Neuronal progenitor cells of the neonatal subventricular zone differentiate and disperse following transplantation into the adult rat striatum

Cell Transplantation

Volumn 7, Issue 2, 1998, Pages 137-156

  Zigova, Tanja ^a   Pencea, Viorica ^a   Betarbet, Ranjita ^a   Wiegand, Stanley J ^b   Alexander, Charlie ^b   Bakay, Roy A E ^a   Luskin, Marla B ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

Cell suspension graft; Migration; Neuronal progenitor cells; Striatum; Survival

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CELL DIFFERENTIATION; CELL MIGRATION; CELL TRANSPLANTATION; CONFERENCE PAPER; CORPUS STRIATUM; GRAFT SURVIVAL; NERVE TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; RAT; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; BRAIN TISSUE TRANSPLANTATION; BROMODEOXYURIDINE; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SURVIVAL; CEREBRAL VENTRICLES; CORPUS STRIATUM; INTERNEURONS; NEURONS; OLFACTORY BULB; OXIDOPAMINE; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS;

EID: 0031942923     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0963-6897(98)00009-8     Document Type: Conference Paper

References (64)

1. Abercrombie, M. Estimation of nuclear population from microtome sections. Anat. Rec. 94:239-247; 1946.
2. Anton, R.; Kordower, J.H.; Maidment, N.T.; Manaster, J.S.; Kane, D.J.; Rabizadeh, S.; Schueller, S.B.; Yang, J.; Rabizadeh, S.; Edwards, R.H. Neural-targeted gene therapy for rodent and primate hemiparkinsonism. Exp. Neurol. 127:207-218; 1994.
3. Bankiewicz, K.S.; Leff, S.E.; Nagy, D.; Jungles, S.; Rokovich, J.; Spratt, K.; Cohen, L.; Libonati, M.; Snyder, R.O.; Mandel, R.J. Practical aspects of the development of ex vivo and in vivo gene therapy for Parkinson's disease. Exp. Neurol. 144:147-156; 1997.
4. Barker, R.A.; Dunnett, S.B.; Faissner, A.; Fawcett, J.W. The time course of loss of dopaminergic neurons and the gliotic reaction surrounding grafts of embryonic mesencephalon to the striatum. Exp. Neurol. 141:79-93; 1996.
5. Betarbet, R.; Zigova, T.; Bakay, R.A.E.; Luskin, M.B. Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int. J. Dev. Neurosci. 14:921-930; 1996.
6. Betarbet, R.; Zigova, T.; Bakay, R.A.E.; Luskin, M.B. Migration patterns of neonatal subventricular zone progenitor cells transplanted into the neonatal striatum. Cell Transplant. 5:165-178; 1996.
7. Betarbet, R.; Zigova, T.; Bakay, R.A.E.; Lindsay, R.M.; Wiegand, S.J.; Luskin, M.B. Short-term survival of neonatal subventricular zone progenitor cells transplanted into the striatum of adult rats. Soc. Neurosci. Abstr. 22:218; 1996.
8. Bignami, A.; Eng, L.F.; Uyeda, C.T. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43:429-435; 1972.
9. Bjorklund, A.; Dunnett, S.B. Neural transplantation in adult rats. In: Dunnett, S.B.; Bjorklund, A., eds. Neural transplantation: A practical approach. New York: Oxford University Press; 1991:57-78.
10. Bjorklund, A. Dopaminergic transplants in experimental parkinsonism: Cellular mechanisms of graft induced functional recovery. Curr. Opin. Neurobiol. 2:683-689; 1992.
11. Brundin, P.; Strecker, R.E.; Widner, H.; Clarke, D.J.; Nilsson, O.G.; Astedt, B.; Lindvall, O.; Bjorklund, A. Human fetal dopamine neurons grafted in a rat model of Parkinson's disease: Immunological aspects, spontaneous and drug-induced behavior, and dopamine release. Exp. Brain Res. 70:192-208; 1988.
