Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells

Apoptosis plays a fundamental role in the regulation of immune responses mediated by neutrophils. Phosphatidylglucoside (PtdGlc), a glycosylated phospholipid abundantly expressed on the surface of human neutrophils, has been implicated in promoting both cellular differentiation and apoptosis. In the...

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Main Authors: Noriko Yokoyama, Roudy Chiminch Ekyalongo, Madoka Kage, Kei Hanafusa, Hitoshi Nakayama, Yoshio Hirabayashi, Kenji Takamori, Kazuhisa Iwabuchi
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1597423/full
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author Noriko Yokoyama
Roudy Chiminch Ekyalongo
Madoka Kage
Madoka Kage
Kei Hanafusa
Kei Hanafusa
Hitoshi Nakayama
Hitoshi Nakayama
Hitoshi Nakayama
Yoshio Hirabayashi
Yoshio Hirabayashi
Kenji Takamori
Kazuhisa Iwabuchi
Kazuhisa Iwabuchi
author_facet Noriko Yokoyama
Roudy Chiminch Ekyalongo
Madoka Kage
Madoka Kage
Kei Hanafusa
Kei Hanafusa
Hitoshi Nakayama
Hitoshi Nakayama
Hitoshi Nakayama
Yoshio Hirabayashi
Yoshio Hirabayashi
Kenji Takamori
Kazuhisa Iwabuchi
Kazuhisa Iwabuchi
author_sort Noriko Yokoyama
collection DOAJ
description Apoptosis plays a fundamental role in the regulation of immune responses mediated by neutrophils. Phosphatidylglucoside (PtdGlc), a glycosylated phospholipid abundantly expressed on the surface of human neutrophils, has been implicated in promoting both cellular differentiation and apoptosis. In the acute myeloid leukemia (AML) cell line HL-60, PtdGlc expression increases during differentiation, and treatment with the anti-PtdGlc monoclonal antibody DIM21 induces early apoptosis. To further investigate the role of PtdGlc in neutrophilic lineage cells, we examined three AML cell lines: HL-60 (AML-M2/M3), KG1 (AML-M1), and KG1a (AML-M0). PtdGlc was highly expressed in HL-60 and KG1 cells but was absent in KG1a cells. Both HL-60 and KG1 cells exhibited early apoptosis following DIM21 treatment, whereas KG1a cells remained resistant regardless of differentiation status. Notably, in KG1 cells, DIM21 induced late-stage apoptosis specifically after ATRA-mediated differentiation, and co-treatment with ATRA and DIM21 significantly enhanced this apoptotic response. Mechanistic analysis revealed that this process was independent of NADPH oxidase and Fas signaling, as neither a reactive oxygen species inhibitor nor a neutralizing anti-Fas antibody altered the apoptotic outcome. Instead, DIM21 activated caspase-3 and caspase-8, suggesting that PtdGlc mediates apoptosis through a caspase-dependent, but NADPH oxidase- and Fas-independent, pathway. Collectively, these findings provide new insight into the apoptotic signaling function of PtdGlc in neutrophilic lineage cells and highlight its potential as a novel therapeutic target in AML.
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spelling doaj-art-35f3bc713bf54f3cb94b7c368850d6cc2025-08-20T03:48:27ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-05-011610.3389/fimmu.2025.15974231597423Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cellsNoriko Yokoyama0Roudy Chiminch Ekyalongo1Madoka Kage2Madoka Kage3Kei Hanafusa4Kei Hanafusa5Hitoshi Nakayama6Hitoshi Nakayama7Hitoshi Nakayama8Yoshio Hirabayashi9Yoshio Hirabayashi10Kenji Takamori11Kazuhisa Iwabuchi12Kazuhisa Iwabuchi13Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanLaboratory of Dermatological Physiology, Faculty of Pharmacy and Pharmaceutical Sciences, Josai University, Saitama, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanLaboratory of Biochemistry, Faculty of Pharmacy, Juntendo University, Urayasu, Chiba, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanInfection Control Nursing, Juntendo University Graduate School of Health Care and Nursing, Chiba, JapanLaboratory of Biochemistry, Juntendo University Faculty of Health Care and Nursing, Chiba, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanCellular Informatics Lab, RIKEN, Saitama, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanInstitute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Chiba, JapanLaboratory of Biochemistry, Faculty of Pharmacy, Juntendo University, Urayasu, Chiba, JapanApoptosis plays a fundamental role in the regulation of immune responses mediated by neutrophils. Phosphatidylglucoside (PtdGlc), a glycosylated phospholipid abundantly expressed on the surface of human neutrophils, has been implicated in promoting both cellular differentiation and apoptosis. In the acute myeloid leukemia (AML) cell line HL-60, PtdGlc expression increases during differentiation, and treatment with the anti-PtdGlc monoclonal antibody DIM21 induces early apoptosis. To further investigate the role of PtdGlc in neutrophilic lineage cells, we examined three AML cell lines: HL-60 (AML-M2/M3), KG1 (AML-M1), and KG1a (AML-M0). PtdGlc was highly expressed in HL-60 and KG1 cells but was absent in KG1a cells. Both HL-60 and KG1 cells exhibited early apoptosis following DIM21 treatment, whereas KG1a cells remained resistant regardless of differentiation status. Notably, in KG1 cells, DIM21 induced late-stage apoptosis specifically after ATRA-mediated differentiation, and co-treatment with ATRA and DIM21 significantly enhanced this apoptotic response. Mechanistic analysis revealed that this process was independent of NADPH oxidase and Fas signaling, as neither a reactive oxygen species inhibitor nor a neutralizing anti-Fas antibody altered the apoptotic outcome. Instead, DIM21 activated caspase-3 and caspase-8, suggesting that PtdGlc mediates apoptosis through a caspase-dependent, but NADPH oxidase- and Fas-independent, pathway. Collectively, these findings provide new insight into the apoptotic signaling function of PtdGlc in neutrophilic lineage cells and highlight its potential as a novel therapeutic target in AML.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1597423/fullphosphatidylglucosideacute myeloid leukemia cellsapoptosiscell deathdifferentiationATRA
spellingShingle Noriko Yokoyama
Roudy Chiminch Ekyalongo
Madoka Kage
Madoka Kage
Kei Hanafusa
Kei Hanafusa
Hitoshi Nakayama
Hitoshi Nakayama
Hitoshi Nakayama
Yoshio Hirabayashi
Yoshio Hirabayashi
Kenji Takamori
Kazuhisa Iwabuchi
Kazuhisa Iwabuchi
Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
Frontiers in Immunology
phosphatidylglucoside
acute myeloid leukemia cells
apoptosis
cell death
differentiation
ATRA
title Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
title_full Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
title_fullStr Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
title_full_unstemmed Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
title_short Phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
title_sort phosphatidylglucoside regulates apoptosis of human neutrophilic lineage cells
topic phosphatidylglucoside
acute myeloid leukemia cells
apoptosis
cell death
differentiation
ATRA
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1597423/full
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