Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations

IntroductionUnderstanding leukemia-associated immunophenotypes (LAIP) could assist in the design of therapies to ameliorate patient benefits in acute myeloid leukemia (AML). In our study, focusing on single-cell heterogeneity in therapeutic resistance, flow cytometric immunophenotyping of the periph...

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Main Authors: Nikolett Gémes, Benedek Rónaszéki, Szabolcs Modok, Zita Borbényi, Imre Földesi, Éva Trucza, Blanka Godza, Zsuzsanna László, Balázs Csernus, László Krenács, Enikő Bagdi, Enikő Szabó, László G. Puskás, Valeria Bertagnolo, Gábor J. Szebeni
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Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1563386/full
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author Nikolett Gémes
Benedek Rónaszéki
Szabolcs Modok
Zita Borbényi
Imre Földesi
Éva Trucza
Blanka Godza
Zsuzsanna László
Balázs Csernus
László Krenács
Enikő Bagdi
Enikő Szabó
László G. Puskás
László G. Puskás
Valeria Bertagnolo
Gábor J. Szebeni
Gábor J. Szebeni
Gábor J. Szebeni
author_facet Nikolett Gémes
Benedek Rónaszéki
Szabolcs Modok
Zita Borbényi
Imre Földesi
Éva Trucza
Blanka Godza
Zsuzsanna László
Balázs Csernus
László Krenács
Enikő Bagdi
Enikő Szabó
László G. Puskás
László G. Puskás
Valeria Bertagnolo
Gábor J. Szebeni
Gábor J. Szebeni
Gábor J. Szebeni
author_sort Nikolett Gémes
collection DOAJ
description IntroductionUnderstanding leukemia-associated immunophenotypes (LAIP) could assist in the design of therapies to ameliorate patient benefits in acute myeloid leukemia (AML). In our study, focusing on single-cell heterogeneity in therapeutic resistance, flow cytometric immunophenotyping of the peripheral blood of therapy-naive and follow-up AML patients versus age and sex-matched healthy controls (HCs) was performed.MethodsThe FACS panel consisted of Viobility 405/520 Fixable Dye, Anti-human CD45, CD19, CD3, CD7, CD33, CD34, CD38, CD64, CD117, CD135, HLA-DR antibodies. Unsupervised clustering algorithms such as Uniform Manifold Approximation and Projection for Dimension Reduction (UMAP) and Flow cytometry data that builds Self-Organizing Maps (FlowSOM) were used to reveal the LAIP. The measurable residual disease (MRD) was monitored by our proposed manual gating. To complement the characterization of peripheral immune cells, Luminex MAGPIX was used to measure the concentration of 31 soluble immune-oncology mediators from the plasma of AML patients and HC.ResultsBoth manual gating, UMAP and FlowSOM showed normalization of LAIP similar to the HC immune landscape following therapy. Eleven metaclusters (MCs) were associated with AML before therapy. The follow-up of AML samples revealed four MCs of therapy sensitive cells, and one MC composed of therapeutic resistant cells (MC12: CD3-CD7-CD33-CD38- CD64- HLA-DR- CD117- CD135-) identified by the FlowSOM analysis. The initial AML blasts in the MRD gate (CD19-, CD45+, CD3-, CD38+/CD34±, CD7+/CD117+, CD117+/CD135+) were detectable at the lowest frequency in our current study at 22 cells per 100,000 (0.022%) CD45+CD3- living singlet parental population. In the plasma of AML patients the levels of BAFF, B7-H2, B7-H4, CD25, MICA, and Siglec-7 were increased versus HCs.ConclusionsThis study focused on understanding the LAIP in AML before and after therapeutic intervention. The study highlights the potential of using single-cell LAIP profiling and immune mediator measurements to monitor therapy response and identify measurable residual disease and therapy resistant cell populations in AML.
