Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques

Abstract: The treatment of monogenetic disorders, such as hemoglobinopathies and lysosomal storage diseases, has markedly improved with the advent of cell and gene therapies, particularly allogeneic or gene-modified autologous stem cell transplantations. However, therapeutic efficacy is reliant on m...

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Main Authors: Nicholas E. Petty, Stefan Radtke, Greta Kanestrom, Emily Fields, Olivier Humbert, Salvatore Fiorenza, Mallory J. Llewellyn, George S. Laszlo, Justin Thomas, Zach Burger, Kyle Swing, Haiying Zhu, Keith R. Jerome, Cameron J. Turtle, Roland B. Walter, Hans-Peter Kiem
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Blood Advances
Online Access:http://www.sciencedirect.com/science/article/pii/S2473952925000916
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author Nicholas E. Petty
Stefan Radtke
Greta Kanestrom
Emily Fields
Olivier Humbert
Salvatore Fiorenza
Mallory J. Llewellyn
George S. Laszlo
Justin Thomas
Zach Burger
Kyle Swing
Haiying Zhu
Keith R. Jerome
Cameron J. Turtle
Roland B. Walter
Hans-Peter Kiem
author_facet Nicholas E. Petty
Stefan Radtke
Greta Kanestrom
Emily Fields
Olivier Humbert
Salvatore Fiorenza
Mallory J. Llewellyn
George S. Laszlo
Justin Thomas
Zach Burger
Kyle Swing
Haiying Zhu
Keith R. Jerome
Cameron J. Turtle
Roland B. Walter
Hans-Peter Kiem
author_sort Nicholas E. Petty
collection DOAJ
description Abstract: The treatment of monogenetic disorders, such as hemoglobinopathies and lysosomal storage diseases, has markedly improved with the advent of cell and gene therapies, particularly allogeneic or gene-modified autologous stem cell transplantations. However, therapeutic efficacy is reliant on maintaining engraftment above a critical threshold. To maintain such engraftment levels, we and others have pursued approaches to shield edited cells from antibody or chimeric antigen receptor (CAR) T-cell–mediated selection. Here, we focused on CD33, which is expressed early on hematopoietic stem and progenitor cells (HSPCs) as well as on myeloid progenitors. Rhesus macaques were engrafted with HSPCs edited to ablate CD33 using either CRISPR/CRISPR-associated protein 9 or adenine base editor. Both editing strategies showed similar post-transplant recovery kinetics and yielded equivalent levels of engraftment. We then created a V-set domain–specific CAR construct (CAR33), validated its functionality in vitro, and treated both animals with autologous CAR33 T cells. CAR33 T cells expanded after infusion and caused specific depletion of CD33WT but not CD33null progeny, leading to a transient enrichment for gene-edited cells in the blood. No depletion was seen in the bone marrow stem cell compartment with CD34+CD90+ HSCs expressing lower levels of CD33 in comparison to monocytes. Thus, we show proof of concept and safety of an epitope editing–based enrichment/protection strategy in macaques.
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spelling doaj-art-b4a1075a14f84b9ab46e59282796d8a22025-08-20T02:58:25ZengElsevierBlood Advances2473-95292025-05-019102367237810.1182/bloodadvances.2024015016Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaquesNicholas E. Petty0Stefan Radtke1Greta Kanestrom2Emily Fields3Olivier Humbert4Salvatore Fiorenza5Mallory J. Llewellyn6George S. Laszlo7Justin Thomas8Zach Burger9Kyle Swing10Haiying Zhu11Keith R. Jerome12Cameron J. Turtle13Roland B. Walter14Hans-Peter Kiem15Translational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA; Medical Scientist Training Program, University of Washington School of Medicine, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA; Division of Hematology and Oncology, Department of Medicine, University of Washington School of Medicine, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA; Medical Scientist Training Program, University of Washington School of Medicine, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WADepartment of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, WADepartment of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, WA; Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA; Division of Hematology and Oncology, Department of Medicine, University of Washington School of Medicine, Seattle, WA; Department of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, WATranslational Science and Therapeutics Division, Fred Hutchinson Cancer Center, Seattle, WA; Division of Hematology and Oncology, Department of Medicine, University of Washington School of Medicine, Seattle, WA; Department of Laboratory Medicine and Pathology, University of Washington School of Medicine, Seattle, WA; Correspondence: Hans-Peter Kiem, Translational Science and Therapeutics Division, Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Center, 1100 Fairview Ave N, D1-100, Seattle, WA 98109-1024;Abstract: The treatment of monogenetic disorders, such as hemoglobinopathies and lysosomal storage diseases, has markedly improved with the advent of cell and gene therapies, particularly allogeneic or gene-modified autologous stem cell transplantations. However, therapeutic efficacy is reliant on maintaining engraftment above a critical threshold. To maintain such engraftment levels, we and others have pursued approaches to shield edited cells from antibody or chimeric antigen receptor (CAR) T-cell–mediated selection. Here, we focused on CD33, which is expressed early on hematopoietic stem and progenitor cells (HSPCs) as well as on myeloid progenitors. Rhesus macaques were engrafted with HSPCs edited to ablate CD33 using either CRISPR/CRISPR-associated protein 9 or adenine base editor. Both editing strategies showed similar post-transplant recovery kinetics and yielded equivalent levels of engraftment. We then created a V-set domain–specific CAR construct (CAR33), validated its functionality in vitro, and treated both animals with autologous CAR33 T cells. CAR33 T cells expanded after infusion and caused specific depletion of CD33WT but not CD33null progeny, leading to a transient enrichment for gene-edited cells in the blood. No depletion was seen in the bone marrow stem cell compartment with CD34+CD90+ HSCs expressing lower levels of CD33 in comparison to monocytes. Thus, we show proof of concept and safety of an epitope editing–based enrichment/protection strategy in macaques.http://www.sciencedirect.com/science/article/pii/S2473952925000916
spellingShingle Nicholas E. Petty
Stefan Radtke
Greta Kanestrom
Emily Fields
Olivier Humbert
Salvatore Fiorenza
Mallory J. Llewellyn
George S. Laszlo
Justin Thomas
Zach Burger
Kyle Swing
Haiying Zhu
Keith R. Jerome
Cameron J. Turtle
Roland B. Walter
Hans-Peter Kiem
Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
Blood Advances
title Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
title_full Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
title_fullStr Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
title_full_unstemmed Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
title_short Protection of CD33-modified hematopoietic stem cell progeny from CD33-directed CAR T cells in rhesus macaques
title_sort protection of cd33 modified hematopoietic stem cell progeny from cd33 directed car t cells in rhesus macaques
url http://www.sciencedirect.com/science/article/pii/S2473952925000916
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