Neurotransmitter receptor activation triggers p27(Kip1) and p21(CIP1) accumulation and G1 cell cycle arrest in oligodendrocyte progenitors

Development

Volumn 126, Issue 5, 1999, Pages 1077-1090

  Ghiani, Cristina A ^a   Eisen, Alex M ^a   Yuan, Xiaoqing ^a   DePinho, Ronald A ^b   McBain, Chris J ^a   Gallo, Vittorio ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

0 2A cells; cAMP; Cyclin kinase inhibitors; Glia; Glutamate receptors; Norepinephrine; Voltage dependent K+ channels

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; ISOPRENALINE; NEUROTRANSMITTER RECEPTOR; NORADRENALIN; PROTEIN P21; PROTEIN P27;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; STEM CELL;

ANIMALS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLINS; G1 PHASE; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; OLIGODENDROGLIA; PHENOTYPE; POTASSIUM CHANNELS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; S PHASE; STEM CELLS; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0033002020     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (85)

1. Aoki, C. (1992). Beta-adrenergic receptors: astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry. J. Neurosci. 12, 781-792.
2. Armstrong, R. C., Friedrich, V. L., Holmes, Jr K. V. and Dubois-Dalcq, M. (1990). In vitro analysis of the oligodendrocyte lineage in mice during demyelination and remyelination. J. Cell Biol. 111, 1183-1195.
3. Astor-Jones, G., Shipley, M. T. and Grzanna, R. (1995). The locus coeruleus. A5 and A7 noradrenergic cell groups. In The Rat Nervous System. 2nd edition (ed. G. Paxinos), pp. 183-213. Academic Press, New York.
4. Baker, S. P., Sumners, C., Pitha, J. and Raizada, M. K. (1986). Characteristics of the β-adrenoceptor from neuronal and glial cells in primary cultures of rat brain. J. Neurochem. 47, 1318-1326.
5. Barres, B. A., Koroshetz, W. J., Swartz, K. J., Chun, L. L. Y. and Corey, D. P. (1990). Ion channel expression by white matter glia: the O-2A glial progenitor cell. Neuron 4, 507-524.
6. Barres, B. A., Lazar, M. and Raff, M. (1994). A novel role for thyroid hormone, glucocorticoids, and retinoic acid in timing of oligodendrocyte development. Development 120, 1097-1108.
7. Berger, T. and Frotscher, M. (1994). Distribution and morphological characteristics of oligodendrocytes in the rat hippocampus in situ and in vitro: an immunocytochemical study with the monoclonal Rip antibody. J. Neurocytol. 23, 61-74.
8. Bernstein, M., Lyons, S. A., Moller, T. and Kettenmann, H. (1996). Receptor-mediated calcium signaling in glial cells from mouse corpus callosum. J. Neurosci. Res. 46, 152-16.1
9. + entry. J. Neurosci. Res. 42, 579-593.
10. Brugarolas, J., Chandrasekaran, C., Gordon, J. I., Beach, D., Jacks, T. and Hannon, G. (1995). Radiation-induced cell cycle arrest is compromised by p21 deficiency. Nature 377, 552-557.
11. Kip1. Genes Dev. 11, 2335-2346.
12. Chvatal, A., Pastor, A., Mauch, M., Sykova, E. and Kettenmann, H. (1995). Distinct populations of identified glial cells in the developing rat spinal cord slice: ion channel properties and cell morphology. Eur. J. Neurosci. 7, 129-142.
13. 1A-adrenoceptors. NeuroReport 4, 1115-1118.
14. Coyle, J. T. and Henry, D. (1973). Catecholamines in fetal and newborn rat brain. J. Neurochem. 21, 61-67.
15. Curtis, R., Cohen, J., Fok-Seang, J., Hanley, M. R., Gregson, N. A., Reynolds, R. and Wilkin, G. P. (1988). Development of macroglial cells in rat cerebellum. I. Use of antibodies to follow early in vivo development and migration of oligodendrocytes. J. Neurocytol. 17, 43-54.
