Coordinated action of NSF and PKC regulates GABAB receptor signaling efficacy

EMBO Journal

Volumn 25, Issue 12, 2006, Pages 2698-2709

  Pontier, Stéphanie M ^a   Lahaie, Nicolas ^a   Ginham, Rachel ^b   St Gelais, Fannie ^c   Bonin, Hélène ^a   Bell, David J ^d   Flynn, Helen ^d   Trudeau, Louis Eric ^c   McIlhinney, Jeffrey ^b   White, Julia H ^d   Bouvier, Michel ^a  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MRC Anat Neuropharmacology Unit   (United Kingdom)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Desensitization; GABAB; Heterodimer; NSF; PKC

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; N ETHYLMALEIMIDE SENSITIVE FACTOR; PEPTIDE; PROTEIN KINASE C; PROTEIN TAT PEP 27; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHO CELL; COMPLEX FORMATION; CONTROLLED STUDY; DESENSITIZATION; HIPPOCAMPUS; MEMBRANE TRANSPORT; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNAPTOSOME;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; DIMERIZATION; GTP-BINDING PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; N-ETHYLMALEIMIDE-SENSITIVE PROTEINS; NEURONS; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; RECEPTORS, GABA-B; SIGNAL TRANSDUCTION; THERMODYNAMICS;

EID: 33745522817     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601157     Document Type: Article

References (49)

