Transforming growth factor alpha attenuates the functional expression of AMPA receptors in cortical GABAergic neurons

Molecular and Cellular Neuroscience

Volumn 31, Issue 4, 2006, Pages 628-641

  Namba, Hisaaki ^a   Nagano, Tadasato ^a   Iwakura, Yuriko ^a   Xiong, Huabao ^a,b   Jourdi, Hussam ^a,c   Takei, Nobuyuki ^a   Nawa, Hiroyuki ^a  

^a NIIGATA UNIVERSITY   (Japan)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

BDNF; EGF; ErbB1; GABA; GluR1; Her1; Neocortex

Indexed keywords

4 (3 BROMOANILINO) 6,7 DIMETHOXYQUINAZOLINE; 4 AMINOBUTYRIC ACID RECEPTOR; AMPA RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUTAMATE RECEPTOR 1; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; MESSENGER RNA; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; DRUG INHIBITION; EMBRYO; IMMUNOHISTOCHEMISTRY; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; UPREGULATION;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA, SERUM-FREE; ELECTROPHYSIOLOGY; ENZYME INHIBITORS; EPIDERMAL GROWTH FACTOR; GAMMA-AMINOBUTYRIC ACID; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; NEURONS; PROTEIN SUBUNITS; QUINAZOLINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, AMPA; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMALIA;

EID: 33645374580     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2005.12.002     Document Type: Article

References (73)

