TGF-β-induced apoptpsis of cerebellar granule neurons is prevented by depolarization

Journal of Neuroscience

Volumn 16, Issue 13, 1996, Pages 4174-4185

  De Luca, Ariane ^a   Weller, Michael ^b   Fontana, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Apoptosis; Cerebellum; Depolarization; Maturation dependence; Potassium; TGF

Indexed keywords

POTASSIUM ION; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CULTURE MEDIUM; DEPOLARIZATION; GRANULE CELL; NERVE CELL CULTURE; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CELL AGING; CELL SURVIVAL; CEREBELLUM; CULTURE MEDIA; CYTOKINES; ELECTROPHYSIOLOGY; HUMANS; NEURONS; POTASSIUM; RATS; RECOMBINANT PROTEINS; TIME FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 0029897649     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-13-04174.1996     Document Type: Article

References (73)

1. 2+ mobilization. Biochem Biophys Res Commun 210:378-383.
2. +-induced depolarization selectively promote the expression of a NMDA-preferring class of the ionotropic glutamate receptor in cerebellar granule cells. Neurosci Lett 137:109-113.
3. Blottner D, Wolf N, Lachmund A, Flanders KC, Unsicker K (1996) TGF-β rescues target-deprived preganglionic sympathetic neurons in the spinal cord. Eur J Neurosci 8:202-210.
4. Chalazonitis A, Kalberg J, Twardzik DR, Morrison RS, Kessler JA (1992) Transforming growth factor-β has neurotrophic actions on sensory neurons in vitro and is synergistic with nerve growth factor. Dev Biol 152:121-132.
5. 3 by glioblastoma cell lines, astrocytes and microglia. J Immunol 148:1404-1410.
6. 2 by postnatal cerebellar neurons and its effect on neuroblast proliferation. Eur J Neurosci 6:766-778.
7. + and NMDA correlate with c-fos protooncogene expression. Neurosci Lett 107:55-62.
8. Didier M, Heaulme M, Soubrie P, Pin J-P (1990) Rapid, sensitive, and simple method for quantification of both neurotoxic and neurotrophic effects of NMDA on cultured cerebellar granule cells. J Neurosci Res 27:25-35.
9. Didier M, Roux P, Piechaczyk M, Mangeat P, Devilliers G, Bockaert J, Pin JP (1992) Long-term expression of the c-fos protein during the in vitro differentiation of cerebellar granule cells induced by potassium and NMDA. Mol Brain Res 12:249-258.
10. D'Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
11. Erecinska M, Nelson D, Chance B (1991) Depolarization-induced changes in cellular energy production. Proc Natl Acacl Sci USA 88:7600-7604.
12. Fischer G (1982) Cultivation of mouse cerebellar cells in serum free, hormonally defined media: survival of neurons. Neirosci Lett 28:325-329.
13. Flanders KC, Lüdecke G, Engels S, Cissel DS, Roberts AB, Kondaiah P, Lafyatis R, Sporn M, Unsicker K (1991) Localization and actions of transforming growth factor-βs in the embryonic nervous syslem. Development 113:183-191.
14. Fontana A, Hengartner H, de Tribolet N, Weber E (1984) Glioblastoma cells release interleukin-1 and factors inhibiting interleukin-2 mediated effects. J Immunol 132:1837-1844.
15. Franklin JL, Johnson EM (1992) Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci 15:501-508.
16. 1 in the central nervous system of transgenic mice resulting in hydrocephalus. J Neuropathol Exp Neurol 54:334-349.
17. Gallo V, Ciotti MT, Coletti A, Aloisi F, Levi G (1982) Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc Natl Acad Sci USA 79:7919-7923.
18. Gallo V, Kingsbury A, Balasz R, Jørgensen OS (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J Neurosci 7:2203-2213.
19. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
20. Ghosh A, Carnahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618-1622.
21. 2+ channel that is regulated by TGF-β. Science 257:91-94.
22. Heine UI, Munoz EF, Flanders KC, Ellingsworth LR, Lam HYP, Thompson NL, Roberts AB, Sporn MB (1987) Role of transforming growth factor-β in the development of the mouse embryo. J Cell Biol 105:2861-2876.
