Subventricular zone neuronal progenitors undergo multiple divisions and retract their processes prior to each cytokinesis

European Journal of Neuroscience

Volumn 26, Issue 3, 2007, Pages 593-604

  Coskun, Volkan ^a,c   Falls, Douglas L ^a   Lane, Richard ^a   Czirok, Andras ^b   Luskin, Marla B ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell cycle; Neurogenesis; Proliferation; Rattus norvegicus; Rostral migratory stream; Videomicroscopy

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINESIS; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SUBVENTRICULAR ZONE;

ANIMALS; ANIMALS, NEWBORN; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL MOVEMENT; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; CYTOKINESIS; INTERNEURONS; LATERAL VENTRICLES; MICROSCOPY, VIDEO; NEURITES; OLFACTORY BULB; RATS; RATS, SPRAGUE-DAWLEY; STEM CELLS; TELENCEPHALON; TIME FACTORS;

EID: 34547631797     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05699.x     Document Type: Article

References (52)

1. Altman, J. Das, G.D. (1966) Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol., 126, 337 389.
2. Bignami, A., Eng, L.F., Dahl, D. Uyeda, C.T. (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res., 43, 429 435.
3. Bonfanti, L. Theodosis, D.T. (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience, 62, 291 305.
4. Coskun, V. Luskin, M.B. (2001) The expression pattern of the cell cycle inhibitor p19(INK4d) by progenitor cells of the rat embryonic telencephalon and neonatal anterior subventricular zone. J. Neurosci., 21, 3092 3103.
5. Coskun, V. Luskin, M.B. (2002) Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J. Neurosci. Res., 69, 795 802.
6. Craig, C.G., Tropepe, V., Morshead, C.M., Reynolds, B.A., 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.
7. Das, T., Payer, B., Cayouette, M. Harris, W.A. (2003) In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron, 37, 597 609.
8. DiCicco-Bloom, E., Townes-Anderson, E. Black, I.B. (1990) Neuroblast mitosis in dissociated culture: regulation and relationship to differentiation. J. Cell Biol., 110, 2073 2086.
9. Doetsch, F. Hen, R. (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr. Opin. Neurobiol., 15, 121 128.
10. Falls, D.L. Luskin, M.B. (2005) Neuronal progenitor cells of the mammalian neonatal anterior subventricular zone. In Rao, M.S. (Ed.), Stem Cells and CNS Development, 2nd Edn. Humana Press, New Jersey.
11. Gage, F.H. (2000) Mammalian neural stem cells. Science, 287, 1433 1438.
12. Gleeson, J.G., Lin, P.T., Flanagan, L.A. Walsh, C.A. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257 271.
13. Gritti, A., Frolichsthal-Schoeller, P., Galli, R., Parati, E.A., Cova, L., Pagano, S.F., Bjornson, C.R. Vescovi, A.L. (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J. Neurosci., 19, 3287 3297.
14. Jacobson, M. (1991) Developmental Neurobiology. Plenum Press, New York.
15. Kornack, D.R. Rakic, P. (2001a) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc. Natl Acad. Sci. U.S.A., 98, 4752 4757.
16. Kornack, D.R. Rakic, P. (2001b) Cell proliferation without neurogenesis in adult primate neocortex. Science, 294, 2127 2130.
17. Kuhn, H.G., Winkler, J., Kempermann, G., Thal, L.J. Gage, F.H. (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.
18. Law, A.K., Pencea, V., Buck, C.R. Luskin, M.B. (1999) Neurogenesis and neuronal migration in the neonatal rat forebrain anterior subventricular zone do not require GFAP-positive astrocytes. Dev. Biol., 216, 622 634.
19. Lee, M.K., Rebhun, L.I. Frankfurter, A. (1990a) Posttranslational modification of class III beta-tubulin. Proc. Natl Acad. Sci. U.S.A., 87, 7195 7199.
20. Lee, M.K., Tuttle, J.B., Rebhun, L.I., Cleveland, D.W. Frankfurter, A. (1990b) The expression and posttranslational modification of a neuron-specific beta-tubulin isotype during chick embryogenesis. Cell Motil. Cytoskel., 17, 118 132.
21. Lois, C. Alvarez-Buylla, A. (1994) Long-distance neuronal migration in the adult mammalian brain. Science, 264, 1145 1148.
22. Luskin, M.B. (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11, 173 189.
23. Luskin, M.B. Boone, M.S. (1994) Rate and pattern of migration of lineally-related olfactory bulb interneurons generated postnatally in the subventricular zone of the rat. Chem. Senses, 6, 695 714.
24. Luskin, M.B. Coskun, V. (2002) The progenitor cells of the embryonic telencephalon and the neonatal anterior subventricular zone differentially regulate their cell cycle. Chem. Senses, 27, 577 580.
25. Luskin, M.B., Zigova, T., Soteres, B.J. Stewart, R.R. (1997) 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.