1. Barclay JW, Craig TJ, Fisher RJ, Ciufo LF, Evans GJ, Morgan A, Burgoyne RD (2003) Phosphorylation of Munc18 by protein kinase C regulates the kinetics of exocytosis. J Biol Chem 278: 10538-10545
2. Becher A, Green A, Ige AO, Wise A, White JH, McIlhinney RA (2004) Ectopically expressed gamma-aminobutyric acid receptor B is functionally down-regulated in isolated lipid raft-enriched membranes. Biochem Biophys Res Commun 321: 981-987
3. Becker-Hapak M, McAllister SS, Dowdy SF (2001) TAT-mediated protein transduction into mammalian cells. Methods 24: 247-256
4. Blumberg PM (1991) Complexities of the protein kinase C pathway. Mol Carcinog 4: 339-344
5. Bomberger JM, Parameswaran N, Hall CS, Aiyar N, Spielman WS (2005) Novel function for receptor activity-modifying proteins (RAMPs) in post-endocytic receptor trafficking. J Biol Chem 280: 9297-9307
6. Cong M, Perry SJ, Hu LA, Hanson PI, Claing A, Lefkowitz RJ (2001) Binding of the beta2 adrenergic receptor to N-ethylmaleimide-sensitive factor regulates receptor recycling. J Biol Chem 276: 45145-45152
7. Couve A, Filippov AK, Connolly CN, Bettler B, Brown DA, Moss SJ (1998) Intracellular retention of recombinant GABAB receptors. J Biol Chem 273: 26361-26367
8. Couve A, Kittler JT, Uren JM, Calver AR, Pangalos MN, Walsh FS, Moss SJ (2001) Association of GABA(B) receptors and members of the 14-3-3 family of signaling proteins. Mol Cell Neurosci 17: 317-328
9. Couve A, Restituito S, Brandon JM, Charles KJ, Bawagan H, Freeman KB, Pangalos MN, Calver AR, Moss SJ (2004) Marlin-1, a novel RNA-binding protein associates with GABA receptors. J Biol Chem 279: 13934-13943
10. Couve A, Thomas P, Calver AR, Hirst WD, Pangalos MN, Walsh FS, Smart TG, Moss SJ (2002) Cyclic AMP-dependent protein kinase phosphorylation facilitates GABA(B) receptor-effector coupling. Nat Neurosci 5: 415-424
11. Dutar P, Nicoll RA (1988) Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties. Neuron 1: 585-591
12. Fairfax BP, Pitcher JA, Scott MG, Calver AR, Pangalos MN, Moss SJ, Couve A (2004) Phosphorylation and chronic agonist treatment atypically modulate GABAB receptor cell surface stability. J Biol Chem 279: 12565-12573
13. Galvez T, Duthey B, Kniazeff J, Blahos J, Rovelli G, Bettler B, Prezeau L, Pin JP (2001) Allosteric interactions between GB1 and GB2 subunits are required for optimal GABA(B) receptor function. EMBO J 20: 2152-2159
14. Gonzalez-Maeso J, Wise A, Green A, Koenig JA (2003) Agonist-induced desensitization and endocytosis of heterodimeric GABAB receptors in CHO-K1 cells. Eur J Pharmacol 481: 15-23
15. Grunewald S, Schupp BJ, Ikeda SR, Kuner R, Steigerwald F, Kornau HC, Kohr G (2002) Importance of the gamma-aminobutyric acid(B) receptor C-termini for G-protein coupling. Mol Pharmacol 61: 1070-1080
16. Hanley JG, Khatri L, Hanson PI, Ziff EB (2002) NSF ATPase and alpha-/beta-SNAPs disassemble the AMPA receptor-PICK1 complex. Neuron 34: 53-67
17. Heydorn A, Sondergaard BP, Hadrup N, Holst B, Haft CR, Schwartz TW (2004) Distinct in vitro interaction pattern of dopamine receptor subtypes with adaptor proteins involved in post-endocytotic receptor targeting. FEBS Lett 556: 276-280
18. Jones KA, Borowsky B, Tamm JA, Craig DA, Durkin MM, Dai M, Yao WJ, Johnson M, Gunwaldsen C, Huang LY, Tang C, Shen Q, Salon JA, Morse K, Laz T, Smith KE, Nagarathnam D, Noble SA, Branchek TA, Gerald C (1998) GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 396: 674-679
19. Kammerer RA, Frank S, Schulthess T, Landwehr R, Lustig A, Engel J (1999) Heterodimerization of a functional GABAB receptor is mediated by parallel coiled-coil alpha-helices. Biochemistry 38: 13263-13269
20. Kaupmann K, Malitschek B, Schuler V, Heid J, Froestl W, Beck P, Mosbacher J, Bischoff S, Kulik A, Shigemoto R, Karschin A, Bettler B (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396: 683-687
21. Kuner R, Kohr G, Grunewald S, Eisenhardt G, Bach A, Kornau HC (1999) Role of heteromer formation in GABAB receptor function. Science 283: 74-77
22. Lee SH, Simonetta A, Sheng M (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43: 221-236
23. Lin RC, Scheller RH (2000) Mechanisms of synaptic vesicle exocytosis. Annu Rev Cell Dev Biol 16: 19-49
24. Lopez-Bendito G, Shigemoto R, Kulik A, Vida I, Fairen A, Lujan R (2004) Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14: 836-848
25. Margeta-Mitrovic M, Jan YN, Jan LY (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27: 97-106
