Actin/α-actinin-dependent transport of AMPA receptors in dendritic spines: Role of the PDZ-LIM protein RIL

Journal of Neuroscience

Volumn 24, Issue 39, 2004, Pages 8584-8594

  Schulz, Torsten W ^a,e   Nakagawa, Terunaga ^b   Licznerski, Pawel ^a   Pawlak, Verena ^a   Kolleker, Alexander ^a   Rozov, Andrei ^a,c   Kim, Jinhyun ^a,d   Dittgen, Tanjew ^a   Köhr, Georg ^a   Sheng, Morgan ^b   Seeburg, Peter H ^a   Osten, Pavel ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d NATIONAL INSTITUTES OF HEALTH   (United States)

^e Responsif GmbH   (Germany)

Author keywords

actinin actin cytoskeleton; AMPA receptor; Dendritic spine; LIM domain; PDZ domain; Transport

Indexed keywords

ACTIN; ALPHA ACTININ; AMPA RECEPTOR; CYTOSKELETON PROTEIN; GLUTAMATE RECEPTOR; LIM PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CARBOXY TERMINAL SEQUENCE; DENDRITIC SPINE; ENDOSOME; FOREBRAIN; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNODETECTION; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RAT; SYNAPTIC TRANSMISSION;

ACTININ; ACTINS; AMINO ACID MOTIFS; ANIMALS; CELLS, CULTURED; DENDRITIC SPINES; DNA-BINDING PROTEINS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; HUMANS; NEURONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECOMBINANT FUSION PROTEINS;

EID: 4744343498     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2100-04.2004     Document Type: Article

References (48)

1. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423-2436.
2. Bach I (2000) The LIM domain: regulation by association. Mech Dev 91:5-17.
3. Baron MD, Davison MD, Jones P, Critchley DR (1987) The structure and function of alpha-actinin. Biochem Soc Trans 15:796-798.
4. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartley M, Deneris E, Maron C, Heinemann S (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249:1033-1037.
5. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576.
6. Buckley K, Kelly RB (1985) Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J Cell Biol 100:1284-1294.
7. Carlin RK, Grab DJ, Cohen RS, Siekevitz P (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86:831-845.
8. Carroll RC, Lissin DV, von Zastrow M, Nicoll RA, Malenka RC (1999) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2:454-460.
9. Cuppen E, Gerrits H, Pepers B, Wieringa B, Hendriks W (1998) PDZ motifs in PTP-BL and RIL bind to internal protein segments in the LIM domain protein RIL. Mol Biol Cell 3:671-683.
10. Cuppen E, van Ham M, Wansink DG, de Leeuw A, Wieringa B, Hendriks W (2000) The zyxin-related protein TRIP6 interacts with PDZ motifs in the adaptor protein RIL and the protein tyrosine phosphatase PTP-BL. Eur J Cell Biol 79:283-293.
11. Djinovic-Carugo K, Gautel M, Ylanne J, Young P (2002) The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett 513:119-123.
12. Dryga SA, Dryga OA, Schlesinger S (1997) Identification of mutations in a Sindbis virus variant able to establish persistent infection in BHK cells: the importance of a mutation in the nsP2 gene. Virology 228:74-83.
13. Fifkova E, Delay RJ (1982) Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 95:345-350.
14. Gruenberg J, Maxfield FR (1995) Membrane transport in the endocytic pathway. Curr Opin Cell Biol 7:552-563.
15. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287:2262-2267.
16. Herb A, Wisden W, Catania MV, Marechal D, Dresse A, Seeburg PH (1997) Prominent dendritic localization in forebrain neurons of a novel mRNA and its product, dendrin. Mol Cell Neurosci 8:367-374.
17. Heynen AJ, Quinlan EM, Bae DC, Bear MF (2000) Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron 28:527-536.
18. Keinanen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMP A-selective glutamate receptors. Science 249:556-560.
19. Kiess M, Scharm B, Aguzzi A, Hajnal A, Klemenz R, Schwarte-Waldhoff I, Schafer R (1995) Expression of ril, a novel LIM domain gene, is down-regulated in Hras-transformed cells and restored in phenotypic revertants. Oncogene 10:61-68.
20. Kim CH, Lisman JE (1999) A role of actin filament in synaptic transmission and long-term potentiation. J Neurosci 19:4314-4324.
21. Kim J, Dittgen T, Nimmerjahn A, Waters J, Pawlak V, Helmchen F, Schlesinger S, Seeburg PH, Osten P (2004) Sindbis vector SINrep(nsP2S726): a tool for rapid heterologous expression with attenuated cytotoxicity in neurons. J Neurosci Methods 133:81-90.
22. Kuroda S, Tokunaga C, Kiyohara Y, Higuchi O, Konishi H, Mizuno K, Gill GN, Kikkawa U (1996) Protein-protein interaction of zinc finger LIM domains with protein kinase C. J Biol Chem 271:31029-31032.
23. Lee SH, Liu L, Wang YT, Sheng M (2002) Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron 36:661-674.
24. Lu W, Man H, Ju W, Trimble WS, MacDonald JF, Wang YT (2001) Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron 29:243-254.
25. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126.
26. Matsuda S, Launey T, Mikawa S, Hirai H (2000) Disruption of AMPA receptor GluR2 clusters following long-term depression induction in cerebellar Purkinje neurons. EMBO J 19:2765-2774.
27. Matus A, Ackermann M, Pehling G, Byers HR, Fujiwara K (1982) High actin concentrations in brain dendritic spines and postsynaptic densities. Proc Natl Acad Sci USA 79:7590-7594.
28. 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- and b-SNAPs. Neuron 21:99-110.
29. Osten P, Khatri L, Perez JL, Kohr G, Giese G, Daly C, Schulz TW, Wensky A, Lee LM, Ziff EB (2000) Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron 27:313-325.
30. Passafaro M, Piech V, Sheng M (2001) Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat Neurosci 4:917-926.
31. Pufall MA, Graves BJ (2002) Autoinhibitory domains: modular effectors of cellular regulation. Annu Rev Cell Dev Biol 18:421-462.
32. Shen L, Liang F, Walensky LD, Huganir RL (2000) Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1N-linked actin cytoskeletal association. J Neurosci 20:7932-7940.
33. Sheng M, Lee SH (2001) AMPA receptor trafficking and the control of synaptic transmission. Cell 105:825-828.
34. 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.
35. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R (1999) Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284:1811-1816.
36. Song I, Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588.
37. Srivastava S, Osten P, Vilim FS, Khatri L, Inman G, States B, Daly C, DeSouza S, Abagyan R, Valtschanoff JG, Weinberg RJ, Ziff EB (1998) Novel anchorage of GluR2/3 to the postsynaptic density by the AMPA receptor-binding protein ABP. Neuron 21:581-591.
38. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
39. Takahashi T, Svoboda K, Malinow R (2003) Experience strengthening transmission by driving AMPA receptors into synapses. Science 299:1585-1588.
40. Vallenius T, Scharm B, Vesikansa A, Luukko K, Schafer R, Makela TP (2004) The PDZ-LIM protein RIL modulates actin stress fiber turnover and enhances the association of alpha-actinin with F-actin. Exp Cell Res 293:117-128.
41. Vandekerckhove J (1990) Actin-binding proteins. Curr Opin Cell Biol 2:41-50.
42. Wang YT, Linden DJ (2000) Expression of cerebellar long-terra depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25:635-647.
43. Wenthold RJ, Petralia RS, Blahos J, II, Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982-1989.
44. Wu R, Durick K, Songyang Z, Cantley LC, Taylor SS, Gill GN (1996) Specificity of LIM domain interactions with receptor tyrosine kinases. J Biol Chem 271:15934-15941.
45. Wu RY, Gill GN (1994) LIM domain recognition of a tyrosine-containing tight turn. J Biol Chem 269:25085-25090.
46. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M (1997) Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385:439-442.
47. Wyszynski M, Kharazia V, Shanghvi R, Rao A, Beggs AH, Craig AM, Weinberg R, Sheng M (1998) Differential regional expression and ultrastructural localization of α-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain. J Neurosci 18:1383-1392.
48. Zhou Q, Xiao M, Nicoll RA (2001) Contribution of cytoskeleton to the internalization of AMPA receptors. Proc Natl Acad Sci USA 98:1261-1266.