16. Curtis, R., Hardy, R., Reynolds, R., Spruce, B. A. and Wilkin, G. P. (1991) Down-regulation of GAP-43 during oligodendrocyte development and lack of expression by astrocytes in vivo: implications for macroglial differentiation. Eur. J. Neurosci. 3, 876-886.
17. Dave, V., Gordon, G. W. and McCarthy, K. D. (1991). Cerebral type 2 astroglia are heterogeneous with respect to their ability to respond to neuroligands linked to calcium mobilization. Glia 4, 440-447.
18. 1 checkpoint control. Cell 82, 675-684.
19. Duffy, S. and MacVicar, B. A. (1995). Adrenergic calcium signaling in astrocyte networks within the hippocampal slice. J. Neurosci. 15, 5535-5550.
20. Durand, B., Gao, F. B. and Raff, M. C. (1997). Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J 16, 306-317.
21. Kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Curr. Biol. 6, 431-440.
22. Eisenbarth, G. S., Walsh, F. S. and Nirenberg, M. (1979). Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. USA 76, 4913-4917.
23. Fanarraga, M. L., Sommer, I. and Griffiths, I. R. (1995). O-2A progenitors of the mouse optic nerve exhibit a developmental pattern of antigen expression different from the rat. Glia 15, 95-104.
24. kipl is expressed at high levels in cells that express a myelinating phenotype J. Neurosci. Res. 50, 373-382.
25. Fulton, B. P., Burne, J. F. and Raff, M. C. (1992). Visualization of O-2A progenitor cells in developing and adult rat optic nerve by quisqualate-stimulated cobalt uptake. J. Neurosci. 12, 4816-4833.
26. Gallo, V. and Armstrong, R. C. (1995). Developmental and growth factor induced regulation of nestin in oligodendrocyte lineage cells. J. Neurosci. 15, 394-406.
27. + channel block. J. Neurosci. 16, 2659-2670.
28. Gao, F. B. and Raff, M. (1997). Cell size control and a cell-intrinsic maturation program in proliferating oligodendrocyte precursor cells. J. Cell. Biol. 138, 1367-1377.
29. -) under different mitogenic control. Neuron 5, 615-625.
30. Hodges-Savola, C., Rogers, S. D., Ghilardi, J. R., Timm, D. R. and Mantyh, P. W. (1996) β-adrenergic receptors regulate astrogliosis and cell proliferation in the central nervous system in vivo. Glia 17, 52-62.
31. Jordan, J., Galindo, M. F., Prehn, J. H. M., Weichselbaum, R. R., Beckett, M., Ghadge, G. D., Roos, R. P., Leiden, J. M. and Miller, R. J. (1997) p53 expression induces apoptosis in hippocampal pyramidal neuron cultures. J. Neurosci. 17, 1397-1405.
32. kipl) of cyclin-dependent kinase 4 activation. Cell 79, 487-496.
33. + channel expression and cell proliferation are regulated by intracellular sodium and membrane depolarization in oligodendrocyte progenitor cells, J. Neurosci. 17, 2669-2682.
34. Kurino, M., Fukunaga, K., Ushio, V. and Miyamoto, E. (1996). Cyclic AMP inhibits activation of mitogen-activated protein kinase and cell proliferation in response to growth factors in cultured rat cortical astrocytes. J. Neurochem. 67, 2246-2255.
35. Levi, G., Gallo, V. and Ciotti, M. T. (1986). Bipotenlial precursors of putative fibrous astrocytes and oligodendrocytes in rat cerebellar cultures express distinct surface features and 'neuron-like' GABA transport. Proc. Natl. Acad. Sci. USA 83, 1504-1508.
36. Levine, J. M., Stincone, F. and Lee, Y. S. (1993). Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7, 307-321.
37. Levison, S. W. and Goldman, J. E. (1993). Both oligodendrocytes and astroeytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10, 201-212.
38. Levitt, P. and Moore, R. Y. (1979). Development of the noradrenergic innervation of neocortex. Brain Res. 162, 243-259.
