Demethylating therapy increases anti-CD123 CAR T cell cytotoxicity against acute myeloid leukemia

Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX...

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Published inNature communications Vol. 12; no. 1; pp. 6436 - 20
Main Authors El Khawanky, Nadia, Hughes, Amy, Yu, Wenbo, Myburgh, Renier, Matschulla, Tony, Taromi, Sanaz, Aumann, Konrad, Clarson, Jade, Vinnakota, Janaki Manoja, Shoumariyeh, Khalid, Miething, Cornelius, Lopez, Angel F., Brown, Michael P., Duyster, Justus, Hein, Lutz, Manz, Markus G., Hughes, Timothy P., White, Deborah L., Yong, Agnes S. M., Zeiser, Robert
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 08.11.2021
Nature Publishing Group
Nature Portfolio
Subjects
59
59/5
631/250
631/67/1990/283/1897
64
64/60
692/4028/67/1059/2325
96/31
Acute Disease
Acute myeloid leukemia
Animals
Antigens
Azacitidine - administration & dosage
CD123 antigen
CD28 antigen
Cell activation
Cell Line, Tumor
Cells, Cultured
Chimeric antigen receptors
Cytotoxicity
Cytotoxicity, Immunologic
DNA Methylation - drug effects
Enzyme Inhibitors - administration & dosage
HEK293 Cells
Hematopoietic stem cells
Hematopoietic system
HL-60 Cells
Humanities and Social Sciences
Humans
Immunogenicity
Immunotherapy, Adoptive - methods
Interleukin-3 Receptor alpha Subunit - immunology
Interleukin-3 Receptor alpha Subunit - metabolism
Intracellular signalling
Kaplan-Meier Estimate
Leukemia
Leukemia, Myeloid - immunology
Leukemia, Myeloid - pathology
Leukemia, Myeloid - therapy
Lymphocytes
Lymphocytes T
Mice
Mice, Knockout
multidisciplinary
Myeloid leukemia
Phosphorylation
Progenitor cells
Receptors, Antigen, T-Cell - immunology
Receptors, Antigen, T-Cell - metabolism
Receptors, Chimeric Antigen - immunology
Receptors, Chimeric Antigen - metabolism
Science
Science (multidisciplinary)
Single-Chain Antibodies - immunology
Toxicity
Tumor necrosis factor-α
Xenograft Model Antitumor Assays - methods
Xenografts
Xenotransplantation
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-021-26683-0

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Abstract Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5′-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4 negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4 negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4 negative anti-CD123 CAR T cells. The success of CAR-T cells for treating acute myeloid leukaemia (AML) is hampered by toxicity to normal cells and low CAR-T cell persistence. Here, the authors show that the demethylating compound 5′-Azacitdine increases anti-CD123 CAR-T cell cytotoxicity against AML.
AbstractList Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5′-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4 negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4 negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4 negative anti-CD123 CAR T cells. The success of CAR-T cells for treating acute myeloid leukaemia (AML) is hampered by toxicity to normal cells and low CAR-T cell persistence. Here, the authors show that the demethylating compound 5′-Azacitdine increases anti-CD123 CAR-T cell cytotoxicity against AML.
Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5′-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4negative anti-CD123 CAR T cells.The success of CAR-T cells for treating acute myeloid leukaemia (AML) is hampered by toxicity to normal cells and low CAR-T cell persistence. Here, the authors show that the demethylating compound 5′-Azacitdine increases anti-CD123 CAR-T cell cytotoxicity against AML.
Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5'-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4 anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4 anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4 anti-CD123 CAR T cells.
Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5'-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4negative anti-CD123 CAR T cells.Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5'-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4negative anti-CD123 CAR T cells.
Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor cells and low CAR T cell persistence. Here, we develop third-generation anti-CD123 CAR T cells with a humanized CSL362-based ScFv and a CD28-OX40-CD3ζ intracellular signaling domain. This CAR demonstrates anti-AML activity without affecting the healthy hematopoietic system, or causing epithelial tissue damage in a xenograft model. CD123 expression on leukemia cells increases upon 5′-Azacitidine (AZA) treatment. AZA treatment of leukemia-bearing mice causes an increase in CTLA-4 negative anti-CD123 CAR T cell numbers following infusion. Functionally, the CTLA-4 negative anti-CD123 CAR T cells exhibit superior cytotoxicity against AML cells, accompanied by higher TNFα production and enhanced downstream phosphorylation of key T cell activation molecules. Our findings indicate that AZA increases the immunogenicity of AML cells, enhancing recognition and elimination of malignant cells by highly efficient CTLA-4 negative anti-CD123 CAR T cells.
The success of CAR-T cells for treating acute myeloid leukaemia (AML) is hampered by toxicity to normal cells and low CAR-T cell persistence. Here, the authors show that the demethylating compound 5′-Azacitdine increases anti-CD123 CAR-T cell cytotoxicity against AML.
ArticleNumber 6436
Author Lopez, Angel F.
Clarson, Jade
Miething, Cornelius
Yu, Wenbo
Vinnakota, Janaki Manoja
Hughes, Amy
Duyster, Justus
Hein, Lutz
Myburgh, Renier
Manz, Markus G.
Yong, Agnes S. M.
Zeiser, Robert
Brown, Michael P.
Shoumariyeh, Khalid
White, Deborah L.
Taromi, Sanaz
El Khawanky, Nadia
Matschulla, Tony
Hughes, Timothy P.
Aumann, Konrad
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  surname: El Khawanky
  fullname: El Khawanky, Nadia
  organization: Precision Medicine Theme, South Australian Health and Medical Research Institute (SAHMRI), School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Faculty of Biology, University of Freiburg
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  organization: School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide
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  organization: Centre for Cancer Biology, SA Pathology and University of South Australia
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  organization: Department of Medical Oncology and Hematology, University Hospital Zurich and University of Zurich, Comprehensive Cancer Center Zurich (CCCZ)
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  orcidid: 0000-0002-4866-6456
  surname: Matschulla
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  organization: Institute of Experimental and Clinical Pharmacology and Toxicology, Division II, Faculty of Medicine, University of Freiburg
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  givenname: Sanaz
  orcidid: 0000-0001-5657-6568
  surname: Taromi
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  organization: Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Faculty of Medical and Life Sciences, University Furtwangen
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  givenname: Konrad
  surname: Aumann
  fullname: Aumann, Konrad
  organization: Department of Pathology, Institute for Clinical Pathology, University Medical Center Freiburg
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  surname: Clarson
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  organization: Precision Medicine Theme, South Australian Health and Medical Research Institute (SAHMRI), Department of Haematology, Royal Adelaide Hospital
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  fullname: Vinnakota, Janaki Manoja
  organization: Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg
– sequence: 10
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  surname: Shoumariyeh
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  organization: Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg
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  givenname: Cornelius
  orcidid: 0000-0003-4699-3805
  surname: Miething
  fullname: Miething, Cornelius
  organization: Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg
– sequence: 12
  givenname: Angel F.
  surname: Lopez
  fullname: Lopez, Angel F.
  organization: School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, Centre for Cancer Biology, SA Pathology and University of South Australia
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  givenname: Michael P.
  orcidid: 0000-0002-5796-1932
  surname: Brown
  fullname: Brown, Michael P.
  organization: School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, Centre for Cancer Biology, SA Pathology and University of South Australia, Cancer Clinical Trials Unit, Department of Medical Oncology, Royal Adelaide Hospital
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  surname: Duyster
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  orcidid: 0000-0003-1297-0007
  surname: Hein
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  organization: Institute of Experimental and Clinical Pharmacology and Toxicology, Division II, Faculty of Medicine, University of Freiburg
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  givenname: Markus G.