12. Chang, H.T.; Wilson, C.J.; Kitai, S.T. A Golgi study of rat neostriatal neurons: Light microscopic analysis. J. Comp. Neurol. 208:107-126; 1982.
13. Chang, P.L.; Capone, J.P.; Brown, G.M. Autologous fibroblast implantation. Feasibility and potential problems in gene replacement therapy. Mol. Biol. Med. 7:461-470; 1990.
14. Choi-Lundberg, D.L.; Lin, Q.; Chang, Y.N.; Chiang, Y.L.; Hay, C.M.; Mohajeri, H.; Davidson, B.L.; Bohn, M.C. Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science 275:838-841; 1997.
15. Cunningham, L.A.; Hansen, J.T.; Short, M.P.; Bohn, M.C. The use of genetically altered astrocytes to provide nerve growth factor to adrenal chromaffin cells grafted into the striatum. Brain Res. 561:192-202; 1991.
16. Dai, Y.; Roman, M.; Naviaux, R.K.; Verma, I.M. Gene therapy via primary myoblasts: Long-term expression of factor IX protein following transplantation in vivo. Proc. Natl. Acad. Sci. USA 89:10892-10895; 1992.
17. Date, I.; Yoshimoto, Y.; Imaoka, T.; Miyoshi, Y.; Furuta, T.; Asari, S.; Ohmoto, T. Effect of host age upon the degree of nigrostriatal dopaminergic system recovery following cografts of adrenal medulla and pretransected peripheral nerve. Brain Res. 637:50-56; 1994.
18. Doetsch, F.; Garcia-Verdugo, J.M.; Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17:5046-5061; 1997.
19. Emerich, D.F.; Winn, S.R.; Linder, M.D. Continued presence of intrastriatal but not intraventricular polymer-encapsulated PC12 cells is required for alleviation of behavioral deficits in parkinsonian rodents. Cell Transplant. 5:589-596; 1996.
20. Fisher, L.J.; Jinnah, H.A.; Kale, L.C.; Higgins, G.A.; Gage, F.H. Survival and function of intrastriatally grafted primary fibroblasts genetically modified to produce L-Dopa. Neuron 6:371-380; 1991.
21. Freund, T.F.; Bolam, J.P.; Bjorklund, A.; Stenevi, U.; Dunnett, S.B.; Powell, J.F.; Smith, A.D. Efferent synaptic connections of grafted dopaminergic neurons reinnervating the host neostriatum: A tyrosine hydroxylase immunocytochemical study. J. Neurosci. 5:603-616; 1985.
22. Gage, F.H.; Fisher, L.J.; Jinnah, J.H.A.; Rosenberg, M.B.; Tuszynski, M.; Friedmann, T. Grafting genetically modified cells to the brain: Conceptual and technical issues. Prog. Brain Res. 82:1-10; 1990.
23. Goldman, J.E. Lineage, migration, and fate determination of postnatal subventricular zone cells in the mammalian CNS. J. Neurooncol. 24:61-64; 1995.
24. Halliday, A.L.; Cepko, C.L. Generation and migration of cells in the developing striatum. Neuron 9:15-26; 1992.
25. Heim, R.C.; Willingham, G.; Freed, W.J. A comparison of solid intraventricular and dissociated intraparenchymal fetal substantia nigra grafts in a rat model of Parkinson's disease: Impaired graft survival is associated with high baseline rotational behavior. Exp. Neurol. 122:5-15; 1993.
26. Heimer, L.; Alheid, G.F.; Zaborsky, L. Basal ganglia. In: Paxinos, G., ed. The rat nervous system. Sydney: Academic Press; 1985:37-86.
27. Horellou, P.; Sabate, O.; Buc-Caron, M.; Mallet, J. Adenovirus-mediated gene transfer to the central nervous system for Parkinson's disease. Exp. Neurol. 144:131-138; 1997.
28. Hu, H.; Rutishauser, U. A septum-derived chemorepulsive factor for migrating olfactory interneuron precursors. Neuron 16:933-940; 1996.
29. Hu, H.; Tomasiewicz, H.; Magnuson, T.; Rutishauser, U. The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron 16:735-743; 1996.
