The neurotransmitter glutamate reduces axonal responsiveness to multiple repellents through the activation of metabotropic glutamate receptor 1

Journal of Neuroscience

Volumn 24, Issue 32, 2004, Pages 7085-7095

  Kreibich, Thomas A ^a   Chalasani, Sreekanth H ^a,b   Raper, Jonathan A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Axon guidance; CAMP; Growth cone; Metabotropic glutamate receptor; Neurotrophic; Semaphorin 3A; Semaphorin 3C; Slit 2; Survival

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMIC ACID; METABOTROPIC RECEPTOR 1; NEUROTRANSMITTER; PERTUSSIS TOXIN; RHO FACTOR; SEMAPHORIN 3A; SEMAPHORIN 3C; SLIT PROTEIN; SLIT2 PROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM; EMBRYO; ENZYME ACTIVATION; GROWTH CONE; IN VITRO STUDY; MORPHOLOGY; MOUSE; NERVE CONDUCTION; NERVE FIBER; NERVE FIBER GROWTH; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; AXONS; CELL SURVIVAL; CELLS, CULTURED; CHICK EMBRYO; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EMBRYO; GANGLIA, SPINAL; GLUTAMIC ACID; GROWTH CONES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; METHOXYHYDROXYPHENYLGLYCOL; MICE; NERVE TISSUE PROTEINS; PROTEIN TRANSPORT; RECEPTORS, CXCR4; RECEPTORS, METABOTROPIC GLUTAMATE; RETINAL GANGLION CELLS; RHO GTP-BINDING PROTEINS; SEMAPHORIN-3A; SEMAPHORINS;

EID: 4143124548     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0349-04.2004     Document Type: Article

References (101)

1. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, Tonegawa S (1994a) Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell 79:365-375.
2. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994b) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79:377-388.
3. Akiyama M, Minami Y, Nakajima T, Moriya T, Shibata S (2001) Calcium and pituitary adenylate cyclase-activating polypeptide induced expression of circadian clock gene mPer1 in the mouse cerebellar granule cell culture. J Neurochem 78:499-508.
4. Aktories K, Mohr C, Koch G (1992) Clostridium botulinum C3 ADP-ribosyltransferase. Curr Top Microbiol Immunol 175:115-131.
5. Aramori I, Nakanishi S (1992) Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8:757-765.
6. Bagchi IC, Huang QH, Means AR (1992) Identification of amino acids essential for calmodulin binding and activation of smooth muscle myosin light chain kinase. J Biol Chem 267:3024-3029.
7. Barbas D, DesGroseillers L, Castellucci VF, Carew TJ, Marinesco S (2003) Multiple serotonergic mechanisms contributing to sensitization in aplysia: evidence of diverse serotonin receptor subtypes. Learn Mem 10:373-386.
8. Bashaw GJ (2004) Semaphorin signaling unplugged; a nervy AKAP cAMP(s) out on plexin. Neuron 42:363-366.
9. Bishop AL, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348:241-255.
10. Blaabjerg M, Fang L, Zimmer J, Baskys A (2003) Neuroprotection against NMDA excitotoxicity by group I metabotropic glutamate receptors is associated with reduction of NMDA stimulated currents. Exp Neurol 183:573-580.
11. Castillo PE, Janz R, Sudhof TC, Tzounopoulos T, Malenka RC, Nicoll RA (1997) Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 388:590-593.
12. Catania MV, Bellomo M, Di Giorgi-Gerevini V, Seminara G, Giuffrida R, Romeo R, De Blasi A, Nicoletti F (2001) Endogenous activation of group-I metabotropic glutamate receptors is required for differentiation and survival of cerebellar Purkinje cells. J Neurosci 21:7664-7673.
13. Cepko CL, Austin CP, Yang X, Alexiades M, Ezzeddine D (1996) Cell fate determination in the vertebrate retina. Proc Natl Acad Sci USA 93:589-595.
14. Chalasani SH, Sabelko KA, Sunshine MJ, Littman DR, Raper JA (2003a) A chemokine, SDF-1, reduces the effectiveness of multiple axonal repellents and is required for normal axon pathfinding. J Neurosci 23:1360-1371.
15. Chalasani SH, Baribaud F, Coughlan CM, Sunshine MJ, Lee VM, Doms RW, Littman DR, Raper JA (2003b) The chemokine stromal cell-derived factor-1 promotes the survival of embryonic retinal ganglion cells. J Neurosci 23:4601-4612.
16. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG (1995) Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82:371-381.
17. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3:339-345.
18. Conn PJ, Pin JP (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37:205-237.
19. Constantine-Paton M, Cline HT, Debski E (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13:129-154.
20. Dong JM, Leung T, Manser E, Lim L (1998) cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha. J Biol Chem 273:22554-22562.
21. D'Onofrio M, Cuomo L, Battaglia G, Ngomba RT, Storto M, Kingston AE, Orzi F, De Blasi A, Di Iorio P, Nicoletti F, Bruno V (2001) Neuroprotection mediated by glial group-II metabotropic glutamate receptors requires the activation of the MAP kinase and the phosphatidylinositol-3-kinase pathways. J Neurochem 78:435-445.
22. Erskine L, McCaig CD (1995) Growth cone neurotransmitter receptor activation modulates electric field-guided nerve growth. Dev Biol 171:330-339.
23. Erskine L, Williams SE, Brose K, Kidd T, Rachel RA, Goodman CS, Tessier-Lavigne M, Mason CA (2000) Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. J Neurosci 20:4975-4982.
24. Feldheim DA, Vanderhaeghen P, Hansen MJ, Frisen J, Lu Q, Barbacid M, Flanagan JG (1998) Topographic guidance labels in a sensory projection to the forebrain. Neuron 21:1303-1313.
25. Feldheim DA, Kim YI, Bergemann AD, Frisen J, Barbacid M, Flanagan JG (2000) Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-574.
26. Flatau G, Lemichez E, Gauthier M, Chardin P, Paris S, Fiorentini C, Boquet P (1997) Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387:729-733.
27. Gietzen K (1983) Comparison of the calmodulin antagonists compound 48/80 and calmidazolium. Biochem J 216:611-616.
28. Ginty DD, Komhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME (1993) Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian dock. Science 260:238-241.
29. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
30. Gopalakrishna R, Anderson WB (1983) Calmodulin interacts with cyclic nucleotide phosphodiesterase and calcineurin by binding to a metal ion-independent hydrophobic region on these proteins. J Biol Chem 258:2405-2409.
