GABARAP: Lessons for synaptogenesis

Neuroscientist

Volumn 9, Issue 3, 2003, Pages 205-216

  Coyle, Joseph E ^a   Nikolov, Dimitar B ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

GABAA receptors; GABARAP; Receptor trafficking; Synapse formation

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ASSOCIATED PROTEIN; ADAPTOR PROTEIN; GEPHYRIN; NEUROTRANSMITTER RECEPTOR; POSTSYNAPTIC RECEPTOR; RECEPTOR PROTEIN; TUBULIN; UNCLASSIFIED DRUG;

CRYSTAL STRUCTURE; HUMAN; INTRACELLULAR TRANSPORT; MICROTUBULE; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; REVIEW; STEADY STATE; SYNAPTOGENESIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CYTOSKELETON; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; SYNAPSES;

EID: 0038513935     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/1073858403009003013     Document Type: Review

References (70)

1. Barnes EM Jr. 2000. Intracellular trafficking of GABA(A) receptors. Life Sci 66(12):1063-70.
2. Bavro VN, Sola M, Bracher A, Kneussel M, Betz H, Weissenhorn W. 2002. Crystal structure of the GABA(A)-receptor-associated protein, GABARAP. EMBO Rep 3(2):183-9.
3. Chang Y, Wang R, Barot S, Weiss DS. 1996. Stoichiometry of a recombinant GABAA receptor. J Neurosci 16:5415-24.
4. Chen L, Wang H, Vicini S, Olsen RW. 2000. The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci U S A 97:11557-62.
5. Colledge M, Froehner SC. 1998. To muster a cluster: anchoring neurotransmitter receptors at synapses. Proc Natl Acad Sci U S A 95:3341-3.
6. Coyle JE, Qamar S, Rajashankar KR, Nikolov DB. 2002. Structure of GABARAP in two conformations: implications for GABA(A) receptor localization and tubulin binding. Neuron 33(1):63-74.
7. Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, and others. 1999. Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2(9):833-9.
8. Duan DR, Pause A, Burgess WH, Aso T, Chen DY, Garrett KP, and others. 1995. Inhibition of transcription elongation by the VHL tumor suppressor protein. Science 269:1402-6.
9. Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B. 1998. Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1:563-71.
10. Farrar SJ, Whiting PJ, Bonnert TP, McKernan RM. 1999. Stoichiometry of a ligand-gated ion channel determined by fluorescence energy transfer. J Biol Chem 274:10100-4.
11. Feng G, Tintrup H, Kirsch J, Nichol MC, Kuhse J, Betz H, and others. 1998. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282:1321-4.
12. Gigant B, Curmi PA, Martin-Barbey C, Charbaut E, Lachkar S, Lebeau L, and others. 2000. The 4 A X-ray structure of a tubulin:stathmin-like domain complex. Cell 102(6):809-16.
13. Green F, O'Hare T, Blackwell A, Enns CA. 2002. Association of human transferrin receptor with GABARAP. FEBS Lett 518(1-3):101-6.
14. Haas A. 1998. NSF - fusion and beyond. Trends Cell Biol 8(12):471-3.
15. Hanley JG, Koulen P, Bedford F, Gordon-Weeks PR, Moss SJ. 1999. The protein MAP-1B links GABA(C) receptors to the cytoskeleton at retinal synapses. Nature 397:66-9.
16. Huang L, Hofer F, Martin GS, Kim SH. 1998. Structural basis for the interaction of Ras with RalGDS. Nat Struct Biol 5:422-6.
17. Huang WP, Scott SV, Kim J, Klionsky DJ. 2000. The itinerary of a vesicle component, Aut7p/Cvt5p, terminates in the yeast vacuole via the autophagy/Cvt pathways. J Biol Chem 275:5845-51.
18. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, and others. 2000. A ubiquitin-like system mediates protein lipidation. Nature 408:488-92.
19. Janin J, Chothia C. 1990. The structure of protein-protein recognition sites. J Biol Chem 265:16027-30.
20. Kanematsu T, Jang IS, Yamaguchi T, Nagahama H, Yoshimura K, Hidaka K, and others. 2002. Role of the PLC-related, catalytically inactive protein p130 in GABA(A) receptor function. EMBO J 21(5):1004-11.
21. Kennedy MB. 2000. Sticking together. Proc Natl Acad Sci U S A 97(21):11135-6.
22. Kim J, Huang WP, Klionsky DJ. 2001. Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J Cell Biol 152:51-64.
23. Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, and others. 2000. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151:263-76.
24. Kirsch J, Wolters I, Triller A, Betz H. 1993. Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366:745-8.
25. Kishida T, Stackhouse TM, Chen F, Lerman MI, Zbar B. 1995. Cellular proteins that bind the von Hippel-Lindau disease gene product: mapping of binding domains and the effect of missense mutations. Cancer Res 55:4544-8.
26. Kittler JT, Rostaing P, Schiavo G, Fritschy JM, Olsen R, Triller A, and others. 2001. The subcellular distribution of gabarap and its ability to interact with NSF suggest a role for this protein in the intracellular transport of gaba(a) receptors. Mol Cell Neurosci 18:13-25.
27. Klionsky DJ, Emr SD. 2000. Autophagy as a regulated pathway of cellular degradation. Science 290:1717-21.
28. Kneussel M. 2002. Dynamic regulation of GABA(A) receptors at synaptic sites. Brain Res Brain Res Rev 39(1):74-83.
29. Kneussel M, Brandstatter JH, Laube B, Stahl S, Muller U, Betz H. 1999. Loss of postsynaptic GABA(A) receptor clustering in gephyrin-deficient mice. J Neurosci 19:9289-97.
30. Kneussel M, Haverkamp S, Fuhrmann JC, Wang H, Wassle H, Olsen RW, and others. 2000. The gamma-aminobutyric acid type A receptor (GABAAR)-associated protein GABARAP interacts with gephyrin but is not involved in receptor anchoring at the synapse. Proc Natl Acad Sci U S A 97:8594-9.
31. Knight D, Harris R, McAlister MS, Phelan JP, Geddes S, Moss SJ, and others. 2002. The X-ray crystal structure and putative ligand-derived peptide binding properties of gamma-aminobutyric acid receptor type A receptor-associated protein. J Biol Chem 277(7):5556-61.
32. Kreusch A, Pfaffinger PJ, Stevens CF, Choe S. 1998. Crystal structure of the tetramerization domain of the Shaker potassium channel. Nature 392(6679):945-8.
33. Lang T, Schaeffeler E, Bernreuther D, Bredschneider M, Wolf DH, Thumm M. 1998. Aut2p and Aut7p, two novel microtubule-associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J 17:3597-607.
34. Legesse-Miller A, Sagiv Y, Porat A, Elazar Z. 1998. Isolation and characterization of a novel low molecular weight protein involved in intra-Golgi traffic. J Biol Chem 273:3105-9.
35. Littauer UZ, Giveon D, Thierauf M, Ginzburg I, Ponstingl H. 1986. Common and distinct tubulin binding sites for microtubule-associated proteins. Proc Natl Acad Sci U S A 83:7162-6.
36. Macdonald RL, Olsen RW. 1994. GABAA receptor channels. Annu Rev Neurosci 17:569-602.
37. Maimone MM, Enigk RE. 1999. The intracellular domain of the nicotinic acetylcholine receptor alpha subunit mediates its coclustering with rapsyn. Mol Cell Neurosci 14:340-54.
38. Mann SS, Hammarback JA. 1994. Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B. J Biol Chem 269:11492-7.
39. Marya PK, Syed Z, Fraylich PE, Eagles PA. 1994. Kinesin and tau bind to distinct sites on microtubules. J Cell Sci 107:339-44.
40. McDonald PH, Cote NL, Lin FT, Premont RT, Pitcher JA, and Lefkowitz RJ. 1999. Identification of NSF as a beta-arrestin1-binding protein. Implications for beta2-adrenergic receptor regulation. J Biol Chem 274:10677-80.
41. Meyer G, Kirsch J, Betz H, Langosch D. 1995. Identification of a gephyrin binding motif on the glycine receptor beta subunit. Neuron 15:563-72.
42. Moss SJ, Smart TG. 2001. Constructing inhibitory synapses. Nat Rev Neurosci 2:240-50.
43. Nassar N, Horn G, Herrmann C, Scherer A, McCormick F, Wittinghofer A. 1995. The 2.2 A crystal structure of the Ras-binding domain of the serine/threonine kinase c-Raf1 in complex with Rap1A and a GTP analogue. Nature 375:554-60.
44. Nishimune A, Isaac JT, Molnar E, Noel J, Nash SR, Tagaya M, and others. 1998. NSF binding to GluR2 regulates synaptic transmission. Neuron 21:87-97.
45. Nogales E, Whittaker M, Milligan RA, Downing KH. 1999. High-resolution model of the microtubule. Cell 96:79-88.
