Neuron-to-glia signaling mediated by excitatory amino acid receptors regulates ErbB receptor function in astroglial cells of the neuroendocrine brain

Journal of Neuroscience

Volumn 23, Issue 3, 2003, Pages 915-926

  Dziedzic, Barbara ^a,b   Prevot, Vincent ^a,d   Lomniczi, Alejandro ^a   Jung, Heike ^a,c   Cornea, Anda ^a   Ojeda, Sergio R ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

^c LILLY DEUTSCHLAND GMBH   (Germany)

^d INSERM   (France)

Author keywords

Astrocytes; erbB receptors; Glutamate receptors; Growth factors; Hypothalamus; Neuron glia signaling; Sexual development

Indexed keywords

AMPA RECEPTOR; ERBB RECEPTOR; EXCITATORY AMINO ACID RECEPTOR; GONADORELIN; LIGAND; METABOTROPIC RECEPTOR; RECEPTOR SUBUNIT; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COMMUNICATION; GLIA; GLIA CELL; GONADORELIN RELEASE; HYPOTHALAMUS; NERVE CELL; NEUROENDOCRINE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PUBERTY; RAT; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 0037321380     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-03-00915.2003     Document Type: Article

References (82)

1. 2+ signal transduction. J Biol Chem 267:13361-13368.
2. Ango F, Pin JP, Tu JC, Xiao B, Worley PF, Bockaert J, Fagni L (2000) Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by Homerl proteins and neuronal excitation. J Neurosci 20:8710-8716.
3. Apostolakis EM, Garai J, Lohmann JE, Clark JH, O'Malley BW (2000) Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents. Mol Endocrinol 14:1086-1098.
4. Arenander AT, de Vellis J, Herschman HR (1989) Induction of c-fos and TIS genes in cultured rat astrocytes by neurotransmitters. J Neurosci Res 24:107-114.
5. Balázs R, Miller S, Romano C, deVries A, Chun Y, Cotman CW (1997) Metabotropic glutamate receptor mGluR5 in astrocytes: pharmacological properties and agonist regulation. J Neurochem 69:151-163.
6. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285.
7. Blankenfeld GV, Kettenmann H (1991) Glutamate and GABA receptors in vertebrate glial cells. Mol Neurobiol 5:31-43.
8. Boudin H, Doan A, Xia J, Shigemoto R, Huganir RL, Worley P, Craig AM (2000) Presynaptic clustering of mGluR7a requires the PICK1 PDZ domain binding site. Neuron 28:485-497.
9. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartley M, Deneris E, Maron C, Heinemann S (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249:1033-1037.
10. Bourguignon J-P, Gérard A, Alvarez Gonzalez ML, Purnelle G, Franchimont P (1995) The role of excitatory amino acids in triggering the onset of puberty. In: The neurobiology of puberty (Plant TM, Lee PA, eds), pp 129-138. Bristol, UK: Journal of Endocrinology.
11. Bourguignon J-P, Lebrethon MC, Gérard A, Purnelle G, Vandersmissen E, Parent AS, Yamanaka C (2000) Amino acid neurotransmission and early ontogeny of pulsatile GnRH secretion from the rat hypothalamus. In: The onset of puberty in perspective (Bourguignon J-P, Plant TM, eds), pp 119-129. Amsterdam: Elsevier.
12. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386:284-287.
13. Bruno V, Sureda FX, Storto M, Casabona G, Caruso A, Knopfel T, Kuhn R, Nicoletti F (1997) The neuroprotective activity of group II metabotropic glutamate receptors requires new protein synthesis and involves a glial-neuronal signaling. J Neurosci 17:1891-1897.
14. Claypool LE, Kasuya E, Saitoh Y, Marzban F, Terasawa E (2000) N-methyl D,L-aspartate induces the release of luteinizing hormone-releasing hormone in the prepubertal and pubertal female rhesus monkey as measured by in vivo push-pull perfusion in the stalk-median eminence. Endocrinology 141:219-228.