31. Hagiwara M, Brindle P, Harootunian A, Armstrong R, Rivier J, Vale W, Tsien R, Montminy MR (1993) Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol 13:4852-4859.
32. Hanson PI, Schulman H (1992) Neuronal Ca2+/calmodulin-dependent protein kinases. Annu Rev Biochem 61:559-601.
33. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796.
34. Hermans E, Challiss RA (2001) Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors: prototypic family C G-protein-coupled receptors. Biochem J 359:465-484.
35. Hopker VH, Shewan D, Tessier-Lavigne M, Poo M, Holt C (1999) Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401:69-73.
36. Hume RI, Role LW, Fischbach GD (1983) Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes. Nature 305:632-634.
37. Iacovelli L, Bruno V, Salvatore L, Melchiorri D, Gradini R, Caricasole A, Barletta E, De Blasi A, Nicoletti F (2002) Native group-III-metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/phosphatidylinositol-3-kinase pathways. J Neurochem 82:216-223.
38. Jackson H, Parks TN (1982) Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 2:1736-1743.
39. Jay TM (2003) Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol 69:375-390.
40. Kano M, Hashimoto K, Kurihara H, Watanabe M, Inoue Y, Aiba A, Tonegawa S (1997) Persistent multiple climbing fiber innervation of cerebellar Purkinje cells in mice lacking mGluR1. Neuron 18:71-79.
41. Kapfhammer JP, Raper JA (1987) Collapse of growth cone structure on contact with specific neurites in culture. J Neurosci 7:201-212.
42. Kaslow HR, Lim LK, Moss J, Lesikar DD (1987) Structure-activity analysis of the activation of pertussis toxin. Biochemistry 26:123-127.
43. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
44. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273:245-248.
45. Koppel AM, Feiner L, Kobayashi H, Raper JA (1997) A 70 amino acid region within the semaphorin domain activates specific cellular response of semaphorin family members. Neuron 19:531-537.
46. Kreimborg KM, Lester ML, Medler KF, Gleason EL (2001) Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. J Neurochem 77:452-465.
47. Linden DJ, Ahn S (1999) Activation of presynaptic cAMP-dependent protein kinase is required for induction of cerebellar long-term potentiation. J Neurosci 19:10221-10227.
48. Lipton SA, Frosch MP, Phillips MD, Tauck DL, Aizenman E (1988) Nicotinic antagonists enhance process outgrowth by rat retinal ganglion cells in culture. Science 239:1293-1296.
49. Liu BP, Strittmatter SM (2001) Semaphorin-mediated axonal guidance via Rho-related G proteins. Curr Opin Cell Biol 13:619-626.
50. Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
51. Lucas DR, Newhouse JP (1957) The toxic effect of sodium L-glutamate on the inner layers of the retina. Am Arch Opthalmol 58:193-201.
52. Luo Y, Raible D, Raper JA (1993) Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
53. Mann F, Miranda E, Weinl C, Harmer E, Holt CE (2003) B-type Eph receptors and ephrins induce growth cone collapse through distinct intracellular pathways. J Neurobiol 57:323-336.
54. Menini A (1999) Calcium signalling and regulation in olfactory neurons. Curr Opin Neurobiol 9:419-426.
55. Metzger F, Wiese S, Sendtner M (1998) Effect of glutamate on dendritic growth in embryonic rat motoneurons. J Neurosci 18:1735-1742.
56. Milner B, Squire LR, Kandel ER (1998) Cognitive neuroscience and the study of memory. Neuron 20:445-468.
57. Neumann S, Bradke F, Tessier-Lavigne M, Basbaum AI (2002) Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34:885-893.
58. Niclou SP, Jia L, Raper JA (2000) Slit2 is a repellent for retinal ganglion cell axons. J Neurosci 20:4962-4974.
59. Nishiyama M, Hoshino A, Tsai L, Henley JR, Goshima Y, Tessier-Lavigne M, Poo MM, Hong K (2003) Cyclic AMP/GMP-dependent modulation of Ca2+ channels sets the polarity of nerve growth-cone turning. Nature 424:990-995.
60. Oinuma I, Katoh H, Harada A, Negishi M (2003) Direct interaction of Rnd1 with Plexin-B1 regulates PDZ-RhoGEF-mediated Rho activation by Plexin-B1 and induces cell contraction in COS-7 cells. J Biol Chem 278:25671-25677.
61. Olney JW (1989) Excitatory amino acids and neuropsychiatric disorders. Biol Psychiatry 26:505-525.
62. Olson MF, Paterson HF, Marshall CJ (1998) Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature 394:295-299.
63. Otani S, Daniel H, Takita M, Crepel F (2002) Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci 22:3434-3444.
64. Pickering DS, Thomsen C, Suzdak PD, Fletcher EJ, Robitaille R, Salter MW, MacDonald JF, Huang XP, Hampson DR (1993) A comparison of two alternatively spliced forms of a metabotropic glutamate receptor coupled to phosphoinositide turnover. J Neurochem 61:85-92.
65. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26.
