Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating

Abstract Hematopoietic ontogeny is characterized by distinct primitive and definitive erythroid lineages. Definitive erythroblasts mature and enucleate extravascularly and form a unique membrane skeleton, composed of spectrin, 4.1R-complex, and ankyrinR-complex components, to survive the vicissitude...

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Autores principales: Yu-Shan Huang, Luis F. Delgadillo, Kathryn H. Cyr, Paul D. Kingsley, Xiuli An, Kathleen E. McGrath, Narla Mohandas, John G. Conboy, Richard E. Waugh, Jiandi Wan, James Palis
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Publicado: Nature Portfolio 2017
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Acceso en línea:https://doaj.org/article/59ae1bf1686e4ba7bff3a96a98431c78
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spelling oai:doaj.org-article:59ae1bf1686e4ba7bff3a96a98431c782021-12-02T16:06:17ZCirculating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating10.1038/s41598-017-05498-42045-2322https://doaj.org/article/59ae1bf1686e4ba7bff3a96a98431c782017-07-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-05498-4https://doaj.org/toc/2045-2322Abstract Hematopoietic ontogeny is characterized by distinct primitive and definitive erythroid lineages. Definitive erythroblasts mature and enucleate extravascularly and form a unique membrane skeleton, composed of spectrin, 4.1R-complex, and ankyrinR-complex components, to survive the vicissitudes of the adult circulation. However, little is known about the formation and composition of the membrane skeleton in primitive erythroblasts, which progressively mature while circulating in the embryonic bloodstream. We found that primary primitive erythroblasts express the major membrane skeleton genes present in similarly staged definitive erythroblasts, suggesting that the composition and formation of this membrane network is conserved in maturing primitive and definitive erythroblasts despite their respective intravascular and extravascular locations. Membrane deformability and stability of primitive erythroblasts, assayed by microfluidic studies and fluorescence imaged microdeformation, respectively, significantly increase prior to enucleation. These functional changes coincide with protein 4.1 R isoform switching and protein 4.1R-null primitive erythroblasts fail to establish normal membrane stability and deformability. We conclude that maturing primitive erythroblasts initially navigate the embryonic vasculature prior to establishing a deformable cytoskeleton, which is ultimately formed prior to enucleation. Formation of an erythroid-specific, protein 4.1R-dependent membrane skeleton is an important feature not only of definitive, but also of primitive, erythropoiesis in mammals.Yu-Shan HuangLuis F. DelgadilloKathryn H. CyrPaul D. KingsleyXiuli AnKathleen E. McGrathNarla MohandasJohn G. ConboyRichard E. WaughJiandi WanJames PalisNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-11 (2017)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Yu-Shan Huang
Luis F. Delgadillo
Kathryn H. Cyr
Paul D. Kingsley
Xiuli An
Kathleen E. McGrath
Narla Mohandas
John G. Conboy
Richard E. Waugh
Jiandi Wan
James Palis
Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
description Abstract Hematopoietic ontogeny is characterized by distinct primitive and definitive erythroid lineages. Definitive erythroblasts mature and enucleate extravascularly and form a unique membrane skeleton, composed of spectrin, 4.1R-complex, and ankyrinR-complex components, to survive the vicissitudes of the adult circulation. However, little is known about the formation and composition of the membrane skeleton in primitive erythroblasts, which progressively mature while circulating in the embryonic bloodstream. We found that primary primitive erythroblasts express the major membrane skeleton genes present in similarly staged definitive erythroblasts, suggesting that the composition and formation of this membrane network is conserved in maturing primitive and definitive erythroblasts despite their respective intravascular and extravascular locations. Membrane deformability and stability of primitive erythroblasts, assayed by microfluidic studies and fluorescence imaged microdeformation, respectively, significantly increase prior to enucleation. These functional changes coincide with protein 4.1 R isoform switching and protein 4.1R-null primitive erythroblasts fail to establish normal membrane stability and deformability. We conclude that maturing primitive erythroblasts initially navigate the embryonic vasculature prior to establishing a deformable cytoskeleton, which is ultimately formed prior to enucleation. Formation of an erythroid-specific, protein 4.1R-dependent membrane skeleton is an important feature not only of definitive, but also of primitive, erythropoiesis in mammals.
format article
author Yu-Shan Huang
Luis F. Delgadillo
Kathryn H. Cyr
Paul D. Kingsley
Xiuli An
Kathleen E. McGrath
Narla Mohandas
John G. Conboy
Richard E. Waugh
Jiandi Wan
James Palis
author_facet Yu-Shan Huang
Luis F. Delgadillo
Kathryn H. Cyr
Paul D. Kingsley
Xiuli An
Kathleen E. McGrath
Narla Mohandas
John G. Conboy
Richard E. Waugh
Jiandi Wan
James Palis
author_sort Yu-Shan Huang
title Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
title_short Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
title_full Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
title_fullStr Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
title_full_unstemmed Circulating primitive erythroblasts establish a functional, protein 4.1R-dependent cytoskeletal network prior to enucleating
title_sort circulating primitive erythroblasts establish a functional, protein 4.1r-dependent cytoskeletal network prior to enucleating
publisher Nature Portfolio
publishDate 2017
url https://doaj.org/article/59ae1bf1686e4ba7bff3a96a98431c78
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