Locating and labeling neural stem cells in the brain

Journal of Cellular Physiology

Volumn 226, Issue 1, 2011, Pages 1-7

  Landgren, Henrik ^a   Curtis, Maurice A ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; VIRUS VECTOR;

AMYGDALOID NUCLEUS; BRAIN CELL; BRAIN CORTEX; CELL LABELING; CELL MATURATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DENTATE GYRUS; HIPPOCAMPUS; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSGENICS;

ANIMALS; BRAIN; HUMANS; NEURAL STEM CELLS; NEURONS;

MAMMALIA;

EID: 78049252796     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22319     Document Type: Review

References (105)

1. Allocca M, Doria M, Petrillo M, Colella P, Garcia-Hoyos M, Gibbs D, Kim SR, Maguire A, Rex TS, Di Vicino U, Cutillo L, Sparrow JR, Williams DS, Bennett J, Auricchio A. 2008. Serotype-dependent packaging of large genes in adeno-associated viral vectors results in effective gene delivery in mice. J Clin Invest 118: 1955-1964.
2. Alonso M, Ortega-Perez I, Grubb MS, Bourgeois JP, Charneau P, Lledo PM. 2008. Turning astrocytes from the rostral migratory stream into neurons: A role for the olfactory sensory organ. J Neurosci 28: 11089-11102.
3. Altman J. 1969. Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137: 433-457.
4. Anderson BJ, Rapp DN, Baek DH, McCloskey DP, Coburn-Litvak PS, Robinson JK. 2000. Exercise influences spatial learning in the radial arm maze. Physiol Behav 70: 425-429.
5. Aucoin MG, Perrier M, Kamen AA. 2008. Critical assessment of current adeno-associated viral vector production and quantification methods. Biotechnol Adv 26: 73-88.
6. Azzouz M, Kingsman SM, Mazarakis ND. 2004. Lentiviral vectors for treating and modeling human CNS disorders. J Gene Med 6: 951-962.
7. Barnabe-Heider F, Meletis K, Eriksson M, Bergmann O, Sabelstrom H, Harvey MA, Mikkers H, Frisen J. 2008. Genetic manipulation of adult mouse neurogenic niches by in vivo electroporation. Nat Methods 5: 189-196.
8. Bedard A, Parent A. 2004. Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151: 159-168.
9. Bedard A, Levesque M, Bernier PJ, Parent A. 2002. The rostral migratory stream in adult squirrel monkeys: Contribution of new neurons to the olfactory tubercle and involvement of the antiapoptotic protein Bcl-2. Eur J Neurosci 16: 1917-1924.
10. Benraiss A, Chmielnicki E, Lerner K, Roh D, Goldman SA. 2001. Adenoviral brain-derived neurotrophic factor induces both neostriatal and olfactory neuronal recruitment from endogenous progenitor cells in the adult forebrain. J Neurosci 21: 6718-6731.
11. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A. 2002. Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci USA 99: 11464-11469.
12. Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Bjork-Eriksson T, Nordborg C, Gage FH, Druid H, Eriksson PS, Frisen J. 2006. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci USA 103: 12564-12568.
13. Cameron HA, McKay RD. 2001. Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435: 406-417.
14. Carlen M, Meletis K, Goritz C, Darsalia V, Evergren E, Tanigaki K, Amendola M, Barnabe-Heider F, Yeung MS, Naldini L, Honjo T, Kokaia Z, Shupliakov O, Cassidy RM, Lindvall O, Frisen J. 2009. Forebrain ependymal cells are Notch-dependent and generate neuroblasts and astrocytes after stroke. Nat Neurosci 12: 259-267.
15. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK. 2000. Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75: 1729-1734.
16. Chow LM, Zhang J, Baker SJ. 2008. Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res 17: 919-928.
17. Cockrell AS, Kafri T. 2007. Gene delivery by lentivirus vectors. Mol Biotechnol 36: 184-204.
18. Colin A, Faideau M, Dufour N, Auregan G, Hassig R, Andrieu T, Brouillet E, Hantraye P, Bonvento G, Deglon N. 2009. Engineered lentiviral vector targeting astrocytes in vivo. Glia 57: 667-679.
19. Consiglio A, Gritti A, Dolcetta D, Follenzi A, Bordignon C, Gage FH, Vescovi AL, Naldini L. 2004. Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc Natl Acad Sci USA 101: 14835-14840.
20. Cooper-Kuhn CM, Kuhn HG. 2002. Is it all DNA repair? Methodological considerations for detecting neurogenesis in the adult brain. Brain Res Dev Brain Res 134: 13-21.
21. Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D. 1996. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16: 2649-2658.