1. S. Assimacopoulos, E.A. Grove, and C.W. Ragsdale Identification of a Pax6-dependent epidermal growth factor family signaling source at the lateral edge of the embryonic cerebral cortex J. Neurosci. 23 2003 6399 6403
2. M.M. Bolton, A.J. Pittman, and D.C. Lo Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures J. Neurosci. 20 2000 3221 3232
3. M. Bos, J. Mendelsohn, Y.M. Kim, J. Albanell, D.W. Fry, and J. Baselga PD153035, a tyrosine kinase inhibitor, prevents epidermal growth factor receptor activation and inhibits growth of cancer cells in a receptor number-dependent manner Clin. Cancer Res. 3 1997 2099 2106
4. J.M. Conner, J.C. Lauterborn, Q. Yan, C.M. Gall, and S. Varon Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport J. Neurosci. 17 1997 2295 2313
5. S.D. Croll, S.J. Wiegand, K.D. Anderson, R.M. Lindsay, and H. Nawa Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF Eur. J. Neurosci. 6 1994 1343 1353
6. A.D. de Lima, and T. Voigt Identification of two distinct populations of gamma-aminobutyric acidergic neurons in cultures of the rat cerebral cortex J. Comp. Neurol. 388 1997 526 540
7. K.L. Eagleson, R.T. Ferri, and P. Levitt Complementary distribution of collagen type IV and the epidermal growth factor receptor in the rat embryonic telencephalon Cereb. Cortex 6 1996 540 549
8. I.J. Fox, and H.I. Kornblum Developmental profile of ErbB receptors in murine central nervous system: implications for functional interactions J. Neurosci. Res. 79 2005 584 597
9. F. Gómez-Pinilla, D.J. Knauer, and M. Nieto-Sampedro Epidermal growth factor receptor immunoreactivity in rat brain. Development and cellular localization Brain Res. 438 1988 385 390
10. J.A. Gorski, S.R. Zeiler, S. Tamowski, and K.R. Jones Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites J. Neurosci. 23 2003 6856 6865
11. R.A. Hall, M. Kessler, and G. Lynch Evidence that high- and low-affinity dl-alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid (AMPA) binding sites reflect membrane-dependent states of a single receptor J. Neurochem. 59 1992 1997 2004
12. M. Hanke, L.M. Farkas, M. Jakob, R. Ries, J. Pohl, and A.M. Sullivan Heparin-binding epidermal growth factor-like growth factor: a component in chromaffin granules which promotes the survival of nigrostriatal dopaminergic neurones in vitro and in vivo Neuroscience 124 2004 757 766
13. R.C. Harris, E. Chung, and R.J. Coffey EGF receptor ligands Exp. Cell Res. 284 2003 2 13
14. Z.J. Huang, A. Kirkwood, T. Pizzorusso, V. Porciatti, B. Morales, M.F. Bear, L. Maffei, and S. Tonegawa BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex Cell 98 1999 739 755
15. M. Iino, K. Goto, W. Kakegawa, H. Okado, M. Sudo, S. Ishiuchi, A. Miwa, Y. Takayasu, I. Saito, K. Tsuzuki, and S. Ozawa Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia Science 292 2001 926 929
16. N.Y. Ip, Y. Li, G.D. Yancopoulos, and R.M. Lindsay Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF J. Neurosci. 13 1993 3394 3405
17. X. Jin, H. Hu, P.H. Mathers, and A. Agmon Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures J. Neurosci. 23 2003 5662 5673
18. K.R. Jones, I. Farinas, C. Backus, and L.F. Reichardt Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development Cell 76 1994 989 999
19. H. Jourdi, and H. Nawa Basic fibroblast growth factor modulates the expression of PDZ domain-containing proteins in cultured cortical neurons Acta Med. Biol. 50 2002 107 115
20. H. Jourdi, Y. Iwakura, M. Narisawa-Saito, K. Ibaraki, H. Xiong, M. Watanabe, Y. Hayashi, N. Takei, and H. Nawa Brain-derived neurotrophic factor signal enhances and maintains the expression of AMPA receptor-associated PDZ proteins in developing cortical neurons Dev. Biol. 263 2003 216 230
21. W. Kamphuis, F. Dijk, and B.J. O'Brien Gene expression of AMPA-type glutamate receptor subunits in rod-type ON bipolar cells of rat retina Eur. J. Neurosci. 18 2003 1085 1092
22. N. Kawahara, K. Mishima, S. Higashiyama, N. Taniguchi, A. Tamura, and T. Kirino The gene for heparin-binding epidermal growth factor-like growth factor is stress-inducible: its role in cerebral ischemia J. Cereb. Blood Flow Metab. 19 1999 307 320
23. V.N. Kharazia, R.J. Wenthold, and R.J. Weinberg GluR1-immunopositive interneurons in rat neocortex J. Comp. Neurol. 368 1996 399 412
24. 2+-binding proteins in rat forebrain neurons Eur. J. Neurosci. 12 2000 2812 2822
25. H.I. Kornblum, H.T. Chugani, K. Tatsukawa, and C.M. Gall Cerebral hemidecortication alters expression of transforming growth factor alpha mRNA in the neostriatum of developing rats Mol. Brain Res. 21 1994 107 114
