BM88 is an early marker of proliferating precursor cells that will differentiate into the neuronal lineage

European Journal of Neuroscience

Volumn 20, Issue 10, 2004, Pages 2509-2523

  Koutmani, Yassemi ^a   Hurel, Catherine ^a   Patsavoudi, Evangelia ^a   Hack, Michael ^b,c   Gotz, Magdalena ^b,c   Thomaidou, Dimitra ^a   Matsas, Rebecca ^a  

^a HELLENIC PASTEUR INSTITUTE   (Greece)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Cell cycle regulation; Neurogenesis; Neuronal precursors; Pax6; Radial glia; Small eye

Indexed keywords

ANTIBODY; BIOLOGICAL MARKER; CYCLIN B1; PROTEIN BM88; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL LINEAGE; CELL PROLIFERATION; CELL SURVIVAL; EMBRYO; GLIA CELL; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; STEM CELL;

AGE FACTORS; AMINO ACID TRANSPORT SYSTEM X-AG; ANIMALS; ANIMALS, NEWBORN; ANTIGENS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; BRAIN; BROMODEOXYURIDINE; CARBOCYANINES; CELL COUNT; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CYCLIN B; EMBRYO; EYE PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; INTERMEDIATE FILAMENT PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULE L1; NEURAL NETWORKS (COMPUTER); NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; PHOSPHOPYRUVATE HYDRATASE; PREGNANCY; PROTEOGLYCANS; RATS; RATS, WISTAR; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIALIC ACIDS; STEM CELLS; THYMIDINE; TIME FACTORS; TRITIUM;

EID: 9644275480     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03724.x     Document Type: Article

References (85)