22. Craig CG, D'sa R, Morshead CM, Roach A, van der Kooy D. 1999. Migrational analysis of the constitutively proliferating subependyma population in adult mouse forebrain. Neuroscience 93: 1197-1206.
23. Curtis MA, Penney EB, Pearson AG, van Roon-Mom WM, Butterworth NJ, Dragunow M, Connor B, Faull RL. 2003. Increased cell proliferation and neurogenesis in the adult human Huntington's disease brain. Proc Natl Acad Sci USA 100: 9023-9027.
24. Curtis MA, Penney EB, Pearson J, Dragunow M, Connor B, Faull RLM. 2005a. 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.
25. Curtis MA, Waldvogel HJ, Synek B, Faull RLM. 2005b. A histochemical and immunohistochemical analysis of the subependymal layer in the normal and Huntington's disease brain. J Chem Neuroanat 30: 55-66.
26. Curtis MA, Faull RL, Glass M. 2006. A novel population of progenitor cells expressing cannabinoid receptors in the subependymal layer of the adult normal and Huntington's disease human brain. J Chem Neuroanat 31: 210-215.
27. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315: 1243-1249.
28. Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, Derksen TA, Zabner J, Ghodsi A, Chiorini JA. 2000. Recombinant adeno-associated virus type 2, 4, and 5 vectors: Transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci USA 97: 3428-3432.
29. Doetsch F. 2003a. The glial identity of neural stem cells. Nat Neurosci 6: 1127-1134.
30. Doetsch F. 2003b. A niche for adult neural stem cells. Curr Opin Genet Dev 13: 543-550.
31. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-5061.
32. Duman RS, Nakagawa S, Malberg J. 2001. Regulation of adult neurogenesis by antidepressant treatment. Neuropsychopharmacology 25: 836-844.
33. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4: 1313-1317.
34. Fasolo A, Peretto P, Bonfanti L. 2002. Cell migration in the rostral migratory stream. Chem Senses 27: 581-582.
35. Foudi A, Hochedlinger K, Van Buren D, Schindler JW, Jaenisch R, Carey V, Hock H. 2009. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol 27: 84-90.
36. Foust KD, Nurre E, Montgomery CL, Hernandez A, Chan CM, Kaspar BK. 2009. Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
37. Fowler CD, Freeman ME, Wang Z. 2003. Newly proliferated cells in the adult male amygdala are affected by gonadal steroid hormones. J Neurobiol 57: 257-269.
38. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM. 2006. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26: 8609-8621.
39. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV. 2004. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nature Neurosci 7: 1233-1241.
40. Geraerts M, Eggermont K, Hernandez-Acosta P, Garcia-Verdugo JM, Baekelandt V, Debyser Z. 2006. Lentiviral vectors mediate efficient and stable gene transfer in adult neural stem cells in vivo. Hum Gene Ther 17: 635-650.
41. Gleason D, Fallon JH, Guerra M, Liu JC, Bryant PJ. 2008. Ependymal stem cells divide asymmetrically and transfer progeny into the subventricular zone when activated by injury. Neuroscience 156: 81-88.
42. Globus JH, Kuhlenbeck H. 1944. The subependymal cell plate (Matrix) and its relationship to brain tumors of the ependymal type. J Neuropathol Exp Neurol 3: 1-35.
43. Goldman SA, Nottebohm F. 1983. Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80: 2390-2394.
44. Goldman SA, Zaremba A, Niedzwiecki D. 1992. In vitro neurogenesis by neuronal precursor cells derived from the adult songbird brain. J Neurosci 12: 2532-2541.
45. Gould E, Reeves AJ, Graziano MSA, Gross CG. 1999. Neurogenesis in the neocortex of adult primates. Science 286: 548-552.
46. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo P, Götz M. 2005. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nature Neurosci 8: 865-872.
47. Han Z, Zhong L, Maina N, Hu Z, Li X, Chouthai NS, Bischof D, Weigel-Van Aken KA, Slayton WB, Yoder MC, Srivastava A. 2008. Stable integration of recombinant adeno-associated virus vector genomes after transduction of murine hematopoietic stem cells. Hum Gene Ther 19: 267-278.
48. Hayes NL, Nowakowski RS. 2000. Exploiting the dynamics of S-phase tracers in developing brain: Interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev Neurosci 22: 44-55.
49. Heintz N. 2001. BAC to the future: The use of bac transgenic mice for neuroscience research. Nat Rev Neurosci 2: 861-870.
50. Hirrlinger J, Scheller A, Hirrlinger PG, Kellert B, Tang W, Wehr MC, Goebbels S, Reichenbach A, Sprengel R, Rossner MJ, Kirchhoff F. 2009. Split-cre complementation indicates coincident activity of different genes in vivo. PLoS ONE 4: e4286.