30. Johnson, G.V.W.; Jope, R.S. The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity and degeneration. J. Neurosci. Res. 33:505-512; 1992.
31. Jones, K.H.; Senft, J.A. An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J. Histochem. Cytochem. 33: 77-80; 1985.
32. Kishi, K. Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J. Comp. Neurol. 258:112-124; 1987.
33. Knusel, B.; Winslow, J.W.; Rosenthal, A.; Hefti, F. Promotion of central cholinergic and dopaminergic neuron differentiation by brain-derived neurotrophic factor but not neurotrophin-3. Proc. Natl. Acad. Sci. USA 88:961-965; 1991.
34. Lee, M.K.; Rebhun, L.I.; Frankfurter, A. Posttranslational modification of class III β-tubulin. Proc. Natl. Acad. Sci. USA 87:7195-7199; 1990.
35. Lee, C.S.; Sauer, H.; Bjorklund, A. Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by intrastriatal 6-hydroxydopamine in the rat. Neuroscience 72:641-653; 1996.
36. Lois, C.; Alvarez-Buylla, A. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148; 1994.
37. Lundberg, C.; Winkler, C.; Whittemore, S.R.; Bjorklund, A. Conditionally immortalized neural progenitor cells grafted to the striatum exhibit site-specific neuronal differentiation and establish connections with the host globus pallidus. Neurobiol. Dis. 3:33-50; 1996.
38. Luskin, M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189; 1993.
39. Luskin, M.B.; McDermott, K. Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 11:211-226; 1994.
40. Luskin, M.B.; Boone, M.S. Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of rat. Chem. Senses 19:695-714; 1994.
41. Luskin, M.B.; Zigova, T.; Soteres, B.J.; Stewart, R.R. Neuronal progenitor cells derived from the anterior subventricular zone of the neonatal rat forebrain continue to proliferate in vitro and express a neuronal phenotype. Mol. Cell. Neurosci. 8:351-366; 1997.
42. Mahalik, T.J.; Finger, T.E.; Stromberg, I.; Olson, L. Substantia nigra transplants into denervated striatum of the rat: Ultrastructure of graft and host interconnections. J. Comp. Neurol. 240:60-70; 1985.
43. Martinez-Serrano, A.; Lundberg, C.; Bjorklund, A. Use of conditionally immortalized neural progenitors for transplantation and gene transfer to the CNS. In: Gage, F.H.; Christen, Y., eds. Isolation, characterization and utilization of CNS stem cells. New York: Springer Verlag; 1997:151-168.
44. Mayer, E.; Dunnett, S.B.; Fawcett, J.W. Mitogenic effect of basic fibroblast growth factor on embryonic ventral mesencephalic dopaminergic neuron precursors. Brain Res. Dev. Brain Res. 72:253-258; 1993.
45. Menezes, J.R.L.; Smith, C.M.; Nelson, C.K.; Luskin, M.B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci. 6:496-508; 1995.
46. Nikkhah, G.; Cunningham, M.G.; Jodicke, A.; Knappe, U.; Bjorklund, A. Improved graft survival and striatal reinnervation by microtransplantation of fetal nigral cell suspensions in the rat Parkinson model. Brain Res. 633:133-143; 1994.
47. Okoye, G.S.; Freed, W.J.; Geller, H.M. Short-term immunosuppression enhances the survival of intracerebral grafts of A7-immortalized glial cells. Exp. Neurol. 128:191-201; 1994.
48. O'Rourke, N.A. Neuronal chain gangs:homotypic contacts support migration into the olfactory bulb. Neuron 16: 1061-1064; 1996.
49. Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates. New York: Academic Press; 1982.
