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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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van Dongen, H. M., Masoumi, N., Witwer, K. W., & Pegtel, D. M. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00063-15 · Cited by 271
Simhadri, V. R., Reiners, K. S., Hansen, H. P., Topolar, D., Simhadri, V. L., Nohroudi, K., Kufer, T. A., Engert, A., & von Strandmann, E. P. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003377 · Cited by 263
Ubiquitination and the Regulation of Membrane Proteins
Foot, N. J., Henshall, T. L., & Kumar, S. (2016) · Physiological Reviews · doi:10.1152/physrev.00012.2016 · Cited by 272
Zhou, H., Zhu, L., Song, J. H., Wang, G., Li, P., Li, W., Luo, P., Sun, X., Wu, J., Liu, Y., et al. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01556-2 · Cited by 273
“Exosomes were first discovered by EG Trams in sheep reticulocytes in 1981 and named by Johnstone 6 years later [18].”
BackgroundPathologic function and therapeutic potential of exosomes in cardiovascular disease
Ailawadi, S., Wang, X., Gu, H., & Fan, G. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.10.008 · Cited by 264
Current Knowledge on Exosome Biogenesis, Cargo-Sorting Mechanism and Therapeutic Implications
Xie, S., Zhang, Q., & Jiang, L. (2022) · Membranes · doi:10.3390/membranes12050498 · Cited by 262
“Due to the particularity of this extracellular vesicle, Johnstone, a pioneer in this field, named it an “exosome” for the first time in 1987 [7].”
BackgroundToward Exosome-Based Therapeutics: Isolation, Heterogeneity, and Fit-for-Purpose Potency
Willis, G. R., Kourembanas, S., & Mitsialis, S. A. (2017) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2017.00063 · Cited by 267
Russell, A. E., Sneider, A., Witwer, K. W., Bergese, P., Bhattacharyya, S. N., Cocks, A., Cocucci, E., Erdbrügger, U., Falcón‐Pérez, J. M., Freeman, D. W., et al. (2019) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2019.1684862 · Cited by 270
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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