Dual roles of CD11b+CD33+HLA-DR-/lowCD14- myeloid-derived suppressor cells with a granulocytic morphology following allogeneic hematopoietic stem cell transplantation: from inflammation promoters to immune suppressors within 90 days

Front Immunol. 2024 Jul 8:15:1403272. doi: 10.3389/fimmu.2024.1403272. eCollection 2024.

Abstract

Introduction: Granulocytic myeloid-derived suppressor cells (G-MDSCs) show fast recovery following allogeneic hematopoietic stem cell transplantation (allo-HSCT) constituting the major part of peripheral blood in the early phase. Although G-MDSCs mediate immune suppression through multiple mechanisms, they may also promote inflammation under specific conditions.

Methods: G-MDSCs were isolated from 82 patients following allo-HSCT within 90 days after allo-HSCT, and their interactions with autologous CD3+ T-cells were examined. T-cell proliferation was assessed by flow cytometry following CFSE staining, while differentiation and interferon-γ secretion were characterized using chemokine receptor profiling and ELISpot assays, respectively. NK cell cytotoxicity was evaluated through co-culture with K562 cells. An aGVHD xenogeneic model in humanized mice was employed to study the in vivo effects of human leukocytes. Furthermore, transcriptional alterations in G-MDSCs were analyzed via RNA sequencing to investigate functional transitions.

Results: G-MDSCs promoted inflammation in the early-stage, by facilitating cytokine secretion and proliferation of T cells, as well as their differentiation into pro-inflammatory T helper subsets. At day 28, patients with a higher number of G-MDSCs exhibited an increased risk of developing grades II-IV aGvHD. Besides, adoptive transfer of G-MDSCs from patients at day 28 into humanized mice exacerbated aGvHD. However, at day 90, G-MDSCs led to immunosuppression, characterized by upregulated expression of indoleamine 2,3-dioxygenase gene and interleukin-10 secretion, coupled with the inhibition of T cell proliferation. Furthermore, transcriptional analysis of G-MDSCs at day 28 and day 90 revealed that 1445 genes were differentially expressed. These genes were associated with various pathways, revealing the molecular signatures of early post-transplant differentiation in G-MDSCs. In addition, genes linked to the endoplasmic reticulum stress were upregulated in patients without aGvHD. The acquisition of immunosuppressive function by G-MDSCs may depend on the activation of CXCL2 and DERL1 genes.

Conclusion: Our findings revealed the alteration in the immune characteristics of G-MDSCs within the first 90 days post-allo-HSCT. Moreover, the quantity of G-MDSCs at day 28 may serve as a predictive indicator for the development of aGvHD.

Keywords: ER-stress; G-MDSCs; HO-1; T cells; aGVHD; allo-HSCT; immunomodulation.

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • CD11b Antigen / immunology
  • CD11b Antigen / metabolism
  • Female
  • Graft vs Host Disease / immunology
  • Granulocytes / immunology
  • Granulocytes / metabolism
  • HLA-DR Antigens / genetics
  • HLA-DR Antigens / immunology
  • HLA-DR Antigens / metabolism
  • Hematopoietic Stem Cell Transplantation* / adverse effects
  • Humans
  • Inflammation / immunology
  • Male
  • Mice
  • Middle Aged
  • Myeloid-Derived Suppressor Cells* / immunology
  • Myeloid-Derived Suppressor Cells* / metabolism
  • Transplantation, Homologous*
  • Young Adult

Substances

  • HLA-DR Antigens
  • CD11b Antigen

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (Nos. 82160046, 82260045) by MN and PZ, respectively. This investigation is also supported by Natural Science Foundation of Guizhou Province, China (Qian Ke He Foundation (2021) No.397; (2022) No.416) received by MN and JC, respectively.