Reduction of AP180 and CALM produces defects in synaptic vesicle size and density

NeuroMolecular Medicine

Volumn 15, Issue 1, 2013, Pages 49-60

  Petralia, Ronald S ^a   Wang, Ya Xian ^a   Indig, Fred E ^b   Bushlin, Ittai ^b   Wu, Fangbai ^b   Mattson, Mark P ^b   Yao, Pamela J ^b  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

AP180; CALM; Hippocampal synapse; Synaptic vesicle

Indexed keywords

CLATHRIN ASSEMBLY LYMPHOID MYELOID PROTEIN; CLATHRIN ASSEMBLY PROTEIN; CLATHRIN ASSEMBLY PROTEIN AP180; ENHANCED GREEN FLUORESCENT PROTEIN; SMALL INTERFERING RNA; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; HIPPOCAMPUS; MICROSCOPY; NERVE CELL; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RNA INTERFERENCE; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CELLS, CULTURED; CLATHRIN-COATED VESICLES; FEMALE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; NERVE TISSUE PROTEINS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RNA INTERFERENCE; RNA, SMALL INTERFERING; SYNAPTIC VESICLES; SYNAPTOPHYSIN; TRANSFECTION;

INVERTEBRATA; MAMMALIA; RATTUS;

EID: 84874730002     PISSN: 15351084     EISSN: 15591174     Source Type: Journal    
DOI: 10.1007/s12017-012-8194-x     Document Type: Article

References (41)