1. 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.
2. Anderson, S., Mione, M., Yun, K. & Rubenstein, J.L. (1999) Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis. Cereb. Cortex, 9, 646-654.
3. Belachew, S., Chittajallu, R., Aguirre, A.A., Yuan, X., Kirby, M., Anderson, S. & Gallo, V. (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J. Cell Biol., 161, 169-186.
4. Boutou, E., Hurel, C. & Matsas, R. (2000) Early expression of the BM88 antigen during neuronal differentiation of P19 embryonal carcinoma cells. Int. J. Dev. Neurosci., 18, 321-328.
5. Bruni, J.E. (1998) Ependymal development, proliferation, and functions: a review. Micros.C Re.S Techn, 41, 2-13.
6. Caviness, V.S. Jr, Goto, T., Tarui, T., Takahashi, T., Bhide, P.G. & Nowakowski, R.S. (2003) Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb. Cortex, 13, 592-598.
7. Cayouette, M. & Raff, M. (2002) Asymmetric segregation of Numb: a mechanism for neural specification from Drosophila to mammals. Nat. Neurosci., 5, 1265-1269.
8. Chenn, A. & McConnell, S.K. (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell, 82, 631-641.
9. Cohen, G.B., Ren, R. & Baltimore, D. (1995) Modular binding domains in signal transduction proteins. Cell, 80, 237-248.
10. Cremisi, R, Philpott, A. & Ohnuma, S. (2003) Cell cycle and cell fate interactions in neural development. Curr. Opin. Neurobiol., 13, 26-33.
11. Desai, A.R. & McConnell, S.K. (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development, 127, 2863-2872.
12. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703-716.
13. Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. (1997) Cellular composition and three-dimensional organization of the subventricular zone of the adult mammalian brain. J. Neurosci., 17, 5046-5061.
14. Dornan, D., Shimizu, H., Burch, L., Smith, A. & Hupp, T.R. (2003) The proline repeat domain of p53 binds directly to the transcriptional coactivator p300 and allosterically controls DNA-dependent acetylation of p53. Mol. Cell. Biol., 23, 8846-8861.
15. Dubreuil, V., Hirsch, M.R., Pattyn, A., Brunet, J.F. & Goridis, C. (2000) The Phox2b transcription factor coordinately regulates neuronal cell cycle exit and identity. Development, 127, 5191-5201.
16. Dye, C.A., Lee, J.K., Atkinson, R.C., Brewster, R., Han, P.L. & Bellen, H.J. (1998) The Drosophila sanpodo gene controls sibling cell fate and encodes a tropomodulin homolog, an actin/tropomyosin-associated protein. Development, 125, 1845-1856.
17. Dyer, M.A. & Cepko, C.L. (2001) p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J. Neurosci., 21, 4259-4271.
18. Edwards, M.A., Yamamoto, M. & Caviness, V.S. Jr (1990) Organisation of radial glia and related cells in the developing murine CNS. An analysis based upon a new monoclonal antibody marker. Neuroscience, 36, 121-144.
19. Estivill-Torrus, G., Pearson, H., van Heyningen, V., Price, D.J. & Rashbass, P. (2002) Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development, 129, 455-466.
20. Ferguson, K.L., Vanderluit, J.L., Hebert, J.M., McIntosh, W.C., Tibbo, E., MacLaurin, J.G., Park, D.S., Wallace, V.A., Vooijs, M., McConnell, S.K. & Slack, R.S. (2002) Telencephalon specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J., 21, 3337-3346.
21. Frise, E., Knoblich, J.A., Younger-Shepherd, S., Jan, L.Y. & Jan, Y.N. (1996) The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl. Acac. Sci. USA, 93, 11925-11932.
22. Gaitanou, M., Buanne, P., Pappa, C., Georgopoulou, N., Mamalaki, A., Tirone, F. & Matsas, R. (2001) Cloning, expression and localization of human BM88 shows that it maps to chromosome 11p15.5, a region implicated in Beckwith-Wiedemann syndrom and tumorigenesis. Biochem. J., 355, 715-724.
23. Georgopoulou, N., Hurel, C., Thomaidou, D. & Matsas, R. (2002) Enhanced neuronal phenotype, altered cell cycle regulation and protection from apoptosis by BM88 over-expression in mouse neuroblastoma cells. 3rd Forum of European Neuroscience Abstracts. Paris, France, 13-17 July 2002.
24. Gotz, M., Hartfuss, E. & Malatesta, P. (2002) Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res. Bull., 57, 777-788.
25. Gotz, M., Stoykova, A. & Gruss, P. (1998) Pax6 controls radial glia differentiation in the cerebral cortex. Neuron, 21, 1031-1044.
26. Gotz, M., Williams, B.P., Boltz, J. & Price, J. (1995) The spacification of neuronal fate: a common precursor for neurotransmitter sub-types in tha rat cerebral cortex in vitro. Eur. J. Neurosci., 7, 889-898.
27. Grove, E.A., Williams, B.P., Li, D.-Q., Hajihosseini, M., Friedrich, A. & Price, J. (1993) Multiple restricted lineages in the embryonic rat cerebral cortex. Development, 117, 553-561.
