Continuous change in membrane and membrane-skeleton organization during development from proerythroblast to senescent red blood cell

Giampaolo Minetti, Cesare Achilli, Cesare Perotti, Annarita Ciana

Research output: Contribution to journalShort survey

1 Citation (Scopus)

Abstract

Within the context of erythropoiesis and the possibility of producing artificial red blood cells (RBCs) in vitro, a most critical step is the final differentiation of enucleated erythroblasts, or reticulocytes, to a fully mature biconcave discocyte, the RBC. Reviewed here is the current knowledge about this fundamental maturational process. By combining literature data with our own experimental evidence we propose that the early phase in the maturation of reticulocytes to RBCs is driven by a membrane raft-based mechanism for the sorting of disposable membrane proteins, mostly the no longer needed transferrin receptor (TfR), to the multivesicular endosome (MVE) as cargo of intraluminal vesicles that are subsequently exocytosed as exosomes, consistently with the seminal and original observation of Johnstone and collaborators of more than 30 years ago (Pan BT, Johnstone RM. Cell. 1983;33:967-978). According to a strikingly selective sorting process, the TfR becomes cargo destined to exocytosis while other molecules, including the most abundant RBC transmembrane protein, band 3, are completely retained in the cell membrane. It is also proposed that while this process could be operating in the early maturational steps in the bone marrow, additional mechanism(s) must be at play for the final removal of the excess reticulocyte membrane that is observed to occur in the circulation. This processing will most likely require the intervention of the spleen, whose function is also necessary for the continuous remodeling of the RBC membrane all along this cell's circulatory life.

Original languageEnglish
Article number286
JournalFrontiers in Physiology
Volume9
Issue numberMAR
DOIs
Publication statusPublished - Mar 26 2018

Fingerprint

Erythroblasts
Skeleton
Erythrocytes
Reticulocytes
Membranes
Transferrin Receptors
Cell Membrane
Erythrocyte Anion Exchange Protein 1
Exosomes
Blood Substitutes
Erythropoiesis
Endosomes
Exocytosis
Membrane Proteins
Spleen
Bone Marrow
Observation

Keywords

  • Artificial red blood cells
  • Autophagy
  • Fluid phase endocytosis
  • Membrane rafts
  • Multivesicular endosome
  • Red blood cell ageing
  • Reticulocyte maturation
  • Spleen

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Continuous change in membrane and membrane-skeleton organization during development from proerythroblast to senescent red blood cell. / Minetti, Giampaolo; Achilli, Cesare; Perotti, Cesare; Ciana, Annarita.

In: Frontiers in Physiology, Vol. 9, No. MAR, 286, 26.03.2018.

Research output: Contribution to journalShort survey

@article{e331658c21bb495184829c5fadde6a49,
title = "Continuous change in membrane and membrane-skeleton organization during development from proerythroblast to senescent red blood cell",
abstract = "Within the context of erythropoiesis and the possibility of producing artificial red blood cells (RBCs) in vitro, a most critical step is the final differentiation of enucleated erythroblasts, or reticulocytes, to a fully mature biconcave discocyte, the RBC. Reviewed here is the current knowledge about this fundamental maturational process. By combining literature data with our own experimental evidence we propose that the early phase in the maturation of reticulocytes to RBCs is driven by a membrane raft-based mechanism for the sorting of disposable membrane proteins, mostly the no longer needed transferrin receptor (TfR), to the multivesicular endosome (MVE) as cargo of intraluminal vesicles that are subsequently exocytosed as exosomes, consistently with the seminal and original observation of Johnstone and collaborators of more than 30 years ago (Pan BT, Johnstone RM. Cell. 1983;33:967-978). According to a strikingly selective sorting process, the TfR becomes cargo destined to exocytosis while other molecules, including the most abundant RBC transmembrane protein, band 3, are completely retained in the cell membrane. It is also proposed that while this process could be operating in the early maturational steps in the bone marrow, additional mechanism(s) must be at play for the final removal of the excess reticulocyte membrane that is observed to occur in the circulation. This processing will most likely require the intervention of the spleen, whose function is also necessary for the continuous remodeling of the RBC membrane all along this cell's circulatory life.",
keywords = "Artificial red blood cells, Autophagy, Fluid phase endocytosis, Membrane rafts, Multivesicular endosome, Red blood cell ageing, Reticulocyte maturation, Spleen",
author = "Giampaolo Minetti and Cesare Achilli and Cesare Perotti and Annarita Ciana",
year = "2018",
month = "3",
day = "26",
doi = "10.3389/fphys.2018.00286",
language = "English",
volume = "9",
journal = "Frontiers in Physiology",
issn = "1664-042X",
publisher = "Frontiers Research Foundation",
number = "MAR",