26. H.I. Kornblum, C.M. Gall, K.B. Seroogy, and J.C. Lauterborn A subpopulation of striatal GABAergic neurons expresses the epidermal growth factor receptor Neuroscience 69 1995 1025 1029
27. H.I. Kornblum, R.J. Hussain, J.M. Bronstein, C.M. Gall, D.C. Lee, and K.B. Seroogy Prenatal ontogeny of the epidermal growth factor receptor and its ligand, transforming growth factor alpha, in the rat brain J. Comp. Neurol. 380 1997 243 261
28. H.I. Kornblum, R. Hussain, J. Wiesen, P. Miettinen, S.D. Zurcher, K. Chow, R. Derynck, and Z. Werb Abnormal astrocyte development and neuronal death in mice lacking the epidermal growth factor receptor J. Neurosci. Res. 53 1998 697 717
29. H.I. Kornblum, S.D. Zurcher, Z. Werb, R. Derynck, and K.B. Seroogy Multiple trophic actions of heparin-binding epidermal growth factor (HB-EGF) in the central nervous system Eur. J. Neurosci. 11 1999 3236 3246
30. D.J. Leahy Structure and function of the epidermal growth factor (EGF/ErbB) family of receptors Adv. Protein Chem. 68 2004 1 27
31. K. Maiese, I. Boniece, D. DeMeo, and J.A. Wagner Peptide growth factors protect against ischemia in culture by preventing nitric oxide toxicity J. Neurosci. 13 1993 3034 3040
32. S. Marty, P. Carroll, A. Cellerino, E. Castren, V. Staiger, H. Thoenen, and D. Lindholm Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidal neurons, including Cajal-Retzius cells, in organotypic slice cultures J. Neurosci. 16 1996 675 687
33. S. Matsuda, S. Mikawa, and H. Hirai Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein J. Neurochem. 73 1999 1765 1768
34. A.K. McAllister Neurotrophins and cortical development Results Probl. Cell Differ. 39 2002 89 112
35. A.K. McAllister, D.C. Lo, and L.C. Katz Neurotrophins regulate dendritic growth in developing visual cortex Neuron 15 1995 791 803
36. M. McLean Bolton, A.J. Pittman, and D.C. Lo Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures J. Neurosci. 20 2000 3221 3232
37. K. Mizuno, J. Carnahan, and H. Nawa Brain-derived neurotrophic factor promotes differentiation of striatal GABAergic neurons Dev. Biol. 165 1994 243 256
38. T. Nagano, Y. Yanagawa, K. Obata, M. Narisawa-Saito, H. Namba, Y. Otsu, N. Takei, and H. Nawa Brain-derived neurotrophic factor upregulates and maintains AMPA receptor currents in neocortical GABAergic neurons Mol. Cell. Neurosci. 24 2003 340 356
39. H. Namba, H. Xiong, T. Futamura, Y. Otsu, N. Takei, and H. Nawa Factors in EGF family reduce spontaneous synaptic activities in developing rat neocortex by downregulating glutamate receptor expressions Abstr.-Soc. Neurosci. 26 2000 223.15
40. H. Namba, N. Takei, and H. Nawa Transforming growth factor α changes firing properties of developing neocortical GABAergic neurons by down-regulation of voltage-gated potassium currents Neuroscience 122 2003 637 646
41. M. Narisawa-Saito, J. Carnahan, K. Araki, T. Yamaguchi, and H. Nawa Brain-derived neurotrophic factor regulates the expression of AMPA receptor proteins in neocortical neurons Neuroscience 88 1999 1009 1014
42. M. Narisawa-Saito, A.J. Silva, T. Yamaguchi, T. Hayashi, T. Yamamoto, and H. Nawa Growth factor-mediated Fyn signaling regulates α-amino-3-hydroxy- 5-methyl-4-isoxazolepropionic acid (AMPA) receptor expression in rodent neocortical neurons Proc. Natl. Acad. Sci. U. S. A. 96 1999 2461 2466
43. M. Narisawa-Saito, Y. Iwakura, M. Kawamura, K. Araki, S. Kozaki, N. Takei, and H. Nawa Brain-derived neurotrophic factor regulates surface expression of alpha-amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid receptors by enhancing the N-ethylmaleimide-sensitive factor/GluR2 interaction in developing neocortical neurons J. Biol. Chem. 277 2002 40901 40910
44. H. Nawa, Y. Bessho, J. Carnahan, S. Nakanishi, and K. Mizuno Regulation of neuropeptide expression in cultured cerebral cortical neurons by brain-derived neurotrophic factor J. Neurochem. 60 1993 772 775
45. L.A. Opanashuk, R.J. Mark, J. Porter, D. Damm, M.P. Mattson, and K.B. Seroogy Heparin-binding epidermal growth factor-like growth factor in hippocampus: modulation of expression by seizures and anti-excitotoxic action J. Neurosci. 19 1999 133 146
46. M. Ozaki, M. Sasner, R. Yano, H.S. Lu, and A. Buonanno Neuregulin-beta induces expression of an NMDA-receptor subunit Nature 390 1997 691 694
47. H. Peng, T.C. Wen, J. Tanaka, N. Maeda, S. Matsuda, J. Desaki, S. Sudo, B. Zhang, and M. Sakanaka Epidermal growth factor protects neuronal cells in vivo and in vitro against transient forebrain ischemia- and free radical-induced injuries J. Cereb. Blood Flow. Metab. 18 1998 349 360
