Brief exposure to neurotrophins produces a calcium-dependent increase in choline acetyltransferase activity in cultured rat septal neurons

Journal of Neurochemistry

Volumn 74, Issue 3, 2000, Pages 988-999

  Nonner, Doris ^a   Barrett, Ellen F ^a   Barrett, John N ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Basal forebrain cholinergic neurons; Brain derived neurotrophic factor; Choline acetyltransferase; Nerve growth factor; Neurotrophin 3; Neurotrophin 4

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM ION; CHOLINE ACETYLTRANSFERASE; CYCLIC AMP; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; NEUROTROPHIN 4; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL SURVIVAL; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRACELLULAR CALCIUM; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; INTRACELLULAR MEMBRANES; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NERVE GROWTH FACTORS; NEURONS; OSMOLAR CONCENTRATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NERVE GROWTH FACTOR; RECEPTOR, TRKA; SEPTUM PELLUCIDUM; TIME FACTORS;

ANIMALIA;

EID: 0033953960     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0740988.x     Document Type: Article

References (80)

1. Alderson R. F., Alterman A. L., Barde Y.-A., and Lindsay R. M. (1990) Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5, 297-306.
2. Alessi D. R., Cuenda A., Cohen P., Dudley D. T., and Saltiel A. R. (1995) PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem. 270, 27489-27494.
3. Alonso A., Faure M.-P., and Beaudet A. (1994) Neurotensin promotes oscillatory bursting behavior and is internalized in basal forebrain cholinergic neurons. J. Neurosci. 14, 5778-5792.
4. 125I]BDNF from brain tissue. Brain Res. 743, 40-48.
5. LNTR reduces NGF binding to TrkA on PC12 cells. Neuron 13, 203-215.
6. Batchelor P. E., Armstrong D. M., Blaker S. N., and Gage F. H. (1989) Nerve growth factor receptor and choline acetyltransferase colocalization in neurons within the rat forebrain: response to fimbria-fornix transection. J. Comp. Neurol. 84, 187-204.
7. Bejanin S., Cervini R., Mallet J., and Berrard S. (1994) A unique gene organization for two cholinergic markers, choline acetyltransferase and a putative vesicular transporter of acetylcholine. J. Biol. Chem. 269, 21944-21947.
8. Benedetti M., Levi A., and Chao M. V. (1993) Differential expression of nerve growth factor receptors leads to altered binding affinity and neurotrophin responsiveness. Proc. Natl. Acad. Sci. USA 90, 7859-7863.
9. Berg M. M., Sternberg D. W., Parada L. F., and Chao M. V. (1992) K-252a inhibits nerve growth factor-induced trk proto-oncogene tyrosine phosphorylation and kinase activity. J. Biol. Chem. 267, 13-16.
10. Berninger B. and Poo M.-M. (1996) Fast actions of neurotrophic factors. Curr. Opin. Neurohiol. 6, 324-330.
11. 2+ elevation in hippocampal neurones. Neuroreport 4, 1303-1306.
12. Berse B. and Blusztajn J. K. (1995) Coordinated up-regulation of choline acetyltransferase and vesicular acetylcholine transporter gene expression by the retinoic acid receptor alpha, cAMP, and leukemia inhibitory factor/ciliary neurotrophic factor signaling pathways in a murine septal cell line. J. Biol. Chem. 270, 22101-22104.
13. Blöchl A. and Thoenen H. (1995) Characterization of nerve growth factor (NGF) release from hippocampal neurons: evidence for a constitutive and an unconventional sodium-dependent regulated pathway. Eur. J. Neurosci. 7, 1220-1228.
14. Blöchl A. and Thoenen H. (1996) Localization of cellular storage compartments and sites of constitutive and activity-dependent release of nerve growth factor (NGF) in primary cultures of hippocampal neurons. Mol. Cell. Neurosci. 7, 173-190.