46. Nymann-Andersen J, Wang H, Chen L, Kittler JT, Moss SJ, Olsen RW. 2002. Subunit specificity and interaction domain between GABA(A) receptor-associated protein (GABARAP) and GABA(A) receptors. J Neurochem 80(5):815-23.
47. Okazaki N, Yan J, Yuasa S, Ueno T, Kominami E, Masuho Y, and others. 2000. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res 85:1-12.
48. Ortells MO, Lunt GG. 1995. Evolutionary history of the ligand-gated ion-channel superfamily of receptors. Trends Neurosci 18:121-7.
49. Osten P, Srivastava S, Inman GJ, Vilim FS, Khatri L, Lee LM, and others. 1998. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and alpha- and beta-SNAPs. Neuron 21:99-110.
50. Passafaro M, Sheng M. 1999. Synaptogenesis: the MAP location of GABA receptors. Curr Biol 9(7):R261-3.
51. Paz Y, Elazar Z, Fass D. 2000. Structure of GATE-16, membrane transport modulator and mammalian ortholog of autophagocytosis factor Aut7p. J Biol Chem 275:25445-50.
52. Phillips WD, Froehner SC. 2002. GABARAP and GABA(A) receptor clustering. Neuron 33(1):4-6.
53. Phillips WD, Maimone MM, Merlie JP. 1991. Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering. J Cell Biol 115:1713-23.
54. Ramarao MK, Bianchetta MJ, Lanken J, Cohen JB. 2001. Role of rapsyn tetratricopeptide repeat and coiled-coil domains in self-association and nicotinic acetylcholine receptor clustering. J Biol Chem 276:7475-83.
55. Ramarao MK, Cohen JB. 1998. Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn. Proc Natl Acad Sci U S A 95:4007-12.
56. Sagiv Y, Legesse-Miller A, Porat A, Elazar Z. 2000. GATE-16, a membrane transport modulator, interacts with NSF and the Golgi v-SNARE GOS-28. EMBO J 19:1494-504.
57. Scannevin RH, Huganir RL. 2000. Postsynaptic organization and regulation of excitatory synapses. Nat Rev Neurosci (2):133-41.
58. Schofield PR, Darlison MG, Fujita N, Burt DR, Stephenson FA, Rodriguez H, and others. 1987. Sequence and functional expression of the GABA A receptor shows a ligand-gated receptor superfamily. Nature 328:221-7.
59. Serrano L, de la Torre J, Maccioni RB, Avila J. 1984. Involvement of the carboxyl-terminal domain of tubulin in the regulation of its assembly. Proc Natl Acad Sci U S A 81:5989-93.
60. Sheng M, Pak DT. 2000. Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu Rev Physiol 62:755-78.
61. 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.
62. Stangler T, Mayr LM, Willbold D. 2002. Solution structure of human GABA(A) receptor-associated protein GABARAP: implications for biological function and its regulation. J Biol Chem 277(16):13363-6.
63. Stebbins CE, Kaelin WG Jr, Pavletich NP. 1999. Structure of the VHL-ElonginC-ElonginB complex: implications for VHL tumor suppressor function. Science 284:455-61.
64. Tanida I, Tanida-Miyake E, Komatsu M, Ueno T, Kominami E. 2002. Human Apg3p/Autlp homologue is an authentic E2 enzyme for multiple substrates, GATE-16, GABARAP, and MAP-LC3, and facilitates the conjugation of hApg12p to hApg5p. J Biol Chem 277(16):13739-44.
65. Tanida I, Tanida-Miyake E, Ueno T, Kominami E. 2001. The human homolog of Saccharomyces cerevisiae Apg7p is a protein-activating enzyme for multiple substrates including human Apg12p, GATE- 16, GABARAP, and MAP-LC3. J Biol Chem 276:1701-6.
66. Tretter V, Ehya N, Fuchs K, Sieghart W. 1997. Stoichiometry and assembly of a recombinant GABAA receptor subtype. J Neurosci 17:2728-37.
67. Unwin N. 1998. The nicotinic acetylcholine receptor of the Torpedo electric ray. J Struct Biol 121:181-90.
68. Wallon G, Rappsilber J, Mann M, Serrano L. 2000. Model for stathmin/OP18 binding to tubulin. EMBO J 19(2):213-22,
69. Wang H, Bedford FK, Brandon NJ, Moss SJ, Olsen RW. 1999. GABA(A)-receptor-associated protein links GABA(A) receptors and the cytoskeleton. Nature 397:69-72.
70. Wang H, Olsen RW. 2000. Binding of the GABA(A) receptor-associated protein (GABARAP) to microtubules and microfilaments suggests involvement of the cytoskeleton in GABARAPGABA(A) receptor interaction. J Neurochem 75:644-55.