Cargando…
Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes
The red blood cell (RBC) is remarkable in its ability to deform as it passages through the vasculature. Its deformability derives from a spectrin-actin protein network that supports the cell membrane and provides strength and flexibility, however questions remain regarding the assembly and maintenan...
Autores principales: | , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Elsevier
2021
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8688873/ https://www.ncbi.nlm.nih.gov/pubmed/34977554 http://dx.doi.org/10.1016/j.yjsbx.2021.100056 |
_version_ | 1784618438853918720 |
---|---|
author | Blanch, Adam J. Nunez-Iglesias, Juan Namvar, Arman Menant, Sebastien Looker, Oliver Rajagopal, Vijay Tham, Wai-Hong Tilley, Leann Dixon, Matthew W.A. |
author_facet | Blanch, Adam J. Nunez-Iglesias, Juan Namvar, Arman Menant, Sebastien Looker, Oliver Rajagopal, Vijay Tham, Wai-Hong Tilley, Leann Dixon, Matthew W.A. |
author_sort | Blanch, Adam J. |
collection | PubMed |
description | The red blood cell (RBC) is remarkable in its ability to deform as it passages through the vasculature. Its deformability derives from a spectrin-actin protein network that supports the cell membrane and provides strength and flexibility, however questions remain regarding the assembly and maintenance of the skeletal network. Using scanning electron microscopy (SEM) and atomic force microscopy (AFM) we have examined the nanoscale architecture of the cytoplasmic side of membrane discs prepared from reticulocytes and mature RBCs. Immunofluorescence microscopy was used to probe the distribution of spectrin and other membrane skeleton proteins. We found that the cell surface area decreases by up to 30% and the spectrin-actin network increases in density by approximately 20% as the reticulocyte matures. By contrast, the inter-junctional distance and junctional density increase only by 3–4% and 5–9%, respectively. This suggests that the maturation-associated reduction in surface area is accompanied by an increase in spectrin self-association to form higher order oligomers. We also examined the mature RBC membrane in the edge (rim) and face (dimple) regions of mature RBCs and found the rim contains about 1.5% more junctional complexes compared to the dimple region. A 2% increase in band 4.1 density in the rim supports these structural measurements. |
format | Online Article Text |
id | pubmed-8688873 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Elsevier |
record_format | MEDLINE/PubMed |
spelling | pubmed-86888732021-12-30 Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes Blanch, Adam J. Nunez-Iglesias, Juan Namvar, Arman Menant, Sebastien Looker, Oliver Rajagopal, Vijay Tham, Wai-Hong Tilley, Leann Dixon, Matthew W.A. J Struct Biol X Review Article The red blood cell (RBC) is remarkable in its ability to deform as it passages through the vasculature. Its deformability derives from a spectrin-actin protein network that supports the cell membrane and provides strength and flexibility, however questions remain regarding the assembly and maintenance of the skeletal network. Using scanning electron microscopy (SEM) and atomic force microscopy (AFM) we have examined the nanoscale architecture of the cytoplasmic side of membrane discs prepared from reticulocytes and mature RBCs. Immunofluorescence microscopy was used to probe the distribution of spectrin and other membrane skeleton proteins. We found that the cell surface area decreases by up to 30% and the spectrin-actin network increases in density by approximately 20% as the reticulocyte matures. By contrast, the inter-junctional distance and junctional density increase only by 3–4% and 5–9%, respectively. This suggests that the maturation-associated reduction in surface area is accompanied by an increase in spectrin self-association to form higher order oligomers. We also examined the mature RBC membrane in the edge (rim) and face (dimple) regions of mature RBCs and found the rim contains about 1.5% more junctional complexes compared to the dimple region. A 2% increase in band 4.1 density in the rim supports these structural measurements. Elsevier 2021-12-08 /pmc/articles/PMC8688873/ /pubmed/34977554 http://dx.doi.org/10.1016/j.yjsbx.2021.100056 Text en © 2021 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
spellingShingle | Review Article Blanch, Adam J. Nunez-Iglesias, Juan Namvar, Arman Menant, Sebastien Looker, Oliver Rajagopal, Vijay Tham, Wai-Hong Tilley, Leann Dixon, Matthew W.A. Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title | Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title_full | Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title_fullStr | Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title_full_unstemmed | Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title_short | Multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
title_sort | multimodal imaging reveals membrane skeleton reorganisation during reticulocyte maturation and differences in dimple and rim regions of mature erythrocytes |
topic | Review Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8688873/ https://www.ncbi.nlm.nih.gov/pubmed/34977554 http://dx.doi.org/10.1016/j.yjsbx.2021.100056 |
work_keys_str_mv | AT blanchadamj multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT nuneziglesiasjuan multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT namvararman multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT menantsebastien multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT lookeroliver multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT rajagopalvijay multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT thamwaihong multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT tilleyleann multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes AT dixonmatthewwa multimodalimagingrevealsmembraneskeletonreorganisationduringreticulocytematurationanddifferencesindimpleandrimregionsofmatureerythrocytes |