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Heme-signaling progresses via NRF2 to educate heme-TAM transformation, tumor cell growth, and invasiveness

ABSTRACT: Heme-signaling progresses via NRF2 to educate heme-TAM transformation, tumor cell growth, and invasiveness

PROVIDER: PRJNA993270 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR25223786.fastq.gz	Fastqsanger.gz
	SRR25223787.fastq.gz	Fastqsanger.gz
	SRR25223788.fastq.gz	Fastqsanger.gz

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Heme-signaling progresses via NRF2 to educate heme-TAM transformation, tumor cell growth, and invasiveness

Project description:Heme-activation of NRF2 is a strong anti-inflammatory signal in macrophages, and analyses in this study indicated that the expressed transcriptome in heme-TAMs was consistently enriched for NRF2 target genes. We have therefore delineated the role of NRF2 in a series of experiments with Nrf2 knockout BMDMs, leading to a locked NRF2-inactive state, and macrophages with a knockout of the cytoplasmic NRF2 capture protein KEAP1, leading to a locked NRF2-active state, irrespective of the presence or absence of heme. To demonstrate that activated NRF2 is sufficient to drive heme-TAM transformation, we analyzed Keap1 knockout macrophages.

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Heme-Nrf2 signaling shifts myeloid differentiation

Project description:Heme is an erythrocyte-derived toxin that drives disease progression in hemolytic anemias. During hemolysis, specialized bone marrow-derived macrophages with a high heme-metabolism capacity orchestrate disease adaptation by removing damaged erythrocytes and heme-protein complexes from the blood and supporting iron recycling for erythropoiesis. Here, we performed single-cell RNA sequencing with RNA velocity analysis of GM-CSF-supplemented mouse bone marrow cultures to assess myeloid differentiation under heme stress. We found that heme-activated NRF2 signaling shifted the differentiation trajectories of cells towards antioxidant, iron-recycling macrophages at the expense of dendritic cells, as these cells were selectively deficient in heme-exposed bone marrow cultures. Heme eliminated the capacity of GM-CSF-supplemented bone marrow cultures to activate antigen-specific T cells. The generation of functionally competent dendritic cells was restored by NRF2 loss. The heme-induced phenotype was reproduced in hemolytic mice with sickle cell disease and spherocytosis and associated with reduced dendritic cell functions in the spleen. Our data provide a novel mechanistic underpinning how hemolytic stress may provoke hyposplenism-related secondary immunodeficiency, which is a critical determinant of mortality in patients with genetic hemolytic anemias.

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Project description:Bulk RNA sequencing revealed that heme exposure induced the phenotype of Hmox1high, Marcohigh, and MHC class IIlow macrophages, demonstrating a strong expression of NRF2-regulated. However, these cells showed weak expression of the TAM marker genes Arg1 and Spp1, indicating that heme treatment alone was insufficient to induce the full heme-TAM phenotype.

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Heme-TAMs prevent cancer cell apoptosis and drive growth, invasiveness, and metastasis

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Heme-Nrf2 signaling shifts myeloid differentiation

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Project description:To study the impact of heme-TAMs on the growth, phenotype, and function of cancer cells, we cultured GFP-MC38 cells either alone or mixed with heme-treated macrophages in microwell plates, enabling us to collect large numbers of uniform spheroids for scRNA-seq. We observed that after four days, the size of GFP-MC38 spheroids regressed, and the tumor cells underwent apoptosis and decayed metabolically. In contrast, the presence of heme-TAMs within spheroids prevented apoptosis, supporting the extended growth of metabolically viable spheroids beyond 10 days of culture.

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Project description:Red blood cell heme drives the generation of TAM-like macrophages with an immunocompromized phenotype

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