The excitoprotective effect of N-methyl-D-aspartate receptors is mediated by a brain-derived neurotrophic factor autocrine loop in cultured hippocampal neurons

Journal of Neurochemistry

Volumn 94, Issue 3, 2005, Pages 713-722

  Jiang, Xueying ^a   Tian, Feng ^b   Mearow, Karen ^c   Okagaki, Peter ^a   Lipsky, Robert H ^b   Marini, Ann M ^a,d  

^a Uniformed Services University of the Health Sciences   (United States)

^b NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^c MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^d UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Autocrine loop; Brain derived neurotrophic factor; Excitotoxicity; Hippocampal neurons; N methyl D aspartate; Neuroprotection

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; HIPPOCAMPUS; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; AGE FACTORS; ANIMALS; ANTIBODIES; AUTOCRINE COMMUNICATION; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; CELLS, CULTURED; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EMBRYO; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; HIPPOCAMPUS; N-METHYLASPARTATE; NEURONS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB; RECEPTORS, N-METHYL-D-ASPARTATE; TIME FACTORS; TYROSINE;

EID: 23244458906     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03200.x     Document Type: Article

References (71)

1. Balazs R., Hack N. and Jorgensen O. S. (1988) Stimulation of the N-methyl-D-aspartate receptor has a trophic effect on differentiating cerebellar granule cells. Neurosci. Lett. 87, 80-86.
2. Bambrick L. L., Yarowsky P. J. and Krueger B. K. (1995) Glutamate as a hippocampal neuron survival factor: an inherited defect in the trisomy 16 mouse. Proc. Natl Acad. Sci. USA 92, 9692-9696.
3. Behar T. N., Scott C. A., Greene C. L., Wen X., Smith S. V., Marie D., Liu Q.-L., Colton C. A. and Barker J. L. (1999) Glutamate acting at NMDA receptor stimulates embryonic cortical neuronal migration. J. Neurosci. 19, 4449-4461.
4. Bhattacharyya A., Watson F. L., Bradlee T. A., Pomeroy S. L., Stiles C. D. and Segal R. A. (1997) Trk receptors function as rapid retrograde signal carriers in the adult nervous system. J. Neurosci. 17, 7007-7016.
5. Black I. B. (1999) Trophic regulation of synaptic plasticity. J. Neurobiol. 41, 108-118.
6. Bliss T. V. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Boeck C. R., Ganzella M., Lottermann A. and Vendite D. (2004) NMDA preconditioning protects against seizures and hippocampal neurotoxicity induced by quinolinic acid in mice. Epilepsia 45, 745-750.
8. Bothwell M. (1995) Functional interactions of neurotrophins and neurotrophin receptors. Ann. Rev. Neurosci. 18, 223-253.
9. Cabelli R. J., Shelton D. L., Segal R. A. and Shatz C. J. (1997) Blockade of endogenous ligands of trkB inhibits formation of ocular dominance columns. Neuron 19, 63-76.
10. Chazot P. L., Coleman S. K., Cik M. and Stephenson F. A. (1994) Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the co-existence of three subunits types within a discrete receptor molecule. J. Biol. Chem. 269, 24403-24409.
11. Cheng B., Furukawa K., O'Keefe J. A., Goodman Y., Kihiko M., Fabian T. and Mattson M. P. (1995) Basic fibroblast growth factor selectively increases AMPA-receptor subunit GluR1 protein level and differentially modulates Ca2+ responses to AMPA and NMDA in hippocampal neurons. J. Neurochem. 65, 2525-2536.
12. Choi D. W. (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623-634.
13. Culmsee C., Gerling N., Lehmann M., Nikolova-Karakashian M., Prehn J. H., Mattson M. P. and Krieglstein J. (2002) Nerve growth factor survival signaling in cultured hippocampal neurons is mediated through TrkA and requires the common neurotrophin receptor P75. Neuroscience 115, 1089-1108.
14. Dingledine R., Broges K., Bowie D. and Traynelis S. F. (1999) The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
15. Duan W., Guo Z. and Mattson M. P. (2001) Brain-derived neurotrophic factor mediates an excitoprotective effect of dietary restriction in mice. J. Neurochem. 76, 619-626.
16. Escandon E., Soppet D., Rosenthal A., Mendoza-Ramirez J. L., Szonyi E., Burton L. E., Henderson C. E., Parada L. F. and Nikolics K. (1994) Regulation of neurotrophin receptor expression during embryonic and postnatal development. J. Neurosci. 14, 2054-2068.
17. Gahring L. C., Meyer E. L. and Rogers S. W. (2003) Nicotine-induced neuroprotection against N-methyl-D-aspartic acid or β-amyloid peptide occurs through independent mechanisms distinguished by pro-inflammatory cytokines. J. Neurochem. 87, 1125-1136.
