Endosomal Compartments Serve Multiple Hippocampal Dendritic Spines from a Widespread Rather Than a Local Store of Recycling Membrane
Open accessAbstract
Endosomes are essential to dendritic and synaptic function in sorting membrane proteins for degradation or recycling, yet little is known about their locations near synapses. Here, serial electron microscopy was used to ascertain the morphology and distribution of all membranous intracellular compartments in distal dendrites of hippocampal CA1 pyramidal neurons in juvenile and adult rats. First, the continuous network of smooth endoplasmic reticulum (SER) was traced throughout dendritic segments and their spines. SER occupied the cortex of the dendritic shaft and extended into 14% of spines. Several types of non-SER compartments were then identified, including clathrin-coated vesicles and pits, large uncoated vesicles, tubular compartments, multivesicular bodies (MVBs), and MVB–tubule complexes. The uptake of extracellular gold particles indicated that these compartments were endosomal in origin. Small, round vesicles and pits that did not contain gold were also identified. The tubular compartments exhibited clathrin-coated tips consistent with the genesis of these small, presumably exosomal vesicles. Approximately 70% of the non-SER compartments were located within or at the base of dendritic spines. Overall, only 29% of dendritic spines had endosomal compartments, whereas 20% contained small vesicles. Small vesicles did not colocalize in spines with endosomes or SER. Three-dimensional reconstructions revealed that up to 20 spines shared a recycling pool of plasmalemmal proteins rather than maintaining independent stores at each spine.
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LTP increases spine volume, a process that requires the addition of membranes whose source remains largely unknown.
“In particular, LTP increases spine volume, a process that requires the addition of membranes whose source remains largely unknown”
From Ral mediates activity‐dependent growth of postsynaptic membranes via recruitment of the exocyst (2013) · cites this paper as Cooney et al, 2002
The Discussion (page unavailable) addresses the possible sources of synaptic receptors inserted during LTP, not membrane added as spines enlarge. Searches for LTP-related spine volume, enlargement, and membrane addition found no passage in our copy stating that LTP increases spine volume or that the source of membrane for such growth is largely unknown. (LLM, conf=0.74)
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Sheng, M., & Hoogenraad, C. C. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060805.160029 · Cited by 1,003 · see citing works
Exosomes are released by cultured cortical neurones
Fauré, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., Boyer, V., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.12.003 · Cited by 896 · see citing works
Ultrastructural evidence for synaptic scaling across the wake/sleep cycle
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Intraneuronal β-amyloid accumulation and synapse pathology in Alzheimer’s disease
Gouras, G. K., Tampellini, D., Takahashi, R. H., & Capetillo-Zarate, E. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0679-9 · Cited by 372 · see citing works
Intraneuronal Aβ accumulation and origin of plaques in Alzheimer's disease
Gouras, G. K., Almeida, C. G., & Takahashi, R. H. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.05.022 · Cited by 338 · see citing works
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Self-citationStewart, M. G., Davies, H. A., Sandi, C., Kraev, I. V., Rogachevsky, V. V., Peddie, C. J., Rodriguez, J. J., Cordero, M. I., Donohue, H. S., Gabbott, P. L. A., et al. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.10.031 · Cited by 197 · see citing works
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Richards, P., Didszun, C., Campesan, S., Simpson, A., Horley, B., Young, K. W., Glynn, P., Cain, K., Kyriacou, C. P., Giorgini, F., et al. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.127 · Cited by 82 · see citing works
Ral mediates activity‐dependent growth of postsynaptic membranes via recruitment of the exocyst
Teodoro, R. O., Pekkurnaz, G., Nasser, A., Higashi‐Kovtun, M. E., Balakireva, M., McLachlan, I. G., Camonis, J., & Schwarz, T. L. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.147 · Cited by 61 · see citing works
The needs of a synapse—How local organelles serve synaptic proteostasis
Grochowska, K. M., Andres‐Alonso, M., Karpova, A., & Kreutz, M. R. (2022) · The EMBO Journal · doi:10.15252/embj.2021110057 · Cited by 38 · see citing works
- Authors
- Cooney, J. R., Hurlburt, J. L., Selig, D. K., Harris, K. M., & Fiala, J. C.
- Affiliations
- Boston University (US)
- ORCID
- Harris, Kristen M.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2002-03-15
- Volume
- 22
- Issue
- 6
- Pages
- 2215-2224
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6758269
- OpenAlex
- W2163895781
- Cited by
- 269
- References
- 1
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 11 · 2023: 5 · 2022: 12 · 2021: 15 · 2020: 11 · 2019: 13 · 2018: 10 · 2017: 13 · 2016: 10 · 2015: 9 · 2014: 8 · 2013: 21 · 2012: 11
- FWCI
- 2.60
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (NS21184)
- Goddard Space Flight Center
- National Institute of Mental Health (MH/DA 57351)
- National Institute on Drug Abuse (R01DA057351)
- National Institute of Neurological Disorders and Stroke (R01NS033574, R01NS021184, NS21184, NS33574, R37NS021184)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- endosomes, dendritic spines, CA1 pyramidal neurons, membrane recycling, smooth endoplasmic reticulum, multivesicular bodies, clathrin-coated vesicles, exosomes, dendritic compartmentalization, membrane protein degradation
- MeSH terms
- Animals, Cell Compartmentation, Cell Membrane, Dendrites, Endocytosis, Exocytosis, Hippocampus, Male, Microscopy, Electron, Endosomes, Gold Compounds, Endoplasmic Reticulum, Smooth, Rats, Long-Evans, Rats, In Vitro Techniques
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