26. Mehes, E., Czirok, A., Hegedus, B., Vicsek, T. Jancsik, V. (2002) Laminin-1 increases motility, path-searching, and process dynamism of rat and mouse Muller glial cells in vitro: implication of relationship between cell behavior and formation of retinal morphology. Cell Motil. Cytoskel., 53, 203 213.
27. Menezes, J.R., Smith, C.M., Nelson, K.C. Luskin, M.B. (1995) The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell. Neurosci., 6, 496 508.
28. Miyata, T., Kawaguchi, A., Okano, H. Ogawa, M. (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron, 31, 727 741.
29. Nguyen-Ba-Charvet, K.T., Picard-Riera, N., Tessier-Lavigne, M., Baron-Van Evercooren, A., Sotelo, C. Chedotal, A. (2004) Multiple roles for slits in the control of cell migration in the rostral migratory stream. J. Neurosci., 24, 1497 1506.
30. Noctor, S.C., Flint, A.C., Weissman, T.A., Dammerman, R.S. Kriegstein, A.R. (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature, 409, 714 720.
31. Noctor, S.C., Martinez-Cerdeno, V., Ivic, L. Kriegstein, A.R. (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci., 7, 136 144.
32. Nowakowski, R.S., Lewin, S.B. Miller, M.W. (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J. Neurocytol., 18, 311 318.
33. Ocbina, P.J., Dizon, M.L., Shin, L. Szele, F.G. (2006) Doublecortin is necessary for the migration of adult subventricular zone cells from neurospheres. Mol. Cell. Neurosci., 33, 126 135.
34. Pencea, V. Luskin, M.B. (2003) Prenatal development of the rodent rostral migratory stream. J. Comp. Neurol., 463, 402 418.
35. Pencea, V., Bingaman, K.D., Freedman, L.J. Luskin, M.B. (2001) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp. Neurol., 172, 1 16.
36. Rakic, P. (1990) Principles of neural cell migration. Experientia, 46, 882 891.
37. Reid, C.B., Liang, I. Walsh, C.A. (1999) Clonal mixing, clonal restriction, and specification of cell types in the developing rat olfactory bulb. J. Comp. Neurol., 403, 106 118.
38. Reynolds, B.A. Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science, 255, 1707 1710.
39. Rousselot, P., Lois, C. Alvarez-Buylla, A. (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of adult mice. J. Comp. Neurol., 351, 51 61.
40. Schwartz, J.H. Westbrook, G.L. (2000) The cytology of neurons. In Kandel, E.R., Schwartz, J.H. Jessell, T.M. (Eds), Principles of Neural Science, 4th Edn. McGraw-Hill, New York, pp. 67 87.
41. Selden, J.R., Dolbeare, F., Clair, J.H., Nichols, W.W., Miller, J.E., Kleemeyer, K.M., Hyland, R.J. DeLuca, J.G. (1993) Statistical confirmation that immunofluorescent detection of DNA repair in human fibroblasts by measurement of bromodeoxyuridine incorporation is stoichiometric and sensitive. Cytometry, 14, 154 167.
42. Smith, C.M. Luskin, M.B. (1998) Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev. Dyn., 213, 220 227.
43. Stewart, R.R., Zigova, T. Luskin, M.B. (1999) Potassium currents in precursor cells isolated from the anterior subventricular zone of the neonatal rat forebrain. J. Neurophysiol., 81, 95 102.
44. Stewart, R.R., Hoge, G.J., Zigova, T. Luskin, M.B. (2002) Neural progenitor cells of the neonatal rat anterior subventricular zone express functional GABA(A) receptors. J. Neurobiol., 50, 305 322.
45. Suzuki, S. Goldman, J.E. (2003) Multiple cell populations in the early postnatal subventricular zone take distinct migratory pathways: a dynamic study of glial and neuronal progenitor migration. J. Neurosci., 23, 4240 4250.
46. Weissman, T., Noctor, S.C., Clinton, B.K., Honig, L.S. Kriegstein, A.R. (2003) Neurogenic radial glial cells in reptile, rodent and human: from mitosis to migration. Cereb. Cortex, 13, 550 559.
47. Wolf, E., Black, I.B. DiCicco-Bloom, E. (1996) Mitotic neuroblasts determine neuritic patterning of progeny. J. Comp. Neurol., 367, 623 635.
48. Wolf, E., Wagner, J.P., Black, I.B. DiCicco-Bloom, E. (1997) Cerebellar granule cells elaborate neurites before mitosis. Brain Res. Dev. Brain Res., 102, 305 308.
49. Wolf, E., Black, I.B. DiCicco-Bloom, E. (1999) Mitotic sympathetic neuroblasts initiate axonal pathfinding in vivo. J. Neurobiol., 40, 366 374.
50. Yang, Y., Geldmacher, D.S. Herrup, K. (2001) DNA replication precedes neuronal cell death in. Alzheimer's disease. J. Neurosci., 21, 2661 2668.
51. Zigova, T. Newman, M.B. (2002) Transplantation into neonatal rat brain as a tool to study properties of stem cells. In Zigova, T., Sanberg, P.R. Sanchez-Ramos, J.R. (Eds), Neural Stem Cells: Methods and Protocols. Humana Press, Totowa, NJ.
52. Zigova, T., Betarbet, R., Soteres, B.J., Brock, S., Bakay, R.A. Luskin, M.B. (1996) 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.