15. Condorelli DF, Dell'Albani P, Corsaro M, Giuffrida R, Caruso A, Trovato Salinaro A, Spinella F, Nicoletti F, Albanese V, Giuffrida Stella AM (1997) Metabotropic glutamate receptor expression in cultured rat astrocytes and human gliomas. Neurochem Res 22:1127-1133.
16. Dissen GA, Romero C, Hirshfield AN, Ojeda SR (2001) Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142:2078-2086.
17. Dong H, O'Brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL (1997) GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386:279-284.
18. Dong J, Opresko LK, Dempsey PJ, Lauffenburger DA, Coffey RJ, Wiley HS (1999) Metalloprotease-mediated ligand release regulates autocrine signaling through the epidermal growth factor receptor. Proc Natl Acad Sci USA 96:6235-6240.
19. Donoso AO, López FJ, Negro-Vilar A (1990) Glutamate receptors of the non-N-methyl-D-aspartic acid type mediate the increase in luteinizing hormone-releasing hormone release by excitatory amino acid in vitro. Endocrinology 126:414-420.
20. Dunbar AJ, Goddard C (2000) Structure-function and biological role of betacellulin. Int J Biochem Cell Biol 32:805-815.
21. Eyigor O, Jennes L (1997) Expression of glutamate receptor subunit mRNAs in gonadotropin-releasing hormone neurons during the sexual maturation of the female rat. Neuroendocrinology 66:122-129.
22. Eyigor O, Jennes L (2000) Kainate receptor subunit-positive gonadotropin-releasing hormone neurons express c-Fos during the steroid-induced luteinizing hormone surge in the female rat. Endocrinology 141:779-786.
23. Foa L, Rajah I, Haas K, Wu GY, Brakeman P, Worley P, Cline H (2001) The scaffold protein, Homer 1b/c, regulates axon pathfinding in the central nervous system in vivo. Nat Neurosci 4:499-506.
24. Gallo V, Ghiani CA (2000) Glutamate receptors in glia: new cells, new inputs, and new functions. Trends Pharmacol Sci 21:252-258.
25. Gore AC, Wu TJ, Rosenberg JI, Roberts JL (1996) Gonadotropin-releasing hormone and NMDA receptor gene expression and colocalization change during puberty in female rats. J Neurosci 16:5281-5289.
26. Grasl-Kraupp B, Schausberger E, Hufnagl K, Gerner C, Low-Baselli A, Rossmanith W, Parzelfall W, Schulte-Hermann R (2002) A novel mechanism for mitogenic signaling via pro-transforming growth factor α within hepatocyte nuclei. Hepatology 35:1372-1380.
27. Hecker KH, Roux KH (1996) High and low annealing temperatures increase both specificity and yield in touchdown and stepdown PCR. Biotechniques 20:478-485.
28. Hollmann M, O'Shea-Greenfield A, Rogers SW, Heinemann S (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342:543-648.
29. Junier M-P, Hill DF, Costa ME, Felder S, Ojeda SR (1993) Hypothalamic lesions that induce female precocious puberty activate glial expression of the epidermal growth factor receptor gene: differential regulation of alternatively spliced transcripts. J Neurosci 13:703-713.
30. Kammermeier PJ, Xiao B, Tu JC, Worley PF, Ikeda SR (2000) Homer proteins regulate coupling of group I metabotropic glutamate receptors to N-type calcium and M-type potassium channels. J Neurosci 20:7238-7245.
31. Lee H-J, Jung K-M, Huang YZ, Bennett LB, Lee JS, Mei L, Kim T-W (2002) Presenilin-dependent γ-secretase-like intramembrane cleavage of erbB-4. J Biol Chem 277:6318-6323.
32. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC (2001) Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3:802-808.
33. Ma YJ, Junier M-P, Costa ME, Ojeda SR (1992) Transforming growth factor α (TGFα) gene expression in the hypothalamus is developmentally regulated and linked to sexual maturation. Neuron 9:657-670.
34. Ma YJ, Berg-von der Emde K, Moholt-Siebert M, Hill DF, Ojeda SR (1994) Region-specific regulation of transforming growth factor α (TGFα) gene expression in astrocytes of the neuroendocrine brain. J Neurosci 14:5644-5651.