}

TY - JOUR

T1 - Continuous change in membrane and membrane-skeleton organization during development from proerythroblast to senescent red blood cell

AU - Minetti, Giampaolo

AU - Achilli, Cesare

AU - Perotti, Cesare

AU - Ciana, Annarita

PY - 2018/3/26

Y1 - 2018/3/26

N2 - Within the context of erythropoiesis and the possibility of producing artificial red blood cells (RBCs) in vitro, a most critical step is the final differentiation of enucleated erythroblasts, or reticulocytes, to a fully mature biconcave discocyte, the RBC. Reviewed here is the current knowledge about this fundamental maturational process. By combining literature data with our own experimental evidence we propose that the early phase in the maturation of reticulocytes to RBCs is driven by a membrane raft-based mechanism for the sorting of disposable membrane proteins, mostly the no longer needed transferrin receptor (TfR), to the multivesicular endosome (MVE) as cargo of intraluminal vesicles that are subsequently exocytosed as exosomes, consistently with the seminal and original observation of Johnstone and collaborators of more than 30 years ago (Pan BT, Johnstone RM. Cell. 1983;33:967-978). According to a strikingly selective sorting process, the TfR becomes cargo destined to exocytosis while other molecules, including the most abundant RBC transmembrane protein, band 3, are completely retained in the cell membrane. It is also proposed that while this process could be operating in the early maturational steps in the bone marrow, additional mechanism(s) must be at play for the final removal of the excess reticulocyte membrane that is observed to occur in the circulation. This processing will most likely require the intervention of the spleen, whose function is also necessary for the continuous remodeling of the RBC membrane all along this cell's circulatory life.

AB - Within the context of erythropoiesis and the possibility of producing artificial red blood cells (RBCs) in vitro, a most critical step is the final differentiation of enucleated erythroblasts, or reticulocytes, to a fully mature biconcave discocyte, the RBC. Reviewed here is the current knowledge about this fundamental maturational process. By combining literature data with our own experimental evidence we propose that the early phase in the maturation of reticulocytes to RBCs is driven by a membrane raft-based mechanism for the sorting of disposable membrane proteins, mostly the no longer needed transferrin receptor (TfR), to the multivesicular endosome (MVE) as cargo of intraluminal vesicles that are subsequently exocytosed as exosomes, consistently with the seminal and original observation of Johnstone and collaborators of more than 30 years ago (Pan BT, Johnstone RM. Cell. 1983;33:967-978). According to a strikingly selective sorting process, the TfR becomes cargo destined to exocytosis while other molecules, including the most abundant RBC transmembrane protein, band 3, are completely retained in the cell membrane. It is also proposed that while this process could be operating in the early maturational steps in the bone marrow, additional mechanism(s) must be at play for the final removal of the excess reticulocyte membrane that is observed to occur in the circulation. This processing will most likely require the intervention of the spleen, whose function is also necessary for the continuous remodeling of the RBC membrane all along this cell's circulatory life.

KW - Artificial red blood cells

KW - Autophagy

KW - Fluid phase endocytosis

KW - Membrane rafts

KW - Multivesicular endosome

KW - Red blood cell ageing

KW - Reticulocyte maturation

KW - Spleen

UR - http://www.scopus.com/inward/record.url?scp=85044604044&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85044604044&partnerID=8YFLogxK

U2 - 10.3389/fphys.2018.00286

DO - 10.3389/fphys.2018.00286

M3 - Short survey

VL - 9

JO - Frontiers in Physiology

JF - Frontiers in Physiology

SN - 1664-042X

IS - MAR

M1 - 286

ER -