Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models

We previously showed correction of sickle cell anemia (SCA) in mice utilizing a lentiviral vector (LV) expressing human γ-globin. Herein, we made a G16D mutation in the γ-globin gene to generate the G16D mutation (GbGM) LV to increase fetal hemoglobin formation. We also generated an insulated versio...

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Main Authors: Archana Shrestha, Devin M. Pillis, Sydney Felker, Mengna Chi, Kimberly Wagner, Oluwabukola T. Gbotosho, Joseph Sieling, Mohammad Shadid, Punam Malik
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Molecular Therapy: Methods & Clinical Development
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Online Access:http://www.sciencedirect.com/science/article/pii/S2329050125000348
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author Archana Shrestha
Devin M. Pillis
Sydney Felker
Mengna Chi
Kimberly Wagner
Oluwabukola T. Gbotosho
Joseph Sieling
Mohammad Shadid
Punam Malik
author_facet Archana Shrestha
Devin M. Pillis
Sydney Felker
Mengna Chi
Kimberly Wagner
Oluwabukola T. Gbotosho
Joseph Sieling
Mohammad Shadid
Punam Malik
author_sort Archana Shrestha
collection DOAJ
description We previously showed correction of sickle cell anemia (SCA) in mice utilizing a lentiviral vector (LV) expressing human γ-globin. Herein, we made a G16D mutation in the γ-globin gene to generate the G16D mutation (GbGM) LV to increase fetal hemoglobin formation. We also generated an insulated version of this LV, GbGMI, inserting a 36-bp insulator from the Foamy virus in the long terminal repeats of the LV. Preclinical batches of GbGM and GbGMI LV showed both were highly efficacious in correcting SCA in mice, with sustained gene transfer in primary transplanted SCA mice and high hematopoietic stem cell (HSC) transduction in colony-forming unit-spleen in secondary transplanted mice. CRISPR-mediated targeting of the proviruses into the LMO2 proto-oncogene showed remarkably reduced LMO2 activation by both insulated and uninsulated LV, compared to the SFFV γ-RV vector targeted to the same locus. We therefore used the GbGM LV to perform preclinical human CD34+ gene transfer. We assessed gene transfer and engraftment of human HSCs in two immunocompromised mouse models: persistent stable GbGM-transduced cell engraftment was comparable to that of untransduced cells with no detrimental effects on hematopoiesis up to 20 weeks post transplant. These robust preclinical studies in mouse and human HSCs allowed its translation into a clinical trial.
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spelling doaj-art-8d700d7589ff4640b365178c6b5b3ce12025-08-20T03:00:07ZengElsevierMolecular Therapy: Methods & Clinical Development2329-05012025-06-0133210143910.1016/j.omtm.2025.101439Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft modelsArchana Shrestha0Devin M. Pillis1Sydney Felker2Mengna Chi3Kimberly Wagner4Oluwabukola T. Gbotosho5Joseph Sieling6Mohammad Shadid7Punam Malik8Division of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USA; Aruvant Sciences, New York, NY 10036, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USAAruvant Sciences, New York, NY 10036, USAAruvant Sciences, New York, NY 10036, USADivision of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center (CCHMC), Cincinnati, OH 45229, USA; Division of Hematology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati, Cincinnati, OH 45229, USA; Corresponding author: Punam Malik, Division of Experimental Hematology and Cancer Biology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229, USA.We previously showed correction of sickle cell anemia (SCA) in mice utilizing a lentiviral vector (LV) expressing human γ-globin. Herein, we made a G16D mutation in the γ-globin gene to generate the G16D mutation (GbGM) LV to increase fetal hemoglobin formation. We also generated an insulated version of this LV, GbGMI, inserting a 36-bp insulator from the Foamy virus in the long terminal repeats of the LV. Preclinical batches of GbGM and GbGMI LV showed both were highly efficacious in correcting SCA in mice, with sustained gene transfer in primary transplanted SCA mice and high hematopoietic stem cell (HSC) transduction in colony-forming unit-spleen in secondary transplanted mice. CRISPR-mediated targeting of the proviruses into the LMO2 proto-oncogene showed remarkably reduced LMO2 activation by both insulated and uninsulated LV, compared to the SFFV γ-RV vector targeted to the same locus. We therefore used the GbGM LV to perform preclinical human CD34+ gene transfer. We assessed gene transfer and engraftment of human HSCs in two immunocompromised mouse models: persistent stable GbGM-transduced cell engraftment was comparable to that of untransduced cells with no detrimental effects on hematopoiesis up to 20 weeks post transplant. These robust preclinical studies in mouse and human HSCs allowed its translation into a clinical trial.http://www.sciencedirect.com/science/article/pii/S2329050125000348sickle cell anemialentiviral vectorhuman gamma-globinfetal hemoglobininsulatorhematopoietic stem cell
spellingShingle Archana Shrestha
Devin M. Pillis
Sydney Felker
Mengna Chi
Kimberly Wagner
Oluwabukola T. Gbotosho
Joseph Sieling
Mohammad Shadid
Punam Malik
Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
Molecular Therapy: Methods & Clinical Development
sickle cell anemia
lentiviral vector
human gamma-globin
fetal hemoglobin
insulator
hematopoietic stem cell
title Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
title_full Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
title_fullStr Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
title_full_unstemmed Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
title_short Preclinical efficacy of a modified gamma-globin lentivirus gene therapy in Berkeley sickle cell anemia mice and human xenograft models
title_sort preclinical efficacy of a modified gamma globin lentivirus gene therapy in berkeley sickle cell anemia mice and human xenograft models
topic sickle cell anemia
lentiviral vector
human gamma-globin
fetal hemoglobin
insulator
hematopoietic stem cell
url http://www.sciencedirect.com/science/article/pii/S2329050125000348
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