35. Ma YJ, Dissen GA, Rage F, Ojeda SR (1996) RNase protection assay. Methods 10:273-278.
36. Ma YJ, Berg-von der Emde K, Rage F, Wetsel WC, Ojeda SR (1997) Hypothalamic astrocytes respond to transforming growth factor α with secretion of neuroactive substances that stimulate the release of luteinizing hormone-releasing hormone. Endocrinology 138:19-25.
37. Ma YJ, Hill DF, Creswick KE, Costa ME, Ojeda SR (1999) Neuregulins signaling via a glial erbB-2/erbB-4 receptor complex contribute to the neuroendocrine control of mammalian sexual development. J Neurosci 19:9913-9927.
38. Martin DL (1992) Synthesis and release of neuroactive substances by glial cells. Glia 5:81-94.
39. Martin LJ, Blackstone CD, Huganir RL, Price DL (1992) Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9:259-270.
40. Martinez de la Escalera G, Choi ALH, Weiner RI (1992) Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc Natl Acad Sci USA 89:1852-1855.
41. Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S (1991) Sequence and expression of a metabotropic glutamate receptor. Nature 349:760-765.
42. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
43. McNaughton LA, Hunt SP (1992) Regulation of gene expression in astrocytes by excitatory amino acids. Mol Brain Res 16:261-266.
44. Miller S, Romano C, Cotman CW (1995) Growth factor upregulation of a phosphoinositide-coupled metabotropic glutamate receptor in cortical astrocytes. J Neurosci 15:6103-6109.
45. Min M-Y, Melyan Z, Kullmann DM (1999) Synaptically released glutamate reduces γ-aminobutyric acid (GABA)ergic inhibition in the hippocampus via kainate receptors. Proc Natl Acad Sci USA 96:9932-9937.
46. Nakahara K, Okada M, Nakanishi S (1997) The metabotropic glutamate receptor mGluR5 induces calcium oscillations in cultured astrocytes via protein kinase C phosphorylation. J Neurochem 69:1467-1475.
47. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11868-11873.
48. Nishimune A, Isaac JTR, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
49. Ojeda SR, Terasawa E (2002) Neuroendocrine regulation of puberty. In: Hormones, brain and behavior, Vol 4 (Pfaff D, Arnold A, Etgen A, Fahrbach S, Moss R, Rubin R, eds), pp 589-659. New York: Elsevier.
50. Ojeda SR, Urbanski HF (1994) Puberty in the rat. In: The physiology of reproduction, 2nd Ed, Vol 2 (Knobil E, Neill JD, eds), pp 363-409. New York: Raven.
51. Ojeda SR, Ma YJ, Lee BJ, Prevot V (2000) Glia-to-neuron signaling and the neuroendocrine control of female puberty. Recent Prog Horm Res 55:197-224.
52. Ojeda SR, Prevot V, Heger S (2001) Regulation of puberty. Curr Opin Endocrinol Diabetes 8:154-160.
53. Parpura V, Basarsky TA, Liu F, Jeftinija K, Jeftinija S, Haydon PG (1994) Glutamate-mediated astrocyte-neuron signaling. Nature 369:744-747.
54. Peavy RD, Chang MSS, Sanders-Bush E, Conn PJ (2001) Metabotropic glutamate receptor 5-induced phosphorylation of extracellular signal-regulated kinase in astrocytes depends on transactivation of the epidermal growth factor receptor. J Neurosci 21:9619-9628.
55. Peppel K, Baglioni C (1990) A simple and fast method to extract RNA from tissue culture cells. Biotechniques 9:711-713.
56. Peschon JJ, Slack JL, Reddy P, Stocking KL, Sunnarborg SW, Lee DC, Russell WE, Castner BJ, Johnson RS, Fitzner JN, Boyce RW, Nelson N, Koslosky CJ, Wolfson MF, Rauch CT, Cerretti DP, Paxton RJ, March CJ, Black RA (1998) An essential role for ectodomain shedding in mammalian development. Science 282:1281-1284.
57. Petch LA, Harris J, Raymond VW, Blasband A, Les DC, Earp HS (1990) A truncated, secreted form of the epidermal growth factor receptor is encoded by an alternatively spliced transcript in normal rat tissue. Mol Cell Biol 10:2973-2982.