18. Ghosh A. and Greenberg M. E. (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268, 239-247.
19. 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.
20. Greene L. A. and Kaplan D. R. (1995) Early events in neurotrophin signalling via Trk and p75 receptors. Curr. Opin. Neurobiol. 5, 579-587.
21. Gwag B. J. and Springer J. E. (1993) Activation of NMDA receptors increases brain-derived neurotrophic factor (BDNF) mRNA expression in the hippocampal formation. Neuroreport 5, 125-128.
22. Hallbook F., Ibanez C. F. and Persson H. (1991) Evolutionary studies of the nerve growth factor family reveal a novel member abundantly expressed in Xenopus ovary. Neuron 6, 845-858.
23. 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.
24. Hohn A., Leibrock J., Bailey K. and Barde Y. A. (1990) Identification and characterization of a novel member of the nerve growth factor/brain-derived neurotrophic factor family. Nature 344, 339-341.
25. Hughes P., Beilharz E., Gluckman P. and Dragunow M. (1993) Brain-derived neurotrophic factor is induced as an immediate early gene following N-methyl-D-aspartate receptor activation. Neuroscience 57, 319-328.
26. 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.
27. Ikonomidou C., Steforvska V. and Turski L. (2000) Neuronal death enhanced by N-methyl-D-aspartate antagonists. Proc. Natl Acad. Sci. USA 97, 12 885-12 890.
28. Ip N. Y., Li Y., Yancopoulos G. D. and Lindsay R. M. (1993) Cultured hippocampal neurons show response to BDNF, NT-3, and NT-4 but not NGF. J. Neurosci. 13, 3394-3405.
29. Jiang X., Zhu D., Okagaki P., Lipsky R., Wu X., Banaudha K., Mearow K. and Marini A. M. (2003) N-methyl-D-aspartate and TrkB receptor activation in cerebellar granule cells: An in vitro model of preconditioning to stimulate intrinsic survival pathways in neurons. Ann. NY Acad. Sci. 993, 134-145.
30. Jiang X., Xu K., Hoberman J., Tian F., Marko A., Waheed J., Harris C., Marini A. M., Enoch M.-A. and Lipsky R. H. (2005) BDNF variation and mood disorders: a novel functional promoter polymorphism and Val66Met are associated with anxiety but have opposing effects. Neuropsychopharmacology (in press).
31. Jones K. R. and Reichardt L. F. (1990) Molecular cloning of a human gene that is a member of the nerve growth factor family. Proc. Natl Acad. Sci. USA 87, 8060-8064.
32. Kaplan D. R., Hempstead B. L., Martin-Zanca D., Chao M. V. and Parada L. F. (1991a) The trk proto-oncogene product: a signal transducing receptor for nerve growth factor. Science 252, 554-558.
33. Kaplan D. R., Martin-Zanca D. and Parada L. F. (1991b) Tyrosine phosphorylation and tyrosine kinase activity of the trk proto-oncogene product induced by NGF. Nature 350, 158-160.
34. Katz L. C. and Shatz C. J. (1996) Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138.
35. Klein R., Nanduri V., Jing S. A., Lamballe F., Tapley P., Bryant S., Cordon-Cardo C., Jones K. R., Reichardt L. F. and Barbacid M. (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66, 395-403.
36. Korhonen L., Napankangas U., Steen H., Chen Y., Martinez R. and Lindholm D. (2004) Differential regulation of X-chromosome-linked inhibitor of apoptosis protein (X1AP) and caspase-3 by NMDA in developing hippocampal neurons; involvement of the mitochondrial pathway in NMDA-mediated neuronal survival. Exp. Cell Res. 295, 290-299.
37. Lamballe F., Klein R. and Barbacid M. (1991) trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 66, 967-979.
38. Laube B., Kuhse J. and Betz H. (1998) Evidence for a tetrameric structure of recombinant NMDA receptors. J. Neurosci. 18, 2954-2961.
39. Lee F. S., Rajagopal R., Kim A. H., Chang P. C. and Chao M. V. (2002) Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J. Biol. Chem. 277, 9096-9102.
40. Levi-Montalcini R. (1987) The nerve growth factor 35 years later. Science 237, 1154-1162.
41. Lin S. Y., Wu K., Levine E. S., Mount H. T., Suen P. C. and Black I. B. (1998) BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20-27.
42. Lindholm D. (1994) Role of neurotrophins in preventing glutamate induced neuronal cell death. J. Neurol. 242, S16-S18.
43. Lipsky R. H. and Goldman D. (2003) Genomics and variation of ionotropic glutamate receptors. Ann. NY Acad. Sci. 1003, 22-35.
44. Lipsky R. H., Xu K., Zhu D., Kelly C., Terhakopian A., Novelli A. and Marini A. M. (2001) NF-κB is a critical determinant for NMDA receptor-mediated neuroprotection. J. Neurochem. 78, 254-264.
45. Maisonpierre P. C., Belluscio L., Squinto S., Ip N. Y., Furth M. E., Lindsay R. M. and Yancopoulos G. D. (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247, 1446-1451.
