Expression of the N-methyl-d-aspartate receptor subunit NR3B regulates dendrite morphogenesis in spinal motor neurons

Neuroscience

Volumn 155, Issue 1, 2008, Pages 145-153

  Prithviraj, R ^a   Inglis, F M ^a  

^a Tulane University   (United States)

Author keywords

activity dependent development; AP5; dendrite branching; dominant negative; filopodia; motoneuron

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR NR3B SUBUNIT;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; EMBRYO; FILOPODIUM; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SPINAL CORD NERVE CELL; STATISTICAL SIGNIFICANCE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; DENDRITES; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; MORPHOGENESIS; NEURONS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SPINAL CORD; TRANSFECTION;

EID: 47249156688     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.03.089     Document Type: Article

References (49)

1. Brown K.M., Wrathall J.R., Yasuda R.P., and Wolfe B.B. Quantitative measurement of glutamate receptor subunit protein expression in the postnatal rat spinal cord. Brain Res Dev Brain Res 137 (2002) 127-133
2. Carriedo S.G., Yin H.Z., and Weiss J.H. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 16 (1996) 4069-4079
3. Chatterton J.E., Awobuluyi M., Premkumar L.S., Takahashi H., Talantova M., Shin Y., Cui J., Tu S., Sevarino K.A., Nakanishi N., Tong G., Lipton S.A., and Zhang D. Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415 (2002) 793-798
4. Ciabarra A.M., Sullivan J.M., Gahn L.G., Pecht G., Heinemann S., and Sevarino K.A. Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15 (1995) 6498-6508
5. Cline H.T. Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11 (2001) 118-126
6. Cline H.T., and Constantine-Paton M. NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J Neurosci 10 (1990) 1197-1216
7. Cramer K.S., and Sur M. Activity-dependent remodeling of connections in the mammalian visual system. Curr Opin Neurobiol 5 (1995) 106-111
8. Cull-Candy S.G., and Leszkiewicz D.N. Role of distinct NMDA receptor subtypes at central synapses. Sci STKE 2004 (2004) re16
9. Cuppini R., Sartini S., Ambrogini P., Falcieri E., Maltarello M.C., and Gallo G. Control of neuron outgrowth by NMDA receptors. J Submicrosc Cytol Pathol 31 (1999) 31-40
10. Dingledine R., Borges K., Bowie D., and Traynelis S.F. The glutamate receptor ion channels. Pharmacol Rev 51 (1999) 7-61
11. Feldmeyer D., and Cull-Candy S. Functional consequences of changes in NMDA receptor subunit expression during development. J Neurocytol 25 (1996) 857-867
12. Fukaya M., Hayashi Y., and Watanabe M. NR2 to NR3B subunit switchover of NMDA receptors in early postnatal motoneurons. Eur J Neurosci 21 (2005) 1432-1436
13. Hebbeler S.L., Verhovshek T., and Sengelaub D.R. N-methyl-D-aspartate receptor blockade inhibits estrogenic support of dendritic growth in a sexually dimorphic rat spinal nucleus. J Comp Neurol 451 (2002) 142-152
14. Hollmann M., and Heinemann S. Cloned glutamate receptors. Annu Rev Neurosci 17 (1994) 31-108
15. Inglis F.M., Zuckerman K.E., and Kalb R.G. Experience-dependent development of spinal motor neurons. Neuron 26 (2000) 299-305
16. Inglis F.M., Furia F., Zuckerman K.E., Strittmatter S.M., and Kalb R.G. The role of nitric oxide and NMDA receptors in the development of motor neuron dendrites. J Neurosci 18 (1998) 10493-10501
17. Inglis F.M., Crockett R., Korada S., Abraham W.C., Hollmann M., and Kalb R.G. The AMPA receptor subunit GluR1 regulates dendritic architecture of motor neurons. J Neurosci 22 (2002) 8042-8051
18. Jeong G.B., Werner M., Gazula V.R., Itoh T., Roberts M., David S., Pfister B., Cohen A., Neve R.L., Hollmann M., and Kalb R. Bi-directional control of motor neuron dendrite remodeling by the calcium permeability of AMPA receptors. Mol Cell Neurosci 32 (2006) 299-314
19. Kalb R.G. Regulation of motor neuron dendrite growth by NMDA receptor activation. Development 120 (1994) 3063-3071
20. Katz L.C., and Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 274 (1996) 1133-1138
21. Maletic-Savatic M., Malinow R., and Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283 (1999) 1923-1927
22. Matsuda K., Kamiya Y., Matsuda S., and Yuzaki M. Cloning and characterization of a novel NMDA receptor subunit NR3B: a dominant subunit that reduces calcium permeability. Brain Res Mol Brain Res 100 (2002) 43-52
23. Matsuda K., Fletcher M., Kamiya Y., and Yuzaki M. Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J Neurosci 23 (2003) 10064-10073