50. Rakic, P. Principles of neural cell migration. Experientia 46:882-891; 1990.
51. Raymon, H.K.; Thode, S.; Gage, F.H. Application of ex vivo gene therapy in the treatment of Parkinson's disease. Exp. Neurol. 144:82-91; 1997.
52. Sabate, O.; Horellou, P.; Vigne, E.; Colin, P.; Perricaudet, M.; Buc-Caron, M.H.; Mallet, J. Transplantation to the rat brain of human neural progenitors which were genetically modified using adenoviruses. Nat. Genet. 9:256-260; 1995.
53. Smart, I.H.M.; Sturrock, R.R. Ontogeny of the neostriatum. In: Divac, I.; Oberg, R., eds. The neostriatum. Oxford: Pergamon Press; 1979:127-146.
54. Snyder, E.Y.; Flax, J.D.; Yandava, B.D.; Park, K.I.; Liu, S.; Rosario, C.M.; Aurora, S. Transplantation and differentiation of neural "stem-like" cells: Possible insights into development and therapeutic potential. In: Gage, F.H.; Christen, Y., eds. Isolation, characterization and utilization of CNS stem cells. New York: Springer Verlag; 1997:173-196.
55. Svendsen, C.N.; Fawcett, J.W.; Bentlage, C.; Dunnett, S.B. Increased survival of rat EGF-generated CNS precursor cells using B27 supplemented medium. Exp. Brain Res. 102:407-414; 1995.
56. Takahashi, T.; Nowakowski, R.S.; Caviness, V.S., Jr. BUdR as an S-phase marker for quantitative studies of cytokinetic behavior in the murine cerebral ventricular zone. J. Neurocytol. 21:185-187; 1992.
57. Ungerstedt, U.; Arbuthnott, G.W. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal system. Brain Res. 24:485-493; 1970.
58. Wang, M.Z.; Jin, P.; Bumcrot, D.A.; Marigo, V.; McMahon, A.P.; Wang, E.A.; Wolf, T.; Pang, K. Induction of dopaminergic neuron phenotype in the midbrain by Sonic hedgehog protein. Nat. Med. 1:1184-1188; 1995.
59. Woods, A.L.; Hall, P.A.; Shepherd, N.A.; Hanby, A.M.; Waseem, N.H.; Lane, D.P.; Levison, D.A. The assessment of proliferating cell nuclear antigen (PCNA) immunostaining in primary gastrointestinal lymphomas and its relationship to histological grade, S+G2+m phase fraction (flow cytometric analysis) and prognosis. Histopathology 19:21-27; 1991.
60. Yoshimoto, Y.; Lin, Q.; Collier, T.J.; Frim, D.M.; Breakfield, X.O.; Bohn, M.C. Astrocytes retrovirally transduced with BDNF elicit behavioral improvement in rat model of Parkinson's disease. Brain Res. 691:25-36; 1995.
61. Zigova, T.; Wiegand, S.J.; Lindsay, R.M.; Luskin, M.B. Intraventricular infusion of BDNF in adult rats increases the proliferation of cells destined for the olfactory bulb. Soc. Neurosci. Abstr. 22:980; 1996.
62. Zigova, T.; Betarbet, R.; Soteres, B.J.; Brock, S.; Bakay, R.A.E.; Luskin, M.B. A comparison of the patterns of migration and the destinations of homotopically transplanted neonatal subventricular zone cells and heterotopically transplanted telencephalic ventricular zone cells. Dev. Biol. 173:459-474; 1996.
63. Zigova, T.; Valadi, N.; Cai, N.; Ge, P.; Lindsay, R.M.; Wiegand, S.J.; Luskin, M.B. The continuous proliferation of cells in the subventricular zone of the adult rat brain: Effect of intraventricular infusion of BDNF. Soc. Neurosci. Abstr. 23:316; 1997.
64. Zigova, T.; Betarbet, R.; Minnen, M.; Bakay, R.A.E.; Lindsay, R.M.; Wiegand, S.J.; Luskin, M.B. Transplantation of neuronal progenitor cells from the neonatal subventricular zone into the neonatal and adult striatum of the rat. Abstracts of the 6th International Neural Transplantation Meeting. 42; 1997.