Macrophages modulate mesenchymal stem cell function via tumor necrosis factor alpha in tooth extraction model.

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Department of Oral Rehabilitation and Regenerative Medicine, Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, 2-5-1 Shikata-cho, Kita-ku, Okayama 700-8525, Japan.

Published: August 2024

Mesenchymal stem cells (MSCs) and macrophages collaboratively contribute to bone regeneration after injury. However, detailed mechanisms underlying the interaction between MSCs and inflammatory macrophages (M1) remain unclear. A macrophage-depleted tooth extraction model was generated in 5-wk-old female C57BL/6J mice using clodronate liposome (12.5 mg/kg/mouse, intraperitoneally) or saline injection (control) before maxillary first molar extraction. Mice were sacrificed on days 1, 3, 5, 7, and 10 after tooth extraction ( = 4). Regenerated bone volume evaluation of tooth extraction socket (TES) and histochemical analysis of CD80M1, CD206M2 (anti-inflammatory macrophages), PDGFRαMSC, and TNF-α cells were performed. In vitro, isolated MSCs with or without TNF-α stimulation (10 ng/mL, 24 h,  = 3) were bulk RNA-sequenced (RNA-Seq) to identify TNF-α stimulation-specific MSC transcriptomes. Day 7 micro-CT and HE staining revealed significantly lower mean bone volume (clodronate vs control: 0.01 mm vs 0.02 mm, <.0001) and mean percentage of regenerated bone area per total TES in clodronate group (41.97% vs 54.03%, <.0001). Clodronate group showed significant reduction in mean number of CD80, TNF-α, PDGFRα, and CD80TNF-α cells on day 5 (306.5 vs 558.8, <.0001; 280.5 vs 543.8, <.0001; 365.0 vs 633.0, <.0001, 29.0 vs 42.5, <.0001), while these cells recovered significantly on day 7 (493.3 vs 396.0, =.0004; 479.3 vs 384.5, =.0008; 593.0 vs 473.0, =.0010, 41.0 vs 32.5, =.0003). RNA-Seq analysis showed that 15 genes (|log2FC| > 5.0, log2TPM > 5) after TNF-α stimulation were candidates for regulating MSC's immunomodulatory capacity. In vivo, and are involved in inflammation and bone formation. , , and knockdown increased osteogenic differentiation of MSCs in vitro. Temporal reduction followed by apparent recovery of TNF-α-producing M1 macrophages and MSCs after temporal macrophage depletion suggests that TNF-α activated MSCs during TES healing. In vitro mimicking the effect of TNF-α on MSCs indicated that there are 15 candidate MSC genes for regulation of immunomodulatory capacity.

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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC11289833PMC
http://dx.doi.org/10.1093/jbmrpl/ziae085DOI Listing

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