1. Ahle, S.; & Ungewickell, E. (1986). Purification and properties of a new clathrin assembly protein. EMBO Journal, 5, 3143-3149.
2. Andreae, L. C.; Fredj, N. B.; & Burrone, J. (2012). Independent vesicle pools underlie different modes of release during neuronal development. Journal of Neuroscience, 32, 1867-1874.
3. Banker, G.; & Cowan, W. M. (1977). Rat hippocampal neurons in dispersed cell culture. Brain Research, 126, 397-425. (Pubitemid 8090742)
4. Brett, T. J.; & Traub, L. M. (2006). Molecular structures of coat and coat-associated proteins: Function follows form. Current Opinion in Cell Biology, 18, 395-406. (Pubitemid 44016063)
5. 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. Annual Reviews of Cell and Developmental Biology, 17, 517-568. (Pubitemid 33096185)
6. Bushlin, I.; Petralia, R. S.; Wu, F.; Harel, A.; Mughal, M. R.; Mattson, M. P.; et al. (2008). Clathrin assembly protein AP180 and CALM differentially control axogenesis and dendrite outgrowth in embryonic hippocampal neurons. Journal of Neuroscience, 28, 10257-10271.
7. Dittman, J.; & Ryan, T. A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annual Reviews of Cell and Developmental Biology, 25, 133-160.
8. Dreyling, M. H.; Martinez-Climent, J. A.; Zheng, M.; Mao, J.; Rowley, J. D.; & Bohlander, S. K. (1996). The t(10;11)(p13;q14) in the U937 cell line results in the fusion of the AF10 gene and CALM, encoding a new member of the AP-3 clathrin assembly protein family. Proceedings of the National Academy of Sciences, 93, 4804-4809. (Pubitemid 26162832)
9. Ford, M. G.; Pearse, B. M.; Higgins, M. K.; Vallis, Y.; Owen, D. J.; Gibson, A.; et al. (2001). Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science, 291, 1051-1055. (Pubitemid 32157415)
10. Harel, A.; Wu, F.; Mattson, M. P.; Morris, C. M.; & Yao, P. J. (2008). Evidence for CALM in directing VAMP2 trafficking. Traffic, 9, 417-429. (Pubitemid 351189000)
11. Kaech, S.; & Banker, G. (2006). Culturing hippocampal neurons. Nature Protocols, 1, 2406-2415.
12. Kay, A. R.; Alfonso, A.; Alford, S.; Cline, H. T.; Holgado, A. M.; Sakmann, B.; et al. (1999). Imaging synaptic activity in intact brain and slices with FM1-43 in C. elegans, lamprey, and rat. Neuron, 24, 809-817. (Pubitemid 30017661)
13. Koo, S. J.; Markovic, S.; Puchkov, D.; Mahrenholz, C. C.; Beceren-Braun, F.; Maritzen, T.; et al. (2011). SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proceedings of the National Academy of Sciences, 108, 13540-13545.
14. Lafer, E. M. (2002). Clathrin-protein interactions. Traffic, 3, 513-520. (Pubitemid 35452888)
15. Li, J.; Wang, Y.; Chiu, S. L.; & Cline, H. T. (2010). Membrane targeted horseradish peroxidase as a marker for correlative fluorescence and electron microscopy studies. Front Neural Circuits, 26, 4-6.
16. Mao, Y.; Chen, J.; Maynard, J. A.; Zhang, B.; & Quiocho, F. A. (2001). A novel all helix fold of the AP180 amino-terminal domain for phosphoinositide binding and clathrin assembly in synaptic vesicle endocytosis. Cell, 104, 433-440. (Pubitemid 32206463)
17. Mattson, M. P.; Dou, P.; & Kater, S. B. (1988). Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. Journal of Neuroscience, 8, 2087-2100.
18. McMahon, H. T.; & Boucrot, E. (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nature Reviews Molecular Cell Biololgy, 12, 517-533.
19. Meyerholz, A.; Hinrichsen, L.; Groos, S.; Esk, P. C.; Brandes, G.; & Ungewickell, E. J. (2005). Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic, 6, 1225-1234. (Pubitemid 41632272)
20. Mitchell, N.; Petralia, R. S, Yao, P. J.; Currier, D. G.; Wang, Y. X.; Kim, A.; et al. (2012). Sonic hedgehog regulates presynaptic terminal size, ultrastructure and function in hippocampal neurons. Journal of Cell Science (Epub ahead of print).
21. Morgan, J. R.; Zhao, X.; Womack, M.; Prasad, K.; Augustine, G. J.; & Lafer, E. M. (1999). A role for the clathrin assembly domain of AP180 in synaptic vesicle endocytosis. Journal of Neuroscience, 19, 10201-10212. (Pubitemid 30228027)
22. Morgan, J. R.; Augustine, G. J.; & Lafer, E. M. (2002). Synaptic vesicle endocytosis: the races, places, and molecular faces. NeuroMolecular Medicine, 2, 101-114. (Pubitemid 37012499)
23. Morris, S. A.; Schroder, S.; Plessmann, U.; Weber, K.; & Ungewickell, E. (1993). Clathrin assembly protein AP180: Primary structure, domain organization and identification of a clathrin binding site. EMBO Journal, 12, 667-675. (Pubitemid 23073714)
24. Nonet, M. L.; Holgado, A. M.; Brewer, F.; Serpe, C. J.; Norbeck, B. A.; Holleran, J.; et al. (1999). UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Molecular Biology of the Cell, 10, 2343-2360. (Pubitemid 29343139)
25. Petralia, R. S.; & Wenthold, R. J. (1999). Immunocytochemistry of NMDA receptors. Methods Molecular Biololgy, 128, 73-92.
26. Petralia, R. S.; & Yao, P. J. (2007). AP180 and CALM in the developing hippocampus: Expression at the nascent synapse and localization to trafficking organelles. Journal of Comparative Neurology, 504, 314-327. (Pubitemid 350012217)
27. Petralia, R. S.; Wang, Y. X.; Hua, F.; Yi, Z.; Zhou, A.; Ge, L.; et al. (2010). Organization of NMDA receptors at extrasynaptic locations. Neuroscience, 167, 68-87.
28. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends in Cell Biology, 14, 167-174. (Pubitemid 38447116)
29. Royle, S. J.; & Lagnado, L. (2010). Clathrin-mediated endocytosis at the synaptic terminal: Bridging the gap between physiology and molecules. Traffic, 11, 1489-1497.
30. Schmid, E. M.; & McMahon, H. T. (2007). Integrating molecular and network biology to decode endocytosis. Nature, 448, 883-888. (Pubitemid 47312770)
31. Schwartz, C. M.; Cheng, A.; Mughal, M. R.; Mattson, M. P.; & Yao, P. J. (2010). Clathrin assembly proteins AP180 and CALM in the embryonic rat brain. Journal of Comparative Neurology, 518, 3803-3818.
32. Staras, K.; Branco, T.; Burden, J. J.; Pozo, K.; Darcy, K.; Marra, V.; et al. (2010). A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron, 66, 37-44.
33. Tebar, F.; Bohlander, S. K.; & Sorkin, A. (1999). Clathrin assembly lymphoid myeloid leukemia (CALM) protein: Localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Molecular Biology of the Cell, 10, 2687-2702. (Pubitemid 29393520)
34. Ungewickell, E. J.; & Hinrichsen, L. (2007). Endocytosis: Clathrin-mediated membrane budding. Current Opinion in Cell Biology, 19, 417-425. (Pubitemid 47271962)
35. Williams, M. E.; Wilke, S. A.; Daggett, A.; Davis, E.; Otto, S.; Ravi, D.; et al. (2011). Cadherin-9 regulates synapse-specific differentiation in the developing hippocampus. Neuron, 71, 640-655.
36. Wu, F.; Matsuoka, Y.; Mattson, M. P.; & Yao, P. J. (2009). The clathrin assembly protein AP180 regulates the generation of amyloid-beta peptide. Biochemical and Biophysical Research Communications, 385, 247-250.
37. Yao, P. J.; Zhang, P.; Mattson, M. P.; & Furukawa, K. (2003). Heterogeneity of endocytic proteins: Distribution of clathrin adaptor proteins in neurons and glia. Neuroscience, 121, 25-37. (Pubitemid 37297611)
38. Yao, P. J.; Petralia, R. S.; Bushlin, I.; Wang, Y.; & Furukawa, K. (2005). Synaptic distribution of the endocytic accessory proteins AP180 and CALM. Journal of Comparative Neurology, 481, 58-69. (Pubitemid 39578770)
39. Ye, W.; & Lafer, E. M. (1995). Bacterially expressed F1-20/AP-3 assembles clathrin into cages with a narrow size distribution: Implications for the regulation of quantal size during neurotransmission. Journal of Neuroscience, 41, 15-26.
40. Zhang, B.; Koh, Y. H.; Beckstead, R. B.; Budnik, V.; Ganetzky, B.; & Bellen, H. J. (1998). Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron, 21, 1465-1475. (Pubitemid 29022547)
41. Zhou, S.; Tannery, N. H.; Yang, J.; Puszkin, S.; & Lafer, E. M. (1993). The synapse- specific phosphoprotein F1-20 is identical to the clathrin assembly protein AP-3. Journal of Biological Chemistry, 268, 12655-12662. (Pubitemid 23182429)