26. Margeta-Mitrovic M, Jan YN, Jan LY (2001) Function of GB1 and GB2 subunits in G protein coupling of GABA(B) receptors. Proc Natl Acad Sci USA 98: 14649-14654
27. Matveeva EA, Whiteheart SW, Vanaman TC, Slevin JT (2001) Phosphorylation of the N-ethylmaleimide-sensitive factor is associated with depolarization- dependent neurotransmitter release from synaptosomes. J Biol Chem 276: 12174-12181
28. Morgan A, Burgoyne RD (2004) Membrane traffic: controlling membrane fusion by modifying NSF. Curr Biol 14: R968-R970
29. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, Collingridge GL, Nakanishi S, Henley JM (1998) NSF binding to GluR2 regulates synaptic transmission. Neuron 21: 87-97
30. Noel J, Ralph GS, Pickard L, Williams J, Molnar E, Uney JB, Collingridge GL, Henley JM (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23: 365-376
31. Osten P, Srivastava S, Inman GJ, Vilim FS, Khatri L, Lee LM, States BA, Einheber S, Milner TA, Hanson PI, Ziff EB (1998) The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and a. Neuron 21: 99-110
32. Perez JL, Khatri L, Chang C, Srivastava S, Osten P, Ziff EB (2001) PICK1 targets activated protein kinase Calpha to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J Neurosci 21: 5417-5428
33. Perroy J, Adam L, Qanbar R, Chenier S, Bouvier M (2003) Phosphorylation-independent desensitization of GABA(B) receptor by GRK4. EMBO J 22: 3816-3824
34. Robbins MJ, Calver AR, Filippov AK, Hirst WD, Russell RB, Wood MD, Nasir S, Couve A, Brown DA, Moss SJ, Pangalos MN (2001) GABA(B2) is essential for g-protein coupling of the GABA(B) receptor heterodimer. J Neurosci 21: 8043-8052
35. Sallese M, Salvatore L, D'Urbano E, Sala G, Storto M, Launey T, Nicoletti F, Knopfel T, De Blasi A (2000) The G-protein-coupled receptor kinase GRK4 mediates homologous desensitization of metabotropic glutamate receptor 1. FASEB J 14: 2569-2580
36. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105: 331-343
37. Sollner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE (1993) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75: 409-418
38. Song I, Kamboj S, Xia J, Dong H, Liao D, Huganir RL (1998) Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors. Neuron 21: 393-400
39. Steinberg JP, Huganir RL, Linden DJ (2004) N-ethylmaleimide-sensitive factor is required for the synaptic incorporation and removal of AMPA receptors during cerebellar long-term depression. Proc Natl Acad Sci USA 101: 18212-18216
40. Thiyagarajan MM, Stracquatanio RP, Pronin AN, Evanko DS, Benovic JL, Wedegaertner PB (2004) A predicted amphipathic helix mediates plasma membrane localization of GRK5. J Biol Chem 279: 17989-17995
41. Thompson SM, Gahwiler BH (1992) Comparison of the actions of baclofen at pre- and postsynaptic receptors in the rat hippocampus in vitro. J Physiol 451: 329-345
42. Tosetti P, Bakels R, Colin-Le Brun I, Ferrand N, Gaiarsa JL, Caillard O (2004) Acute desensitization of presynaptic GABAB-mediated inhibition and induction of epileptiform discharges in the neonatal rat hippocampus. Eur J Neurosci 19: 3227-3234
43. Tremblay E, Ben Ari Y, Roisin MP (1995) Different GABAB-mediated effects on protein kinase C activity and immunoreactivity in neonatal and adult rat hippocampal slices. J Neurochem 65: 863-870
44. Virlon B, Firsov D, Cheval L, Reiter E, Troispoux C, Guillou F, Elalouf JM (1998) Rat G protein-coupled receptor kinase GRK4: identification, functional expression, and differential tissue distribution of two splice variants. Endocrinology 139: 2784-2795
45. White JH, McIllhinney RA, Wise A, Ciruela F, Chan WY, Emson PC, Billinton A, Marshall FH (2000) The GABAB receptor interacts directly with the related transcription factors CREB2 and ATFx. Proc Natl Acad Sci U S A 97: 13967-13972
46. White JH, Wise A, Main MJ, Green A, Fraser NJ, Disney GH, Barnes AA, Emson P, Foord SM, Marshall FH (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396: 679-682
47. White JH, Wise A, Marshall FH (2002) Heterodimerization of gamma-aminobutyric acid B receptor subunits as revealed by the yeast two-hybrid system. Methods 27: 301-310
48. Whiteheart SW, Matveeva EA (2004) Multiple binding proteins suggest diverse functions for the N-ethylmaleimide sensitive factor. J Struct Biol 146: 32-43
49. Zou S, Li L, Pei L, Vukusic B, Van Tol HH, Lee FJ, Wan Q, Liu F (2005) Protein-protein coupling/uncoupling enables dopamine D2 receptor regulation of AMPA receptor-mediated excitotoxicity. J Neurosci 25: 4385-4395