Centrosome function is critical during terminal erythroid differentiation

Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule‐organizing center, is requ...

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Published inThe EMBO journal Vol. 41; no. 14; pp. e108739 - n/a
Main Authors Tátrai, Péter, Gergely, Fanni
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 18.07.2022
Blackwell Publishing Ltd
John Wiley and Sons Inc
Subjects
Anemia
Anemia, Macrocytic
Animals
blood
Cell Cycle Proteins - genetics
Cell differentiation
Centrosome
Centrosomes
Chemotherapy
Chromosome Segregation
Chromosomes
Depletion
Differentiation
EMBO06
EMBO11
EMBO18
Embryo fibroblasts
Enucleation
Erythroblasts
Erythrocytes
Erythroid cells
Erythropoiesis
Fetuses
Fibroblasts
Liver
Mice
Microtubules
Mitosis
mitotic spindle
Morphology
Nutrient deficiency
p53 Protein
Progenitor cells
Reticulocytes
Spindle Apparatus - genetics
Spindles
Tetraploidy
erythropoiesis
centrosome
blood
enucleation
mitotic spindle
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Abstract Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule‐organizing center, is required as well. Mice lacking the conserved centrosome component, CDK5RAP2, are likely to have defective erythroid differentiation because they develop macrocytic anemia. Here, we show that fetal liver‐derived, CDK5RAP2‐deficient erythroid progenitors generate fewer and larger reticulocytes, hence recapitulating features of macrocytic anemia. In erythroblasts, but not in embryonic fibroblasts, loss of CDK5RAP2 or pharmacological depletion of centrosomes leads to highly aberrant spindle morphologies. Consistent with such cells exiting mitosis without chromosome segregation, tetraploidy is frequent in late‐stage erythroblasts, thereby giving rise to fewer but larger reticulocytes than normal. Our results define a critical role for CDK5RAP2 and centrosomes in spindle formation specifically during blood production. We propose that disruption of centrosome and spindle function could contribute to the emergence of macrocytic anemias, for instance, due to nutritional deficiency or exposure to chemotherapy. Synopsis Immature erythroid cells differentiate into red blood cells by undergoing a defined number of cell divisions followed by ejection of their nuclei. This study investigates the role of centrosomes in this process using ex vivo differentiation of fetal liver‐derived erythroid progenitors in mice. The conserved centrosomal protein CDK5RAP2 facilitates erythroid differentiation both ex vivo and in vivo Centrosomes and CDK5RAP2 are crucial for normal spindle assembly in erythroblasts but not in embryonic fibroblasts Erythroblasts lacking CDK5RAP2 or centrosomes develop tetraploidy TP53 is activated in erythroblasts lacking CDK5RAP2 or centrosomes but is not responsible for the observed defects in erythropoiesis Unlike embryonic fibroblasts, erythroblasts do not expand their centrosomes in mitosis Graphical Abstract While centrosomal CDK5RAP2 is not essential for gamma‐tubulin recruitment during the mammalian cell cycle, its absence causes erythroid enucleation defects leading to macrocytic anemia.
AbstractList Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule-organizing center, is required as well. Mice lacking the conserved centrosome component, CDK5RAP2, are likely to have defective erythroid differentiation because they develop macrocytic anemia. Here, we show that fetal liver-derived, CDK5RAP2-deficient erythroid progenitors generate fewer and larger reticulocytes, hence recapitulating features of macrocytic anemia. In erythroblasts, but not in embryonic fibroblasts, loss of CDK5RAP2 or pharmacological depletion of centrosomes leads to highly aberrant spindle morphologies. Consistent with such cells exiting mitosis without chromosome segregation, tetraploidy is frequent in late-stage erythroblasts, thereby giving rise to fewer but larger reticulocytes than normal. Our results define a critical role for CDK5RAP2 and centrosomes in spindle formation specifically during blood production. We propose that disruption of centrosome and spindle function could contribute to the emergence of macrocytic anemias, for instance, due to nutritional deficiency or exposure to chemotherapy.
Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule‐organizing center, is required as well. Mice lacking the conserved centrosome component, CDK5RAP2, are likely to have defective erythroid differentiation because they develop macrocytic anemia. Here, we show that fetal liver‐derived, CDK5RAP2‐deficient erythroid progenitors generate fewer and larger reticulocytes, hence recapitulating features of macrocytic anemia. In erythroblasts, but not in embryonic fibroblasts, loss of CDK5RAP2 or pharmacological depletion of centrosomes leads to highly aberrant spindle morphologies. Consistent with such cells exiting mitosis without chromosome segregation, tetraploidy is frequent in late‐stage erythroblasts, thereby giving rise to fewer but larger reticulocytes than normal. Our results define a critical role for CDK5RAP2 and centrosomes in spindle formation specifically during blood production. We propose that disruption of centrosome and spindle function could contribute to the emergence of macrocytic anemias, for instance, due to nutritional deficiency or exposure to chemotherapy. Synopsis Immature erythroid cells differentiate into red blood cells by undergoing a defined number of cell divisions followed by ejection of their nuclei. This study investigates the role of centrosomes in this process using ex vivo differentiation of fetal liver‐derived erythroid progenitors in mice. The conserved centrosomal protein CDK5RAP2 facilitates erythroid differentiation both ex vivo and in vivo Centrosomes and CDK5RAP2 are crucial for normal spindle assembly in erythroblasts but not in embryonic fibroblasts Erythroblasts lacking CDK5RAP2 or centrosomes develop tetraploidy TP53 is activated in erythroblasts lacking CDK5RAP2 or centrosomes but is not responsible for the observed defects in erythropoiesis Unlike embryonic fibroblasts, erythroblasts do not expand their centrosomes in mitosis While centrosomal CDK5RAP2 is not essential for gamma‐tubulin recruitment during the mammalian cell cycle, its absence causes erythroid enucleation defects leading to macrocytic anemia.
Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule‐organizing center, is required as well. Mice lacking the conserved centrosome component, CDK5RAP2, are likely to have defective erythroid differentiation because they develop macrocytic anemia. Here, we show that fetal liver‐derived, CDK5RAP2‐deficient erythroid progenitors generate fewer and larger reticulocytes, hence recapitulating features of macrocytic anemia. In erythroblasts, but not in embryonic fibroblasts, loss of CDK5RAP2 or pharmacological depletion of centrosomes leads to highly aberrant spindle morphologies. Consistent with such cells exiting mitosis without chromosome segregation, tetraploidy is frequent in late‐stage erythroblasts, thereby giving rise to fewer but larger reticulocytes than normal. Our results define a critical role for CDK5RAP2 and centrosomes in spindle formation specifically during blood production. We propose that disruption of centrosome and spindle function could contribute to the emergence of macrocytic anemias, for instance, due to nutritional deficiency or exposure to chemotherapy. While centrosomal CDK5RAP2 is not essential for gamma‐tubulin recruitment during the mammalian cell cycle, its absence causes erythroid enucleation defects leading to macrocytic anemia.
Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated reticulocytes. Microtubules are important for enucleation, but it is not known if the centrosome, a key microtubule‐organizing center, is required as well. Mice lacking the conserved centrosome component, CDK5RAP2, are likely to have defective erythroid differentiation because they develop macrocytic anemia. Here, we show that fetal liver‐derived, CDK5RAP2‐deficient erythroid progenitors generate fewer and larger reticulocytes, hence recapitulating features of macrocytic anemia. In erythroblasts, but not in embryonic fibroblasts, loss of CDK5RAP2 or pharmacological depletion of centrosomes leads to highly aberrant spindle morphologies. Consistent with such cells exiting mitosis without chromosome segregation, tetraploidy is frequent in late‐stage erythroblasts, thereby giving rise to fewer but larger reticulocytes than normal. Our results define a critical role for CDK5RAP2 and centrosomes in spindle formation specifically during blood production. We propose that disruption of centrosome and spindle function could contribute to the emergence of macrocytic anemias, for instance, due to nutritional deficiency or exposure to chemotherapy. Synopsis Immature erythroid cells differentiate into red blood cells by undergoing a defined number of cell divisions followed by ejection of their nuclei. This study investigates the role of centrosomes in this process using ex vivo differentiation of fetal liver‐derived erythroid progenitors in mice. The conserved centrosomal protein CDK5RAP2 facilitates erythroid differentiation both ex vivo and in vivo Centrosomes and CDK5RAP2 are crucial for normal spindle assembly in erythroblasts but not in embryonic fibroblasts Erythroblasts lacking CDK5RAP2 or centrosomes develop tetraploidy TP53 is activated in erythroblasts lacking CDK5RAP2 or centrosomes but is not responsible for the observed defects in erythropoiesis Unlike embryonic fibroblasts, erythroblasts do not expand their centrosomes in mitosis Graphical Abstract While centrosomal CDK5RAP2 is not essential for gamma‐tubulin recruitment during the mammalian cell cycle, its absence causes erythroid enucleation defects leading to macrocytic anemia.
Author Tátrai, Péter
Gergely, Fanni
AuthorAffiliation 3 Present address: Solvo Biotechnology Budapest Hungary
2 Department of Biochemistry University of Oxford Oxford UK
1 Cancer Research UK Cambridge Institute Li Ka Shing Centre University of Cambridge Cambridge UK
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Issue 14
Keywords erythropoiesis
centrosome
blood
enucleation
mitotic spindle
Language English
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Snippet Red blood cells are produced by terminal erythroid differentiation, which involves the dramatic morphological transformation of erythroblasts into enucleated...
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StartPage e108739
SubjectTerms Anemia
Anemia, Macrocytic
Animals
blood
Cell Cycle Proteins - genetics
Cell differentiation
Centrosome
Centrosomes
Chemotherapy
Chromosome Segregation
Chromosomes
Depletion
Differentiation
EMBO06
EMBO11
EMBO18
Embryo fibroblasts
Enucleation
Erythroblasts
Erythrocytes
Erythroid cells
Erythropoiesis
Fetuses
Fibroblasts
Liver
Mice
Microtubules
Mitosis
mitotic spindle
Morphology
Nutrient deficiency
p53 Protein
Progenitor cells
Reticulocytes
Spindle Apparatus - genetics
Spindles
Tetraploidy
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Title Centrosome function is critical during terminal erythroid differentiation
URI https://link.springer.com/article/10.15252/embj.2021108739
https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fembj.2021108739
https://www.ncbi.nlm.nih.gov/pubmed/35678476
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Volume 41
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