Coordinated PKA and PKC phosphorylation suppresses RXR-mediated ER retention and regulates the surface delivery of NMDA receptors

Neuropharmacology

Volumn 45, Issue 6, 2003, Pages 755-767

  Scott, Derek B ^a   Blanpied, Thomas A ^a   Ehlers, Michael D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

ER retention; Glutamate receptors; Phosphorylation; PKA; PKC; RXR; Trafficking

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE C; RECEPTOR SUBUNIT;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DNA FLANKING REGION; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME PHOSPHORYLATION; ENZYME REGULATION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SECRETION; SIGNAL TRANSDUCTION; SYNAPSE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ARGININE; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDOPLASMIC RETICULUM; HUMANS; MOLECULAR SEQUENCE DATA; NEURONS; PHOSPHORYLATION; PROTEIN KINASE C; RATS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 1542614144     PISSN: 00283908     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0028-3908(03)00250-8     Document Type: Article

References (61)

1. Ali D.W., Salter M.W. NMDA receptor regulation by Src kinase signalling in excitatory synaptic transmission and plasticity. Curr. Opin. Neurobiol. 11:2001;336-342.
2. Altier C., Dubel S.J., Barrere C., Jarvis S.E., Stotz S.C., Spaetgens R.L., Scott J.D., Cornet V., De Waard M., Zamponi G.W., Nargeot J., Bourinet E. Trafficking of L-type calcium channels mediated by the postsynaptic scaffolding protein AKAP79. J. Biol. Chem. 277:2002;33598-33603.
3. Aridor M., Balch W.E. Kinase signaling initiates coat complex II (COPII) recruitment and export from the mammalian endoplasmic reticulum. J. Biol. Chem. 275:2000;35673-35676.
4. Barria A., Malinow R. Subunit-specific NMDA receptor trafficking to synapses. Neuron. 35:2002;345-353.
5. Barry M.F., Ziff E.B. Receptor trafficking and the plasticity of excitatory synapses. Curr. Opin. Neurobiol. 12:2002;279-286.
6. Bear M.F., Abraham W.C. Long-term depression in hippocampus. Annu. Rev. Neurosci. 19:1996;437-462.
7. Beaver C.J., Ji Q., Fischer Q.S., Daw N.W. Cyclic AMP-dependent protein kinase mediates ocular dominance shifts in cat visual cortex. Nat. Neurosci. 4:2001;159-163.
8. Bergmann J.E. Using temperature-sensitive mutants of VSV to study membrane protein biogenesis. Methods Cell Biol. 32:1989;85-110.
9. Carroll R.C., Zukin R.S. NMDA-receptor trafficking and targeting: implications for synaptic transmission and plasticity. Trends Neurosci. 25:2002;571-577.
10. Chang S.Y., Di A., Naren A.P., Palfrey H.C., Kirk K.L., Nelson D.J. Mechanisms of CFTR regulation by syntaxin 1A and PKA. J. Cell Sci. 115:2002;783-791.
11. Choi W.S., Chahdi A., Kim Y.M., Fraundorfer P.F., Beaven M.A. Regulation of phospholipase D and secretion in mast cells by protein kinase A and other protein kinases. Ann. N. Y. Acad. Sci. 968:2002;198-212.
12. Colledge M., Dean R.A., Scott G.K., Langeberg L.K., Huganir R.L., Scott J.D. Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron. 27:2000;107-119.
13. Crump F.T., Dillman K.S., Craig A.M. cAMP-dependent protein kinase mediates activity-regulated synaptic targeting of NMDA receptors. J. Neurosci. 21:2001;5079-5088.
14. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr. Opin. Neurobiol. 11:2001;327-335.
15. Dunah A.W., Standaert D.G. Dopamine D1 receptor-dependent trafficking of striatal NMDA glutamate receptors to the postsynaptic membrane. J. Neurosci. 21:2001;5546-5558.
16. Dunah A.W., Wang Y., Yasuda R.P., Kameyama K., Huganir R.L., Wolfe B.B., Standaert D.G. Alterations in subunit expression, composition, and phosphorylation of striatal N-methyl-D-aspartate glutamate receptors in a rat 6-hydroxydopamine model of Parkinson's disease. Mol. Pharmacol. 57:2000;342-352.
