摘要
Background:
The enthesis is a pivotal target tissue in spondyloarthritis (SpA), marked by inflammation in both the enthesis soft tissue (EST) and the contiguous anchoring peri-entheseal bone (PEB) [1]. The healthy human spinal enthesis harbors resident mesenchymal stem cells (MSCs), myeloid cells, innate immune cell populations, while notably lacking FOXP3+ regulatory T cells (Treg) [2, 3]. In a previous investigation, we posited that MSCs within the enthesis, as opposed to regulatory T cells, are pivotal contributors to the observed physiological immunomodulation in this tissue [4]. Objectives:
This study seeks to elucidate whether the immunosuppressive pathway mediated by CD39/CD37 ectonucleotidase enzymes and adenosine is responsible for the immunosuppressive effects exerted by entheseal MSCs. Methods:
Samples from healthy spinous processes and interspinous ligaments were divided into EST and PEB regions, enzymatically digested, and analyzed via flow cytometry. Cells were expanded to passage 3-5 (n=5) for co-culture experiments. CD4+ CD25- cells (T cells) were isolated from a single healthy donor and induced to proliferate using CD3/CD28 stimulation. Co-culture of MSCs and T cells was conducted at ratios of 1:1, 1:2, 1:4, and 1:8 for 5 days. The Flowjo software was employed to calculate the T cell proliferation index. Treg-related markers, including CD73 and CD39, were assessed cytometrically in PEB and EST. CD39 and CD73 were blocked using POM-1 and AOPCP, followed by co-culture with stimulated T cells for 5 days. Total adenosine production was measured using an Adenosine Assay Kit. Results:
Activated T cells significantly upregulated CD39/CD73 on MSCs (EST and PEB) surfaces (P<0.001). In vivo uncultured EST and PEB MSCs exhibited the expression of CD39/CD73, affirming the translational relevance of this study. Co-culture of MSCs EST and PEB with activated T cells at a 1:1 ratio resulted in a significant suppression of T cell proliferation by 79% and 89%, respectively, compared to activated T cells alone. RNA-seq analysis of MSCs post co-culture indicated the upregulation of 390 genes and downregulation of 306 genes in EST MSCs, while 119 genes were upregulated, and 90 genes were downregulated in PEB MSCs (P<0.05). This analysis revealed the upregulation of shared immunosuppression pathways with Treg cells, including ENTPD3 (CD39), NT5E (CD73), CTLA-4, IL10, CCR4, CCR8, Foxp3, PTGER4, IL6, IDO1, PDL-1. Along with the upregulation of osteogenesis markers (CASR, APL) and downregulation of adipogenic markers (PPARG, SFRP4) and chondrogenic markers (GDF6, COL1A2). Simultaneously, IL17A and IL17F were upregulated and TGFβ downregulated. Blockage of CD39, CD73, and dual blockage increased T cell proliferation at 1:1 ratio with EST MSCs by 17.4%, 23.1%, and 52.2%, and with PEB MSCs by 32.1%, 41.9%, and 54.7%, respectively. This increase in T cell proliferation occurred concurrently with the inhibition of adenosine production. RNA-seq analysis of MSCs after adenosine inhibition via dual blockage of CD39/CD73 influenced immunosuppression markers shared with Treg cell pathways, resulting in the downregulation of CTLA-4, IL10, FOXP3, HLA-G, IL6, and IDO1, while CCR4, CCR8, and Foxp3 worked independently of adenosine production. Adenosine inhibition suppressed osteogenesis markers (CASR, APL) in EST and PEB MSCs, while upregulating adipogenic markers (PPARG, SFRP4). Conclusion:
This study provides evidence that the MSCs derived from enthesal tissues possess an intrinsic immunomodulation capacity regulated by inflammation. These findings exert a significant influence on T cell activity, supporting the involvement of the CD39/73 adenosine pathway. REFERENCES:
[1] Benjamin, M. et al., Scand J Med Sci Sports, 2009. 19(4): p. 520-7. [2] Watad, A., et al.,. Annals of the Rheumatic Diseases, 2020. 79(8): p. 1044. [3] Russell, T., et al.,. Cells, 2021. 10(2).4. [4] Altaie, A., et al., op0105, Annals of the Rheumatic Diseases, 2023. 82(Suppl 1): p. 70-71. Acknowledgements:
NIL. Disclosure of Interests:
None declared.