Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation

Nature Neuroscience

Volumn 11, Issue 4, 2008, Pages 457-466

  Correia, Susana S ^a   Bassani, Silvia ^b   Brown, Tyler C ^a   Lisé, Marie France ^c   Backos, Donald S ^a   El Husseini, Alaa ^c   Passafaro, Maria ^b   Esteban, José A ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; MOLECULAR MOTOR; MYOSIN VA; RAB11 PROTEIN;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; FLUORESCENCE; HIPPOCAMPUS; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; RNA INTERFERENCE; STATISTICAL ANALYSIS; SYNAPTIC TRANSMISSION;

ANIMALS; CELLS, CULTURED; CORE BINDING FACTORS; DENDRITIC SPINES; ENDOSOMES; GTP-BINDING PROTEINS; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MICE; MOLECULAR MOTOR PROTEINS; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN TRANSPORT; RATS; RECEPTORS, AMPA; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 41149119949     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn2063     Document Type: Article

References (50)

1. Kennedy, M.J. & Ehlers, M.D. Organelles and trafficking machinery for postsynaptic plasticity. Annu. Rev. Neurosci. 29, 325-362 (2006).
2. Park, M. et al. Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52, 817-830 (2006).
3. Shi, S.H. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816 (1999).
4. + channel subunit Kv4.2 in hippocampal neurons. Neuron 54, 933-947 (2007).
5. Shepherd, J.D. & Huganir, R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23, 613-643 (2007).
6. Passafaro, M., Piech, V. & Sheng, M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917-926 (2001).
7. Shi, S., Hayashi, Y., Esteban, J.A. & Malinow, R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343 (2001).
8. Luscher, C. et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron 24, 649-658 (1999).
9. Nishimune, A. et al. NSF binding to GluR2 regulates synaptic transmission. Neuron 21, 87-97 (1998).
10. Song, I. et al. Interaction of the N-ethylmaleimide- sensitive factor with AMPA receptors. Neuron 21, 393-400 (1998).
11. Hayashi, Y. et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267 (2000).
12. Carlisle, H.J. & Kennedy, M.B. Spine architecture and synaptic plasticity. Trends Neurosci. 28, 182-187 (2005).
13. Karcher, R.L., Deacon, S.W. & Gelfand, V.I. Motor-cargo interactions: the key to transport specificity. Trends Cell Biol. 12, 21-27 (2002).
14. Osterweil, E., Wells, D.G. & Mooseker, M.S. A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J. Cell Biol. 168, 329-338 (2005).
15. Lise, M.F. et al. Involvement of myosin Vb in glutamate receptor trafficking. J. Biol. Chem. 281, 3669-3678 (2006).
16. Triller, A. & Choquet, D. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!. Trends Neurosci. 28, 133-139 (2005).
17. Mercer, J.A., Seperack, P.K., Strobel, M.C., Copeland, N.G. & Jenkins, N.A. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, 709-713 (1991).
18. Naisbitt, S. et al. Interaction of the postsynaptic density-95/guanylate kinase domain-associated protein complex with a light chain of myosin-V and dynein. J. Neurosci. 20, 4524-4534 (2000).
19. Walikonis, R.S. et al. Identification of proteins in the postsynaptic density fraction by mass spectrometry. J. Neurosci. 20, 4069-4080 (2000).
20. Yoshimura, A. et al. myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr. Biol. 16, 2345-2351 (2006).
21. Pastural, E. et al. Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat. Genet. 16, 289-292 (1997).
22. Sanal, O. et al. An allelic variant of Griscelli disease: presentation with severe hypotonia, mental-motor retardation and hypopigmentation consistent with Elejalde syndrome (neuroectodermal melanolysosomal disorder). J. Neurol. 247, 570-572 (2000).
23. Tabb, J.S., Molyneaux, B.J., Cohen, D.L., Kuznetsov, S.A. & Langford, G.M. Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234 (1998).
