NMDA receptor activation modulates programmed cell death during early post-natal retinal development: A BDNF-dependent mechanism

Journal of Neurochemistry

Volumn 95, Issue 1, 2005, Pages 244-253

  Martins, Rodrigo A P ^a   Silveira, Mariana S ^a   Curado, Marco R ^a   Police, Angela I ^a   Linden, Rafael ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Amacrine cells; Development; Excitotoxicity; Glutamate; Neurotrophins; Programmed cell death

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; DIZOCILPINE; GLUTAMIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NEUROTROPHIN 4; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EXPLANT; IN VIVO STUDY; NEUROPROTECTION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN CONTENT; RAT; RECEPTOR UPREGULATION; RETINA DEVELOPMENT;

EID: 25644446105     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03360.x     Document Type: Article

References (64)

1. Adams S. M., Rivero Vaccari J. C. and Corriveau R. A. (2004) Pronounced cell death in the absence of NMDA receptors in the developing somatosensory thalamus. J. Neurosci. 24, 9441-9450.
2. de Araujo E. G. and Linden R. (1993) Trophic factors produced by retinal cells increase the survival of retinal ganglion cells in vitro. Eur. J. Neurosci. 5, 1181-1188.
3. Barnstable C. J. (1993) Glutamate and GABA in retinal circuitry. Curr. Opin. Neurobiol. 3, 520-525.
4. Berninger B., Marty S., Zafra F., da Penha B. M., Thoenen H. and Lindholm D. (1995) GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121, 2327-2335.
5. Bhave S. V., Ghoda L. and Hoffman P. L. (1999) Brain-derived neurotrophic factor mediates the anti-apoptotic effect of NMDA in cerebellar granule neurons: signal transduction cascades and site of ethanol action. J. Neurosci. 19, 3277-3286.
6. Brenneman D. E., Forsythe I. D., Nicol T. and Nelson P. G. (1990) N-methyl-D-aspartate receptors influence neuronal survival in developing spinal cord cultures. Brain Res. Dev. Brain Res. 51, 63-68.
7. Cameron H. A., Hazel T. G. and McKay R. D. (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J. Neurobiol. 36, 287-306.
8. Cellerino A. and Kohler K. (1997) Brain-derived neurotrophic factor/ neurotrophin-4 receptor TrkB is localized on ganglion cells and dopaminergic amacrine cells in the vertebrate retina. J. Comp. Neurol. 386, 149-160.
9. Cepko C. L. (1999) The roles of intrinsic and extrinsic cues and bHLH genes in the determination of retinal cell fates. Curr. Opin. Neurobiol. 9, 37-46.
10. Coskun V. and Luskin M. B. (2002) Intrinsic and extrinsic regulation of the proliferation and differentiation of cells in the rodent rostral migratory stream. J. Neurosci. Res. 69, 795-802.
11. Cusato K., Bosco A., Linden R. and Reese B. E. (2002) Cell death in the inner nuclear layer of the retina is modulated by BDNF. Brain Res. Dev. Brain Res. 139, 325-330.
12. Du J., Feng L., Yang F. and Lu B. (2000) Activity- and Ca(2+)-dependent modulation of surface expression of brain-derived neurotrophic factor receptors in hippocampal neurons. J. Cell Biol. 150, 1423-1434.
13. Dyer M. A. and Cepko C. L. (2001) Regulating proliferation during retinal development. Nat. Rev. Neurosci. 2, 333-342.
14. Ferguson K. L. and Slack R. S. (2003) Growth factors: can they promote neurogenesis? Trends Neurosci. 26, 283-285.
15. Fiske B. K. and Brunjes P. C. (2001) NMDA receptor regulation of cell death in the rat olfactory bulb. J. Neurobiol 47, 223-232.
16. Ghosh A., Carnahan J. and Greenberg M. E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618-1623.
17. Gould E., Cameron H. A. and McEwen B. S. (1994) Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J. Comp. Neurol. 340, 551-565.
18. Grunder T., Kohler K., Kaletta A. and Guenther E. (2000a) The distribution and developmental regulation of NMDA receptor subunit proteins in the outer and inner retina of the rat. J. Neurobiol. 44, 333-342.
19. Grunder T., Kohler K. and Guenther E. (2000b) Distribution and developmental regulation of AMPA receptor subunit proteins in rat retina. Invest. Ophthalmol. Vis. Sci. 41, 3600-3606.
