The developmental expression of neuronal nitric oxide synthase in cerebellar granule cells is sensitive to GABA and neurotrophins

Developmental Neuroscience

Volumn 19, Issue 3, 1997, Pages 283-290

  Baader, Stephan L ^a   Bucher, Sabine ^a   Schilling, Karl ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Cerebellum; Development; Electrical activity; GABA; Granule cell; Neurotrophic factor; Nitric oxide synthase

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM ION; NEUROTRANSMITTER; NEUROTROPHIN; NEUROTROPHIN 3; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CEREBELLUM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FETUS; GRANULE CELL; INNERVATION; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE;

EID: 0030943803     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000111217     Document Type: Article

References (40)

1. Linden DJ. Connor JA: Long-term synaptic depression. Annu Rev Neurosci 1995:18:319-357.
2. Bliss TVP. Collingridgc GL: A synaptic model of memory': Long-term potentiation in the hippocampus. Nature 1993;361:31-39.
3. Vallano ML. Lambolez B. Audinat E. Rossier J: Neuronal activity differentially regulates NMDA receptor subunit expression in cerebellar granule cells. J Neurosci 1996:16:631-639.
4. Scil FJ. Drakc-Baumann R: Reduced cortical inhibitory svnaptogencsis in organotypic cerebellar cultures developing in the absence of neuronal activity. J Comp Neurol 1994,342: 366-377.
5. Schilling K. Dickinson MH. Connor JA. Morgan JI: Electrical activity in cerebellar cultures determines Purkinje cell dendritic growth patterns. Neuron 1991:7:891-902.
6. Ghosh A. Camahan J. Greenberg ME: Requirement for BDNF in activity-dependent survival of cortical neurons. Science 1994:263: 1618-1623.
7. Schuman EM. Madison DV: Nitric oxide and synaptic function. Annu Rev Neurosci 1994: 17:153-183.
8. Jaffrey SR. Snyder SH: Nitric oxide: A neural messenger. Annu Rev Cell Dev Biol 1995:11: 417-440.
9. Dawson TM. Dawson VL: Nitric oxide synthase: Role as a transmiuer/mediator in the brain and endocrine system. Annu Rev Med 1996:47:219-227.
10. Mavcr B. Klalt P. Bohmc E. Schmidt K: Regulation of neuronal nitric oxide and cyclic GMP formation bv Ca*. J Ncurochcm 1992:59: 2024-2029.
11. Baader SL. Schilling K: Glutamate receptors mediate dynamic regulation of nitric oxide synthase expression in cerebellar granule cells. J Neurosci 1996; 16:1440-1449.
12. Huber KA. Krieglstcin K. Unsickcr K: The neurotrophins BDNF. NT-3 and-4, but not NGF. TGF-beta-l and GDNF increase the number of NADPH-diaphorasc-reactivc neurons in rat spinal cord cultures. Neuroscience 1995:69:771-779.
13. Novikov L, Novikova L. Kallcrth JO: Brain-derived neurotrophic factor promotes survival and blocks nitric oxide synthase expression in adult rat spinal motoneurons after ventral root avulsion. Neurosci Lett 1995:200:45-48.
14. Engelc J, Schilling K: Growth factor-induced c-fos expression defines distinct subsets of midbrain dopaminergic neurons. Neuroscience 1996:73:397-406.
15. Dawson TM. Bred! DS. Fotuhi M. Hwang PM, Snyder SH: Nitric oxide synthase and neuronal NADPH-diaphorase are identical in brain and peripheral tissue. Proc Natl Acad Sci USA 1991:88:7797-7801.
16. Matsumolo T, Nakane M. Pollock JS. Kuk JE, Forstermann U: A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci Lett 1993:155: 61-64.
17. Schilling K, Schmidt HHHW, Baader SL: Nitric oxide synthase expression reveals compartments of cerebellar granule cells and suggests a role for mossy fibers in their development. Neuroscience 1994:59:893-903.
18. Schilling K. Luk D. Morgan JI. Curran T: Regulation of a fos-lacZ fusion gene: A paradigm for quantitative analysis of stimulus-transcription coupling. Proc Natl Acad Sci USA 1991; 88:5665-5669.
