Differential requirements for clathrin in receptor-mediated endocytosis and maintenance of synaptic vesicle pools

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 4, 2009, Pages 1139-1144

  Sato, Ken ^a   Ernstrom, Glen G ^b   Watanabe, Shigeki ^b   Weimer, Robby M ^b   Chen, Chih Hsiung ^c   Sato, Miyuki ^a   Siddiqui, Ayesha ^c   Jorgensen, Erik M ^b   Grant, Barth D ^c  

^a GUNMA UNIVERSITY   (Japan)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

Caenorhabditis elegans; Synapse

Indexed keywords

CLATHRIN; CLATHRIN HEAVY CHAIN;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENDOCYTOSIS; GENETIC CODE; NEUROMUSCULAR FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TEMPERATURE SENSITIVITY;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CLATHRIN HEAVY CHAINS; ENDOCYTOSIS; MUTATION; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; RECEPTORS, CELL SURFACE; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

ANIMALIA; CAENORHABDITIS ELEGANS; METAZOA;

EID: 59049094826     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0809541106     Document Type: Article

References (38)

1. Brodsky FM, Chen CY, Knuehl C, Towler MC, Wakeham DE (2001) Biological basket weaving: Formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol 17:517-568.
2. Heuser J (1980) Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84:560-583.
3. Heuser JE, Reese TS (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57:315-344.
4. Maycox PR, Link E, Reetz A, Morris SA, Jahn R (1992) Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J Cell Biol 118:1379-1388.
5. Bazinet C, Katzen AL, Morgan M, Mahowald AP, Lemmon SK (1993) The Drosophila clathrin heavy chain gene: Clathrin function is essential in a multicellular organism. Genetics 134:1119-1134.
6. Grant B, Hirsh D (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10:4311-4326.
7. Lemmon SK, Pellicena-Palle A, Conley K, Freund CL (1991) Sequence of the clathrin heavy chain from Saccharomyces cerevisiae and requirement of the COOH terminus for clathrin function. J Cell Biol 112:65-80.
8. Chen CY, Graham TR (1998) An arf1 Δ synthetic lethal screen identifies a new clathrin heavy chain conditional allele that perturbs vacuolar protein transport in Saccharomyces cerevisiae. Genetics 150:577-589.
9. Fotin A, et al. (2004) Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432:573-579.
10. Poupon V, et al. (2008) Clathrin light chains function in mannose phosphate receptor trafficking via regulation of actin assembly. Proc Natl Acad Sci USA 105:168-173.
11. Boehm M, Bonifacino JS (2001) Adaptins: The final recount. Mol Biol Cell 12:2907-2920.
12. Hinrichsen L, Harborth J, Andrees L, Weber K, Ungewickell EJ (2003) Effect of clathrin heavy chain- and α-adaptin-specific small inhibitory RNAs on endocytic accessory proteins and receptor trafficking in HeLa cells. J Biol Chem 278:45160-45170.
13. Liu SH, Wong ML, Craik CS, Brodsky FM (1995) Regulation of clathrin assembly and trimerization defined using recombinant triskelion hubs. Cell 83:257-267.
14. Slepnev VI, De Camilli P (2000) Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Reviews Neuroscience 1:161-172.
15. Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371-375.
16. Murthy VN, De Camilli P (2003) Cell biology of the presynaptic terminal. Annu Rev Neurosci 26:701-728.
17. Altun-Gultekin Z, et al. (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C elegans. Development 128:1951-1969.
18. Salcini AE, et al. (2001) The Eps15 C. elegans homologue EHS-1 is implicated in synaptic vesicle recycling. Nat Cell Biol 3:755-760.
19. Rand JB, Johnson CD (1995) Genetic pharmacology: Interactions between drugs and gene products in Caenorhabditis elegans. Methods Cell Biol 48:187-204.
20. Lewis JA, Wu CH, Berg H, Levine JH (1980) The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 95:905-928.
21. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol (London) 117:109-128.
22. Dittman JS, Kaplan JM (2008) Behavioral impact of neurotransmitter- activated G-protein-coupled receptors: Muscarinic and GABAB receptors regulate Caenorhabditis elegans locomotion. J Neurosci 28:7104-7112.
23. Doi M, Iwasaki K (2002) Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33:249-259.
24. Heerssen H, Fetter RD, Davis GW (2008) Clathrin dependence of synaptic-vesicle formation at the Drosophila neuromuscular junction. Curr Biol 18:401-409.
25. Kasprowicz J, et al. (2008) Inactivation of clathrin heavy chain inhibits synaptic recycling but allows bulk membrane uptake. J Cell Biol 182:1007-1016.
26. Beck S, et al. (2002) Fluorophore-assisted light inactivation: A high-throughput tool for direct target validation of proteins. Proteomics 2:247-255.
27. Bennett EM, Chen CY, Engqvist-Goldstein AE, Drubin DG, Brodsky FM (2001) Clathrin hub expression dissociates the actin-binding protein Hip1R from coated pits and disrupts their alignment with the actin cytoskeleton. Traffic 2:851-858.
28. Chen CY, Brodsky FM (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.
29. Granseth B, Odermatt B, Royle SJ, Lagnado L (2006) Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51:773-786.
30. Ferguson SM, et al. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316:570-574.
31. Hayashi M, et al. (2008) Cell- and stimulus-dependent heterogeneity of synaptic vesicle endocytic recycling mechanisms revealed by studies of dynamin 1-null neurons. Proc Natl Acad Sci USA 105:2175-2180.
32. Ceccarelli B, Hurlbut WP, Mauro A (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57:499-524.
33. An S, Zenisek D (2004) Regulation of exocytosis in neurons and neuroendocrine cells. Curr Opin Neurobiol 14:522-530.
34. Kidokoro Y (2006) Vesicle trafficking and recycling at the neuromuscular junction: Two pathways for endocytosis. Int Rev Neurobiol 75:145-164.
35. Kaksonen M, Toret CP, Drubin DG (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123:305-320.
36. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71-94.
37. Kamath RS, Ahringer J (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30:313-321.
38. Richmond JE, Davis WS, Jorgensen EM (1999) UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci 2:959-964.