Calcyon is necessary for activity-dependent AMPA receptor internalization and LTD in CA1 neurons of hippocampus

European Journal of Neuroscience

Volumn 29, Issue 1, 2009, Pages 42-54

  Davidson, Heather Trantham ^a,d   Xiao, Jiping ^b,d   Dai, Rujuan ^c,d   Bergson, Clare ^d  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^d MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

ADHD; Clathrin mediated endocytosis; Glutamate transmission; Schizophrenia; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CLATHRIN; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID; PROTEIN CALCYON; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; GENE DELETION; HIPPOCAMPUS; LONG TERM DEPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ACTION POTENTIALS; ANIMALS; CELL MEMBRANE; CLATHRIN; ENDOCYTOSIS; EXCITATORY AMINO ACID AGONISTS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; LONG-TERM SYNAPTIC DEPRESSION; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, AMPA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 58149133718     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06563.x     Document Type: Article

References (56)

1. Adesnik, H., Nicoll, R.A. England, P.M. (2005) Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron, 48, 977 985.
2. Alberi, S., Boda, B., Steiner, P., Nikonenko, I., Hirling, H. Muller, D. (2005) The endosomal protein NEEP21 regulates AMPA receptor-mediated synaptic transmission and plasticity in the hippocampus. Mol. Cell. Neurosci., 29, 313 319.
3. Ali, M.K. Bergson, C. (2003) Elevated intracellular calcium triggers recruitment of the receptor cross-talk accessory protein calcyon to the plasma membrane. J. Biol. Chem., 278, 51654 51663.
4. Beattie, E.C., Carroll, R.C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M. Malenka, R.C. (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci., 3, 1291 1300.
5. Bonifacino, J.S. Lippincott-Schwartz, J. (2003) Coat proteins: shaping membrane transport. Nat. Rev. Mol. Cell Biol., 4, 409 414.
6. Bredt, D.S. Nicoll, R.A. (2003) AMPA receptor trafficking at excitatory synapses. Neuron, 40, 361 379.
7. Brodsky, F.M., Chen, C.Y., Knuehl, C., Towler, M.C. Wakeham, D.E. (2001) Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol., 17, 517 568.
8. Brown, T.C., Tran, I.C., Backos, D.S. Esteban, J.A. (2005) NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron, 45, 81 94.
9. Carroll, R.C., Beattie, E.C., Xia, H., Luscher, C., Altschuler, Y., Nicoll, R.A., Malenka, R.C. von Zastrow, M. (1999a) Dynamin-dependent endocytosis of ionotropic glutamate receptors. Proc. Natl Acad. Sci. USA, 96, 14112 14117.
10. Carroll, R.C., Lissin, D.V., von Zastrow, M., Nicoll, R.A. Malenka, R.C. (1999b) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat. Neurosci., 2, 454 460.
11. Chen, C.Y. Brodsky, F.M. (2005) Huntingtin-interacting protein 1 (Hip1) and Hip1-related protein (Hip1R) bind the conserved sequence of clathrin light chains and thereby influence clathrin assembly in vitro and actin distribution in vivo. J. Biol. Chem., 280, 6109 6117.
12. Chowdhury, S., Shepherd, J.D., Okuno, H., Lyford, G., Petralia, R.S., Plath, N., Kuhl, D., Huganir, R.L. Worley, P.F. (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron, 52, 445 459.
13. Cottrell, J.R., Borok, E., Horvath, T.L. Nedivi, E. (2004) CPG2: a brain- and synapse-specific protein that regulates the endocytosis of glutamate receptors. Neuron, 44, 677 690.
14. Ehlers, M.D. (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron, 28, 511 525.
15. Girard, M., Allaire, P.D., McPherson, P.S. Blondeau, F. (2005) Non-stoichiometric relationship between clathrin heavy and light chains revealed by quantitative comparative proteomics of clathrin-coated vesicles from brain and liver. Mol. Cell Proteomics., 4, 1145 1154.
16. Heuser, J.E. Anderson, R.G. (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol., 108, 389 400.
17. Huang, F., Khvorova, A., Marshall, W. Sorkin, A. (2004) Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J. Biol. Chem., 279, 16657 16661.
18. Ito, M. (1989) Long-term depression. Annu. Rev. Neurosci., 12, 85 102.
19. Kastning, K., Kukhtina, V., Kittler, J.T., Chen, G., Pechstein, A., Enders, S., Lee, S.H., Sheng, M., Yan, Z. Haucke, V. (2007) Molecular determinants for the interaction between AMPA receptors and the clathrin adaptor complex AP-2. Proc. Natl Acad. Sci. USA, 104, 2991 2996.
20. Kesner, R.P. Rolls, E.T. (2001) Role of long-term synaptic modification in short-term memory. Hippocampus, 11, 240 250.
21. Lakadamyali, M., Rust, M.J. Zhuang, X. (2006) Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell, 124, 997 1009.
22. Lee, H.K., Kameyama, K., Huganir, R.L. Bear, M.F. (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron, 21, 1151 1162.
23. Lee, S.H., Liu, L., Wang, Y.T. 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. Lee, S.H., Simonetta, A. Sheng, M. (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron, 43, 221 236.
