Modular UBE2H-CTLH E2-E3 complexes regulate erythroid maturation

The development of haematopoietic stem cells into mature erythrocytes – erythropoiesis – is a controlled process characterized by cellular reorganization and drastic reshaping of the proteome landscape. Failure of ordered erythropoiesis is associated with anaemias and haematological malignancies. Al...

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Published ineLife Vol. 11
Main Authors Sherpa, Dawafuti, Mueller, Judith, Karayel, Özge, Xu, Peng, Yao, Yu, Chrustowicz, Jakub, Gottemukkala, Karthik V, Baumann, Christine, Gross, Annette, Czarnecki, Oliver, Zhang, Wei, Gu, Jun, Nilvebrant, Johan, Sidhu, Sachdev S, Murray, Peter J, Mann, Matthias, Weiss, Mitchell J, Schulman, Brenda A, Alpi, Arno F
Format Journal Article
LanguageEnglish
Published England eLife Sciences Publications Ltd 02.12.2022
eLife Sciences Publications, Ltd
Subjects
Blood cancer
Cell Biology
Cell cycle
CRISPR
CTLH E3 complex
E3 ubiquitin ligase
Enucleation
Enzymes
Erythrocytes
Erythropoiesis
Gene expression
Guanine Nucleotide Exchange Factors
Hematopoietic stem cells
Human
Humans
Malignancy
Maturation
Microtubule-Associated Proteins
Post-translation
Progenitor cells
Proteins
Proteome
Proteomes
Proteomics
Reproducibility
Stem cells
UBE2H
Ubiquitin
Ubiquitin-conjugating enzyme
Ubiquitin-Conjugating Enzymes - genetics
Ubiquitin-protein ligase
Ubiquitylation
CTLH E3 complex
UBE2H
cell biology
proteomics
Ubiquitylation
E3 ubiquitin ligase
erythropoiesis
human
Online AccessGet full text
ISSN2050-084X
2050-084X
DOI10.7554/eLife.77937

