Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling - PubMed (original) (raw)
Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling
P R Maycox et al. J Cell Biol. 1992 Sep.
Abstract
The recycling of synaptic vesicles in nerve terminals is thought to involve clathrin-coated vesicles. However, the properties of nerve terminal coated vesicles have not been characterized. Starting from a preparation of purified nerve terminals obtained from rat brain, we isolated clathrin-coated vesicles by a series of differential and density gradient centrifugation steps. The enrichment of coated vesicles during fractionation was monitored by EM. The final fraction consisted of greater than 90% of coated vesicles, with only negligible contamination by synaptic vesicles. Control experiments revealed that the contribution by coated vesicles derived from the axo-dendritic region or from nonneuronal cells is minimal. The membrane composition of nerve terminal-derived coated vesicles was very similar to that of synaptic vesicles, containing the membrane proteins synaptophysin, synaptotagmin, p29, synaptobrevin and the 116-kD subunit of the vacuolar proton pump, in similar stoichiometric ratios. The small GTP-binding protein rab3A was absent, probably reflecting its dissociation from synaptic vesicles during endocytosis. Immunogold EM revealed that virtually all coated vesicles carried synaptic vesicle proteins, demonstrating that the contribution by coated vesicles derived from other membrane traffic pathways is negligible. Coated vesicles isolated from the whole brain exhibited a similar composition, most of them carrying synaptic vesicle proteins. This indicates that in nervous tissue, coated vesicles function predominantly in the synaptic vesicle pathway. Nerve terminal-derived coated vesicles contained AP-2 adaptor complexes, which is in agreement with their plasmalemmal origin. Furthermore, the neuron-specific coat proteins AP 180 and auxilin, as well as the alpha a1 and alpha c1-adaptins, were enriched in this fraction, suggesting a function for these coat proteins in synaptic vesicle recycling.
Similar articles
- The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin.
Takei K, Mundigl O, Daniell L, De Camilli P. Takei K, et al. J Cell Biol. 1996 Jun;133(6):1237-50. doi: 10.1083/jcb.133.6.1237. J Cell Biol. 1996. PMID: 8682861 Free PMC article. - Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling.
Zhang JZ, Davletov BA, Südhof TC, Anderson RG. Zhang JZ, et al. Cell. 1994 Sep 9;78(5):751-60. doi: 10.1016/s0092-8674(94)90442-1. Cell. 1994. PMID: 8087843 - A conserved clathrin assembly motif essential for synaptic vesicle endocytosis.
Morgan JR, Prasad K, Hao W, Augustine GJ, Lafer EM. Morgan JR, et al. J Neurosci. 2000 Dec 1;20(23):8667-76. doi: 10.1523/JNEUROSCI.20-23-08667.2000. J Neurosci. 2000. PMID: 11102472 Free PMC article. - Clathrin and synaptic vesicle endocytosis: studies at the squid giant synapse.
Augustine GJ, Morgan JR, Villalba-Galea CA, Jin S, Prasad K, Lafer EM. Augustine GJ, et al. Biochem Soc Trans. 2006 Feb;34(Pt 1):68-72. doi: 10.1042/BST0340068. Biochem Soc Trans. 2006. PMID: 16417485 Free PMC article. Review. - Endocytosis: an assembly protein for clathrin cages.
McMahon HT. McMahon HT. Curr Biol. 1999 May 6;9(9):R332-5. doi: 10.1016/s0960-9822(99)80206-1. Curr Biol. 1999. PMID: 10330371 Review.
Cited by
- Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics.
Wasiak S, Legendre-Guillemin V, Puertollano R, Blondeau F, Girard M, de Heuvel E, Boismenu D, Bell AW, Bonifacino JS, McPherson PS. Wasiak S, et al. J Cell Biol. 2002 Sep 2;158(5):855-62. doi: 10.1083/jcb.200205078. Epub 2002 Sep 3. J Cell Biol. 2002. PMID: 12213833 Free PMC article. - Revisiting the Role of Clathrin-Mediated Endoytosis in Synaptic Vesicle Recycling.
Milosevic I. Milosevic I. Front Cell Neurosci. 2018 Feb 6;12:27. doi: 10.3389/fncel.2018.00027. eCollection 2018. Front Cell Neurosci. 2018. PMID: 29467622 Free PMC article. Review. - Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions.
Watanabe S, Liu Q, Davis MW, Hollopeter G, Thomas N, Jorgensen NB, Jorgensen EM. Watanabe S, et al. Elife. 2013 Sep 3;2:e00723. doi: 10.7554/eLife.00723. Elife. 2013. PMID: 24015355 Free PMC article. - A dynamin 1-, dynamin 3- and clathrin-independent pathway of synaptic vesicle recycling mediated by bulk endocytosis.
Wu Y, O'Toole ET, Girard M, Ritter B, Messa M, Liu X, McPherson PS, Ferguson SM, De Camilli P. Wu Y, et al. Elife. 2014 Jun 24;3:e01621. doi: 10.7554/eLife.01621. Elife. 2014. PMID: 24963135 Free PMC article. - Rat liver endocytic coated vesicles do not exhibit ATP-dependent acidification in vitro.
Fuchs R, Ellinger A, Pavelka M, Mellman I, Klapper H. Fuchs R, et al. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4811-5. doi: 10.1073/pnas.91.11.4811. Proc Natl Acad Sci U S A. 1994. PMID: 8197139 Free PMC article.
References
- J Cell Biol. 1991 Sep;114(5):869-80 - PubMed
- J Cell Biol. 1991 Sep;114(5):881-91 - PubMed
- Trends Biochem Sci. 1991 Jun;16(6):208-13 - PubMed
- J Biol Chem. 1990 Mar 25;265(9):4814-20 - PubMed
- J Neurosci Res. 1991 Aug;29(4):461-73 - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources
Molecular Biology Databases
Research Materials