Oral squamous cell carcinomas drive monocytes into immunosuppressive CD25+CD163+CD206+ macrophages
Ontology highlight
ABSTRACT:
PROVIDER: PRJNA1111562 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR29025628_1.fastq.gz | Fastqsanger.gz | |||
| SRR29025628_2.fastq.gz | Fastqsanger.gz | |||
| SRR29025629_1.fastq.gz | Fastqsanger.gz | |||
| SRR29025629_2.fastq.gz | Fastqsanger.gz | |||
| SRR29025630_1.fastq.gz | Fastqsanger.gz |
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Project description:Tumor-associated macrophages (TAMs) are major cellular components in the tumor microenvironment of oral squamous cell carcinomas (OSCCs). Most of these TAMs derive from circulating monocytes that differentiate in situ. In this work, we show that cell culture media (CM) derived from two OSCC cell lines, H413 and TR146, promote monocyte differentiation into M2 macrophages, characterized by a high expression of CD163, CD206 and a low expression of CD11c, CD86 and HLA-DR. These monocyte-derived macrophages (moMΦ) differentiated by CM from H413 cells were unable to activate allogeneic T cells, and inhibited T cell activation and proliferation induced by CD3/CD28 stimulation. By culturing monocytes with fractionated H413-CM, we found that soluble proteins mediated CD163+CD206+ moMΦ differentiation, discarding a role for small metabolites and extracellular vesicles. Differential proteomic analyses on H413-CM fractions revealed the presence of several proteins, including the complement factor H or plasminogen activator inhibitor, as potential candidates to induce CD163+CD206+ moMΦ differentiation. Finally, RNAseq transcriptomic analyses of H413 CM conditioned moMΦ, identified a signature expression profile involving cytokines and cytokine receptors, which surprisingly included IL2RA (CD25). CD25 enhanced expression was confirmed on H143-CM moMΦ. Collectively, these data indicate that the CM from OSCC cell lines promotes the differentiation of monocytes into functionally immunosuppressive macrophages and overall, our work contributes to the understanding of how OSCCs create an immunosuppressive cellular environment that favors tumor growth.
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Project description:CD163 macrophages, which can be identified in different tissues of individuals such as the colon and tumor tissues, possessed markedly immunosuppressive functions on immune cells, especially effective cells such as CD8 cells. However, the mechanism(s) by which CD163 macrophages inhibit immune responses remains to be illusive. Using single cell-sequence techniques, we identified CD163+ macrophage subset in the colon tissues. Meanwhile, we also characterized CD163+ macrophage associated immune cell populations and subpopulations in mouse colon tissues. Deletion of CD163+ macrophage subset could markedly increase the proportions of CD8 and NK cells. Mechanistically, CD163+ macrophage subpopulations can inhibit the proliferation of CD8 and NK cells through inhibitory molecules CD94/NKG2a (KLRD1/KLRC1 in mice) and their ligand HLA-E /H2-T23 (Human/mice) on the surface of CD163+ macrophages. Importantly, CD163 in macrophages could promote the expression of HLA-E/H2-T23 expression through inducing the expression of signal peptide peptidase (SPP), offering a target for immunotherapy in CD8 and NK cells associated immunosuppressive diseases such as tumor. Taken together, we demonstrate that CD163+macrophage subpopulation plays a critical role in suppressing CD8 and NK cells through CD163 mediated HLA-E/H2-T23.
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Project description:CD206 is a common marker of a putative immunosuppressive ‘M2’ state in tumor-associated macrophages (TAMs). We made a novel conditional CD206 (Mrc1) knock-in mouse to specifically visualize and/or deplete CD206+ TAMs. Early depletion of CD206+ macrophages and monocytes (Mono/Macs) led to the indirect loss of conventional type I dendritic cells (cDC1), CD8 T cells and NK cells in tumors. CD206+ TAMs robustly expressed CXCL9, contrasting with stress-responsive Spp1-expressing TAMs and immature monocytes, which became prominent with early depletion. CD206+ TAMs differentially attracted activated CD8 T cells, and the NK and CD8 T cells in CD206-depleted tumors were deficient in Cxcr3, and cDC1-supportive Xcl1 and Flt3l expression. Disrupting this key anti-tumor axis decreased tumor control by antigen-specific T cells in mice. In human cancers, a CD206Replete, but not a CD206Depleted Mono/Mac gene signature correlated robustly with CD8 T cell, cDC1 and NK signatures, and associated with better survival. These findings negate the unqualified classification of CD206+ ‘M2-like’ macrophages as immunosuppressive.
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Project description:The direct and indirect effects of targeting specific tumor-associated macrophage (TAM) subsets in cancer are not well-defined. TAM targeting strategies are frequently based on the ‘M1’ or ‘M2’ polarization categories, even as substantial data challenges this binary modeling of macrophage cell state. One molecule consistently referenced as a delineator of a putative immunosuppressive ‘M2’ state is the surface protein CD206. We thus made a novel conditional CD206 (Mrc1) knock-in mouse to specifically visualize and/or deplete CD206+ TAMs and assess their correspondence with pro-tumoral immunity. Early, but not late depletion of CD206+ macrophages and monocytes (here, ‘Mono/Macs’) led to an indirect loss of a key anti-tumor network of NK cells, conventional type I dendritic cells (cDC1) and CD8 T cells. Among myeloid cells, we found that the CD206+ TAMs are the primary producers of CXCL9, and able to differentially attract activated CD8 T cells. In contrast, a population of stress-responsive TAMs (“Hypoxic” or Spp1+) and immature monocytes, which lack CD206 expression and become prominent following early depletion, expressed markedly diminished levels of CXCL9. Those NK and CD8 T cells which enter CD206-depleted tumors express vastly reduced levels of the corresponding receptor Cxcr3, the cDC1-attracting chemokine Xcl1 and cDC1 growth factor Flt3l transcripts. Consistent with the loss of this critical network, early CD206+ TAM depletion decreased tumor control by antigen specific CD8 T cells in mice. Likewise, in humans, the CD206Replete, but not the CD206Depleted Mono/Mac gene signature correlated robustly with CD8 T cell, NK cell and stimulatory cDC1 gene signatures and transcriptomic signatures skewed towards CD206Replete Mono/Macs associated with better survival. Together, these findings negate the unqualified classification of CD206+ ‘M2-like’ macrophages as immunosuppressive and provide further evidence of the context-dependence of macrophage function in tumors.
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