17. Ehlers M.D., Tingley W.G., Huganir R.L. Regulated subcellular distribution of the NR1 subunit of the NMDA receptor. Science. 269:1995;1734-1737.
18. Ellgaard L., Helenius A. Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4:2003;181-191.
19. Flores-Hernandez J., Cepeda C., Hernandez-Echeagaray E., Calvert C.R., Jokel E.S., Fienberg A.A., Greengard P., Levine M.S. Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J. Neurophysiol. 88:2002;3010-3020.
20. Gomez L.L., Alam S., Smith K.E., Horne E., Dell'Acqua M.L. Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin. J. Neurosci. 22:2002;7027-7044.
21. Goodnight J.A., Mischak H., Kolch W., Mushinski J.F. Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts. Isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J. Biol. Chem. 270:1995;9991-10001.
22. Grosshans D.R., Clayton D.A., Coultrap S.J., Browning M.D. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 5:2002;27-33.
23. Hall R.A., Soderling T.R. Differential surface expression and phosphorylation of the N-methyl-D-aspartate receptor subunits NR1 and NR2 in cultured hippocampal neurons. J. Biol. Chem. 272:1997;4135-4140.
24. Hirschberg K., Miller C.M., Ellenberg J., Presley J.F., Siggia E.D., Phair R.D., Lippincott-Schwartz J. Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J. Cell. Biol. 143:1998;1485-1503.
25. 2-terminal targeting motifs direct dual specificity A-kinase-anchoring protein 1 (D-AKAP1) to either mitochondria or endoplasmic reticulum. J. Cell Biol. 145:1999;951-959.
26. Huh K.H., Wenthold R.J. Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem. 274:1999;151-157.
27. Klauck T.M., Faux M.C., Labudda K., Langeberg L.K., Jaken S., Scott J.D. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science. 271:1996;1589-1592.
28. Kristensen B., Birkelund S., Jorgensen P.L. Trafficking of Na, K-ATPase fused to enhanced green fluorescent protein is mediated by protein kinase A or C. J. Membr. Biol. 191:2003;25-36.
29. Lan J.Y., Skeberdis V.A., Jover T., Grooms S.Y., Lin Y., Araneda R.C., Zheng X., Bennett M.V., Zukin R.S. Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 4:2001;382-390.
30. Lin D., Sterling H., Lerea K.M., Giebisch G., Wang W.H. Protein kinase C (PKC)-induced phosphorylation of ROMK1 is essential for the surface expression of ROMK1 channels. J. Biol. Chem. 277:2002;44278-44284.
31. Lin J.W., Wyszynski M., Madhavan R., Sealock R., Kim J.U., Sheng M. Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J. Neurosci. 18:1998;2017-2027.
32. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. Neurosci. 3:2002;175-190.
33. Ma D., Zerangue N., Raab-Graham K., Fried S.R., Jan Y.N., Jan L.Y. Diverse trafficking patterns due to multiple traffic motifs in G protein-activated inwardly rectifying potassium channels from brain and heart. Neuron. 33:2002;715-729.
34. Malenka R.C., Nicoll R.A. Long-term potentiation - a decade of progress? Science. 285:1999;1870-1874.
35. Malide D., Yewdell J.W., Bennink J.R., Cushman S.W. The export of major histocompatibility complex class i molecules from the endoplasmic reticulum of rat brown adipose cells is acutely stimulated by insulin. Mol. Biol. Cell. 12:2001;101-114.
36. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:2002;103-126.
37. Malinow R., Mainen Z.F., Hayashi Y. LTP mechanisms: from silence to four-lane traffic. Curr. Opin. Neurobiol. 10:2000;352-357.
38. Margeta-Mitrovic M., Jan Y.N., Jan L.Y. A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron. 27:2000;97-106.
39. McIlhinney R.A., Le Bourdelles B., Molnar E., Tricaud N., Streit P., Whiting P.J. Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology. 37:1998;1355-1367.
40. Nishimura N., Balch W.E. A di-acidic signal required for selective export from the endoplasmic reticulum. Science. 277:1997;556-558.