24. Matus A. Growth of dendritic spines: a continuing story. Curr Opin Neurobiol 15 (2005) 67-72
25. McAllister A.K. Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10 (2000) 963-973
26. Niell C.M., Meyer M.P., and Smith S.J. In vivo imaging of synapse formation on a growing dendritic arbor. Nat Neurosci 7 (2004) 254-260
27. Niemann S., Kanki H., Fukui Y., Takao K., Fukaya M., Hynynen M.N., Churchill M.J., Shefner J.M., Bronson R.T., Brown Jr. R.H., Watanabe M., Miyakawa T., Itohara S., and Hayashi Y. Genetic ablation of NMDA receptor subunit NR3B in mouse reveals motoneuronal and nonmotoneuronal phenotypes. Eur J Neurosci 26 (2007) 1407-1420
28. Nishi M., Hinds H., Lu H.P., Kawata M., and Hayashi Y. Motoneuron-specific expression of NR3B, a novel NMDA-type glutamate receptor subunit that works in a dominant-negative manner. J Neurosci 21 (2001) RC185
29. Oshima S., Fukaya M., Masabumi N., Shirakawa T., Oguchi H., and Watanabe M. Early onset of NMDA receptor GluR epsilon 1 (NR2A) expression and its abundant postsynaptic localization in developing motoneurons of the mouse hypoglossal nucleus. Neurosci Res 43 (2002) 239-250
30. Portera-Cailliau C., Pan D.T., and Yuste R. Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J Neurosci 23 (2003) 7129-7142
31. Prithviraj R., Kelly K.M., Espinoza-Lewis R., Hexom T., Clark A.B., and Inglis F.M. Differential regulation of dendrite complexity by AMPA receptor subunits GluR1 and GluR2 in motor neurons. Dev Neurobiol 68 (2008) 247-264
32. Rajan I., and Cline H.T. Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18 (1998) 7836-7846
33. Rajan I., Witte S., and Cline H.T. NMDA receptor activity stabilizes presynaptic retinotectal axons and postsynaptic optic tectal cell dendrites in vivo. J Neurobiol 38 (1999) 357-368
34. Rashid N.A., and Cambray-Deakin M.A. N-methyl-D-aspartate effects on the growth, morphology and cytoskeleton of individual neurons in vitro. Brain Res Dev Brain Res 67 (1992) 301-308
35. Robert A., Howe J.R., and Waxman S.G. Development of glutamatergic synaptic activity in cultured spinal neurons. J Neurophysiol 83 (2000) 659-670
36. h and HCN1 protein expression later in life. Eur J Neurosci 23 (2006) 3346-3358
37. Smothers C.T., and Woodward J.J. Pharmacological characterization of glycine-activated currents in HEK 293 cells expressing N-methyl-D-aspartate NR1 and NR3 subunits. J Pharmacol Exp Ther 322 (2007) 739-748
38. Stegenga S.L., and Kalb R.G. Developmental regulation of N-methyl-D-aspartate- and kainate-type glutamate receptor expression in the rat spinal cord. Neuroscience 105 (2001) 499-507
39. Sucher N.J., Akbarian S., Chi C.L., Leclerc C.L., Awobuluyi M., Deitcher D.L., Wu M.K., Yuan J.P., Jones E.G., and Lipton S.A. Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15 (1995) 6509-6520
40. Tapia J.C., Cardenas A.M., Nualart F., Mentis G.Z., Navarrete R., and Aguayo L.G. Neurite outgrowth in developing mouse spinal cord neurons is modulated by glycine receptors. Neuroreport 11 (2000) 3007-3010
41. Ulfhake B., and Cullheim S. Postnatal development of cat hind limb motoneurons. II: In vivo morphology of dendritic growth cones and the maturation of dendrite morphology. J Comp Neurol 278 (1988) 88-102
42. Vandenberghe W., Ihle E.C., Patneau D.K., Robberecht W., and Brorson J.R. AMPA receptor current density, not desensitization, predicts selective motoneuron vulnerability. J Neurosci 20 (2000) 7158-7166
43. Vaughn J.E., Henrikson C.K., and Grieshaber J.A. A quantitative study of synapses on motor neuron dendritic growth cones in developing mouse spinal cord. J Cell Biol 60 (1974) 664-672
44. Vogel M.W., and Prittie J. Purkinje cell dendritic arbors in chick embryos following chronic treatment with an N-methyl-D-aspartate receptor antagonist. J Neurobiol 26 (1995) 537-552
45. Walton K.D., and Navarrete R. Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol 433 (1991) 283-305
46. Watanabe M., Mishina M., and Inoue Y. Distinct spatiotemporal distributions of the N-methyl-D-aspartate receptor channel subunit mRNAs in the mouse cervical cord. J Comp Neurol 345 (1994) 314-319
47. Wong R.O., and Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3 (2002) 803-812
48. Yuste R., and Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24 (2001) 1071-1089
49. Zona C., Pieri M., and Carunchio I. Voltage-dependent sodium channels in spinal cord motor neurons display rapid recovery from fast inactivation in a mouse model of amyotrophic lateral sclerosis. J Neurophysiol 96 (2006) 3314-3322