51. Jakobsson J, Ericson C, Jansson M, Bjork E, Lundberg C. 2003. Targeted transgene expression in rat brain using lentiviral vectors. J Neurosci Res 73: 876-885.
52. Jin D, Liu HX, Hirai H, Torashima T, Nagai T, Lopatina O, Shnayder NA, Yamada K, Noda M, Seike T, Fujita K, Takasawa S, Yokoyama S, Koizumi K, Shiraishi Y, Tanaka S, Hashii M, Yoshihara T, Higashida K, Islam MS, Yamada N, Hayashi K, Noguchi N, Kato I, Okamoto H, Matsushima A, Salmina A, Munesue T, Shimizu N, Mochida S, Asano M, Higashida H. 2007. CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 446: 41-45.
53. Johansson CB, Momma S, Clarke DL, Risling M, Lendahl U, Frisen J. 1999. Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96: 25-34.
54. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130: 391-399.
55. Kokoeva MV, Yin H, Flier JS. 2007. Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505: 209-220.
56. Kornack DR, Rakic P. 2001. Cell proliferation without neurogenesis in adult primate neocortex. Science 294: 2127-2130.
57. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. 1997. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17: 5820-5829.
58. Kukekov VG, Laywell ED, Suslov O, Davies K, Scheffler B, Thomas LB, O'Brien TF, Kusakabe M, Steindler DA. 1999. Multipotent stem/progenitor cells with similar properties arise from two neurogenic regions of adult human brain. Exp Neurol 156: 333-344.
59. Kwon EJ, Lasiene J, Jacobson BE, Park IK, Horner PJ, Pun SH. 2010. Targeted nonviral delivery vehicles to neural progenitor cells in the mouse subventricular zone. Biomaterials 31: 2417-2424.
60. Lewandoski M. 2001. Conditional control of gene expression in the mouse. Nat Rev Genet 2: 743-755.
61. Lewis PD. 1968. Mitotic activity in the primate subependymal layer and the genesis of gliomas. Nature 217: 974-975.
62. Liu G, Martins IH, Chiorini JA, Davidson BL. 2005. Adeno-associated virus type 4 (AAV4) targets ependyma and astrocytes in the subventricular zone and RMS. Gene Ther 12: 1503-1508.
63. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264: 1145-1148.
64. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. 1996. Chain migration of neuronal precursors. Science 271: 978-981.
65. Lucassen PJ, Stumpel MW, Wang Q, Aronica E. 2010. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 58: 940-949.
66. Luskin MB, Boone MS. 1994. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem Senses 19: 695-714.
67. Magavi SS, Leavitt BR, Macklis JD. 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405: 951-955.
68. Malberg JE, Duman RS. 2003. Cell proliferation in adult hippocampus is decreased by inescapable stress: Reversal by fluoxetine treatment. Neuropsychopharmacology 28: 1562-1571.
69. Malberg JE, Eisch AJ, Nestler EJ, Duman RS. 2000. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20: 9104-9110.
70. Manev R, Uz T, Manev H. 2001. Fluoxetine increases the content of neurotrophic protein S100beta in the rat hippocampus. Eur J Pharmacol 420: R1-R2.
71. Manji HK, Moore GJ, Chen G. 1999. Lithium at 50: Have the neuroprotective effects of this unique cation been overlooked? Biol Psychiatry 46: 929-940.
72. Manji HK, Moore GJ, Chen G. 2000a. Clinical and preclinical evidence for the neurotrophic effects of mood stabilizers: Implications for the pathophysiology and treatment of manic-depressive illness. Biol Psychiatry 48: 740-754.
73. Manji HK, Moore GJ, Chen G. 2000b. Lithium up-regulates the cytoprotective protein Bcl-2 in the CNS in vivo: A role for neurotrophic and neuroprotective effects in manic depressive illness. J Clin Psychiatry 61: 82-96.
74. McCarty DM, Young SM. Jr., Samulski RJ. 2004. Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu Rev Genet 38: 819-845.
75. Miletic H, Fischer YH, Neumann H, Hans V, Stenzel W, Giroglou T, Hermann M, Deckert M, Von Laer D. 2004. Selective transduction of malignant glioma by lentiviral vectors pseudotyped with lymphocytic choriomeningitis virus glycoproteins. Hum Gene Ther 15: 1091-1100.
76. Mitchell RS, Beitzel BF, Schroder AR, Shinn P, Chen H, Berry CC, Ecker JR, Bushman FD. 2004. Retroviral DNA integration: ASLV, HIV, and MLV show distinct target site preferences. PLoS Biol 2: E234.
77. Mori T, Tanaka K, Buffo A, Wurst W, Kuhn R, Gotz M. 2006. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. Glia 54: 21-34.