28. Guardavaccaro, D., Corrente, G., Covone, F., Micheli, L., D'Agnano, I., Starace, G., Caruso, M. & Tirone, F. (2000) Arrest of G1-S progression by the p53-inducible gene Pc3 is Rb dependent and relies on the inhibition cyclin Dl transcription. Mol. Cell. Neurosci., 20, 1797-1815.
29. Hartfuss, E., Galli, R., Heins, N. & Gotz, M. (2001) Characterization of CNS precursor subtypes and radial glia. Dev. Biol., 229, 15-30.
30. Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K.L., Hack, M.A., Chapouton, P., Barde, Y.A. & Gotz, M. (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci., 5, 308-315.
31. Isshiki, T., Pearson, B., Holbrook, S. & Doe, C.Q. (2001) Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell, 106, 511-521.
32. Kornack, D.R. & Rakic, P. (1995) Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron, 15, 311-321.
33. Leavitt, B.R., Hernit-Grant, C.S. & Macklis, J.D. (1999) Mature astrocytes transform into transitional radial glia within adult mouse neocortex that supports directed migration of transplanted immature neurons. Exp. Neurol., 157, 43-57.
34. Levitt, P. & Rakic, P. (1980) Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J. Comp. Neurol., 193, 815-840.
35. Li, Y. & Chopp, M. (1999) Temporal profile of nestin expression after focal cerebral ischemia in adult rat. Brain Res., 838, 1-10.
36. Li, L. & Vaessin, H. (2000) Pan-naural Prospero terminates cell proliferation during Drosophila Neurogenesis. Genes Dev., 14, 147-151.
37. Liu, G., Nozell, S., Xiao, H. & Chen, X. (2004) ΔNp73β is active in transactivation and growth supression. Mol. Cell. Biol., 24, 487-501.
38. Lo, L., Tiveron, M.-C. & Anderson, D.J. (1998) MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples panneuronal and subtype-specific components of autonomic neuronal identity. Development, 125, 609-620.
39. Lois, C. & Alvarez-Buylla, A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl. Acad. Sci. USA, 90, 2074-2077.
40. Luskin, MB., Parnavelas, J.G. & Bartfield, J.A. (1993) Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci., 13, 1730-1750.
41. Magavi, S.S., Leavitt, B.R. & Macklis, J.D. (2000) Induction of neurogenesis in the neocortex of adult mice. Nature, 405, 951-955.
42. Malatesta, P., Gotz, M., Barsacchi, G., Price, J., Zoncu, R. & Cremisi, F. (2000b) PC3 overexpression affects the pattern of cell division of rat cortical precursors. Mech. Dev., 90, 17-28.
43. Malatesta, P., Hartfuss, E. & Gotz, M. (2000a) Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development, 127, 5253-5263.
44. Mamalaki, A., Boutou, E., Hurel, C., Patsavoudi, E., Tzartos, S. & Matsas, R. (1995) The BM88 antigen, a novel neuron-specific molecule, enhances the differentiation of mouse neuroblastoma cells. J. Biol. Chem., 270, 14201-14208.
45. Mione, M.C., Cavanagh, J.F., Harris, B. & Parnavelas, J.G. (1997) Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J. Neurosci., 17, 2018-2029.
46. Mione, M.C., Danevic, C., Boardman, P., Harris, B. & Parnavelas, J.G. (1994) Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons. J. Neurosci., 14, 107-123.
47. Misson, J.-P., Edwards, M.A., Yamamoto, M. & Caviness, V.S. Jr (1988) Identification of radial glial cells within the developing murine central nervous system: Studies based upon a new immunohistochemical marker. Dev. Brain. Res., 44, 95-108.
48. Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron, 31, 727-741.
49. Morrow, T., Song, M.R. & Ghosh, A. (2001) Sequential specification of neurons and glia by developmentally regulated extracellular factors. Development, 18, 3585-3594.
50. Mullen, R.J., Buck, C.R. & Smith, A.M. (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development, 116, 201-211.
51. Nieto, M., Schuurmans, C., Britz, O. & Guillemot, F. (2001) Neural bHLH genes control the neuronal versus glial fate decision in cortical progenitors. Neuron, 29, 401-403.
52. Nishiyama, A. (2001) NG2 cells in the brain: a novel glial cell population. Hum. Cell., 14, 77-82.
53. 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.
54. Noctor, S.C., Flint, A.C., Weissman, T.A., Wong, W.S., Clinton, B.K. & Kriegstein, A.R. (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial H glia. J. Neurosci., 22, 3161-3173.
55. Nowakowski, R.S., Caviness, V.S. Jr, Takahashi, T. & Hayes, N.L. (2002) Population dynamics during cell proliferation and neuronogenesis in the developing murine neocortex. Results Probl. Cell Differ., 39, 1-25.
56. Ohnuma, S., Hopper, S., Wang, K.C., Philpott, A. & Harris, W.A. (2002) Coordinating retinal histogenesis: early cell cycle exit enhances early cell fate determination in Xenopus retina. Development, 129, 2435-2446.