15. Boulanger L. and Poo M.-M. (1999) Gating of BDNF-induced synaptic potentiation by cAMP. Science 284, 1982-1984.
16. Cheng B. and Mattson M. P. (1994) NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 607, 275-285.
17. Courtney M. J., Åkerman K. E. O., and Coffey E. T. (1997) Neurotrophins protect cultured cerebellar granule neurons against the early phase of cell death by a two-component mechanism. J. Neurosci. 17, 4201-4211.
18. D'Arcangelo G., Paradiso K., Shepherd D., Brehm P., Halegoua S., and Mandel G. (1993) Neuronal growth factor regulation of two different sodium channel types through distinct signal transduction pathways. J. Cell Biol. 122, 915-921.
19. +] after transection and resealing in lizard peripheral myelinated axons. J. Physiol. (Lond.) 498, 295-307.
20. Davies A. M., Lee K.-F., and Jaenisch R. (1993) p75-deficient trigeminal sensory neurons have an altered response to NGF but not other neurotrophins. Neuron 11, 565-574.
21. Dawbarn D., Allen S. U., and Semenenko F. M. (1988) Coexistence of choline acetyltransferase and nerve growth factor receptors in the rat basal forebrain. Neurosci. Lett. 94, 138-144.
22. Dudley D. T., Pang L., Decker S. J., Bridges A. J., and Saltiel A. R. (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 92, 7686-7689.
23. 2+/calmodulin-dependent protein kinase IV: role in transcriptional regulation. J. Biol. Chem. 269, 15520-15527.
24. Erickson J. D., Varoqui H., Schäfer M. K.-H., Modi W., Diebler M.-F., Weihe E., Rand J., Eiden L. E., Bonner T. I., and Usdin T. B. (1994) Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J. Biol. Chem. 269, 21929-21932.
25. 2+-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16, 233-236.
26. Finkbeiner S., Tavazoie S. F., Maloratsky A., Jacobs K. M., Harris K. M., and Greenberg M. E. (1997) CREB: a major mediator of neuronal neurotrophin responses. Neuron 19, 1031-1047.
27. Fonnum R. (1969) Radiochemical micro assays for the determination of choline acetyltransferase and acetylcholinesterase activities. Biochem. J. 115, 465-472.
28. Friedman W. J., Ibáñez C. F., Hallbook F., Persson H., Cain L. D., Dreyfus C. F., and Black I. B. (1993) Differential actions of neurotrophins in the locus coeruleus and basal forebrain. Exp. Neurol. 119, 72-78.
29. NGFR and up-regulation by nerve growth factor. J. Comp. Neurol. 341, 324-339.
30. Goodman L. J., Valverde J., Lim F., Geschwind M. D., Federoff H. J., Geller A. I., and Hefti F. (1996) Regulated release and polarized localization of brain-derived neurotrophic factor in hippocampal neurons. Mol. Cell. Neurosci. 7, 222-238.
31. Gundersen R. and Barrett J. N. (1979) Neuronal chemotaxis: chick dorsal root axons turn toward elevated concentrations of nerve growth factor. Science 206, 1079-1080.
32. Gundersen R. and Barrett J. N. (1980) Characterization of the turning response of dorsal root neurites toward nerve growth factor. J. Cell Biol. 87, 546-554.
33. Hantzopoulos P. A., Suri C., Glass D. J., Goldfarb M. P., and Yancopoulos G. D. (1994) The low affinity NGF receptor, p75, can collaborate with each of the Trks to potentiate functional responses to the neurotrophins. Neuron 13, 187-201.
34. Hempstead B. L., Martin-Zanca D., Kaplan D. R., Parada L. F., and Chao M. V. (1991) High-affinity NGF binding requires coexpression of the trk proto-oncogene and the low-affinity NGF receptor. Nature 350, 678-683.
35. trk mRNA marks the NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron 9, 465-478.
36. Huber L. J. and Chao M. V. (1995) A potential interaction of p75 and trkA NGF receptors demonstrated by affinity cross-linking and immunoprecipitation. J. Neurosci. Res. 40, 557-563.
37. Kang H. J. and Schuman E. M. (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267, 1658-1662.