39. Luskin, M. B. and McDermott, K. (1994). Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 7, 9-18.
40. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B. and Jacks, T. (1995). p53-Dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9, 935-944.
41. Martin-Castellanos, C. and Moreno, S. (1997). Recent advances on cyclins, CDKs and CDK inhibitors. Trends Cell. Biol. 7, 95-98.
42. McCarthy, K. D. (1983). An autoradiographic analysis of beta-adrenergic receptors on immunocytochemically defined astroglia. J. Pharmacol. Exp. Ther 226, 282-290.
43. 1 increased adenosine 3′:5′-cyclic monophosphate levels in primary cultures of glia. J. Cyclic Nucleotide Res. 4, 15-26.
44. McCarthy, K. D. and deVellis, J. (1980). Preparation of separate astroglial and oligodendroglia cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
45. McKinnon, R. D., Matsui, T., Dubois-Dalcq, M. and Aaronson, S. A. (1990). FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5, 603-614.
46. McMorris, F. A. (1983). Cyclic AMP induction of the myelin enzyme 2′,3′-cyclic nucteolide 3′-phosphohydrolase in rat oligodendrocytes. J. Neurochem. 41, 506-515.
47. + channels in cell proliferation. News Physiol. Sci. 9, 105-110.
48. Cip1 in muscle and other terminally differentiating cells. Science 267, 1024-1027.
49. Paspalas, C. D. and Papadopoulos, G. C. (1996). Ultrastructural relationships between noradrenergic nerve fibers and non-neuronal elements in the rat cerebral cortex. Glia 17, 133-146.
50. Patneau, D. K., Wright, P. W., Winters, C., Mayer, M. L. and Gallo, V. (1994). Glial cells of the oligodendrocyte lineage express both kainate-and AMPA-preferring subtypes of glutamate receptor. Neuron 12, 357-371.
51. Pende, M., Fisher, T. L., Simpson, P. B., Russell, J. T., Blenis, J. and Gallo, V. (1997). Neurotransmitter and growth factor-induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinasc C. and mitogen-activated protein kinase/ribosomal S6 kinase pathway. J. Neurosci. 17, 1291-1301.
52. Pleasure, D., Parris, J., Stern, J., Grinspan, J. and Kim, S. U. (1986). Incorporation of tritiated galactose into galactocerebroside by cultured rat oligodendrocyles: Effects of cyclic adenosine 3′,5′-monophospliLite analogues. J. Neurochem. 46, 300-302.
53. Kip1, a cyclin-dependent kinase inhibitor and a potent mediator of extracellular antimitogenic signals. Cell 78, 59-66.
54. Kip1, a cyclin-cdk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8, 9-22.
55. Arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 92, 713-723.
56. Raff, M. C., Miller, R. H. and Noble, M. (1983). A glial progenitor cell that develops in vitro inlo an astrocyte or an oligodendrocyle depending on culture medium. Nature 303, 390-396.
57. Raible, D. W. and McMorris, F. A. (1989). Cyclic AMP regulates the rate of differentiation of oligodendrocytes without changing the lineage commitment of their progenitors. Dev. Biol. 133, 437-446.
58. Raible, D. W. and McMorris, F. A. (1993). Oligodendrocyte differentiation and progenitor cell proliferation are independently regulated by cyclic AMP. J. Neurosci. Res., 34, 287-294.
59. Reynolds, R. and Wilkin, G. P. (1988). Development of macroglial cells in rat cerebellum. II. An in situ immunohistochemical study of oligodendroglial lineage from precursor to mature myelinating cell. Development 102, 409-425.
60. Rohrer, D. K. and Kobilka B. K. (1998) Insights from in vivo modification of adrenergic receptor gene expression. Annu. Rev. Pharmacol. Toxicol. 38, 351-373.
61. Ross, M. E. (1996). Cell division and the nervous system: regulating the cycle from neural differentiation to death. Trends Neurosci. 19, 62-68.
