NMDA receptors regulate developmental gap junction uncoupling via CREB signaling

Nature Neuroscience

Volumn 8, Issue 12, 2005, Pages 1720-1726

  Arumugam, Harsha ^a   Liu, Xinhuai ^a   Colombo, Paul J ^a   Corriveau, Roderick A ^b   Belousov, Andrei B ^a  

^a Tulane University   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CONNEXIN 36; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIZOCILPINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; EMBRYO; FEMALE; GAP JUNCTION; HYPOTHALAMUS; KNOCKOUT MOUSE; MALE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION;

ACTION POTENTIALS; ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELLS, CULTURED; CONNEXINS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOWN-REGULATION; FEMALE; GAP JUNCTIONS; HYPOTHALAMUS; MALE; MICE; MICE, KNOCKOUT; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 28044453528     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1588     Document Type: Article

References (50)

1. Becker, D.L. & Mobbs, P. Connexin alpha1 and cell proliferation in the developing chick retina. Exp. Neurol. 156, 326-332 (1999).
2. Bani-Yaghoub, M., Underhill, T.M. & Naus, C.C. Gap junction blockage interferes with neuronal and astroglial differentiation of mouse P19 embryonal carcinoma cells. Dev. Genet. 24, 69-81 (1999).
3. Lin, J.H. et al. Gap-junction-mediated propagation and amplification of cell injury. Nat. Neurosci. 1, 494-500 (1998).
4. Lo Turco, J.J. & Kriegstein, A.R. Clusters of coupled neuroblasts in embryonic neocortex. Science 252, 563-566 (1991).
5. Allen, F. & Warner, A. Gap junctional communication during neuromuscular junction formation. Neuron 6, 101-111 (1991).
6. Walton, K.D. & Navarrete, R. Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J. Physiol. (Lond.) 433, 283-305 (1991).
7. Peinado, A., Yuste, R. & Katz, L.C. Gap junctional communication and the development of local circuits in neocortex. Cereb. Cortex 3, 488-498 (1993).
8. Personius, K., Chang, Q., Bittman, K., Panzer, J. & Balice-Gordon, R. Gap junctional communication among motor and other neurons shapes patterns of neural activity and synaptic connectivity during development. Cell. Commun. Adhes. 8, 329-333 (2001).
9. Roerig, B. & Feller, M.B. Neurotransmitters and gap junctions in developing neural circuits. Brain Res. Brain Res. Rev. 32, 86-114 (2000).
10. Bennett, M.V. & Zukin, R.S. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41, 495-511 (2004).
11. Naus, C.C. & Bani-Yaghoub, M. Gap junctional communication in the developing central nervous system. Cell Biol. Int. 22, 751-763 (1998).
12. Kandler, K. & Katz, L.C. Neuronal coupling and uncoupling in the developing nervous system. Curr. Opin. Neurobiol. 5, 98-105 (1995).
13. Kandler, K. & Katz, L.C. Coordination of neuronal activity in developing visual cortex by gap junction-mediated biochemical communication. J. Neurosci. 18, 1419-1427 (1998).
14. Meyer, T. Cell signaling by second messenger waves. Cell 64, 675-678 (1991).
15. Ben-Ari, Y. Developing networks play a similar melody. Trends Neurosci. 24, 353-360 (2001).
16. Garaschuk, O., Linn, J., Eilers, J. & Konnerth, A. Large-scale oscillatory calcium waves in the immature cortex. Nat. Neurosci. 3, 452-459 (2000).
17. Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S. & Shatz, C.J. Requirement for cholinergic synaptic transmission in the propagation of spontaneous retinal waves. Science 272, 1182-1187 (1996).
18. Wong, R.O. Retinal waves and visual system development. Annu. Rev. Neurosci. 22, 29-47 (1999).
19. Milner, L.D. & Landmesser, L.T. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J. Neurosci. 19, 3007-3022 (1999).
20. Strata, F. et al. A pacemaker current in dye-coupled hilar interneurons contributes to the generation of giant GABAergic potentials in developing hippocampus. J. Neurosci. 17, 1435-1446 (1997).
21. Chang, Q., Gonzalez, M., Pinter, M.J. & Balice-Gordon, R.J. Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J. Neurosci. 19, 10813-10828 (1999).
22. Mentis, G.Z., Diaz, E., Moran, L.B. & Navarrete, R. Increased incidence of gap junctional coupling between spinal motoneurones following transient blockade of NMDA receptors in neonatal rats. J. Physiol. (Lond.) 544, 757-764 (2002).