24. 2+ store in the dendritic spine of Purkinje cells in mice. Neurosci. Lett. 215, 169-172 (1996).
25. Petralia, R.S. et al. Glutamate receptor targeting in the postsynaptic spine involves mechanisms that are independent of myosin Va. Eur. J. Neurosci. 13, 1722-1732 (2001).
26. Miyata, M. et al. Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 28, 233-244 (2000).
27. Schnell, E. & Nicoll, R.A. Hippocampal synaptic transmission and plasticity are preserved in myosin Va mutant mice. J. Neurophysiol. 85, 1498-1501 (2001).
28. Wenthold, R.J., Petralia, R.S., Blahos, J., II & Niedzielski, A.S. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989 (1996).
29. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. & Parton, R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924 (1996).
30. Brown, J.R., Simonetta, K.R., Sandberg, L.A., Stafford, P. & Langford, G.M. Recombinant globular tail fragment of myosin-V blocks vesicle transport in squid nerve cell extracts. Biol. Bull. 201, 240-241 (2001).
31. Lapierre, L.A. et al. myosin vb is associated with plasma membrane recycling systems. Mol. Biol. Cell 12, 1843-1857 (2001).
32. Rodriguez, O.C. & Cheney, R.E. Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J. Cell Sci. 115, 991-1004 (2002).
33. Zhu, J.J., Esteban, J.A., Hayashi, Y. & Malinow, R. Postnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity. Nat. Neurosci. 3, 1098-1106 (2000).
34. Watt, A.J., van Rossum, M.C., MacLeod, K.M., Nelson, S.B. & Turrigiano, G.G. Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 26, 659-670 (2000).
35. Gerges, N.Z., Brown, T.C., Correia, S.S. & Esteban, J.A. Analysis of Rab protein function in neurotransmitter receptor trafficking at hippocampal synapses. Methods Enzymol. 403, 153-166 (2005).
36. Ehrlich, I. & Malinow, R. Postsynaptic density-95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci. 24, 916-927 (2004).
37. Piccini, A. & Malinow, R. Critical postsynaptic density-95/disc large/zonula occludens-1 interactions by glutamate receptor 1 (GluR1) and GluR2 required at different subcellular sites. J. Neurosci. 22, 5387-5392 (2002).
38. Ryu, J. et al. A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49, 175-182 (2006).
39. Park, M., Penick, E.C., Edwards, J.G., Kauer, J.A. & Ehlers, M.D. Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972-1975 (2004).
40. Brown, T.C., Correia, S.S., Petrok, C.N. & Esteban, J.A. Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J. Neurosci. 27, 13311-13315 (2007).
41. Seabra, M.C. & Coudrier, E. Rab GTPases and myosin motors in organelle motility. Traffic 5, 393-399 (2004).
42. Jordens, I., Marsman, M., Kuijl, C. & Neefjes, J. Rab proteins, connecting transport and vesicle fusion. Traffic 6, 1070-1077 (2005).
43. Krementsov, D.N., Krementsova, E.B. & Trybus, K.M. myosin V: regulation by calcium, calmodulin and the tail domain. J. Cell Biol. 164, 877-886 (2004).
44. Lynch, G., Larson, J., Kelso, S., Barrionuevo, G. & Schottler, F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 305, 719-721 (1983).
45. Barral, D.C. et al. Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J. Clin. Invest. 110, 247-257 (2002).
46. Cao, T.T., Chang, W., Masters, S.E. & Mooseker, M.S. myosin-Va binds to and mechanochemically couples microtubules to actin filaments. Mol. Biol. Cell 15, 151-161 (2004).
47. Ali, M.Y. et al. myosin Va maneuvers through actin intersections and diffuses along microtubules. Proc. Natl. Acad. Sci. USA 104, 4332-4336 (2007).
48. Huang, J.D. et al. Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267-270 (1999).
49. Mehta, A.D. et al. myosin-V is a processive actin-based motor. Nature 400, 590-593 (1999).
50. Dunah, A.W. et al. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat. Neurosci. 8, 458-467 (2005).