62. Roy, M. L. and Sontheimer, H. (1995). β-Adrenergic modulation of glial inwardly rectifying potassium channels. J. Neurochem. 64, 1576-1584.
63. Sakhi, S., Bruce, A., Sun, N., Tocco, G., Baudry, M. and Schreiber, S. S. (1994). p53 induction is associated with neuronal damage in the centra] nervous system. Proc. Natl. Acad. Sci. USA 91, 7525-7529.
64. Serrano, M., Lee, H. W., Chin, L., Cordon-Cardo, C., Beach, D. and DePinho, R. A. (1996). Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27-37.
65. Skapek, S. X., Rhee, J., Spicer, D. B. and Lassar, A. B. (1995). Inhibition of myogenic differentiation in proliferating myoblasts by cyclin D1-dependent kinase. Science 267, 1022-1024.
66. Sommer, I. and 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.
67. Sontheimer, H., Trotter, J., Schachner, M. and Kettenmann, H. (1989). Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 12, 1135-1145.
68. Stallcup, W. B. (1981). The NG2 antigen, a putative lineage marker.
69. Immunofluorescent localization in primary cultures of rat brain. Dev. Biol. 83, 154-165.
70. Stallcup, W. B. and Beasley, L. (1987). Potential glial precursor cells of the optic nerve express the NG2 proteoglycan. J. Neurosci. 7, 2737-2744.
71. Steinhäuser, C. and Gallo, V. (1996). News on glutamate receptors in glial cells. Trends Neurosci. 19, 339-345.
72. Stone, K. A. and Ariano, M. A. (1989). Are glial cells targets of the central noradrenergic system?. A review of the evidence. Brain Res. Rev. 14, 297-309.
73. Stone, E. A., Sessler, K. M. and Weimin, L. (1990). Glial localization of adenylate-cyclase-coupled β-adrenoceptors in rat forebrain slices. Brain Rex. 530, 295-300.
74. Thomas, S. A., Matsumoto, A. M. and Palmiter, R. D. (1995). Noradrenaline is essential for mouse fetal development. Nature 374, 643-646.
75. kipl accompany glial cell differentiation of Central Glia-4 cells. J. Biol. Chem. 272, 442-447.
76. Kip1 in oligodendrocyte progenitor cells results in cell cycle growth arrest. J. Neurobiol. 36, 431-440.
77. Tohyama, T., Lee, V. M. Y., Rorke, L. B., Marvin, M., McKay R. D. G. and Trojanowski, J. Q. (1992). Nestin expression in embryonic human neuroepithelium and in human neuroepithelial tumor cells. Lab. Invest. 66, 303-313.
78. Vick, R. S., Collins, J. M. and DeVries, G. H. (1992). Cell cycle and proliferation dynamics of adult rat oligodendrocytes. J. Neurosci. Res., 33, 75-81.
79. + oligodendrocytes in postnatal rat cerebellum: analysis in unfixed tissue slices using anti-glycolipid antibodies. J. Neurosci. Res. 33, 338-353.
80. Wigginton, S. A. and Minneman, K. P. (1991). Comparison of calcium ionophore and receptor-activated inositol phosphate formation in primary glial cell cultures. Eur. J. Pharmacol. 208, 239-247.
81. Wonderlin, W. F. and Strobl, J. S. (1996). Potassium channels, proliferation and G1 progression. J. Membrane Biol. 154, 91-107.
82. Yuan, X., Eisen, A. M., McBain, C. J. and Gallo, V. (1998). A role for glutamate in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125, 2901-2914.
83. Zerlin, M., Levison, S. and Goldman, J. E. (1995). Early patterns of migration, morphogenesis, and intermediate filament expression of subventricular zone cells in the postnatal rat forebrain. J. Neurosci. 15, 7238-7249.
84. Zhang, Y., Xiong, Y. and Yarbrough, W. G. (1998). ARF promotes MDM2 degradation and stabilises p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppressor pathways. Cell 92, 725-734.
85. Zhou, Q.-Y., Qualfe, C. J. and Palmiter, R. D. (1995). Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640-643.