L. E., Ramakrishnan, C., and Deisseroth, K. (2010) Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465, 788 -792