48. V. Petegnief, B. Friguls, C. Sanfeliu, C. Sunol, and A.M. Planas Transforming growth factor-alpha attenuates N-methyl-d-aspartic acid toxicity in cortical cultures by preventing protein synthesis inhibition through an Erk1/2-dependent mechanism J. Biol. Chem. 278 2003 29552 29559
49. J.T. Porter, B. Cauli, J.F. Staiger, B. Lambolez, J. Rossier, and E. Audinat Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex Eur. J. Neurosci. 10 1998 3617 3628
50. A.G. Rabchevsky, J.M. Weinitz, M. Coulpier, C. Fages, M. Tinel, and M.P. Junier A role for transforming growth factor alpha as an inducer of astrogliosis J. Neurosci. 18 1998 10541 10552
51. S. Reibel, B. Vivien-Roels, B.T. Le, Y. Larmet, J. Carnahan, C. Marescaux, and A. Depaulis Overexpression of neuropeptide Y induced by brain-derived neurotrophic factor in the rat hippocampus is long lasting Eur. J. Neurosci. 12 2000 595 605
52. B.A. Reynolds, and S. Weiss Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system Science 255 1992 1707 1710
53. B.A. Reynolds, and S. Weiss Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell Dev. Biol. 175 1996 1 13
54. S. Rozen, and H. Skaletsky Primer3 on the WWW for general users and for biologist programmers Methods Mol. Biol. 132 2000 365 386
55. L.C. Rutherford, S.B. Nelson, and G.G. Turrigiano BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses Neuron 21 1998 521 530
56. G. Seifert, and C. Steinhauser Ionotropic glutamate receptors in astrocytes Prog. Brain Res. 132 2001 287 299
57. K.B. Seroogy, K.H. Lundgren, D.C. Lee, K.M. Guthrie, and C.M. Gall Cellular localization of transforming growth factor-alpha mRNA in rat forebrain J. Neurochem. 60 1993 1777 1782
58. N.T. Sherwood, and D.C. Lo Long-term enhancement of central synaptic transmission by chronic brain-derived neurotrophic factor treatment J. Neurosci. 19 1999 7025 7036
59. M. Sibilia, J.P. Steinbach, L. Stingl, A. Aguzzi, and E.F. Wagner A strain-independent postnatal neurodegeneration in mice lacking the EGF receptor EMBO J. 17 1998 719 731
60. S. Standley, N. Irvin, and M. Baudry Differential subcellular localization of two populations of glutamate/AMPA receptors in the rat telencephalon Neurochem. Int. 25 1994 287 293
61. 3H]AMPA) binding sites represent immature and mature forms of AMPA receptors and are composed of differentially glycosylated subunits J. Neurochem. 70 1998 2434 2445
62. E. Suzuki, M. Kessler, and A.C. Arai C-terminal truncation affects kinetic properties of GluR1 receptors Mol. Cell. Neurosci. 29 2005 1 10
63. N. Takei, K. Sasaoka, K. Inoue, M. Takahashi, Y. Endo, and H. Hatanaka Brain-derived neurotrophic factor increases the stimulation-evoked release of glutamate and the levels of exocytosis-associated proteins in cultured cortical neurons from embryonic rats J. Neurochem. 68 1997 370 375
64. D.W. Threadgill, A.A. Dlugosz, L.A. Hansen, T. Tennenbaum, U. Lichti, D. Yee, C. LaMantia, T. Mourton, K. Herrup, R.C. Harris, J.A. Barnard, S.H. Yuspa, R.J. Coffey, and T. Magnuson Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype Science 269 1995 230 234
65. C. Vicario-Abejon, D. Owens, R. McKay, and M. Segal Role of neurotrophins in central synapse formation and stabilization Nat. Rev., Neurosci. 3 2002 965 974
66. H.R. Widmer, and F. Hefti Stimulation of GABAergic neuron differentiation by NT-4/5 in cultures of rat cerebral cortex Dev. Brain Res. 80 1994 279 284
67. M.J. Wirth, A. Brun, J. Grabert, S. Patz, and P. Wahle Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5 Development 130 2003 5827 5838
68. C.J. Xian, and X.F. Zhou EGF family of growth factors: essential roles and functional redundancy in the nerve system Front. Biosci. 9 2004 85 92
69. H. Xiong, M. Narisawa-Saito, H. Jourdi, and H. Nawa The glutamate receptor-mediated regulation of brain-derived neurotrophic factor production by cytokines in central nervous system Abstr.-Soc. Neurosci. 25 1999 407.10
70. M. Yamada, T. Ikeuchi, and H. Hatanaka The neurotrophic action and signalling of epidermal growth factor Prog. Neurobiol. 51 1997 19 37
71. H.J. Yau, H.F. Wang, C. Lai, and F.C. Liu Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences Cereb. Cortex 13 2003 252 264
72. H. Yin, D. Turetsky, D.W. Choi, and J.H. Weiss Cortical neurones with Ca2+ permeable AMPA/kainate channels display distinct receptor immunoreactivity and are GABAergic Neurobiol. Dis. 1 1994 43 49
73. D. Yokomaku, H. Jourdi, A. Kakita, T. Nagano, H. Takahashi, N. Takei, and H. Nawa ErbB1 receptor ligands attenuate the expression of synaptic scaffolding proteins, GRIP1 and SAP97, in developing neocortex Neuroscience 136 2005 1037 1047