46. Marini A. M. and Novelli A. (1991) The glutamate uptake blocker DL-threo-3-hydroxyaspartate reduces NMDA receptor activation by glutamate in cultured neurons. Eur. J. Pharm. 194, 131-132.
47. Marini A. M. and Paul S. M. (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.
48. Marini A. M., Rabin S. I., 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.
49. Marini A. M., Ueda Y. and June C. H. (1999) Intracellular survival pathways against glutamate receptor agonist excitotoxicity in cultured neurons: intracellular calcium responses. Ann. NY Acad. Sci. 890, 421-437.
50. Marini A. M., Jiang X., Wu X., Tian F., Zhu D., Okagaki P. and Lipsky R. H. (2004) Brain-derived neurotrophic factor and NF-κB: from genomics to molecular biology to phenotype. Restorative Neurol. Neurosci. 22, 121-130.
51. Mattson M. P. (2003) Excitotoxic and excitoprotective mechanisms. Neuromolecular Med. 3, 65-94.
52. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activites in hippocampal neurons. J. Neurochem. 65, 1740-1751.
53. Mayer M. L., Westbrook G. L. and Guthrie P. B. (1984) Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309, 261-263.
54. Monyer H., Burnashev N., Laurie D. J., Sakmann B. and Seeburg P. H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
55. Ogita K., Okuda H., Yamamoto Y., Nishiyama N. and Yoneda Y. (2003) In vivo neuroprotective role of NMDA receptors against kainate-induced excitotoxicity in murine hippocampal pyramidal neurons. J. Neurochem. 85, 1336-1346.
56. Reiprich P., Kilb W. and Luhmann H. J. (2004) Neonatal NMDA receptor blockade disturbs neuronal migration in rat somatosensory cortex in vivo. Cereb Cortex e-publication.
57. Ritter L. M., Vazquez D. M. and Meador-Woodruff J. H. (2002) Ontogeny of inotropic glutamate receptor subunit expression in the rat hippocampus. Dev. Brain Res. 139, 227-236.
58. Rodriguez-Tebar A., Dechant G. and Barde Y. A. (1990) Binding of brain-derived neurotrophic factor to the nerve growth factor receptor. Neuron 4, 487-492.
59. Rosenthal A., Goeddel D. V., Nguyen T., Lewis M., Shih A., Laramee G. R., Nikolics K. and Winslow J. W. (1990) Primary structure and biological activity of a novel human neurotrophic factor. Neuron 4, 767-773.
60. Rossler O. G., Giehl K. M. and Thiel G. (2004) Neuroprotection of immortalized hippocampal neurones by brain-derived neurotrophic factor and Raf-1 protein kinase: role of extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase. J. Neurochem. 88, 1240-1252.
61. Saarelainen T., Vaittinen S. and Castren E. (2001) trkB-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell Mol. Neurobiol. 21, 429-435.
62. Schwartz P. M., Borghesani P. R., Levy R. L., Pomeroy S. L. and Segal R. A. (1997) Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning. Neuron 19, 269-281.
63. Segal R. A., Pomeroy S. L. and Stiles C. D. (1995) Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J. Neurosci. 15, 4970-4981.
64. Suen P. C., Wu K., Levine E. S., Mount H. T., Xu J. L., Lin S. Y. and Black I. B. (1997) Brain-derived neurotrophic factor rapidly enhances phosphorylation of the postsynaptic N-methyl-D-aspartate receptor subunit 1. Proc. Natl Acad. Sci. USA 94, 8191-8195.
65. Takai H., Katayama K.-I., Uetsuka K., Nakayama H. and Doi K. (2002) Distribution of N-methyl-D-aspartate receptors in the developing rat brain. Exp. Mol. Pathol. 75, 89-94.
66. Thoenen H. (1991) The changing scene of neurotrophic factors. Trends Neurosci. 14, 165-170.
67. Timmusk T., Palm K., Metsis M., Reintam T., Paalme V., Saarma M. and Persson H. (1993) Multiple promoters direct tissue-specific expression of the rat BDNF gene. Neuron 10, 475-489.
68. Turski L. and Olney J. W. (1999) Blockade of NMDA receptors and apoptotic neurodegeneration in the developing brain. Science 283, 70-74.
69. Wu X., Zhu D., Jiang X., Okagaki P., Mearow K., Zhu G., McCall S., Banaudha K., Lipsky R. H. and Marini A. M. (2004) AMPA protects cultured neurons against glutamate excitotoxicity through a phosphatidylinositol 3-kinase-dependent activation in extracellular signal-regulated kinase to upregulate BDNF gene expression. J. Neurochem. 90, 807-818.
70. Yen L.-H., Sibley J. R. and Constantine-Paton M. (1993) Fine-structural alterations and clustering of developing synapses after chronic treatments with low levels of NMDA. J. Neurosci. 13, 4949-4960.
71. Zafra F., Castren E., Thoenen H. and Lindholm D. (1991) Interplay between glutamate and γ-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc. Natl Acad. Sci. USA 88, 10 037-10 041.