23. Connors, B.W., Benardo, L.S. & Prince, D.A. Coupling between neurons of the developing rat neocortex. J. Neurosci. 3, 773-782 (1983).
24. Peinado, A., Yuste, R. & Katz, L.C. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10, 103-114 (1993).
25. Venance, L., Glowinski, J. & Giaume, C. Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices. J. Physiol. (Lond.) 559, 215-230 (2004).
26. Kandler, K. & Katz, L.C. Relationship between dye coupling and spontaneous activity in developing ferret visual cortex. Dev. Neurosci. 20, 59-64 (1998).
27. Hatton, G.I. Synaptic modulation of neuronal coupling. Cell Biol. Int. 22, 765-780 (1998).
28. Rash, J.E. et al. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc. Natl. Acad. Sci. USA 97, 7573-7578 (2000).
29. Belluardo, N. et al. Expression of connexin36 in the adult and developing rat brain. Brain Res. 865, 121-138 (2000).
30. Long, M.A., Jutras, M.J., Connors, B.W. & Burwell, R.D. Electrical synapses coordinate activity in the suprachiasmatic nucleus. Nat. Neurosci. 8, 61-66 (2005).
31. Srinivas, M. et al. Functional properties of channels formed by the neuronal gap junction protein connexin36. J. Neurosci. 19, 9848-9855 (1999).
32. Bessho, Y., Nawa, H. & Nakanishi, S. Selective up-regulation of an NMDA receptor subunit mRNA in cultured cerebellar granule cells by K(+)-induced depolarization and NMDA treatment. Neuron 12, 87-95 (1994).
33. Hardingham, G.E., Fukunaga, Y. & Bading, H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat. Neurosci. 5, 405-414 (2002).
34. Greenberg, M.E. & Ziff, E.B. Signal transduction in the postsynaptic neuron: activity-dependent regulation of gene expression. in Synapses (eds. Cowan, M.W., Sudhof, T.C. & Stevens, C.F.) 357-391 (Johns Hopkins Univ. Press, Baltimore, 2001).
35. Lonze, B.E. & Ginty, D.D. Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623 (2002).
36. Carlezon, W.A., Jr. et al. Regulation of cocaine reward by CREB. Science 282, 2272-2275 (1998).
37. Guzowski, J.F. & McGaugh, J.L. Antisense oligodeoxynucleotide- mediated disruption of hippocampal cAMP response element binding protein levels impairs consolidation of memory for water maze training. Proc. Natl. Acad. Sci. USA 94, 2693-2698 (1997).
38. Venance, L. et al. Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. USA 97, 10260-10265 (2000).
39. Connors, B.W. & Long, M.A. Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 27, 393-418 (2004).
40. Galarreta, M. & Hestrin, S. Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2, 425-433 (2001).
41. Xia, Z. & Storm, D.R. Regulatory Properties of the Mammalian Adenylyl Cyclases Ch. 7, 105-134 (R.G. Landes Austin, Texas, 1996).
42. Kornhuber, J. & Weller, M. Psychotogenicity and N-methyl-D-aspartate receptor antagonism: implications for neuroprotective pharmacotherapy. Biol. Psychiatry 41, 135-144 (1997).
43. Facchinetti, F. et al. Structural, neurochemical and behavioural consequences of neonatal blockade of NMDA receptor through chronic treatment with CGP 39551 or MK-801. Brain Res. Dev. Brain Res. 74, 219-224 (1993).
44. Belousov, A.B., Hunt, N.D., Raju, R.P. & Denisova, J.V. Calcium-dependent regulation of cholinergic cell phenotype in the hypothalamus in vitro. J. Neurophysiol. 88, 1352-1362 (2002).
45. Aberg, N.D., Ronnback, L. & Eriksson, P.S. Connexin43 mRNA and protein expression during postnatal development of defined brain regions. Brain Res. Dev. Brain Res. 115, 97-101 (1999).
46. Belousov, A.B. & van den Pol, A.N. Local synaptic release of glutamate from neurons in the rat hypothalamic arcuate nucleus. J. Physiol. (Lond.) 499, 747-761 (1997).
47. Belousov, A.B., O'Hara, B.F. & Denisova, J.V. Acetylcholine becomes the major excitatory neurotransmitter in the hypothalamus in vitro in the absence of glutamate excitation. J. Neurosci. 21, 2015-2027 (2001).
48. Luther, J.A. & Tasker, J.G. Voltage-gated currents distinguish parvocellular from magnocellular neurones in the rat hypothalamic paraventricular nucleus. J. Physiol. (Lond.) 523, 193-209 (2000).
49. Li, Y., Erzurumlu, R.S., Chen, C., Jhaveri, S. & Tonegawa, S. Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76, 427-437 (1994).
50. Sugiura, N., Patel, R.G. & Corriveau, R.A. N-methyl-D-aspartate receptors regulate a group of transiently expressed genes in the developing brain. J. Biol. Chem. 276, 14257-14263 (2001).