20. Hansen H. H., Briem T., Dzietko M. et al. (2004) Mechanisms leading to disseminated apoptosis following NMDA receptor blockade in the developing rat brain. Neurobiol. Dis. 16, 440-453.
21. Haydar T. F., Wang F., Schwartz M. L. and Rakic P. (2000) Differential modulation of proliferation in the neocortical ventricular and subventricular zones. J. Neurosci. 20, 5764-5774.
22. Horsburgh G. M. and Sefton A. J. (1987) Cellular degeneration and synaptogenesis in the developing retina of the rat. J. Comp. Neurol. 263, 553-566.
23. Huang E. J. and Reichardt L. F. (2003) Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642.
24. Hughes P. E., Young D., Preston K. M., Yan Q. and Dragunow M. (1998) Differential regulation by MK801 of immediate-early genes, brain-derived neurotrophic factor and trk receptor mRNA induced by a kindling after-discharge. Brain Res. Mol. Brain Res. 53, 138-151.
25. Ikonomidou C., Bosch F., Miksa M., Bittigau P., Vockler J., Dikranian K., Tenkova T. I., Stefovska V., Turski L. and Olney J. W. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74.
26. Job C. and Tan S. S. (2003) Constructing the mammalian neocortex: the role of intrinsic factors. Dev. Biol. 257, 221-232.
27. Johansson K., Bruun A., Torngren M. and Ehinger B. (2000) Development of glutamate receptor subunit 2 immunoreactivity in postnatal rat retina. Vis. Neurosci. 17, 737-742.
28. Johnson J., Tian N., Caywood M. S., Reimer R. J., Edwards R. H. and Copenhagen D. R. (2003) Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J. Neurosci. 23, 518-529.
29. Kaplan D. R. and Miller F. D. (2000) Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10, 381-391.
30. Kingsbury T. J., Murray P. D., Bambrick L. L. and Krueger B. K. (2003) Ca(2+)-dependent regulation of TrkB expression in neurons. J. Biol. Chem. 278, 40 744-40 748.
31. Komuro H. and Rakic P. (1993) Modulation of neuronal migration by NMDA receptors. Science 260, 95-97.
32. Linden R., Rehen S. K. and Chiarini L. B. (1999) Apoptosis in developing retinal tissue. Prog. Retina. Eye Res. 18, 133-165.
33. Linden R., Martins R. A. P. and Silveira M. (2005) Control of programmed cell death by neurotransmitters and neuropeptides in the developing mammalian retina. Prog. Retinal Eye Res. 24, 457-491.
34. Lindholm D., Castren E., Berzaghi M., Blochl A. and Thoenen H. (1994) Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain - implications for neuronal plasticity. J. Neurobiol. 25, 1362-1372.
35. LoTurco J. J., Owens D. F., Heath M. J., Davis M. B. and Kriegstein A. R. (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15, 1287-1298.
36. Mansour-Robaey S., Clarke D. B., Wang Y. C., Bray G. M. and Aguayo A. J. (1994) Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc. Natl Acad. Sci. USA 91, 1632-1636.
37. Marini A. M., Rabin S. J., Lipsky R. H. and Mocchetti I. (1998) Activity-dependent release of brain-derived neurotrophic factor underlies the neuroprotective effect of N-methyl-D-aspartate. J. Biol. Chem. 273, 29 394-29 399.
38. Marquardt T. (2003) Transcriptional control of neuronal diversification in the retina. Prog. Retin Eye Res. 22, 567-577.
39. Massey S. C. and Redburn D. A. (1987) Transmitter circuits in the vertebrate retina. Prog. Neurobiol. 28, 55-96.
40. 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.
41. Monti B. and Contestabile A. (2000) Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur. J. Neurosci. 12, 3117-3123.
42. Monti B., Marri L. and Contestabile A. (2002) NMDA receptor-dependent CREB activation in survival of cerebellar granule cells during in vivo and in vitro development. Eur. J. Neurosci. 16, 1490-1498.
43. Nakazawa T., Nakano I., Sato M., Nakamura T., Tamai M. and Mori N. (2002) Comparative expression profiles of Trk receptors and Shc-related phosphotyrosine adapters during retinal development: potential roles of N-Shc/ShcC in brain-derived neurotrophic factor signal transduction and modulation. J. Neurosci. Res. 68, 668-680.