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spelling doaj-art-05500cddac6c454ea7da1c66c6e4902e2025-08-20T02:26:41ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-04-011610.3389/fimmu.2025.15633861563386Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulationsNikolett Gémes0Benedek Rónaszéki1Szabolcs Modok2Zita Borbényi3Imre Földesi4Éva Trucza5Blanka Godza6Zsuzsanna László7Balázs Csernus8László Krenács9Enikő Bagdi10Enikő Szabó11László G. Puskás12László G. Puskás13Valeria Bertagnolo14Gábor J. Szebeni15Gábor J. Szebeni16Gábor J. Szebeni17Laboratory of Functional Genomics, Core Facility, HUN-REN Biological Research Center, Szeged, HungaryDepartment of Internal Medicine, Hematology Center, Faculty of Medicine, University of Szeged, Szeged, HungaryDepartment of Internal Medicine, Hematology Center, Faculty of Medicine, University of Szeged, Szeged, HungaryDepartment of Internal Medicine, Hematology Center, Faculty of Medicine, University of Szeged, Szeged, HungaryFaculty of Medicine, Institute of Laboratory Medicine, University of Szeged, Szeged, HungaryFaculty of Medicine, Institute of Laboratory Medicine, University of Szeged, Szeged, HungaryDepartment of Medical Genetics, University of Szeged, Szeged, HungaryDepartment of Medical Genetics, University of Szeged, Szeged, Hungary1st Department of Pathology and Experimental Cancer Research, Faculty of Medicine, Semmelweis University, Budapest, HungaryLaboratory of Tumor Pathology and Molecular Diagnostics, Szeged, HungaryLaboratory of Tumor Pathology and Molecular Diagnostics, Szeged, HungaryLaboratory of Functional Genomics, Core Facility, HUN-REN Biological Research Center, Szeged, HungaryLaboratory of Functional Genomics, Core Facility, HUN-REN Biological Research Center, Szeged, HungaryAvidin Ltd., Szeged, HungaryUniversity of Ferrara, Department of Morphology, Surgery and Experimental Medicine, Ferrara, ItalyLaboratory of Functional Genomics, Core Facility, HUN-REN Biological Research Center, Szeged, HungaryDepartment of Internal Medicine, Hematology Center, Faculty of Medicine, University of Szeged, Szeged, HungaryAstridbio Technologies Ltd., Szeged, HungaryIntroductionUnderstanding leukemia-associated immunophenotypes (LAIP) could assist in the design of therapies to ameliorate patient benefits in acute myeloid leukemia (AML). In our study, focusing on single-cell heterogeneity in therapeutic resistance, flow cytometric immunophenotyping of the peripheral blood of therapy-naive and follow-up AML patients versus age and sex-matched healthy controls (HCs) was performed.MethodsThe FACS panel consisted of Viobility 405/520 Fixable Dye, Anti-human CD45, CD19, CD3, CD7, CD33, CD34, CD38, CD64, CD117, CD135, HLA-DR antibodies. Unsupervised clustering algorithms such as Uniform Manifold Approximation and Projection for Dimension Reduction (UMAP) and Flow cytometry data that builds Self-Organizing Maps (FlowSOM) were used to reveal the LAIP. The measurable residual disease (MRD) was monitored by our proposed manual gating. To complement the characterization of peripheral immune cells, Luminex MAGPIX was used to measure the concentration of 31 soluble immune-oncology mediators from the plasma of AML patients and HC.ResultsBoth manual gating, UMAP and FlowSOM showed normalization of LAIP similar to the HC immune landscape following therapy. Eleven metaclusters (MCs) were associated with AML before therapy. The follow-up of AML samples revealed four MCs of therapy sensitive cells, and one MC composed of therapeutic resistant cells (MC12: CD3-CD7-CD33-CD38- CD64- HLA-DR- CD117- CD135-) identified by the FlowSOM analysis. The initial AML blasts in the MRD gate (CD19-, CD45+, CD3-, CD38+/CD34±, CD7+/CD117+, CD117+/CD135+) were detectable at the lowest frequency in our current study at 22 cells per 100,000 (0.022%) CD45+CD3- living singlet parental population. In the plasma of AML patients the levels of BAFF, B7-H2, B7-H4, CD25, MICA, and Siglec-7 were increased versus HCs.ConclusionsThis study focused on understanding the LAIP in AML before and after therapeutic intervention. The study highlights the potential of using single-cell LAIP profiling and immune mediator measurements to monitor therapy response and identify measurable residual disease and therapy resistant cell populations in AML.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1563386/fullsingle-cell immunophenotypingleukemia-associated immunophenotypeacute myeloid leukemiadrug resistanceminimal residual diseaseluminex MAGPIX
spellingShingle Nikolett Gémes
Benedek Rónaszéki
Szabolcs Modok
Zita Borbényi
Imre Földesi
Éva Trucza
Blanka Godza
Zsuzsanna László
Balázs Csernus
László Krenács
Enikő Bagdi
Enikő Szabó
László G. Puskás
László G. Puskás
Valeria Bertagnolo
Gábor J. Szebeni
Gábor J. Szebeni
Gábor J. Szebeni
Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
Frontiers in Immunology
single-cell immunophenotyping
leukemia-associated immunophenotype
acute myeloid leukemia
drug resistance
minimal residual disease
luminex MAGPIX
title Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
title_full Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
title_fullStr Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
title_full_unstemmed Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
title_short Multiplex immunophenotyping of human acute myeloid leukemia patients revealed single -cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
title_sort multiplex immunophenotyping of human acute myeloid leukemia patients revealed single cell heterogeneity with special attention on therapy sensitive and therapy resistant subpopulations
topic single-cell immunophenotyping
leukemia-associated immunophenotype
acute myeloid leukemia
drug resistance
minimal residual disease
luminex MAGPIX
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1563386/full
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