MAGI-1 modulates AMPA receptor synaptic localization and behavioral plasticity in response to prior experience

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Emtage, Lesley ^a   Chang, Howard ^a   Tiver, Rebecca ^a   Rongo, Christopher ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; AMPA RECEPTOR SUBUNIT GLR 1; AMPA RECEPTOR SUBUNIT GLR 2; CELL PROTEIN; ISOPROTEIN; MAGI 1 PROTEIN; MAGI 1L PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL PLASTICITY; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; EXPERIENCE; GLUTAMATERGIC SYNAPSE; HABITUATION; LOCOMOTION; LONG TERM MEMORY; MECHANICAL STIMULATION; NONHUMAN; PLASTICITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; STIMULUS RESPONSE; TOUCH; UBIQUITINATION;

EID: 84864286265     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004613     Document Type: Article

References (46)

1. Bredt DS, Nicoll RA (2003) AMPA receptor trafficking at excitatory synapses. Neuron 40: 361-379.
2. Malenka RC (2003) Synaptic plasticity and AMPA receptor trafficking. Ann N Y Acad Sci 1003: 1-11.
3. Dobrosotskaya I, Guy RK, James GL (1997) MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein-protein interaction domains. J Biol Chem 272: 31589-31597.
4. Hirao K, Hata Y, Ide N, TakeuchiM, Irie M, et al. (1998) A novel multiple PDZ domain-containing molecule interacting with N-methyl-D-aspartate receptors and neuronal cell adhesion proteins. J Biol Chem 273: 21105-21110.
5. Wu Y, Dowbenko D, Spencer S, Laura R, Lee J, et al. (2000) Interaction of the tumor suppressor PTEN/MMAC with a PDZ domain of MAGI3, a novel membrane-associated guanylate kinase. J Biol Chem 275: 21477-21485.
6. Hirao K, Hata Y, Yao I, Deguchi M, Kawabe H, et al. (2000) Three isoforms of synaptic scaffolding molecule and their characterization. Multimerization between the isoforms and their interaction with N-methyl-D-aspartate receptors and SAP90/PSD-95-associated protein. J Biol Chem 275: 2966-2972.
7. Iida J, Ishizaki H, Okamoto-Tanaka M, Kawata A, Sumita K, et al. (2007) SSCAM{ alpha} is a Scaffold to Mediate NMDA Receptor-dependent RhoA Activation in Dendrites. Mol Cell Biol.
8. Hart AC, Sims S, Kaplan JM (1995) Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378: 82-85.
9. Maricq AV, Peckol E, Driscoll M, Bargmann CI (1995) Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378: 78-81.
10. Mellem JE, Brockie PJ, Zheng Y, Madsen DM, Maricq AV (2002) Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36: 933-944.
11. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV (2001) Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 21: 1510-1522.
12. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, et al. (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5: 956-964.
13. Hills T, Brockie PJ, Maricq AV (2004) Dopamine and glutamate control arearestricted search behavior in Caenorhabditis elegans. J Neurosci 24: 1217-1225.
14. Chang HC, Rongo C (2005) Cytosolic tail sequences and subunit interactions are critical for synaptic localization of glutamate receptors. J Cell Sci 118: 1945-1956.
15. Giles AC, Rose JK, Rankin CH (2006) Investigations of learning and memory in Caenorhabditis elegans. Int Rev Neurobiol 69: 37-71.
16. Wicks SR, Rankin CH (1995) Integration of mechanosensory stimuli in Caenorhabditis elegans. J Neurosci 15: 2434-2444.
17. Rankin CH, Beck CD, Chiba CM (1990) Caenorhabditis elegans: a new model system for the study of learning and memory. Behav Brain Res 37: 89-92.
18. Beck CD, Rankin CH (1995) Heat shock disrupts long-term memory consolidation in Caenorhabditis elegans. Learn Mem 2: 161-177.
19. Rose JK, Kaun KR, Chen SH, Rankin CH (2003) GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J Neurosci 23: 9595-9599.
20. Rongo C, Whitfield CW, Rodal A, Kim SK, Kaplan JM (1998) LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell 94: 751-759.