23. Iseki S, Osumi-Yamashita N, Miyazono K, Franzén P, Ichijo H, Ohlani H, Hayashi Y, Eto K (1995) Localization of transforming growth factor-β type I and type II receptors in mouse development. Exp Cell Res 219:339-347.
24. 2 promote neurite sprouting and elongation of cultured rat hippocampal neurons. Brain Res 639:21-25.
25. Johnson EM, Deckwerth TL (1993) Molecular mechanisms of developmental neuronal death. Annu Rev Neurosci 16:31-46.
26. 1 with multiple repeat sequences. Cell 61:1051-1061.
27. Kessler JA, Ludlam WH, Freidin MM, Hall DH, Michaelson MD, Spray DC, Dougherty M, Batter DK (1993) Cytokine-induced programmed death of cultured sympathetic neurons. Neuron 11:1123-1132.
28. Kingsbury AE, Gallo V, Woodhams PL, Balász R (1985) Survival, morphology and adhesion properties of cerebellar interneurones cultured in chemically defined and serum-supplemented medium. Dev Brain Res 17:17-25.
29. + toxicity. EMBO J 14:736-742.
30. 1 expression is initiated in adult auditory neurons by sectioning of the auditory nerve. NeuroReport 3:295-298.
31. 1. Cancer Res 52:385-388.
32. 1 stimulates expression of nerve growth factor in the rat CNS. NeuroReport 1:9-12.
33. 1 in the rat brain after a localized cerebral injury. Brain Res 587:216-225.
34. 1 and cyclic AMP promote apoptosis in resting human B lymphocytes. J Immunol 1634-1643.
35. 1 and cancer chemotherapy compounds in myeloid leukemic cells. Blood 80:1750-1757.
36. 1, during lymphocyte activation. J Immunol 145:1415-1422.
37. Mahanthappa NK, Schwarting GA (1993) Peptide growth factor control of olfactory neurogenesis and neuron survival in vitro: roles of EGF and TGF-βs. Neuron 10:293-305.
38. Maher F, Simpson IA (1994) Modulation of expression of glucose transporters GLUT3 and GLUT1 by potassium and N-methyl-D-aspartate in cultured cerehellar granule neurons. Mol Cell Neurosci 5:369-375.
39. Marini AS, Paul SM (1992) N-methyl-D-aspartate receptor mediated neuroprotection in cerebellar granule cells requires new RNA and protein synthesis. Proc Natl Acad Sci USA 89:6555-6559.
40. 1 is a potent survival factor for rat embryo motorneurons in culture. Dev Brain Res 52:175-181.
41. Massagué J (1990) The transforming growth factor-β family. Annu Rev Cell Biol 6:597-641.
42. Moran J, Patel AJ (1989) Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during development. Dev Brain Res 46:97-105.
43. 1 mRNA increases in macrophage/microglial cells of the hippocampus in response to deafferentation and kainic acid-induced neurodegeneration. Exp Neurol 120:291-301.
44. 2+ oscillations in cardiac myocytes. Biochem Biophys Res Commun 204:678-684.
45. Nicoletti F, Wroblewski JT, Novelli A, Alho H, Guidotti A, Costa E (1986) The activation of inositol phospholipid metabolism as a signal-transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. J Neurosci 6:1905-1911.
46. Novelli A, Reilly JA, Lysko PG, Henneberry RC (1988) Glutamate becomes neurotoxic via the N-methyl-D-aspartate receptor when intracellular energy levels are reduced. Brain Res 451:205-212.
47. Oberhammer F, Sedivy R, Jirtle R, Schulte-Hermann R (1991) Role of pro and mature TGF-β1 in cell death (apoptosis) of hepatocytes. Naunyn Schmiedebergs Arch Pharmacol Suppl 343:R24.
48. 1. Proc Natl Acad Sci USA 89:5408-5412.
49. 1, and fibronectin messenger RNA in rat brain: responses to injury and cell-type localization. Neuroscience 54:893-907.
50. Pearson H, Graham ME, Burgoyne RD (1992) Relationship between intracellular free calcium concentration and NMDA-induced cerebellar granule cell survival in vitro. Eur J Neurosci 4:1369-1375.
51. Peng L, Zhang X, Hertz L (1994) High extracellular potassium concentrations stimulate oxidative metabolism in a glutamatergic neuronal culture and glycolysis in cultured astrocytes but have no stimulatory effect in a GABAergic neuronal culture. Brain Res 663:168-172.
