A bipotent neural progenitor cell line cloned from a cerebellum of an adult p53-deficient mouse generates both neurons and oligodendrocytes

European Journal of Neuroscience

Volumn 21, Issue 11, 2005, Pages 2903-2911

  Tominaga, Mitsutoshi ^a   Honda, Shinya ^a   Okada, Atsumasa ^a   Ikeda, Akifumi ^a   Kinoshita, Seiji ^a   Tomooka, Yasuhiro ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

Author keywords

Cell lineage; Clonal cell line; p53 deficiency; Thyroid hormone

Indexed keywords

CALBINDIN; DNA; GENE PRODUCT; MESSENGER RNA; PROTEIN MATH1; PROTEIN P53; PROTEIN ZIC 1; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG; ZEBRIN;

ANIMAL CELL; ARTICLE; ASTROCYTE; CARCINOGENICITY; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL POPULATION; CELL STRUCTURE; CEREBELLUM; CONTROLLED STUDY; CULTURE MEDIUM; DNA SYNTHESIS; GABAERGIC TRANSMISSION; MITOSIS; MOLECULAR CLONING; MOUSE; NERVE CELL; NERVE CELL CULTURE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; STEM CELL;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; CELL PROLIFERATION; CEREBELLUM; CLONE CELLS; CULTURE MEDIA, SERUM-FREE; DNA-BINDING PROTEINS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; INTERNEURONS; ISOENZYMES; MALE; MICE; MICE, KNOCKOUT; MICE, NUDE; NEURONS; OLIGODENDROGLIA; PAX2 TRANSCRIPTION FACTOR; STEM CELLS; TRANSCRIPTION FACTORS; TRIIODOTHYRONINE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 21444435398     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04119.x     Document Type: Article

References (72)

1. Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M. & Mikoshiba, K. (1994) A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem., 63, 1880-1890.
2. Baas, D., Bourbeau, D., Sarlieve, L.L., Ittel, M.E., Dussault, J.H. & Puymirat, J. (1997) Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia, 19, 324-332.
3. Barres, B.A., Lazar, M.A. & Raff, M.C. (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development, 120, 1097-1108.
4. Batini, C. (1990) Cerebellar localization and colocalization of GABA and calcium binding protein-D28K. Arch. Ital. Biol., 128, 127-149.
5. Ben-Arie, N., Bellen, H.J., Armstrong, D.L., McCall, A.E., Gordadze, P.R., Guo, Q., Matzuk, M.M. & Zoghbi, H.Y. (1997) Math1 is essential for genesis of cerebellar granule neurons. Nature, 390, 169-172.
6. 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.
7. Billon, N., Terrinoni, A., Jolicoeur, C., McCarthy, A., Richardson, W.D., Melino, G. & Raff, M. (2004) Roles for p53 and p73 during oligodendrocyte development. Development, 131, 1211-1220.
8. Butt, A.M., Hornby, M.F., Ibrahim, M., Kirvell, S., Graham, A. & Berry, M. (1997) PDGF-alpha receptor and myelin basic protein mRNAs are not coexpressed by oligodendrocytes in vivo: a double in situ hybridization study in the anterior medullary velum of the neonatal rat. Mol. Cell Neurosci., 8, 311-322.
9. Casarosa, S., Fode, C. & Guillemot, F. (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development, 126, 525-534.
10. Donehower, L.A., Harvey, M., Slagle, B.L., McArthur, M.J., Montgomery, C.A. Jr, Butel, J.S. & Bradley, A. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature, 356, 215-221.
11. Durand, B. & Raff, M. (2000) A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays, 22, 64-71.
12. Gabay, L., Lowell, S., Rubin, L.L. & Anderson, D.J. (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron, 40, 485-499.
13. Gage, F.H. (2000) Mammalian neural stem cells. Science, 287, 1433-1438.
14. Gao, W.Q. & Hatten, M.E. (1994) Immortalizing oncogenes subvert the establishment of granule cell identity in developing cerebellum. Development, 120, 1059-1070.
15. Goodrich, L.V., Milenkovic, L., Higgins, K.M. & Scott, M.P. (1997) Altered neural cell fates and medulloblastoma in mouse patched mutants. Science, 277, 1109-1113.
16. Hanazono, M., Nakagawa, E., Aizawa, S. & Tomooka, Y. (1998) Establishment of prostatic cell line 'Pro9ad' from a p53-deficient mouse. Prostate, 36, 102-109.
17. Hatten, M.E., Alder, J., Zimmerman, K. & Heintz, N. (1997) Genes involved in cerebellar cell specification and differentiation. Curr. Opin. Neurobiol., 7, 40-47.
18. He, W., Ingraham, C., Rising, L., Goderie, S. & Temple, S. (2001) Multipotent stem cells from the mouse basal forebrain contribute GABAergic neurons and oligodendrocytes to the cerebral cortex during embryogenesis. J. Neurosci., 21, 8854-8862.
19. Itahana, K., Dimri, G. & Campisi, J. (2001) Regulation of cellular senescence by p53. Eur. J. Biochem., 268, 2784-2791.
20. Jacobson, M. (1991) Developmental Neurobiology, 3rd edn. Plenum Press, New York.
21. Kalyani, A., Hobson, K. & Rao, M.S. (1997) Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev. Biol., 186, 202-223.
22. Leber, S.M., Breedlove, S.M. & Sanes, J.R. (1990) Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord. J. Neurosci., 10, 2451-2462.
23. Leclerc, N., Gravel, C. & Hawkes, R. (1988) Development of parasagittal zonation in the rat cerebellar cortex: MabQ113 antigenic bands are created postnatally by the suppression of antigen expression in a subset of Purkinje cells. J. Comp. Neurol., 273, 399-420.
24. Liu, Y. & Rao, M.S. (2004) Olig genes are expressed in a heterogeneous population of precursor cells in the developing spinal cord. Glia, 45, 67-74.
25. Lu, Q.R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C.D. & Rowitch, D.H. (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell, 109, 75-86.
26. Lu, Q.R., Yuk, D., Alberta, J.A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A.P., Stiles, C.D. & Rowitch, D.H. (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron, 25, 317-329.
27. Maricich, S.M. & Herrup, K. (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J. Neurobiol., 41, 281-294.
28. Miller, R.H. (2002) Regulation of oligodendrocyte development in the vertebrate CNS. Prog. Neurobiol., 67, 451-467.
29. Milosevic, A. & Goldman, J.E. (2002) Progenitors in the postnatal cerebellar white matter are antigenically heterogeneous. J. Comp. Neurol., 452, 192-203.
30. Minakawa, M., Sugimoto, T., Aizawa, S. & Tomooka, Y. (1998) Cerebellar cell lines established from a p53-deficient adult mouse. Brain Res., 813, 172-176.
31. Miyata, T., Maeda, T. & Lee, J.E. (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev., 13, 1647-1652.
32. Morimura, S., Tashiro, F. & Ueno, Y. (1990) Establishment and characterization of cell lines (Kagura-1 and Kagura-2) from aflatoxin B1-induced rat hepatoma. Chem. Pharm. Bull. (Tokyo), 38, 460-463.
33. Mujtaba, T., Piper, D.R., Kalyani, A., Groves, A.K., Lucero, M.T. & Rao, M.S. (1999) Lineage-restricted neural precursors can be isolated from both, the mouse neural tube and cultured ES cells. Dev. Biol., 214, 113-127.
34. -/- mouse cerebellum. Brain Res., 959, 11-19.
35. Oliver, T.G. & Wechsler-Reya, R.J. (2004) Getting at the root and stem of brain rumors. Neuron, 42, 885-888.
36. Palmer, T.D., Takahashi, J. & Gage, F.H. (1997) The adult rat hippocampus contains primordial neural stem cells. Mol. Cell Neurosci., 8, 389-404.
37. Parnavelas, J.G. & Nadarajah, B. (2001) Radial glial cells, are they really glia? Neuron, 31, 881-884.
38. Pevny, L.H., Sockanathan, S., Placzek, M. & Lovell-Badge, R. (1998) A role for SOX1 in neural determination. Development, 125, 1967-1978.
39. Peyron, F., Timsit, S., Thomas, J.L., Kagawa, T., Ikenaka, K. & Zalc, B. (1997) In situ expression of PLP/DM-20, MBP, and CNP during embryonic and postnatal development of the jimpy mutant and of transgenic mice overexpressing PLP. J. Neurosci. Res., 50, 190-201.
