Cited by 197Acute Myeloid Leukemia ResearchRetinoids in leukemia and cellular processesIron Metabolism and Disorders

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Targeting iron homeostasis induces cellular differentiation and synergizes with differentiating agents in acute myeloid leukemia

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Callens, Celine, Coulon, Séverine, Naudin, Jerome, Radford-Weiss, Isabelle, Boissel, Nicolas, Raffoux, Emmanuel, Wang, Pamella Huey Mei, Agarwal, Saurabh, Tamouza, Houda, Paubelle, Etienne, Asnafi, Vahid, Ribeil, Jean-Antoine, Dessen, Philippe, Canioni, Danielle, Chandesris, Olivia, Rubio, Marie Therese, Beaumont, Carole, Benhamou, Marc, Dombret, Hervé, Macintyre, Elizabeth, Monteiro, Renato C., Moura, Ivan C., Hermine, Olivier·2010·Journal of Experimental Medicine

DOI 10.1084/jem.20091488PMC PMC2856037

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Abstract

Differentiating agents have been proposed to overcome the impaired cellular differentiation in acute myeloid leukemia (AML). However, only the combinations of all-trans retinoic acid or arsenic trioxide with chemotherapy have been successful, and only in treating acute promyelocytic leukemia (also called AML3). We show that iron homeostasis is an effective target in the treatment of AML. Iron chelating therapy induces the differentiation of leukemia blasts and normal bone marrow precursors into monocytes/macrophages in a manner involving modulation of reactive oxygen species expression and the activation of mitogen-activated protein kinases (MAPKs). 30% of the genes most strongly induced by iron deprivation are also targeted by vitamin D3 (VD), a well known differentiating agent. Iron chelating agents induce expression and phosphorylation of the VD receptor (VDR), and iron deprivation and VD act synergistically. VD magnifies activation of MAPK JNK and the induction of VDR target genes. When used to treat one AML patient refractory to chemotherapy, the combination of iron-chelating agents and VD resulted in reversal of pancytopenia and in blast differentiation. We propose that iron availability modulates myeloid cell commitment and that targeting this cellular differentiation pathway together with conventional differentiating agents provides new therapeutic modalities for AML.

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Authors: Callens, C., Coulon, S., Naudin, J., Radford-Weiss, I., Boissel, N., Raffoux, E., Wang, P. H. M., Agarwal, S., Tamouza, H., Paubelle, E., Asnafi, V., Ribeil, J.-A., Dessen, P., Canioni, D., Chandesris, O., Rubio, M. T., Beaumont, C., Benhamou, M., Dombret, H., Macintyre, E., Monteiro, R. C., Moura, I. C., & Hermine, O.
Affiliations: Centre National de la Recherche Scientifique UMR 8147, Paris 75015, France 1
Centre National de la Recherche Scientifique (FR)
Faculté de Médecine, Université René Descartes Paris V, Institut Fédératif Necker, Paris 75015, France 2
Assistance Publique – Hôpitaux de Paris (FR)
Inserm (FR)
Hôpital Necker-Enfants Malades (FR)
Institut Gustave Roussy (FR)
Corresponding author: Hermine, Olivier
ORCID: Naudin, Jerome
Boissel, Nicolas
Raffoux, Emmanuel
Agarwal, Saurabh
Asnafi, Vahid
Ribeil, Jean-Antoine
Dessen, Philippe
Benhamou, Marc
Dombret, Hervé
Macintyre, Elizabeth
Monteiro, Renato C.
Moura, Ivan C.
Hermine, Olivier
Venue: Journal of Experimental Medicine
Publisher: Rockefeller University Press
Published: 2010-04-05
Volume: 207
Issue: 4
Pages: 731-750
ISSN: 0022-1007 (ISSN-L)
1540-9538
DOI: 10.1084/jem.20091488
PMC: PMC2856037
OpenAlex: W2137774959
Cited by: 197
References: 76
Citations by year: 2026: 2 · 2025: 8 · 2024: 5 · 2023: 14 · 2022: 11 · 2021: 15 · 2020: 13 · 2019: 9 · 2018: 13 · 2017: 12 · 2016: 11 · 2015: 13 · 2014: 13 · 2013: 9 · 2012: 20
FWCI: 11.44
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: The Journal of Experimental Medicine (publishedVersion)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
HAL (submittedVersion)
Funders: Institut National de la Santé et de la Recherche Médicale
Fondation pour la Recherche Médicale
Fondation de France
Topics: Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Keywords: acute myeloid leukemia, iron homeostasis, iron chelation, iron starvation, cell differentiation, vitamin D3, vitamin D receptor, reactive oxygen species, monocyte-to-macrophage differentiation, pancytopenia, combination therapy, refractory leukemia
MeSH terms: Iron Deficiencies, Aged, Animals, Antibodies, Monoclonal, Blood Cell Count, Cell Differentiation, Cholecalciferol, Drug Synergism, Female, Granulocytes, Hematopoietic Stem Cells, Homeostasis, Humans, Hydroxycholecalciferols, Iron, Iron Chelating Agents, Male, Mice, Nude, Monocytes, Phosphorylation, Receptors, Transferrin, Leukemia, Myeloid, Acute, Antigens, CD, Gene Expression, Apoptosis, Reactive Oxygen Species, Receptors, Calcitriol, Lipopolysaccharide Receptors, Gene Expression Profiling, Mitogen-Activated Protein Kinases, Xenograft Model Antitumor Assays, CD11b Antigen, Cell Line, Tumor, JNK Mitogen-Activated Protein Kinases, Cell Proliferation, Mice, Kaplan-Meier Estimate

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Targeting iron homeostasis induces cellular differentiation and synergizes with differentiating agents in acute myeloid leukemia

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