52. 2 inhibits cerebrovascular changes and brain edema formation in the tumor necrosis factor α-independent early phase of experimental pneumococcal meningitis. J Exp Med 176:265-268.
53. Piani D, Frei K, Quang Do K, Cuánod M, Fontana A (1991) Murine brain macrophages induce NMDA receptor mediated neurotoxicity in vitro by secreting glutamate. Neuroscience Lett 133:159-162.
54. 3 are potent survival factors for midbrain dopaminergic neurons. Neuron 13:1245-1252.
55. 1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse neocortex from ischemic injury in vivo. J Cereb Blood Flow Metab 13:521-525.
56. Prehn JHM, Peruche B, Unsicker K, Krieglstein J (1993b) Isoform-speciflc effects of transforming growth factors-β on degeneration of primary neuronal cultures induced by cytotoxic hypoxia or glutamate. J Neurochem 60:1665-1672.
57. Prehn JHM, Bindokas VP, Marcuccilli CJ, Krajewski S, Reed JC, Miller RJ (1994) Regulation of neuronal Bcl-2 expression and calcium homeostasis by transforming growth factor type β confers wide-ranging protection on rat hippocampal neurons. Proc Natl Acad Sci USA 91:12599-12603.
58. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD (1993) Programmed cell death and the control of cell survival. Science 262:695-700.
59. Resink A, Hack N, Boer GJ, Balász R (1994) Growth conditions differentially modulate the vulnerability of developing cerebellar granule cells to excitatory amino acids. Brain Res 655:222-232.
60. 2 and NGF differentially regulate neural recognition molecule expression by cultured astrocytes. J Cell Biol 115:473-484.
61. Tymianski M, Wang LY, MacDonald JF (1994) Alteration of neuronal calcium homeostasis and excitotoxic vulnerability by chronic depolarization. Brain Res 648:291-295.
62. Unsicker K, Flanders KC, Cissel DS, Lafyatis R, Sporn MB (1991) Transforming growth factor beta isoforms in the adult rat central and peripheral nervous system. Neuroscience 44:613-625.
63. 1 is in plaques in Alzheimer and Down pathologies. NeuroReport 4:69-72.
64. Weller M, Marini AM, Paul SM (1992) Niacinamide blocks 3-acetylpyridine toxicity of cerebellar granule cells in vitro. Brain Res 594:160-164.
65. 2 induces apoptosis of murine T cell clones without down-regulating bcl-2 mRNA expression. Eur J Immunol 24:1293-1300.
66. Weller M, Frei K, Groscurth P, Krammer PH, Yonekawa Y, Fontana A (1994b) Anti-Fas/APO-1 antibody-mediated apoptosis of cultured human glioma cells. Induction and modulation of sensitivity by cytokines. J Clin Invest 94:954-964.
67. Weller M, Malipiero U, Aguzzi A, Reed JC, Fontana A (1995a) Protooncogene bcl-2 gene transfer abrogates Fas/APO-1 antibody- mediated apoptosis of human malignant glioma cells and confers resistance to chemotherapeutic drugs and therapeutic irradiation. J Clin Invest 95:2633-2643.
68. Weller M, Malipiero U, Rensing-Ehl A, Barr PJ, Fontana A (1995b) Fas/APO-1 gene transfer for human malignant glioma. Cancer Res 55:2936-2944.
69. Weller M, Fontana A (1996) The failure of current immunotherapy for malignant glioma. Tumor-derived TGF-β, T cell apoptosis and the immune privilege of the brain. Brain Res Rev, in press.
70. Wood KA, Dipasquale B, Youle RJ (1993) In situ labeling of granule cells for apoptosis-associated DNA fragmentation reveals different mechanisms of cell loss in developing cerebellum. Neuron 11:621-632.
71. Wrann M, Bodmer S, de Martin R, Siepl C, Hofer-Warbinek R, Frei K, Hofer E, Fontana A (1987) T cell suppressor factor from human glioblastoma cells is a 12.5 kDa protein closely related to transforming growth factor-beta. EMBO J 6:1633-1636.
72. Yan G-M, Ni B, Weller M, Wood KA, Paul SM (1994) Depolarization or glutamate receptor activation blocks apoptotic cell death of cultured cerebellar granule neurons. Brain Res 656:43-51.
73. 1 induces apoptotic cell death in cultured human gastric carcinoma cells. Cancer Res 52:4042-4045.