58. Petralia RS, Wang W-X, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic, and glial localizations. Neuroscience 71:949-976.
59. Plant TM (1994) Puberty in primates. In: The physiology of reproduction, 2nd Ed, Vol 2 (Knobil E, Neill J, eds), pp 453-485. New York: Raven.
60. Plant TM, Gay VL, Marshall GR, Arslan M (1989) Puberty in monkeys is triggered by chemical stimulation of the hypothalamus. Proc Natl Acad Sci USA 86:2506-2510.
61. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A (1999) EGF receptor transactivation by G-protein receptors requires metalloproteinase cleavage of pro-HB-EGF. Nature 402:884-888.
62. Prevot V, Rio C, Cho GJ, Ma YJ, Heger S, Neville CM, Rosenthal NA, Ojeda SR, Corfas G (2003) Normal female sexual development requires neuregulin-erbB receptor signaling in hypothalamic astrocytes. J Neurosci 23:230-239.
63. Püschel AW, O'Connor V, Betz H (1994) The N-ethylmaleimide-sensitive fusion protein (NSF) is preferentially expressed in the nervous system. FEBS Lett 347:55-58.
64. 2 by activating a glia-to-neuron signaling pathway. J Neurosci 17:9145-9156.
65. Rio C, Buxbaum JD, Peschon JJ, Corfas G (2002) Tumor necrosis factor-α-converting enzyme is required for cleavage of erbB-4/HER4. J Biol Chem 275:10379-10387.
66. Rodriguez-Moreno A, Lerma J (1998) Kainate receptor modulation of GABA release involves a metabotropic function. Neuron 20:1211-1218.
67. Satake S, Saitow F, Yamada J, Konishi S (2000) Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 3:551-558.
68. Shirakabe K, Wakatsuki S, Kurisaki T, Fujisawa-Sehara A (2001) Roles of meltrin β/ADAM 19 in the processing of neuregulin. J Biol Chem 276:9352-9358.
69. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21:393-400.
70. Staudinger J, Zhou J, Burgess R, Elledge SJ, Olson EN (1995) PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J Cell Biol 128:263-271.
71. Tanabe Y, Masu M, Ishii T, Shigemoto R, Nakanishi S (1992) A family of metabotropic glutamate receptors. Neuron 8:169-179.
72. Terasawa E (1999) Hypothalamic control of the onset of puberty. Curr Opin Endocrinol Diabetes 6:44-49.
73. Testa CM, Standaert DG, Young AB, Penny Jr JB (1994) Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J Neurosci 14:3005-3018.
74. Thind KK, Goldsmith PC (1995) Glutamate and GABAergic neurointeractions in the monkey hypothalamus: a quantitative immunomorphological study. Neuroendocrinology 61:471-485.
75. 3 receptors. Neuron 21:717-726.
76. Urbanski HF, Ojeda SR (1987) Activation of luteinizing hormone-releasing hormone release advances the onset of female puberty. Neuroendocrinology 46:273-276.
77. Urbanski HF, Ojeda SR (1990) A role for N-methyl-D-aspartate (NMDA) receptors in the control of LH secretion and initiation of female puberty. Endocrinology 126:1774-1776.
78. van den Pol AN, Trombley PQ (1993) Glutamate neurons in hypothalamus regulate excitatory transmission. J Neurosci 13:2829-2836.
79. van den Pol AN, Romano C, Ghosh P (1995) Metabotropic glutamate receptor mGluR5 subcellular distribution and developmental expression in hypothalamus. J Comp Neurol 362:134-150.
80. Xia J, Zhang X, Staudinger J, Huganir RL (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22:179-187.
81. Xiao B, Tu JC, Petralia RS, Yuan JP, Doan A, Breder CD, Ruggiero A, Lanahan AA, Wenthold RJ, Worley PF (1998) Homer regulates the association of group 1 metabotropic glutamate receptors with multivalent complexes of Homer-related, synaptic proteins. Neuron 21:707-716.
82. Zhou W, Carpenter G (2000) Heregulin-dependent trafficking and cleavage of erbB-4. J Biol Chem 275:34737-34743.