38. Kaufman L. M. and Barrett J. N. (1983) Serum factor supporting long-term survival of rat central neurons in culture. Science 220, 1394-1396.
39. Kawamoto J. C. and Barrett J. N. (1986) Cryopreservation of primary neurons for tissue culture. Brain Res. 384, 84-93.
40. Knipper M., Leung L. S., Zhao D., and Rylett R. J. (1994a) Short-term modulation of glutamatergic synapses in adult rat hippocampus by NGF. Neuroreport 5, 2433-2436.
41. Knipper M., da Penha Berzaghi M., Blöchl A., Breer H., Thoenen H., and Lindholm D. (19946) Positive feedback between acetylcholine and the neurotrophins nerve growth factor and brain-derived neurotrophic factor in the rat hippocampus. Eur. J. Neurosci. 6, 668-671.
42. Knüsel B. and Hefti F. (1992) K-252 compounds: modulators of neurotrophin signal transduction. J. Neurochem. 59, 1987-1996.
43. Knüsel B., Rabin S., Widmer H. R., Hefti F., and Kaplan D. R. (1992) Neurotrophin induced trk receptor phosphorylation and cholinergic neuron response in primary cultures of embryonic rat brain neurons. Neuroreport 3, 885-888.
44. Lessmann V., Gottmann K., and Heumann R. (1994) BDNF and NT-4/5 enhance glutamatergic synaptic transmission in cultured hippocampal neurones. Neuroreport 6, 21-25.
45. Levine E., Dreyfus C., Black I., and Plummer M. (1995) Differential effects of NGF and BDNF on voltage-gated calcium currents in embryonic basal forebrain neurons. J. Neurosci. 15, 3084-3091.
46. Li Y., Holtzman D. M., Kromer L. F., Kaplan D. R., Chua-Couzens J., Clary D. O., Knüsel B., and Mobley W. C. (1995) Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J. Neurosci. 15, 2888-2905.
47. Lohof A. M., Ip N. Y., and Poo M.-M. (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363, 350-353.
48. trk binding: implications for multi-subunit polypeptide receptors. J. Biol. Chem. 269, 6884-6891.
49. Marsh H. N. and Palfrey H. C. (1996) Neurotrophin-3 and brain-derived neurotrophic factor activate multiple signal transduction events but are not survival factors for hippocampal pyramidal neurons. J. Neurochem. 67, 952-963.
50. trkB in primary hippocampal pyramidal cell culture. J. Neurosci. 13, 4281-4292.
51. McAllister A. K., Katz L. C., and Lo D. C. (1996) Neurotrophin regulation of cortical dendritic growth requires activity. Neuron 17, 1057-1064.
52. Merlio J. P., Ernfors P., and Persson H. (1992) Molecular cloning of rat trkC and distribution of cells expressing messenger RNAs for the members of the trk family in the rat central nervous system. Neuroscience 51, 513-532.
53. Merritt J. E., Jacob R., and Hallam T. J. (1989) Use of manganese to discriminate between calcium influx and mobilization from internal stores in stimulated human neutrophils. J. Biol. Chem. 264, 1522-1527.
54. Meyer-Franke A., Wilkinson G. A., Kruttgen A., Hu M., Munro E., Hanson M. G. Jr., Reichardt L. F., and Barres B. A. (1998) Depolarization and cAMP elevation rapidly recruit TrkB to the plasma membrane of CNS neurons. Neuron 21, 681-693.
55. Moises H. C., Womble M. D., Washburn M. S., and Williams L. R. (1995) Nerve growth factor facilitates cholinergic neurotransmission between nucleus basalis and the amygdala in rat: an electrophysiological analysis. J. Neurosci. 15, 8131-8142.
56. Muroya K., Hashimoto Y., Hattori S., and Nakamura S. (1992) Specific inhibition of NGF receptor tyrosine kinase activity by K-252a. Biochim. Biophys. Acta 1135, 353-356.
57. Nonner D., Brass B. J., Barrett E. F., and Barrett J. N. (1993) Reversibility of nerve growth factor's enhancement of choline acetyltransferase activity in cultured embryonic rat septum. Exp. Neurol. 122, 196-208.
58. Nonner D., Barrett E. F., and Barrett J. N. (1996) Neurotrophin effects on survival and expression of cholinergic properties in cultured rat septal neurons under normal and stress conditions. J. Neurosci. 16, 6665-6675.
