Sodium channel activation augments NMDA receptor function and promotes neurite outgrowth in immature cerebrocortical neurons

Journal of Neuroscience

Volumn 29, Issue 10, 2009, Pages 3288-3301

  George, Joju ^a   Dravid, Shashank M ^a   Prakash, Anand ^a   Xie, Jun ^a,b   Peterson, Jennifer ^c   Jabba, Sairam V ^a   Baden, Daniel G ^d   Murray, Thomas F ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SHANXI MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF NORTH CAROLINA WILMINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREVETOXIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE I; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM; PROTEIN TYROSINE KINASE; SODIUM; TYROSINE; VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CALCIUM TRANSPORT; CELL ADHESION; CHANNEL GATING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPOLARIZATION; DRUG MECHANISM; DRUG POTENTIATION; EMBRYO; ENZYME ACTIVATION; EXTRACELLULAR SPACE; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL STIMULATION; NERVE FIBER GROWTH; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RECEPTOR BLOCKING; RECEPTOR UPREGULATION; SODIUM CELL LEVEL; SODIUM TRANSPORT;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; MARINE TOXINS; MEMBRANE POTENTIALS; MICE; NEURITES; NEURONS; OXOCINS; PREGNANCY; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM CHANNELS;

EID: 63849305126     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6104-08.2009     Document Type: Article

References (70)

