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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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Mittal, S., Gupta, P., Chaluvally–Raghavan, P., & Pradeep, S. (2020) · Cancers · doi:10.3390/cancers12123563 · Cited by 76
Exosomes: A New Pathway for Cancer Drug Resistance
Zhong, Y., Li, H., Li, P., Chen, Y., Zhang, M., Yuan, Z., Zhang, Y., Xu, Z., Luo, G. Q., Fang, Y., et al. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.743556 · Cited by 77
“as vesicles that containing non-essential proteins that are expelled from cells (2) following the fusion of microvesicles with the cell membranes (3).”
BackgroundExosomes in the tumor microenvironment: Promoting cancer progression
Jin, Y., Xing, J., Xu, K., Liu, D., & Zhuo, Y. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1025218 · Cited by 82
“In the 1970s, Johnstone discovered vesicle-like lipid particles secreted by cells during the culture of sheep reticulocytes, which were isolated and named as exosomes (1).”
BackgroundShedding and uptake of gangliosides and glycosylphosphatidylinositol-anchored proteins
Lauc, G., & Heffer, M. (2005) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2005.11.014 · Cited by 77
Siree, A., Sonoda, H., Kinouchi, M., Oshikawa, S., Takahashi, S., Hoshino, Y., Sinlapadeelerdkul, T., Yokota‐Ikeda, N., Matsuzaki, T., & Ikeda, M. (2018) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00184.2017 · Cited by 78
Morelli, A. E. (2005) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2005.01197.x · Cited by 76
Dendritic cell-derived exosomes for cancer immunotherapy: hope and challenges
Tian, H., & Li, W. (2017) · Annals of Translational Medicine · doi:10.21037/atm.2017.02.23 · Cited by 76
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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