  orcidid: 0000-0002-4676-7931
  surname: Manz
  fullname: Manz, Markus G.
  organization: Department of Medical Oncology and Hematology, University Hospital Zurich and University of Zurich, Comprehensive Cancer Center Zurich (CCCZ)
– sequence: 17
  givenname: Timothy P.
  surname: Hughes
  fullname: Hughes, Timothy P.
  organization: Precision Medicine Theme, South Australian Health and Medical Research Institute (SAHMRI), School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, Department of Haematology, Royal Adelaide Hospital
– sequence: 18
  givenname: Deborah L.
  surname: White
  fullname: White, Deborah L.
  organization: Precision Medicine Theme, South Australian Health and Medical Research Institute (SAHMRI), School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, School of Biological Sciences, Faculty of Science, University of Adelaide
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  givenname: Agnes S. M.
  orcidid: 0000-0001-9452-1533
  surname: Yong
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  email: agnes.yong@health.wa.gov.au
  organization: Precision Medicine Theme, South Australian Health and Medical Research Institute (SAHMRI), School of Medicine, Faculty of Health and Medical Sciences, University of Adelaide, Department of Haematology, Royal Perth Hospital, School of Medicine, The University of Western Australia
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  orcidid: 0000-0001-6565-3393
  surname: Zeiser
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  email: robert.zeiser@uniklinik-freiburg.de
  organization: Department of Medicine I, Medical Center - University of Freiburg, Faculty of Medicine, University of Freiburg, Signaling Research Centres BIOSS and CIBSS-Centre for Integrative Biological Signalling Studies, University of Freiburg
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34750374$$D View this record in MEDLINE/PubMed
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2021. The Author(s).
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SSID ssj0000391844
Score 2.6040804
Snippet Successful treatment of acute myeloid leukemia (AML) with chimeric antigen receptor (CAR) T cells is hampered by toxicity on normal hematopoietic progenitor...
The success of CAR-T cells for treating acute myeloid leukaemia (AML) is hampered by toxicity to normal cells and low CAR-T cell persistence. Here, the authors...
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pubmedcentral
proquest
pubmed
crossref
springer
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 6436
SubjectTerms 59
59/5
631/250
631/67/1990/283/1897
64
64/60
692/4028/67/1059/2325
96/31
Acute Disease
Acute myeloid leukemia
Animals
Antigens
Azacitidine - administration & dosage
CD123 antigen
CD28 antigen
Cell activation
Cell Line, Tumor
Cells, Cultured
Chimeric antigen receptors
Cytotoxicity
Cytotoxicity, Immunologic
DNA Methylation - drug effects
Enzyme Inhibitors - administration & dosage
HEK293 Cells
Hematopoietic stem cells
Hematopoietic system
HL-60 Cells
Humanities and Social Sciences
Humans
Immunogenicity
Immunotherapy, Adoptive - methods
Interleukin-3 Receptor alpha Subunit - immunology
Interleukin-3 Receptor alpha Subunit - metabolism
Intracellular signalling
Kaplan-Meier Estimate
Leukemia
Leukemia, Myeloid - immunology
Leukemia, Myeloid - pathology
Leukemia, Myeloid - therapy
Lymphocytes
Lymphocytes T
Mice
Mice, Knockout
multidisciplinary
Myeloid leukemia
Phosphorylation
Progenitor cells
Receptors, Antigen, T-Cell - immunology
Receptors, Antigen, T-Cell - metabolism
Receptors, Chimeric Antigen - immunology
Receptors, Chimeric Antigen - metabolism
Science
Science (multidisciplinary)
Single-Chain Antibodies - immunology
Toxicity
Tumor necrosis factor-α
Xenograft Model Antitumor Assays - methods
Xenografts
Xenotransplantation
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Title Demethylating therapy increases anti-CD123 CAR T cell cytotoxicity against acute myeloid leukemia
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