1. Bading H, Ginty DD, Greenberg ME (1993) Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181-186.
2. Baxter DF, Kirk M, Garcia AF, Raimondi A, Holmqvist MH, Flint KK, Bojanic D, Distefano PS, Curtis R, Xie Y (2002) A novel membrane potential-sensitive fluorescent dye improves cell-based assays for ion channels. J Biomol Screen 7:79-85.
3. Berman FW, Murray TF (2000) Brevetoxin-induced autocrine excitotoxicity is associated with manifold routes of Ca2+ influx. J Neurochem 74:1443-1451.
4. Cao Z, George J, Baden DG, Murray TF (2007) Brevetoxin-induced phosphorylation of Pyk2 and Src in murine neocortical neurons involves distinct signaling pathways. Brain Res 1184:17-27.
5. Cao Z, George J, Gerwick WH, Baden DG, Rainier JD, Murray TF (2008) Influence of lipid soluble gating modifier toxins on sodium influx in neocortical neurons. J Pharmacol Exp Ther 326:604-613.
6. Catterall WA, Gainer M (1985) Interaction of brevetoxin A with a new receptor site on the sodium channel. Toxicon 23:497-504.
7. Chen Y, Ghosh A (2005) Regulation of dendritic development by neuronal activity. J Neurobiol 64:4-10.
8. Cheng C, Fass DM, Reynolds IJ (1999) Emergence of excitotoxicity in cultured forebrain neurons coincides with larger glutamate-stimulated [Ca(2 +)](i) increases and NMDA receptor mRNA levels. Brain Res 849:97-108.
9. Choi DW, Maulucci-Gedde M, Kriegstein AR (1987) Glutamate neurotoxicity in cortical cell culture. J Neurosci 7:357-368.
10. Cline HT (2001) Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11:118-126.
11. Dargent B, Paillart C, Carlier E, Alcaraz G, Martin-Eauclaire MF, Couraud F (1994) Sodium channel internalization in developing neurons. Neuron 13:683-690.
12. Diarra A, Sheldon C, Church J (2001) In situ calibration and [H+] sensitivity of the fluorescent Na+ indicator SBFI. Am J Physiol Cell Physiol 280:C1623-C1633.
13. Dravid SM, Baden DG, Murray TF (2005) Brevetoxin augments NMDA receptor signaling in murine neocortical neurons. Brain Res 1031:30-38.
14. Ehrenberg B, Montana V, Wei MD, Wuskell JP, Loew LM (1988) Membrane potential can be determined in individual cells from the nernstian distribution of cationic dyes. Biophys J 53:785-794.
15. Erreger K, Dravid SM, Banke TG, Wyllie DJ, Traynelis SF (2005) Subuni-tspecific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signalling profiles. J Physiol 563:345-358.
16. Ewald RC, Van Keuren-Jensen KR, Aizenman CD, Cline HT (2008) Roles of NR2A and NR2B in the development of dendritic arbor morphology in vivo. J Neurosci 28:850-861.
17. Frandsen A, Schousboe A (1990) Development of excitatory amino acid induced cytotoxicity in cultured neurons. Int J Dev Neurosci 8:209-216.
18. Gomez TM, Spitzer NC (2000) Regulation of growth cone behavior by calcium: new dynamics to earlier perspectives. J Neurobiol 44:174-183.
19. Griffiths R, Malcolm C, Ritchie L, Frandsen A, Schousboe A, Scott M, Rumsby P, Meredith C (1997) Association of c-fos mRNA expression and excitotoxicity in primary cultures of mouse neocortical and cerebellar neurons. J Neurosci Res 48:533-542.
20. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100.
21. Hardingham GE, Bading H (2003) The Yin and Yang of NMDA receptor signalling. Trends Neurosci 26:81-89.
22. Hille B (1992) Ionic channels of excitable membranes, pp 403-411. Sunderland, MA: Sinauer.
23. Hodgkin AL, Huxley AF (1952) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 116:449-472.
24. Hui K, Fei GH, Saab BJ, Su J, Roder JC, Feng ZP (2007) Neuronal calcium sensor-1 modulation of optimal calcium level for neurita outgrowth. Development 134:4479-4489.
25. Jeglitsch G, Rein K, Baden DG, Adams DJ (1998) Brevetoxin-3 (PbTx-3) and its derivatives modulate single tetrodotoxin-sensitive sodium channels in rat sensory neurons. J Pharmacol Exp Ther 284:516-525.
26. Kim HG, Fox K, Connors BW (1995) Properties of excitatory synaptic events in neurons of primary somatosensory cortex of neonatal rats. Cereb Cortex 5:148-157.
27. King AE, Chung RS, Vickers JC, Dickson TC (2006) Localization of glutamate receptors in developing cortical neurons in culture and relationship to susceptibility to excitotoxicity. J Comp Neurol 498:277-294.
28. Koh JY, Choi DW (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20:83-90.
29. Konur S, Ghosh A (2005) Calcium signaling and the control of dendritic development. Neuron 46:401-405.
30. Kuner T, Augustine GJ (2000) A genetically encoded ratiometric neurotechnique indicator for chloride: Capturing chloride transients in cultured hippocampal neurons. Neuron 27:447-459.
31. Lee LJ, Lo FS, Erzurumlu RS (2005) NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci 25:2304-2311.
32. Lipton SA, Nakanishi N (1999) Shakespeare in love-with NMDA receptors? Nat Med 5:270-271.
33. Liu Z, Stafstrom CE, Sarkisian M, Tandon P, Yang Y, Hori A, Holmes GL (1996) Age-dependent effects of glutamate toxicity in the hippocampus. Brain Res Dev Brain Res 97:178-184.
34. Marks JD, Boriboun C, Wang J (2005) Mitochondrial nitric oxide mediates decreased vulnerability of hippocampal neurons from immature animals to NMDA. J Neurosci 25:6561-6575.