40. Raff, M.C., Mirsky, R., Fields, K.L., Lisak, R.P., Dorfman, S.H., Silberberg, D.H., Gregson, N.A., Leibowitz, S. & Kennedy, M.C. (1978) Galactocerebroside is a specific cell-surface antigenic marker for oligodendrocytes in culture. Nature, 274, 813-816.
41. Rao, M.S. (1999) Multipotent and restricted precursors in the central nervous system. Anal Rec., 257, 137-148.
42. Rao, M. & Mayer-Proschel, M. (1997) Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev. Biol., 188, 48-63.
43. Redies, C., Lendahl, U. & McKay, R.D. (1991) Differentiation and heterogeneity in T-antigen immortalized precursor cell lines from mouse cerebellum. J. Neurosci. Res., 30, 601-615.
44. 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.
45. Ryder, E.F., Snyder, E.Y. & Cepko, C.L. (1990) Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J. Neurobiol., 21, 356-375.
46. Schuurmans, C. & Guillemot, F. (2002) Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol., 12, 26-34.
47. Sembritzki, O., Hagel, C., Lamszus, K., Deppert, W. & Bohn, W. (2002) Cytoplasmic localization of wild-type p53 in glioblastomas correlates with expression of vimentin and glial fibrillary acidic protein. Neuro-Oncol., 4, 171-178.
48. 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.
49. Sommer, I. & Schachner, M. (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev. Biol., 83, 311-327.
50. Spassky, N., Goujet-Zalc, C., Parmantier, E., Olivier, C., Martinez, S., Ivanova, A., Ikenaka, K., Macklin, W., Cerruti, I., Zalc, B. & Thomas, J.L. (1998) Multiple restricted origin of oligodendrocytes. J. Neurosci., 18, 8331-8343.
51. Sternberger, N.H., Itoyama, Y., Kies, M.W. & Webster, H.D. (1978) Myelin basic protein demonstrated immunocytochemically in oligodendroglia prior to myelin sheath formation. Proc. Natl Acad. Sci. USA, 75, 2521-2524.
52. Takayama, C. & Inoue, Y. (2004) Morphological development and maturation of the GABAergic synapses in the mouse cerebellar granular layer. Brain Res. Bev. Brain Res., 150, 177-190.
53. Takebayashi, H., Yoshida, S., Sugimori, M., Kosako, H., Kominami, R., Nakafuku, M. & Nabeshima, Y. (2000) Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech. Dev., 99, 143-148.
54. Tanahashi, K., Shibahara, S., Ogawa, M., Hanazono, M., Aizawa, S. & Tomooka, Y. (2002) Establishment and characterization of clonal cell lines from the vagina of p53-deficient young mice. In Vitro Cell Dev. Biol. Anim., 38, 547-556.
55. Tohyama, T., Lee, V.M., Rorke, L.B., Marvin, M., McKay, R.D. & Trojanowski, J.Q. (1992) Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest., 66, 303-313.
56. Tominaga, M. & Tomooka, Y. (2002) Novel genes cloned from a neuronal cell line newly established from a cerebellum of an adult p53 (-/-) mouse. Biochem. Biophys. Res. Commun., 297, 473-479.
57. Tomooka, Y. & Aizawa, S. (1998) Cell lines established from fetal brains of p53-deficient mice. Cell Struct. Funct., 23, 101-107.
58. Tomooka, Y., Kitani, H., Jing, N., Matsushima, M. & Sakakura, T. (1993) Reconstruction of neural tube-like structures in vitro from primary neural precursor cells. Proc. Natl Acad. Sci. USA, 90, 9683-9687.
59. Tong, W.M., Ohgaki, H., Huang, H., Granier, C., Kleihues, P. & Wang, Z.Q. (2003) Null mutation of DNA strand break-binding molecule poly (ADP-ribose) polymerase causes medulloblastomas in p53 (-/-) mice. Am. J. Pathol., 162, 343-352.
60. Tsukada, T., Tomooka, Y., Takai, S., Ueda, Y., Nishikawa, S., Yagi, T., Tokunaga, T., Takeda, N., Suda, Y., Abe, S., Matsuo, I., Ikawa, Y. & Aizawa, S. (1993) Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene, 8, 3313-3322.
61. Uchida, N., Buck, D.W., He, D., Reitsma, M.J., Masek, M., Phan, T.V., Tsukamoto, A.S., Gage, F.H. & Weissman, I.L. (2000) Direct isolation of human central nervous system stem cells. Proc. Natl Acad. Sci. USA, 97, 14720-14725.
62. Umezu, T., Hanazono, M., Aizawa, S. & Tomooka, Y. (2003) Characterization of newly established clonal oviductal cell lines and differential hormonal regulation of gene expression. In Vitro Cell Dev. Biol. Anim., 39, 146-156.
63. Wang, D., Villasante, A., Lewis, S.A. & Cowan, N.J. (1986) The mammalian beta-tubulin repertoire: hematopoietic expression of a novel, heterologous beta-tubulin isotype. J. Cell Biol., 103, 1903-1910.
64. Wilhelmsson, U., Eliasson, C., Bjerkvig, R. & Pekny, M. (2003) Loss of GFAP expression in high-grade astrocytomas does not contribute to tumor development or progression. Oncogene, 22, 3407-3411.
65. Williams, B.P., Read, J. & Price, J. (1991) The generation of neurons and oligodendrocytes from a common precursor cell. Neuron, 7, 685-693.
66. Wood, J.N. & Anderton, B.H. (1981) Monoclonal antibodies to mammalian neurofilaments. Biosci. Report, 1, 263-268.
67. Woodruff, R.H., Tekki-Kessaris, N., Stiles, C.D., Rowitch, D.H. & Richardson, W.D. (2001) Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives. Int. J. Dev. Neurosci., 19, 379-385.
68. Yokota, N., Aruga, J., Takai, S., Yamada, K., Hamazaki, M., Iwase, T., Sugimura, H. & Mikoshiba, K. (1996) Predominant expression of human zic in cerebellar granule cell lineage and medulloblastoma. Cancer Res., 56, 377-383.
69. Zappone, M.V., Galli, R., Catena, R., Meani, N., De Biasi, S., Mattel, E., Tiveron, C., Vescovi, A.L., Lovell-Badge, R., Ottolenghi, S. & Nicolis, S.K. (2000) Sox2 regulatory sequences direct expression of a (beta) -geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development, 127, 2367-2382.
70. Zhang, L. & Goldman, J.E. (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron, 16, 47-54.
71. Zhou, Q. & Anderson, D.J. (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109, 61-73.
72. Zhou, Q., Wang, S. & Anderson, D.J. (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron, 25, 331-343.