44. Nguyen L., Rigo J. M., Rocher V., Belachew S., Malgrange B., Rogister B., Leprince P. and Moonen G. (2001) Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305, 187-202.
45. Pallas S. L. (2001) Intrinsic and extrinsic factors that shape neocortical specification. Trends Neurosci. 24, 417-423.
46. da Penha B. M., Cooper J., Castren E., Zafra F., Sofroniew M., Thoenen H. and Lindholm D. (1993) Cholinergic regulation of brain-derived neurotrophic factor (BDNF) and nerve growth factor (NGF) but not neurotrophin-3 (NT-3) mRNA levels in the developing rat hippocampus. J. Neurosci. 13, 3818-3826.
47. Perez M. T. and Caminos E. (1995) Expression of brain-derived neurotrophic factor and of its functional receptor in neonatal and adult rat retina. Neurosci. Lett. 183, 96-99.
48. Pinzon-Duarte G., Arango-Gonzalez B., Guenther E. and Kohler K. (2004) Effects of brain-derived neurotrophic factor on cell survival, differentiation and patterning of neuronal connections and Muller glia cells in the developing retina. Eur. J. Neurosci. 19, 1475-1484.
49. Pow D. V. and Barnett N. L. (1999) Changing patterns of spatial buffering of glutamate in developing rat retinae are mediated by the Muller cell glutamate transporter GLAST. Cell Tissue Res. 297, 57-66.
50. Rehen S. K., Varella M. H., Freitas F. G., Moraes M. O. and Linden R. (1996) Contrasting effects of protein synthesis inhibition and of cyclic AMP on apoptosis in the developing retina. Development 122, 1439-1448.
51. Rickman D. W. and Brecha N. C. (1995) Expression of the protooncogene, trk, receptors in the developing rat retina. Vis. Neurosci. 12, 215-222.
52. Rickman D. W. and Rickman C. B. (1996) Suppression of trkB expression by antisense oligonucleotides alters a neuronal phenotype in the rod pathway of the developing rat retina. Proc. Natl Acad. Sci USA 93, 12 564-12 569.
53. Rocha M., Martins R. A. and Linden R. (1999) Activation of NMDA receptors protects against glutamate neurotoxicity in the retina: evidence for the involvement of neurotrophins. Brain Res. 827, 79-92.
54. Rohrer B., Korenbrot J., LaVail M., Reichardt L. and Xu B. (1999) Role of neurotrophin receptor TrkB in the maturation of rod photoreceptors and establishment of synaptic transmission to the inner retina. J. Neurosci. 19, 8919-8930.
55. Scarisbrick I. A., Isackson P. J. and Windebank A. J. (1999) Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 in the adult rat spinal cord: regulation by the glutamate receptor agonist kainic acid. J. Neurosci. 19, 7757-7769.
56. Shieh P. B., Hu S. C., Bobb K., Timmusk T. and Ghosh A. (1998) Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20, 727-740.
57. Sometani A., Kataoka H., Nitta A., Fukumitsu H., Nomoto H. and Furukawa S. (2001) Transforming growth factor-β1 enhances expression of brain-derived neurotrophic factor and its receptor, TrkB, in neurons cultured from rat cerebral cortex. J. Neurosci. Res. 66, 369-376.
58. Sucher N. J., Kohler K., Tenneti L., Wong H. K., Grunder T., Fauser S., Wheeler-Schilling T., Nakanishi N., Lipton S. A. and Guenther E. (2003) N-methyl-D-aspartate receptor subunit NR3A in the retina: developmental expression, cellular localization, and functional aspects. Invest. Ophthalmol Vis. Sci. 44, 4451-4456.
59. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20, 709-726.
60. Thorenson W. B. and Witkovsky P. (1999) Glutamate receptors and circuits in the vertebrate retina. Prog. Retin Eye Res. 18, 765-810.
61. Tian N. and Copenhagen D. R. (2001) Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32, 439-449.
62. Weidman T. A. and Kuwabara T. (1968) Postnatal development of the rat retina. An electron microscopic study. Arch. Ophthalmol. 79, 470-484.
63. Wong W. T. and Wong R. O. (2001) Changing specificity of neurotransmitter regulation of rapid dendritic remodeling during synaptogenesis. Nat. Neurosci. 4, 351-352.
64. Zhang S. S., Fu X. Y. and Barnstable C. J. (2002) Molecular aspects of vertebrate retinal development. Mol. Neurobiol. 26, 137-152.