35. Mayer ML, Westbrook GL, Guthrie PB (1984) Voltage-dependent block by Mg2 + of NMDA responses in spinal cord neurones. Nature 309:261-263.
36. McAllister AK (2000) Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10:963-973.
37. Miller FD, Kaplan DR (2003) Signaling mechanisms underlying dendrite formation. Curr Opin Neurobiol 13:391-398.
38. Mitrovic N, George AL Jr, Horn R (2000) Role of domain 4 in sodium channel slow inactivation. J Gen Physiol 115:707-718.
39. Mizuta I, Katayama M, Watanabe M, Mishina M, Ishii K (1998) Developmental expression of NMDA receptor subunits and the emergence of glutamate neurotoxicity in primary cultures of murine cerebral cortical neurons. Cell Mol Life Sci 54:721-725.
40. Ong BH, Tomaselli GF, Balser JR (2000) A structural rearrangement in the sodium channel pore linked to slow inactivation and use dependence. J Gen Physiol 116:653-662.
41. Poli MA, Mende TJ, Baden DG (1986) Brevetoxins, unique activators of voltage-sensitive sodium channels, bind to specific sites in rat brain synaptosomes. Mol Pharmacol 30:129-135.
42. Qin F (2004) Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys J 86:1488-1501.
43. Rajan I, Cline HT (1998) Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18:7836-7846.
44. Ramoa AS, McCormick DA (1994) Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections. J Neurosci 14:2089-2097.
45. Redmond L, Kashani AH, Ghosh A (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron 34:999-1010.
46. + signals in spines and dendrites. J Neurosci 21:4207-4214.
47. Rose CR, Ransom BR (1997) Regulation of intracellular sodium in cultured rat hippocampal neurones. J Physiol 499:573-587.
48. Rose CR, Kovalchuk Y, Eilers J, Konnerth A (1999) Two-photon Na+imaging in spines and fine dendrites of central neurons. Pflugers Arch 439:201-207.
49. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5:317-328.
50. Saneyoshi T, Wayman G, Fortin D, Davare M, Hoshi N, Nozaki N, Natsume T, Soderling TR (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57:94-107.
51. Schmitt JM, Wayman GA, Nozaki N, Soderling TR (2004) Calcium activation of ERK mediated by calmodulin kinase I. J Biol Chem 279:24064-24072.
52. Schorge S, Elenes S, Colquhoun D (2005) Maximum likelihood fitting of single channel NMDA activity with a mechanism composed of independent dimers of subunits. J Physiol 569:395-418.
53. Sin WC, Haas K, Ruthazer ES, Cline HT (2002) Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases. Nature 419:475-480.
54. Solem M, McMahon T, Messing RO (1995) Depolarization-induced neurite outgrowth in PC12 cells requires permissive, low level NGF receptor stimulation and activation of calcium/calmodulin-dependent protein kinase. J Neurosci 15:5966-5975.
55. Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R (2002) STO-609, a specific inhibitor of the Ca(2 + )/calmodulin-dependent protein kinase kinase. J Biol Chem 277:15813-15818.
56. Tokumitsu H, Inuzuka H, Ishikawa Y, Kobayashi R (2003) A single amino acid difference between alpha and beta Ca2+/calmodulin-dependent protein kinase kinase dictates sensitivity to the specific inhibitor, STO609. J Biol Chem 278:10908-10913.
57. Tolias KF, Bikoff JB, Burette A, Paradis S, Harrar D, Tavazoie S, Weinberg RJ, Greenberg ME (2005) The Rac1-GEF Tiaml couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45:525-538.
58. Trombley PQ, Westbrook GL (1991) Voltage-gated currents in identified rat olfactory receptor neurons. J Neurosci 11:434-444.
59. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90:2964-2972.
60. Ultanir SK, Kim JE, Hall BJ, Deerinck T, Ellisman M, Ghosh A (2007) Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Natl Acad Sci U S A 104:19553-19558.
61. Wayman GA, Kaech S, Grant WF, Davare M, Impey S, Tokumitsu H, Nozaki N, Banker G, Soderling TR (2004) Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J Neurosci 24:3786-3794.
62. Wayman GA, Impey S, Marks D, Saneyoshi T, Grant WF, Derkach V, Soderling TR (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50:897-909.
63. West AE, Griffith EC, Greenberg ME (2002) Regulation of transcription factors by neuronal activity. Nat Rev Neurosci 3:921-931.
64. Whiteaker KL, Gopalakrishnan SM, Groebe D, Shieh CC, Warrior U, Burns DJ, Coghlan MJ, Scott VE, Gopalakrishnan M (2001) Validation of FLIPR membrane potential dye for high throughput screening of potassium channel modulators. J Biomol Screen 6:305-312.
65. Williams K, Russell SL, Shen YM, Molinoff PB (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 10:267-278.
66. Wong RO, Ghosh A (2002) Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3:803-812.
67. Xin WK, Kwan CL, Zhao XH, Xu J, Ellen RP, McCulloch CA, Yu XM (2005) A functional interaction of sodium and calcium in the regulation of NMDA receptor activity by remote NMDA receptors. J Neurosci 25:139-148.
68. Yu XM (2006) The role of intracellular sodium in the regulation of NMDA-receptor-mediated channel activity and toxicity. Mol Neurobiol 33:63-80.
69. Yu XM, Salter MW (1998) Gain control of NMDA-receptor currents by intracellular sodium. Nature 396:469-474.
70. Yu XM, Askalan R, Keil GJ 2nd, Salter MW (1997) NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.