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Abstract The development of haematopoietic stem cells into mature erythrocytes – erythropoiesis – is a controlled process characterized by cellular reorganization and drastic reshaping of the proteome landscape. Failure of ordered erythropoiesis is associated with anaemias and haematological malignancies. Although the ubiquitin system is a known crucial post-translational regulator in erythropoiesis, how the erythrocyte is reshaped by the ubiquitin system is poorly understood. By measuring the proteomic landscape of in vitro human erythropoiesis models, we found dynamic differential expression of subunits of the CTLH E3 ubiquitin ligase complex that formed maturation stage-dependent assemblies of topologically homologous RANBP9- and RANBP10-CTLH complexes. Moreover, protein abundance of CTLH’s cognate E2 ubiquitin conjugating enzyme UBE2H increased during terminal differentiation, and UBE2H expression depended on catalytically active CTLH E3 complexes. CRISPR-Cas9-mediated inactivation of CTLH E3 assemblies or UBE2H in erythroid progenitors revealed defects, including spontaneous and accelerated erythroid maturation as well as inefficient enucleation. Thus, we propose that dynamic maturation stage-specific changes of UBE2H-CTLH E2-E3 modules control the orderly progression of human erythropoiesis.
AbstractList The development of haematopoietic stem cells into mature erythrocytes - erythropoiesis - is a controlled process characterized by cellular reorganization and drastic reshaping of the proteome landscape. Failure of ordered erythropoiesis is associated with anaemias and haematological malignancies. Although the ubiquitin system is a known crucial post-translational regulator in erythropoiesis, how the erythrocyte is reshaped by the ubiquitin system is poorly understood. By measuring the proteomic landscape of in vitro human erythropoiesis models, we found dynamic differential expression of subunits of the CTLH E3 ubiquitin ligase complex that formed maturation stage-dependent assemblies of topologically homologous RANBP9- and RANBP10-CTLH complexes. Moreover, protein abundance of CTLH's cognate E2 ubiquitin conjugating enzyme UBE2H increased during terminal differentiation, and UBE2H expression depended on catalytically active CTLH E3 complexes. CRISPR-Cas9-mediated inactivation of CTLH E3 assemblies or UBE2H in erythroid progenitors revealed defects, including spontaneous and accelerated erythroid maturation as well as inefficient enucleation. Thus, we propose that dynamic maturation stage-specific changes of UBE2H-CTLH E2-E3 modules control the orderly progression of human erythropoiesis.
The development of haematopoietic stem cells into mature erythrocytes - erythropoiesis - is a controlled process characterized by cellular reorganization and drastic reshaping of the proteome landscape. Failure of ordered erythropoiesis is associated with anaemias and haematological malignancies. Although the ubiquitin system is a known crucial post-translational regulator in erythropoiesis, how the erythrocyte is reshaped by the ubiquitin system is poorly understood. By measuring the proteomic landscape of in vitro human erythropoiesis models, we found dynamic differential expression of subunits of the CTLH E3 ubiquitin ligase complex that formed maturation stage-dependent assemblies of topologically homologous RANBP9- and RANBP10-CTLH complexes. Moreover, protein abundance of CTLH's cognate E2 ubiquitin conjugating enzyme UBE2H increased during terminal differentiation, and UBE2H expression depended on catalytically active CTLH E3 complexes. CRISPR-Cas9-mediated inactivation of CTLH E3 assemblies or UBE2H in erythroid progenitors revealed defects, including spontaneous and accelerated erythroid maturation as well as inefficient enucleation. Thus, we propose that dynamic maturation stage-specific changes of UBE2H-CTLH E2-E3 modules control the orderly progression of human erythropoiesis.The development of haematopoietic stem cells into mature erythrocytes - erythropoiesis - is a controlled process characterized by cellular reorganization and drastic reshaping of the proteome landscape. Failure of ordered erythropoiesis is associated with anaemias and haematological malignancies. Although the ubiquitin system is a known crucial post-translational regulator in erythropoiesis, how the erythrocyte is reshaped by the ubiquitin system is poorly understood. By measuring the proteomic landscape of in vitro human erythropoiesis models, we found dynamic differential expression of subunits of the CTLH E3 ubiquitin ligase complex that formed maturation stage-dependent assemblies of topologically homologous RANBP9- and RANBP10-CTLH complexes. Moreover, protein abundance of CTLH's cognate E2 ubiquitin conjugating enzyme UBE2H increased during terminal differentiation, and UBE2H expression depended on catalytically active CTLH E3 complexes. CRISPR-Cas9-mediated inactivation of CTLH E3 assemblies or UBE2H in erythroid progenitors revealed defects, including spontaneous and accelerated erythroid maturation as well as inefficient enucleation. Thus, we propose that dynamic maturation stage-specific changes of UBE2H-CTLH E2-E3 modules control the orderly progression of human erythropoiesis.
Author Xu, Peng
Gross, Annette
Gottemukkala, Karthik V
Zhang, Wei
Nilvebrant, Johan
Chrustowicz, Jakub
Czarnecki, Oliver
Sherpa, Dawafuti
Mueller, Judith
Sidhu, Sachdev S
Mann, Matthias
Weiss, Mitchell J
Yao, Yu
Murray, Peter J
Karayel, Özge
Alpi, Arno F
Schulman, Brenda A
Baumann, Christine
Gu, Jun
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Keywords CTLH E3 complex
UBE2H
cell biology
proteomics
Ubiquitylation
E3 ubiquitin ligase
erythropoiesis
human
Language English
License 2022, Sherpa, Mueller, Karayel et al.
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Department of Molecular and Cellular Biology, College of Biological Science, University of Guelph, Guelph, Canada.
These authors contributed equally to this work.
Division of Protein Engineering, School of Chemistry, Biotechnology and Health, Royal Institute of Technology, Stockholm, Sweden.
Institute of Diabetes and Regeneration Research, Helmholtz Centre Munich, Neuherberg, Germany.
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Snippet The development of haematopoietic stem cells into mature erythrocytes – erythropoiesis – is a controlled process characterized by cellular reorganization and...
The development of haematopoietic stem cells into mature erythrocytes - erythropoiesis - is a controlled process characterized by cellular reorganization and...
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SubjectTerms Blood cancer
Cell Biology
Cell cycle
CRISPR
CTLH E3 complex
E3 ubiquitin ligase
Enucleation
Enzymes
Erythrocytes
Erythropoiesis
Gene expression
Guanine Nucleotide Exchange Factors
Hematopoietic stem cells
Human
Humans
Malignancy
Maturation
Microtubule-Associated Proteins
Post-translation
Progenitor cells
Proteins
Proteome
Proteomes
Proteomics
Reproducibility
Stem cells
UBE2H
Ubiquitin
Ubiquitin-conjugating enzyme
Ubiquitin-Conjugating Enzymes - genetics
Ubiquitin-protein ligase
Ubiquitylation
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Title Modular UBE2H-CTLH E2-E3 complexes regulate erythroid maturation
URI https://www.ncbi.nlm.nih.gov/pubmed/36459484
https://www.proquest.com/docview/2759791935
https://www.proquest.com/docview/2746389732
https://pubmed.ncbi.nlm.nih.gov/PMC9718529
https://urn.kb.se/resolve?urn=urn:nbn:se:kth:diva-322617
https://doaj.org/article/34cf5cd0625f4e91870c6fb2f280211e
Volume 11
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