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Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes)
Open accessAbstract
Vesicles are released during the in vitro culture of sheep reticulocytes which can be harvested by centrifugation at 100,000 X g for 90 min. These vesicles contain a number of activities, characteristic of the reticulocyte plasma membrane, which are known to diminish or disappear upon reticulocyte maturation. The activities include acetylcholinesterase, cytochalasin B binding (glucose transporter) nucleoside binding (i.e. nucleoside transporter), Na+-independent amino acid transport, and the transferrin receptor. Enzymes of cytosolic origin are not detectable or are present at low activity in the vesicles. Cultures of whole blood, mature red cells, or white cells do not yield comparable levels of these activities, supporting the conclusion that the activities arise from the reticulocytes. In addition, the lipid composition of the vesicles shows the high sphingomyelin content characteristic of sheep red cell plasma membranes, but not white cell or platelet membranes, also consistent with the conclusion that the vesicles are of reticulocyte origin. It is suggested that vesicle externalization may be a mechanism for shedding of specific membrane functions which are known to diminish during maturation of reticulocytes to erythrocytes.
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“Exosomes range between 30–100 nm in diameter, have a bilayered membrane (Johnstone et al., 1987) and express surface marker such as CD63 (Christianson et al., 2013).”
From Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism (2016) · cites this paper as Johnstone et al., 1987
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Ravindranath, M. H., Hilali, F. E., & Filippone, E. J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.667834 · Cited by 54
“It was noted that small vesicles were formed by inward budding inside an intra-cellular endosome, leading to the formation of a multi-vesicular body (MVB), which could then fuse with the plasma membrane and release outside its internal vesicles (110).”
BackgroundChen, T.-Y., Gonzalez‐Kozlova, E., Soleymani, T., Salvia, S. L., Kyprianou, N., Sahoo, S., Tewari, A. K., Cordon‐Cardo, C., Stolovitzky, G. A., & Dogra, N. (2021) · iScience · doi:10.1016/j.isci.2022.104414 · Cited by 59
“Subsequently, MVBs fuse with the plasma membrane resulting in the release of exosomes to the extracellular environment(Johnstone et al., 1987; Trams et al., 1981).”
BackgroundInfluentialUbiquitinated Proteins in Exosomes Secreted by Myeloid-Derived Suppressor Cells
Burke, M. C., Oei, M. S., Edwards, N. J., Ostrand‐Rosenberg, S., & Fenselau, C. (2014) · Journal of Proteome Research · doi:10.1021/pr500854x · Cited by 55
Exosome and its roles in cardiovascular diseases
Wang, Z., Zheng, X., & Zhao, S. (2014) · Heart Failure Reviews · doi:10.1007/s10741-014-9469-0 · Cited by 57
Elashiry, M., Elsayed, R., & Cutler, C. W. (2021) · Cells · doi:10.3390/cells11010115 · Cited by 58
“The discovery of EXO in the late 1980s led to the initial notion that they were waste products result from cellular damage [16].”
BackgroundDimov, I., Veličković, L. J., & Stefanović, V. (2009) · The Scientific World JOURNAL · doi:10.1100/tsw.2009.128 · Cited by 55
Exosomes for Immunotherapy of Cancer
Chaput, N., Schartz, N., André, F., & Zitvogel, L. (2003) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-0081-0_17 · Cited by 55
Song, Z., Xu, Y., Zhang, L., Zhou, L., Zhang, Y., Han, Y., Li, X., Yü, P., Qu, Y., Zhao, W., et al. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.565479 · Cited by 55
Radiolabelling of Extracellular Vesicles for PET and SPECT imaging
Khan, A. A., & de Rosales, R. T. M. (2021) · Nanotheranostics · doi:10.7150/ntno.51676 · Cited by 59
Metadata
- Authors
- Johnstone, R. M., Adam, M., Hammond, J. R., Orr, L., & Turbide, C.
- Affiliations
- McGill University (CA)
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1987-07
- Volume
- 262
- Issue
- 19
- Pages
- 9412-9420
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W1915536483
- Semantic Scholar
- 9e8f5a8482d60e384e3dcd94080a64e9f387e3ae
- Cited by
- 2,931
- References
- 51
- Citations by year
- 2026: 132 · 2025: 231 · 2024: 281 · 2023: 285 · 2022: 291 · 2021: 296 · 2020: 276 · 2019: 197 · 2018: 157 · 2017: 134 · 2016: 131 · 2015: 79 · 2014: 76 · 2013: 46 · 2012: 53
- FWCI
- 1.93
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
- Keywords
- reticulocyte maturation, exosomes, vesicle formation, membrane shedding, acetylcholinesterase, glucose transporters, nucleoside transporters, amino acid transport, transferrin receptor, sphingomyelin, sheep red blood cells, membrane lipid composition
- MeSH terms
- Acetylcholinesterase, Amino Acids, Animals, Carrier Proteins, Cell Membrane, Cells, Cultured, Cytochalasin B, Glyceraldehyde-3-Phosphate Dehydrogenases, Leucine, Membrane Proteins, Monosaccharide Transport Proteins, Receptors, Transferrin, Reticulocytes, Sheep, Sodium, Thioinosine, Nucleoside Transport Proteins
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