αI-spectrin represents evolutionary optimization of spectrin for red blood cell deformability.

Animals Biological Evolution Erythrocyte Deformability Erythrocyte Membrane Erythrocytes Mice Spectrin

Journal

Biophysical journal
ISSN: 1542-0086
Titre abrégé: Biophys J
Pays: United States
ID NLM: 0370626

Informations de publication

Date de publication:
07 09 2021
Historique:
received: 22 03 2021
revised: 21 07 2021
accepted: 28 07 2021
pubmed: 6 8 2021
medline: 29 10 2021
entrez: 5 8 2021
Statut: ppublish

Résumé

Spectrin tetramers of the membranes of enucleated mammalian erythrocytes play a critical role in red blood cell survival in circulation. One of the spectrins, αI, emerged in mammals with enucleated red cells after duplication of the ancestral α-spectrin gene common to all animals. The neofunctionalized αI-spectrin has moderate affinity for βI-spectrin, whereas αII-spectrin, expressed in nonerythroid cells, retains ancestral characteristics and has a 10-fold higher affinity for βI-spectrin. It has been hypothesized that this adaptation allows for rapid make and break of tetramers to accommodate membrane deformation. We have tested this hypothesis by generating mice with high-affinity spectrin tetramers formed by exchanging the site of tetramer formation in αI-spectrin (segments R0 and R1) for that of αII-spectrin. Erythrocytes with αIIβI presented normal hematologic parameters yet showed increased thermostability, and their membranes were significantly less deformable; under low shear forces, they displayed tumbling behavior rather than tank treading. The membrane skeleton is more stable with αIIβI and shows significantly less remodeling under deformation than red cell membranes of wild-type mice. These data demonstrate that spectrin tetramers undergo remodeling in intact erythrocytes and that this is required for the normal deformability of the erythrocyte membrane. We conclude that αI-spectrin represents evolutionary optimization of tetramer formation: neither higher-affinity tetramers (as shown here) nor lower affinity (as seen in hemolytic disease) can support the membrane properties required for effective tissue oxygenation in circulation.

Identifiants

DOI: 10.1016/j.bpj.2021.07.027 PMID: 34352252 PMC: PMC8456306
pubmed: 34352252
pii: S0006-3495(21)00637-8
doi: 10.1016/j.bpj.2021.07.027
pmc: PMC8456306
pii:
doi:

Substances chimiques

Spectrin 12634-43-4

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

3588-3599

Subventions

Organisme : NIDDK NIH HHS
ID : P01 DK032094
Pays : United States

Informations de copyright

Copyright © 2021 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Auteurs

John Hale (J)

The Red Cell Physiology Laboratory, The New York Blood Center, New York, New York. Electronic address: jhale@nybc.org.

Xiuli An (X)

Membrane Biology Laboratory, The New York Blood Center, New York, New York.

Xinhua Guo (X)

Membrane Biology Laboratory, The New York Blood Center, New York, New York.

Erjing Gao (E)

The Red Cell Physiology Laboratory, The New York Blood Center, New York, New York.

Julien Papoin (J)

Nelkin Laboratory of Pediatric Oncology and Laboratory of Developmental Erythropoiesis, The Feinstein Institutes for Medical Research, Manhasset, New York.

Lionel Blanc (L)

Nelkin Laboratory of Pediatric Oncology and Laboratory of Developmental Erythropoiesis, The Feinstein Institutes for Medical Research, Manhasset, New York; Department of Molecular Medicine and Pediatrics, Zucker School of Medicine at Hofstra/Northwell, Hempstead, New York.

Christopher D Hillyer (CD)

The Red Cell Physiology Laboratory, The New York Blood Center, New York, New York.

Walter Gratzer (W)

Randall Division of Cell and Molecular Biophysics, King's College London, London, United Kingdom.

Anthony Baines (A)

Department of Biosciences, University of Kent, Canterbury, United Kingdom.

Narla Mohandas (N)

The Red Cell Physiology Laboratory, The New York Blood Center, New York, New York.

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Classifications MeSH

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questionsmedicales.fr › Phénomènes biologiques › Évolution biologique › αI-spectrin represents evolutionary...
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questionsmedicales.fr › Systèmes sanguin et immunitaire › Sang › Cellules sanguines › Érythrocytes › Membrane érythrocytaire › αI-spectrin represents evolutionary...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Sang › Cellules sanguines › Érythrocytes › αI-spectrin represents evolutionary...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › αI-spectrin represents evolutionary...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Spectrine › αI-spectrin represents evolutionary...