19. Smcvnc RJ. Schilling K, Robertson L. Luk D. Obcrdick J. Curran T. Morgan JI: Fos-LacZ transgenic mice: Mapping sites of gene induction in the central nervous system. Neuron 1992;8:13-23.
20. Oberdick J. Lcvinthal F. Levinthal C: A Purkinje cell differentiation markershowsa partial DNA sequence homology to the cellular sis/PDGF2 gene. Neuron 1988:1:367-376.
21. J* of rat cerebellar granule cells in cxplant cultures. J Neurosci 1987;7:1384-4001.
22. Alaimo-Bcuret D. Matus A: Changes in the cytoplasmic distribution of microtubule-associated protein protein 2 during the differentiation of cultured cerebellar granule cells. Neuroscience 1985:14:1103-1115.
23. Segal RA. Takahashi H. McKay RDG: Changes in ncurotrophin responsiveness during the development of cerebellar granule neurons. Neuron 1992:9:1041-1052.
24. Leingartner A, Heisenberg CP, Kolbeck R. Thoenen H, Lindholm D: Brain-derived neurotrophic factor increases neurotrophin-3 expression in cerebellar granule neurons. J Biol Chcm 1994;269:828-830.
25. Gao B, Fritschy JM: Cerebellar granule cells in vitro recapitulate the in vivo pattern of GABA, i-rcccptor subunit expression. Dev Brain Res 1995:88:1-16.
26. Zhang ZG, Chopp M, Gautant S, Zaloga C, Zhang RL. Schmidt HHHW, Pollock JS, Forstermann U: Uprcgulation of neuronal nitric oxide synthase and mRNA, and selective sparing of nitric oxide synthase-containing neurons after focal cerebral ischemia in rat. Brain Res 1994:654:85-95.
27. Brcdt DS. Snyder SH: Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia, and olfactory epithelium. Neuron 1994:13:301-313.
28. Segal RA, Pomeroy SL. Stiles CD: Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J Neurosci 1995:15:4970-4981.
29. Aronica E. Condorelli DF, Nicolclti F. Dellal-bani P. Amico C. Balazs R: Metabotropic glutamate receptors in cultured granule cells- Developmental profile. J Ncurochcm 1993:60: 559-565.
30. Cherubini E. Gaiarsa JL. Bcnari Y: GABA: An excitatory transmitter in early postnatal life. Trends Neurosci 1991;14:515-519.
31. a activation induces Ca* rise in pyramidal cells and intemeurons from rat neonatal hippocampal slices. J Physiol 1995;487:319-329.
32. Van den Pol AN. Obrietan K. Chen G: Excitatory actions of GABA after neuronal trauma. J Neurosci 1996;16:4283-4292.
33. Verge VM. Zhang X, Xu XJ, Wiescnfeld-Hal-lin Z. Hokfclt T: Marked increase in nitric oxide synthase mRNA in rat dorsal root ganglia after peripheral axotomy: In situ hybridization and functional studies. Proc Nall Acad Sci USA 1992;89:11617-11621.
34. Hattcn ME, Hcintz N: Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 1995:18:385-408.
35. Rocamora N, Garcialadona FJ, Palacios JM. Mcngod G: Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Mol Brain Res 1993;17:1-8.
36. Hirsch DB, Steiner JP. Dawson TM, Mammen A, Hayek E, Snyder SH: Neurotransmitter release regulated by nitric oxide in PC-12 cells and brain synaptosomes. Curr Biol 1993;3: 749-754.
37. Engelc J. Bohn MC: The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro arc mediated by mesencephalic glia. J Neurosci 1991; 11:3070-3078.
38. Kang H. Schuman EM: Long-lasting ncurotro-phin-induccd enhancement of synaptic transmission in the adult hippocampus. Science 1995:267:1658.
39. Kim HG. Wan gT, Olafsson P, Lu B: Neurotrophin-3 potentiates neuronal activity and inhibits gamma-aminobutyratergic synaptic transmission in conical neurons. Proc Nall Acad Sci USA 1994;91:12341-12345.
40. Smeync RJ, Chu T, Lcwin A, Bian F, Crisman SS. Kunsch C, Lira SA, Oberdick J: Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 1995:6:230-251