25. Lin, J.W., Ju, W., Foster, K., Lee, S.H., Ahmadian, G., Wyszynski, M., Wang, Y.T. Sheng, M. (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat. Neurosci., 3, 1282 1290.
26. Loerke, D., Wienisch, M., Kochubey, O. Klingauf, J. (2005) Differential control of clathrin subunit dynamics measured with EW-FRAP microscopy. Traffic, 6, 918 929.
27. Luscher, C., Xia, H., Beattie, E.C., Carroll, R.C., von Zastrow, M., Malenka, R.C. Nicoll, R.A. (1999) Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron, 24, 649 658.
28. Lynch, G. Baudry, M. (1984) The biochemistry of memory: a new and specific hypothesis. Science, 224, 1057 1063.
29. Malenka, R.C. Bear, M.F. (2004) LTP and LTD: an embarrassment of riches. Neuron, 44, 5 21.
30. Malinow, R. (2003) AMPA receptor trafficking and long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, 707 714.
31. Man, H.Y., Lin, J.W., Ju, W.H., Ahmadian, G., Liu, L., Becker, L.E., Sheng, M. Wang, Y.T. (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron, 25, 649 662.
32. Metzler, M., Legendre-Guillemin, V., Gan, L., Chopra, V., Kwok, A., McPherson, P.S. Hayden, M.R. (2001) HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein. J. Biol. Chem., 276, 39271 39276.
33. Mueller, V.J., Wienisch, M., Nehring, R.B. Klingauf, J. (2004) Monitoring clathrin-mediated endocytosis during synaptic activity. J. Neurosci., 24, 2004 2012.
34. Myme, C.I., Sugino, K., Turrigiano, G.G. Nelson, S.B. (2003) The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J. Neurophysiol., 90, 771 779.
35. Noel, J., Ralph, G.S., Pickard, L., Williams, J., Molnar, E., Uney, J.B., Collingridge, G.L. Henley, J.M. (1999) Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron, 23, 365 376.
36. Oakman, S.A. Meador-Woodruff, J.H. (2004) Calcyon transcript expression in macaque brain. J. Comp. Neurol., 468, 264 276.
37. Palmer, C.L., Lim, W., Hastie, P.G., Toward, M., Korolchuk, V.I., Burbidge, S.A., Banting, G., Collingridge, G.L., Isaac, J.T. Henley, J.M. (2005) Hippocalcin functions as a calcium sensor in hippocampal LTD. Neuron, 47, 487 494.
38. Park, M., Penick, E.C., Edwards, J.G., Kauer, J.A. Ehlers, M.D. (2004) Recycling endosomes supply AMPA receptors for LTP. Science, 305, 1972 1975.
39. 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.
40. Redmond, L., Kashani, A.H. Ghosh, A. (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron, 34, 999 1010.
41. Rial Verde, E.M., Lee-Osbourne, J., Worley, P.F., Malinow, R. Cline, H.T. (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron, 52, 461 474.
42. Saberan-Djoneidi, D., Marey-Semper, I., Picart, R., Studler, J.M., Tougard, C., Glowinski, J. Levi-Strauss, M. (1995) A 19-kDa protein belonging to a new family is expressed in the Golgi apparatus of neural cells. J. Biol. Chem., 270, 1888 1893.
43. Saberan-Djoneidi, D., Picart, R., Escalier, D., Gelman, M., Barret, A., Tougard, C., Glowinski, J. Levi-Strauss, M. (1998) A 21-kDa polypeptide belonging to a new family of proteins is expressed in the Golgi apparatus of neural and germ cells. J. Biol. Chem., 273, 3909 3914.
44. Sheng, M. Hyoung, L.S. (2003) AMPA receptor trafficking and synaptic plasticity: major unanswered questions. Neurosci. Res., 46, 127 134.
45. Shi, S., Hayashi, Y., Esteban, J.A. Malinow, R. (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell, 105, 331 343.
46. Steiner, P., Sarria, J.C., Glauser, L., Magnin, S., Catsicas, S. Hirling, H. (2002) Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD. J. Cell Biol., 157, 1197 1209.
47. Steiner, P., Alberi, S., Kulangara, K., Yersin, A., Sarria, J.C., Regulier, E., Kasas, S., Dietler, G., Muller, D., Catsicas, S. Hirling, H. (2005) Interactions between NEEP21, GRIP1 and GluR2 regulate sorting and recycling of the glutamate receptor subunit GluR2. EMBO J., 24, 2873 2884.
48. Sun, X., Zhao, Y. Wolf, M.E. (2005) Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J. Neurosci., 25, 7342 7351.
49. Teyler, T.J. Discenna, P. (1984) Long-term potentiation as a candidate mnemonic device. Brain Res., 319, 15 28.
50. Ungewickell, E. Ungewickell, H. (1991) Bovine brain clathrin light chains impede heavy chain assembly in vitro. J. Biol. Chem., 266, 12710 12714.
51. Wang, Y.T. Linden, D.J. (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron, 25, 635 647.
52. Wenthold, R.J., Petralia, R.S., Blahos, J. II. Niedzielski, A.S. (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci., 16, 1982 1989.
53. Wu, X., Zhao, X., Baylor, L., Kaushal, S., Eisenberg, E. Greene, L.E. (2001) Clathrin exchange during clathrin-mediated endocytosis. J. Cell Biol., 155, 291 300.
54. Xiao, J., Dai, R., Negyessy, L. Bergson, C. (2006) Calcyon, a novel partner of clathrin light chain, stimulates clathrin-mediated endocytosis. J. Biol. Chem., 281, 15182 15193.
55. Zelenin, S., Aperia, A. Diaz, H.R. (2002) Calcyon in the rat brain: cloning of cDNA and expression of mRNA. J. Comp. Neurol., 446, 37 45.
56. Zhang, J., Yang, Y., Li, H., Cao, J. Xu, L. (2005) Amplitude/frequency of spontaneous mEPSC correlates to the degree of long-term depression in the CA1 region of the hippocampal slice. Brain Res., 1050, 110 117.