59. Nonomura T., Nishio C., Lindsay R. M., and Hatanaka H. (1995) Cultured basal forebrain cholinergic neurons from postnatal rats show both overlapping and non-overlapping responses to the neurotrophins. Brain Res. 683, 129-139.
60. Nye S. H., Squinto S. P., Glass D. J., Stitt T. N., Hantzopoulos P., Macchi M. J., Lindsay N. S., Ip N. Y., and Yancopoulos G. D. (1992) K-252a and staurosporine selectively block autophosphorylation of neurotrophin receptors and neurotrophin-mediated responses. Mol. Biol. Cell 3, 677-686.
61. Pang L., Sawada T., Decker S. J., and Saltiel A. R. (1995) Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J. Biol. Chem. 270, 13585-13588.
62. Pongrac J. L. and Rylett R. J. (1998) NGF-induction of the expression of ChAT mRNA in PC12 cells and primary cultures of embryonic rat basal forebrain. Brain Res. Mol. Brain Res. 62, 25-34.
63. Quirin-Stricker C., Mauvais C., and Schmitt M. (1997) Transcriptional activation of human choline acetyltransferase by AP2- and NGF-induced factors. Mol. Brain Res. 49, 165-174.
64. Rodríguez-Tébar A., Dechant G., and Barde Y.-A. (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron 4, 487-492.
65. Rodríguez-Tébar A., Dechant G., Götz R., and Barde Y.-A. (1992) Binding of neurotrophin-3 to its neuronal receptors and interacions with nerve growth factor and brain-derived neurotrophic factor. EMBO J. 11, 917-922.
66. Sobreviela T., Clary D. O., Reichardt L. F., Bradabur M. M., and Mufson E. J. (1994) TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. J. Comp. Neurol. 350, 587-611.
67. Steininger T. L., Wainer B. H., Klein R., Barbacid M., and Palfrey H. C. (1993) High-affinity nerve growth factor receptor (Trk) immunoreactivity is localized in cholinergic neurons of the basal forebrain and striatum in the adult rat brain. Brain Res. 612, 330-335.
68. Stoop R. and Poo, M.-M. (1996) Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J. Neurosci. 16, 3256-3264.
69. 125]neurotensin binding sites to cholinergic neurons of the rat nucleus basalis magnocellularis. Neuroscience 36, 377-391.
70. A synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 17, 2959-2966.
71. Tapley P., Lamballe F., and Barbacid M. (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7, 371-381.
72. Tedeschi, B., Barrett J. N., and Keane R. W. (1986) Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells. J. Cell Biol. 102, 2244-2253.
73. Thoenen H. (1995) Neurotrophins and neuronal plasticity. Science 270, 593-598.
74. 2+-/calmodulin dependent protein kinase II. J. Biol. Chem. 265, 4315-4320.
75. Toledo-Aral J. J., Brehm P., Halegoua S., and Mandel G. (1995) A single pulse of nerve growth factor triggers long-term neuronal excitability through sodium channel gene induction. Neuron 14, 607-611.
76. Toussaint J. L., Geoffrey V., Schmitt M., Werner A., Garnier J. M., Simoni P., and Kempf J. (1992) Human choline acetyltransferase (CHAT): partial gene sequence and potential control regions. Genomics 12, 412-416.
77. 125I-nerve growth factor in rat sympathetic neurons in compartmented cultures. J. Neurosci. 17, 1282-1290.
78. Verdi J. M., Birren S. J., Ibáñez C. F., Persson H., Kaplan D. R., Benedetti M., Chao M. V., and Anderson D. J. (1994) p75NTR regulates Trk signal transaction and NGF-induced neuronal differentiation in MAH cells. Neuron 12, 733-745.
79. Whittemore S. R. and Seiger Å. (1987) The expression, localization and functional significance of β-nerve growth factor in the central nervous system. Brain Res. Rev. 12, 439-464.
80. Yan J. and Barrett J. N. (1998) Purification from bovine serum of a survival-promoting factor for cultured central neurons and its identification as selenoprotein-P. J. Neurosci. 18, 8682-8691.