57. Patsavoudi, E., Hurel, C. & Matsas, R. (1989) Neuron- and myelin-specific monoclonal antibodies recognizing cell-surface antigens of the central and peripheral nervous system. Neuroscience, 30, 463-478.
58. Patsavoudi, E., Hurel, C. & Matsas, R. (1991) Purification and characterization of neuron-specific surface antigen defined by monoclonal antibody BM88. J. Neurochem., 56, 782-788.
59. Patsavoudi, E., Merkouri, E., Thomaidou, D., Sandillon, F., Alonso, G. & Matsas, R. (1995) Characterization and localization of the BM88 antigen in the developing and adult rat brain. J. Neurosci. Res., 40, 506-518.
60. Peretto, P., Merighi, A., Fasolo, A. & Bonfanti, L. (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res. Bull., 42, 9-21.
61. Politis, P., Geissen, M., Rohrer, H. & Matsas, R. (2004) BM88 is a cell intrinsic determinant that regulates initiation of pan-neuronal and sub-type specific differentiation of spinal cord neurons. 4th Forum of European Neuroscience Abstracts. Lisbon, Portugal, 10-14 July 2004.
62. Qian, X., Goderie, S.K., Shen, Q., Stem, J.H. & Temple, S. (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development, 125, 3143-3152.
63. Qian, X., Shen, Q., Goderie, S.K, He, W., Capela, A, Davis, A.A. & Temple, S. (2000) Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron, 28, 69-80.
64. Rao, M.S. (1999) Multipotent and restricted precursors in the central nervous system. Anat. Rec., 257, 137-148.
65. Rhyu, M.S., Jan, L.Y. & Yan, Y.N. (1994) Asymmetric distribution of Numb protein during division of sensory organ precursor cell confers distinct fates to daughter cells. Cell, 76, 477-491.
66. Shen, Q., Zhong, W., Jan, Y.N. & Temple, S. (2002) Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development, 129, 4843-4853.
67. Shibata, T., Yamada, K., Watanabe, M., Ikenaka, K., Wada, K., Tanaka, K. & Inoue, Y. (1997) Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord. J. Neurosci., 17, 9212-9219.
68. Simeone, A., Acampora, D., Gulisano, M., Stornaiuolo, A. & Boncinelli, E. (1992) Nested expression domains of four homeobox genes in developing rostral brain. Nature, 358, 687-690.
69. Soriano, E., Alvarado-Mallart, R.M., Dumesnil, N., Del Rio, J.A. & Sotelo, C. (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron, 4, 563-577.
70. Stoycova, A., Fritsch, R., Walther, C. & Gruss, P. (1996) Forebrain patterning defects in Small eye mutant mice. Development, 122, 3453-3465.
71. Stoykova, A., Treichel, D., Hallonet, M. & Gruss, P. (2000) Pax6 modulates the dorsoventral patterning of the mammalian telenchephalon. J. Neurosci., 20, 8042-8050.
72. Takahashi, T., Nowakowski, R.S. & Caviness, V.S. Jr (1994) Mode of cell proliferation in the developing mouse neocortex. Proc. Natl. Acad. Sci. USA, 91, 375-379.
73. Takahashi, T., Nowakowski, R.S. & Caviness, V.S. Jr (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci., 15, 6046-6057.
74. Takahashi, T., Nowakowski, R.S. & Caviness, V.S. Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci., 16, 6183-6196.
75. Tarabykin, V., Stoykova, A., Usman, N. & Gruss, P. (2001) Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development, 128, 1983-1993.
76. Temple, S. & Qian, X. (1996) Vertebrate neural progenitor cells: subtypes and regulation. Curr. Opin. Neurob., 6, 11-17.
77. Thomaidou, D., Mione, M.C., Cavanagh, J.F. & Parnavelas, J.G. (1997) Apoptosis and its relation to the cell cycle in the developing cerebral cortex. J. Neurosci., 17, 1075-1085.
78. Toma, J.G., El-Bizri, H., Barnabe-Heider, R, Aloyz, R. & Miller, F.D. (2000) Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J. Neurosci., 20, 7648-7656.
79. Tori, M., Matsuzaki, F., Osumi, N., Kaibuchi, K., Nakamura, S., Casarosa, S., Guillemot, F. & Nakafuku, M. (1999) Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development, 126, 443-456.
80. Wakamatsu, Y., Maynard, T.M. & Weston, J.A. (2000) Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development, 127, 2811-2821.
81. Walker, K.K. & Levine, A.J. (1996) Identification of a novel p53 functional domain that is necessary for efficient growth supression. Proc. Nat. Acad. Sci. USA, 93, 15335-15340.
82. Walsh, C. & Cepko, C.L. (1992) Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science, 255, 434-440.
83. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W. & Schreiber, S.L. (1994) Structural basis for the binding of proline-rich peptides to SH3 domains. Cell, 76, 933-945.
84. Zhong, W., Feder, J.N., Jiang, M.M., Jan, L.Y & Jan, Y.N. (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron, 17, 43-53.
85. Zhong, W., Jiang, M.M., Weinmaster, G., Jan, L.Y. & Jan, Y.N. (1997) Differential expression of mammalian Numb, Numblike and Notch 1 suggests distinct roles during mouse cortical neurogenesis. Development, 124, 1887-1897.