BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice

Abstract: Genetic depletion of the transcriptional repressor BCL11A in red blood cell precursors alleviates β-hemoglobinopathies by inducing the fetal γ-globin genes. However, additional erythroid genes are regulated by BCL11A and the effects of its deficiency on erythropoiesis are insufficiently de...

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Main Authors: Yoonjeong Jang, Ruopeng Feng, Lance E. Palmer, Thiyagaraj Mayuranathan, Yu Yao, Kalin Mayberry, Sheng Zhou, Jian Xu, Jeffrey M. Gossett, Guolian Kang, Yong Cheng, Jonathan S. Yen, Mitchell J. Weiss
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Blood Advances
Online Access:http://www.sciencedirect.com/science/article/pii/S2473952925001338
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author Yoonjeong Jang
Ruopeng Feng
Lance E. Palmer
Thiyagaraj Mayuranathan
Yu Yao
Kalin Mayberry
Sheng Zhou
Jian Xu
Jeffrey M. Gossett
Guolian Kang
Yong Cheng
Jonathan S. Yen
Mitchell J. Weiss
author_facet Yoonjeong Jang
Ruopeng Feng
Lance E. Palmer
Thiyagaraj Mayuranathan
Yu Yao
Kalin Mayberry
Sheng Zhou
Jian Xu
Jeffrey M. Gossett
Guolian Kang
Yong Cheng
Jonathan S. Yen
Mitchell J. Weiss
author_sort Yoonjeong Jang
collection DOAJ
description Abstract: Genetic depletion of the transcriptional repressor BCL11A in red blood cell precursors alleviates β-hemoglobinopathies by inducing the fetal γ-globin genes. However, additional erythroid genes are regulated by BCL11A and the effects of its deficiency on erythropoiesis are insufficiently described. We discovered that Cas9 disruption of the BCL11A intron 2 erythroid enhancer in CD34+ hematopoietic stem and progenitor cells using a clinically approved strategy caused impaired expansion and apoptosis of erythroid precursors in vitro and reduced repopulation of the erythroid compartment after xenotransplantation into immunodeficient mice. Mutant colony-forming unit erythroid cells, proerythroblasts, and basophilic erythroblasts exhibited dysregulation of 94 genes (more than twofold change, false discovery rate < 0.05), 25 of which are likely direct targets of BCL11A. Differentially expressed genes were associated with a range of biological pathways that affect cell expansion and survival. Our findings reveal that BCL11A regulates additional aspects of erythropoiesis beyond γ-globin gene repression, with unknown clinical consequences.
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spelling doaj-art-5cca6e32ced04c53aaeca7716f5f21fe2025-08-20T02:34:53ZengElsevierBlood Advances2473-95292025-06-019112722273210.1182/bloodadvances.2024015574BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into miceYoonjeong Jang0Ruopeng Feng1Lance E. Palmer2Thiyagaraj Mayuranathan3Yu Yao4Kalin Mayberry5Sheng Zhou6Jian Xu7Jeffrey M. Gossett8Guolian Kang9Yong Cheng10Jonathan S. Yen11Mitchell J. Weiss12Department of Hematology, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TN; Center for Stem Cell Research (a unit of inStem, Bengaluru), Christian Medical College Campus, Vellore, IndiaDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TNExperimental Cellular Therapeutics Laboratory, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Pathology, Center of Excellence for Leukemia Studies, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Biostatistics, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Biostatistics, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TNDepartment of Hematology, St. Jude Children’s Research Hospital, Memphis, TN; Jonathan S. Yen, Department of Hematology, St. Jude Children’s Research Hospital, 262 Danny Thomas Pl, MS#355, Memphis, TN 38105-3678;Department of Hematology, St. Jude Children’s Research Hospital, Memphis, TN; Correspondence: Mitchell J. Weiss, Department of Hematology, St. Jude Children’s Research Hospital, 262 Danny Thomas Pl, MS#355, Memphis, TN 38105-3678;Abstract: Genetic depletion of the transcriptional repressor BCL11A in red blood cell precursors alleviates β-hemoglobinopathies by inducing the fetal γ-globin genes. However, additional erythroid genes are regulated by BCL11A and the effects of its deficiency on erythropoiesis are insufficiently described. We discovered that Cas9 disruption of the BCL11A intron 2 erythroid enhancer in CD34+ hematopoietic stem and progenitor cells using a clinically approved strategy caused impaired expansion and apoptosis of erythroid precursors in vitro and reduced repopulation of the erythroid compartment after xenotransplantation into immunodeficient mice. Mutant colony-forming unit erythroid cells, proerythroblasts, and basophilic erythroblasts exhibited dysregulation of 94 genes (more than twofold change, false discovery rate < 0.05), 25 of which are likely direct targets of BCL11A. Differentially expressed genes were associated with a range of biological pathways that affect cell expansion and survival. Our findings reveal that BCL11A regulates additional aspects of erythropoiesis beyond γ-globin gene repression, with unknown clinical consequences.http://www.sciencedirect.com/science/article/pii/S2473952925001338
spellingShingle Yoonjeong Jang
Ruopeng Feng
Lance E. Palmer
Thiyagaraj Mayuranathan
Yu Yao
Kalin Mayberry
Sheng Zhou
Jian Xu
Jeffrey M. Gossett
Guolian Kang
Yong Cheng
Jonathan S. Yen
Mitchell J. Weiss
BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
Blood Advances
title BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
title_full BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
title_fullStr BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
title_full_unstemmed BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
title_short BCL11A-deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
title_sort bcl11a deficient human erythropoiesis is impaired in vitro and after xenotransplantation into mice
url http://www.sciencedirect.com/science/article/pii/S2473952925001338
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