66. Pizzi M, Benarese M, Boroni F, Goffi F, Valerio A, Spano PF (2000) Neuroprotection by metabotropic glutamate receptor agonists on kainate-induced degeneration of motor neurons in spinal cord slices from adult rat. Neuropharmacology 39:903-910.
67. Qiu J, Cai D, Dai H, McAtee M, Hoffman PN, Bregman BS, Filbin MT (2002) Spinal axon regeneration induced by elevation of cyclic AMP. Neuron 34:895-903.
68. Rane SG (1987) Neuromuscular synaptic transmission in Limulus polyphemus-II. Release of amino acid putative transmitters from the neuromuscular preparation. Comp Biochem Physiol C 87:131-137.
69. Riedel G, Platt B, Micheau J (2003) Glutamate receptor function in learning and memory. Behav Brain Res 140:1-47.
70. Ritzenthaler S, Suzuki E, Chiba A (2000) Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons. Nat Neurosci 3:1012-1017.
71. Roseboom PH, Klein DC (1995) Norepinephrine stimulation of pineal cyclic AMP response element-binding protein phosphorylation: primary role of a beta-adrenergic receptor/cyclic AMP mechanism. Mol Pharmacol 47:439-449.
72. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
73. Sattler R, Tymianski M (2001) Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 24:107-129.
74. Schmidt G, Sehr P, Wilm M, Selzer J, Mann M, Aktories K (1997) Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387:725-729.
75. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, Rathjen FG (2002) cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159:489-498.
76. Schoepp DD, Jane DE, Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38:1431-1476.
77. Schulman H (1993) The multifunctional Ca2+/calmodulin-dependent protein kinases. Curr Opin Cell Biol 5:247-253.
78. Shaywitz AJ, Greenberg ME (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861.
79. Shewan D, Dwivedy A, Anderson R, Holt CE (2002) Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat Neurosci 5:955-962.
80. Shigemoto R, Nakanishi S, Mizuno N (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322:121-135.
81. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, Poo M (1998) Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281:1515-1518.
82. Song HJ, Ming GL, Poo MM (1997) cAMP-induced switching in turning direction of nerve growth cones. Nature 388:275-279.
83. Spillson AB, Russell JW (2003) Metabotropic glutamate receptor regulation of neuronal cell death. Exp Neurol 184 [Suppl 1]:S97-S105.
84. Sun YA, Poo MM (1987) Evoked release of acetylcholine from the growing embryonic neuron. Proc Natl Acad Sci USA 84:2540-2544.
85. Takano H, Fukushi H, Morishima Y, Shirasaki Y (2003) Calmodulin and calmodulin-dependent kinase II mediate neuronal cell death induced by depolarization. Brain Res 962:41-47.
86. Terman JR, Kolodkin AL (2004) Nervy links protein kinase a to plexin-mediated semaphorin repulsion. Science 303:1204-1207.
87. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
88. Toms NJ, Jane DE, Tse HW, Roberts PJ (1995) Characterization of metabotropic glutamate receptor-stimulated phosphoinositide hydrolysis in rat cultured cerebellar granule cells. Br J Pharmacol 116:2824-2827.
89. Tong G, Malenka RC, Nicoll RA (1996) Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron 16:1147-1157.
90. Torok K, Trentham DR (1994) Mechanism of 2-chloro-(epsilon-amino-Lys75)- [6-[4-(N,N-diethylamino)phenyl]-1,3,5-triazin-4-yl]calmodulin interactions with smooth muscle myosin light chain kinase and derived peptides. Biochemistry 33:12807-12820.
91. Vanderklish PW, Edelman GM (2002) Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 99:1639-1644.
92. Vlahos CJ, Matter WF, Hui KY, Brown RF (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 269:5241-5248.
93. Waltereit R, Weller M (2003) Signaling from cAMP/PKA to MAPK and synaptic plasticity. Mol Neurobiol 27:99-106.
94. Wong WT, Sanes JR, Wong RO (1998) Developmentally regulated spontaneous activity in the embryonic chick retina. J Neurosci 18:8839-8852.
95. Xiang Y, Li Y, Zhang Z, Cui K, Wang S, Yuan XB, Wu CP, Poo MM, Duan S (2002) Nerve growth cone guidance mediated by G protein-coupled receptors. Nat Neurosci 5:843-848.
96. Young RW (1985) Cell differentiation in the retina of the mouse. Anat Rec 212:199-205.
97. Yu TW, Bargmann CI (2001) Dynamic regulation of axon guidance. Nat Neurosci [Suppl] 4:1169-1176.
98. Yuan XB, Jin M, Xu X, Song YQ, Wu CP, Poo MM, Duan S (2003) Signalling and crosstalk of Rho GTPases in mediating axon guidance. Nat Cell Biol 5:38-45.
99. Zheng JQ, Felder M, Connor JA, Poo MM (1994) Turning of nerve growth cones induced by neurotransmitters. Nature 368:140-144.
100. Zhu H, Ryan K, Chen S (1999) Cloning of novel splice variants of mouse mGluR1. Brain Res Mol Brain Res 73:93-103.
101. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91-102.