21. Schaefer H, Rongo C (2006) KEL-8 is a substrate receptor for CUL3-dependent ubiquitin ligase that regulates synaptic glutamate receptor turnover. Mol Biol Cell 17: 1250-1260.
22. Dreier L, Burbea M, Kaplan JM (2005) LIN-23-mediated degradation of betacatenin regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Neuron 46: 51-64.
23. Glodowski DR, Chen CC, Schaefer H, Grant BD, Rongo C (2007) RAB-10 regulates glutamate receptor recycling in a cholesterol-dependent endocytosis pathway. Mol Biol Cell 18: 4387-4396.
24. Chun DK, McEwen JM, Burbea M, Kaplan JM (2008) UNC-108/Rab2 Regulates Postendocytic Trafficking in Caenorhabditis elegans. Mol Biol Cell 19: 2682-2695.
25. Burbea M, Dreier L, Dittman JS, Grunwald ME, Kaplan JM (2002) Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35: 107-120.
26. Rose JK, Kaun KR, Rankin CH (2002) A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to longterm memory in Caenorhabditis elegans. Learn Mem 9: 130-137.
27. Zheng Y, Brockie PJ, Mellem JE, Madsen DM, Maricq AV (1999) Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24: 347-361.
28. Firestein BL, Brenman JE, Aoki C, Sanchez-Perez AM, El-Husseini AE, et al. (1999) Cypin: a cytosolic regulator of PSD-95 postsynaptic targeting. Neuron 24: 659-672.
29. Shim J, Umemura T, Nothstein E, Rongo C (2004) The unfolded protein response regulates glutamate receptor export from the endoplasmic reticulum. Mol Biol Cell 15: 4818-4828.
30. Firestein BL, Rongo C (2001) DLG-1 is a MAGUK similar to SAP97 and is required for adherens junction formation. Mol Biol Cell 12: 3465-3475.
31. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2000) Effectiveness of specific RNA-mediated interference through ingested doublestranded RNA in Caenorhabditis elegans. Genome Biology 2(1): 1-10.
32. Brockie PJ, Mellem JE, Hills T, Madsen DM, Maricq AV (2001) The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31: 617-630.
33. Chalfie M, Sulston J (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82: 358-370.
34. Lai CC, Hong K, Kinnell M, Chalfie M, Driscoll M (1996) Sequence and transmembrane topology of MEC-4, an ion channel subunit required for mechanotransduction in Caenorhabditis elegans. J Cell Biol 133: 1071-1081.
35. Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17: 8259-8269.
36. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242.
37. Walker CS, Brockie PJ, Madsen DM, Francis MM, Zheng Y, et al. (2006) Reconstitution of invertebrate glutamate receptor function depends on stargazin-like proteins. Proc Natl Acad Sci U S A 103: 10781-10786.
38. Zhao B, Khare P, Feldman L, Dent JA (2003) Reversal frequency in Caenorhabditis elegans represents an integrated response to the state of the animal and its environment. J Neurosci 23: 5319-5328.
39. Tsalik EL, Hobert O (2003) Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J Neurobiol 56: 178-197.
40. Gray JM, Hill JJ, Bargmann CI (2005) A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A 102: 3184-3191.
41. Chen BL, Hall DH, Chklovskii DB (2006) Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci U S A 103: 4723-4728.
42. White JG, Southgate E, Thomson JN, Brenner S (1984) The structure of the nervous system of the nematod caenorhabditis elegans. Philosophical Transactions of the Royal Society, London B 314: 1-340.
43. Kindt KS, Quast KB, Giles AC, De S, Hendrey D, et al. (2007) Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 55: 662-676.
44. Mendoza-Topaz C, Urra F, Barria R, Albornoz V, Ugalde D, et al. (2008) DLGS97/SAP97 is developmentally upregulated and is required for complex adult behaviors and synapse morphology and function. J Neurosci 28: 304-314.
45. McLaughlin M, Hale R, Ellston D, Gaudet S, Lue RA, et al. (2002) The distribution and function of alternatively spliced insertions in hDlg. J Biol Chem 277: 6406-6412.
46. Schluter OM, Xu W, Malenka RC (2006) Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51: 99-111.