41. Okabe S., Miwa A., Okado H. Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. J. Neurosci. 19:1999;7781-7792.
42. Perez-Otano I., Schulteis C.T., Contractor A., Lipton S.A., Trimmer J.S., Sucher N.J., Heinemann S.F. Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J. Neurosci. 21:2001;1228-1237.
43. Prybylowski K., Fu Z., Losi G., Hawkins L.M., Luo J., Chang K., Wenthold R.J., Vicini S. Relationship between availability of NMDA receptor subunits and their expression at the synapse. J. Neurosci. 22:2002;8902-8910.
44. Quinlan E.M., Philpot B.D., Huganir R.L., Bear M.F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 2:1999;352-357.
45. Roche K.W., Standley S., McCallum J., Dune Ly C., Ehlers M.D., Wenthold R.J. Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4:2001;794-802.
46. Ron D., Jiang Z., Yao L., Vagts A., Diamond I., Gordon A. Coordinated movement of RACK1 with activated betaIIPKC. J. Biol. Chem. 274:1999;27039-27046.
47. Scott D.B., Blanpied T.A., Swanson G.T., Zhang C., Ehlers M.D. An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21:2001;3063-3072.
48. Sevier C.S., Weisz O.A., Davis M., Machamer C.E. Efficient export of the vesicular stomatitis virus G protein from the endoplasmic reticulum requires a signal in the cytoplasmic tail that includes both tyrosine-based and di-acidic motifs. Mol. Biol. Cell. 11:2000;13-22.
49. Shanks R.A., Steadman B.T., Schmidt P.H., Goldenring J.R. AKAP350 at the Golgi apparatus. I. Identification of a distinct Golgi apparatus targeting motif in AKAP350. J. Biol. Chem. 277:2002;40967-40972.
50. Sim A.T., Scott J.D. Targeting of PKA, PKC and protein phosphatases to cellular microdomains. Cell. Calcium. 26:1999;209-217.
51. Snyder G.L., Fienberg A.A., Huganir R.L., Greengard P. A dopamine/D1 receptor/protein kinase A/dopamine- and cAMP-regulated phosphoprotein (Mr 32 kDa)/protein phosphatase-1 pathway regulates dephosphorylation of the NMDA receptor. J. Neurosci. 18:1998;10297-10303.
52. Standley S., Roche K.W., McCallum J., Sans N., Wenthold R.J. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron. 28:2000;887-898.
53. Teasdale R.D., Jackson M.R. Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the golgi apparatus. Annu. Rev. Cell. Dev. Biol. 12:1996;27-54.
54. Tingley W.G., Ehlers M.D., Kameyama K., Doherty C., Ptak J.B., Riley C.T., Huganir R.L. Characterization of protein kinase A and protein kinase C phosphorylation of the N-methyl-D-aspartate receptor NR1 subunit using phosphorylation site-specific antibodies. J. Biol. Chem. 272:1997;5157-5166.
55. Turrigiano G.G., Nelson S.B. Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10:2000;358-364.
56. Wenthold R.J., Prybylowski K., Standley S., Sans N., Petralia R.S. Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43:2003;335-358.
57. Westphal R.S., Tavalin S.J., Lin J.W., Alto N.M., Fraser I.D., Langeberg L.K., Sheng M., Scott J.D. Regulation of NMDA receptors by an associated phosphatase-kinase signaling complex. Science. 285:1999;93-96.
58. Xia H., Hornby Z.D., Malenka R.C. An ER retention signal explains differences in surface expression of NMDA and AMPA receptor subunits. Neuropharmacology. 41:2001;714-723.
59. Yu W., Niwa T., Fukasawa T., Hidaka H., Senda T., Sasaki Y., Niki I. Synergism of protein kinase A, protein kinase C, and myosin light-chain kinase in the secretory cascade of the pancreatic beta-cell. Diabetes. 49:2000;945-952.
60. Zerangue N., Schwappach B., Jan Y.N., Jan L.Y. A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron. 22:1999;537-548.
61. Zerangue N., Malan M.J., Fried S.R., Dazin P.F., Jan Y.N., Jan L.Y., Schwappach B. Analysis of endoplasmic reticulum trafficking signals by combinatorial screening in mammalian cells. Proc. Natl. Acad. Sci. USA. 98:2001;2431-2436.