78. Morris RG, Hagan JJ, Rawlins JN. 1986. Allocentric spatial learning by hippocampectomised rats: A further test of the "spatial mapping" and "working memory" theories of hippocampal function. Q J Exp Psychol B 38: 365-395.
79. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D. 1994. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071-1082.
80. Nagy A. 2000. Cre recombinase: The universal reagent for genome tailoring. Genesis 26: 99-109.
81. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Van Evercooren AB. 1999. Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11: 4357-4366.
82. Nam HS, Benezra R. 2009. High levels of Id1 expression define B1 type adult neural stem cells. Cell Stem Cell 5: 515-526.
83. Nonaka S, Katsube N, Chuang DM. 1998. Lithium protects rat cerebellar granule cells against apoptosis induced by anticonvulsants, phenytoin and carbamazepine. J Pharmacol Exp Ther 286: 539-547.
84. Obermair FJ, Fiorelli R, Schroeter A, Beyeler S, Blatti C, Zoerner B, Thallmair M. 2010. A novel classification of quiescent and transit amplifying adult neural stem cells by surface and metabolic markers permits a defined simultaneous isolation. Stem Cell Res.
85. Pastrana E, Cheng LC, Doetsch F. 2009. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA 106: 6387-6392.
86. Platel JC, Gordon V, Heintz T, Bordey A. 2009. GFAP-GFP neural progenitors are antigenically homogeneous and anchored in their enclosed mosaic niche. Glia 57: 66-78.
87. Privat A, Leblond CP. 1972. The subependymal layer and neighboring region in the brain of the young rat. J Comp Neurol 146: 277-302.
88. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M, Gonzalez-Perez O, Mirzadeh Z, Gil-Perotin S, Romero-Rodriguez R, Berger MS, Garcia-Verdugo JM, Alvarez-Buylla A. 2006. Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 494: 415-434.
89. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
90. Ross HH, Levkoff LH, Marshall GP II, Caldeira M, Steindler DA, Reynolds BA, Laywell ED. 2008. Bromodeoxyuridine induces senescence in neural stem and progenitor cells. Stem Cells 26: 3218-3227.
91. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311: 629-632.
92. Senatorov VV, Ren M, Kanai H, Wei H, Chuang DM. 2004. Short-term lithium treatment promotes neuronal survival and proliferation in rat striatum infused with quinolinic acid, an excitotoxic model of Huntington's disease. Mol Psychiatry 9: 371-385.
93. Slezak M, Goritz C, Niemiec A, Frisen J, Chambon P, Metzger D, Pfrieger FW. 2007. Transgenic mice for conditional gene manipulation in astroglial cells. Glia 55: 1565-1576.
94. Smith RH. 2008. Adeno-associated virus integration: Virus versus vector. Gene Ther 15: 817-822.
95. Stein CS, Martins I, Davidson BL. 2005. The lymphocytic choriomeningitis virus envelope glycoprotein targets lentiviral gene transfer vector to neural progenitors in the murine brain. Mol Ther 11: 382-389.
96. Thomas CE, Ehrhardt A, Kay MA. 2003. Progress and problems with the use of viral vectors for gene therapy. Nat Rev Genet 4: 346-358.
97. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E. 2004. Defining the epithelial stem cell niche in skin. Science 303: 359-363.
98. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
99. Wakade CG, Mahadik SP, Waller JL, Chiu FC. 2002. Atypical neuroleptics stimulate neurogenesis in adult rat brain. J Neurosci Res 69: 72-79.
100. Watson DJ, Kobinger GP, Passini MA, Wilson JM, Wolfe JH. 2002. Targeted transduction patterns in the mouse brain by lentivirus vectors pseudotyped with VSV, Ebola, Mokola, LCMV, or MuLV envelope proteins. Mol Ther 5: 528-537.
101. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA. 1996. Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599-7609.
102. Willing AE, Zigova T, Milliken M, Poulos S, Saporta S, McGrogan M, Snable G, Sanberg PR. 2002. Lithium exposure enhances survival of NT2N cells (hNT neurons) in the hemiparkinsonian rat. Eur J Neurosci 16: 2271-2278.
103. Yoshimura S, Takagi Y, Harada J, Teramoto T, Thomas SS, Waeber C, Bakowska JC, Breakefield XO, Moskowitz MA. 2001. FGF-2 regulation of neurogenesis in adult hippocampus after brain injury. Proc Natl Acad Sci USA 98: 5874-5879.
104. Zigova T, Pencea V, Betarbet R, Wiegand SJ, Alexander C, Bakay RA, Luskin MB. 1998. Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum. Cell Transplant 7: 137-156.
105. Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. 2008. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16: 1073-1080.