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TNF-α-elicited miR-29b potentiates resistance to apoptosis in peripheral blood monocytes from patients with rheumatoid arthritis

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Abstract

CD14-positive monocytes from patients with rheumatoid arthritis (RA) are more resistant to apoptosis, which promotes their persistence at the inflammatory site and thereby contributes crucially to immunopathology. We sought to elucidate one mechanism underlying this unique pathogenesis: resistance to apoptosis and the potential involvement of miR-29b in this process. CD14-positive peripheral blood monocytes (PBMs) from RA patients were observed to be resistant to spontaneous apoptosis compared to PBMs from healthy volunteers. Intriguingly, expression of miR-29b was significantly upregulated in PBMs from RA patients than those from healthy volunteers, and this upregulation was correlated with RA disease activity. Functionally, forced expression of the exogenous miR-29b in CD14-positive Ctrl PBMs conferred resistance to spontaneous apoptosis and Fas-induced death, thereafter enhancing the production of major proinflammatory cytokines in there cells. Following identification of the potential miR-29b target transcripts using bioinformatic algorithms, we showed that miR-29b could directly bind to the 3′-UTR of the high-mobility group box-containing protein 1 (HBP1) and inhibited its transcription in PBMs. Importantly, stable expression of the exogenous HBP1 in differentiated THP-1 monocytes effectively abolished miR-29b-elicited resistance to Fas-induced apoptosis. Finally, among patients with RA and good clinical responses to immunotherapy, expression levels of miR-29b were significantly compromised in those treated with infliximab (a TNF-α inhibitor) but not in those treated with tocilizumab (a humanized mAb against the IL-6 receptor), pointing to a potential association between miR-29b activation and TNF-α induction. The available data collectively suggest that TNF-α-elicited miR-29b potentiates resistance to apoptosis in PBMs from RA patients via inhibition of HBP1 signaling, and testing patients for miR-29b/HBP1 expression ratios may provide more accurate prognostic information and could influence the recommended course of immunotherapy.

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Acknowledgements

This work was supported by Natural Science Foundation of Shaanxi (2016JM8147, 2017SF247), Shaanxi Provincial Administration of Ttraditional Chinese Medicine Research Projects (2017LCMS057), Xi’an Science and Technology Project [201805096YX4SF30(14)], Xi’an Traditional Chinese Medicine Research Project (2018).

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SFig. 1 Flow cytometry dot plot confirmed that the majority of isolated PBMs in our study were nonclassical (CD14+CD16++) PBMs.

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SFig. 2 THP-1 and THP-1/HBP1 cells were seeded at a density of 1.1 × 105 cells/cm2 onto tissue culture treated polystyrene (TCPS) cell culture dishes (Thermo Fisher Scientific) and cultured in basal medium supplemented with 5 ng/ml of PMA for 48 h to differentiate the cells towards resting state (M-) macrophages. Cells were then washed with basal medium and cultured for another 24 h. Subsequently, medium was replaced either with medium containing 100 ng/ml of LPS plus 20 ng/ml of IFNγ to induce polarization to M1-like macrophages or with medium containing 20 ng/ml of IL-4 to induce polarization to M2-like macrophages, respectively. At the end of 6 or 24 h after polarization stimulation, cells were harvested and subjected to RT-PCR analysis. M1-like polarized macrophages were characterized by increased expression levels of TNFα, CXCL10, and CD197 mRNA, while M2-like polarized macrophages were characterized by increased expression levels of CXCL22 and CD206 mRNA. Apparently, stable expression of HBP1 in THP-1 cells had no any effects on their polarization.

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Ren, B., Liu, J., Wu, K. et al. TNF-α-elicited miR-29b potentiates resistance to apoptosis in peripheral blood monocytes from patients with rheumatoid arthritis. Apoptosis 24, 892–904 (2019). https://doi.org/10.1007/s10495-019-01567-3

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