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Disrupted homeostasis of synovial hyaluronic acid and its associations with synovial mast cell proteases of rheumatoid arthritis patients and collagen-induced arthritis rats

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Abstract

Hyaluronic acid (HA) is the main component of the extracellular matrix (ECM) of joints, and it is important for a lubricating joint during body movement. Degradation is the main metabolic process of HA in vivo. Hyaluronidases (HAase) were known for HA degradation. The inflammation-induced HA rapid-metabolism can reduce HA viscosity and concentration in joints. Mast cells (MC) containing their specific proteases were found in synovium tissue. It is unclear if MC-proteases could be involved in HA degradation pathways. This study aims to explore the correlations between HA concentration vs mast cell proteases, or matrix metalloproteinase-2/9 (MMP-2/9) and to investigate the association of MC-specific proteases with disrupted synovial HA homeostasis in rheumatoid arthritis (RA) or collagen-induced arthritis rats. The synovial fluid samples from no-RA and RA patients were collected; the collagen-induced arthritis (CIA) rat model was established; HA concentration and the activities of MC-protease and MMP-2/9 in the samples were detected, and the correlations were analyzed. In vitro interaction experiment was carried out by mixing MC-proteases with HA to observe the degradation speed. The HA concentrations in synovial fluids were decreased in RA patients and CIA rats compared with those in no-RA subjects or normal rats respectively. The activities of mast cell proteases in synovial fluids were increased and positively correlated with MMP-9, but negatively correlated with HA concentrations. In vitro study, the addition of MC-chymase and tryptase promoted the speed in HA degradation. MC-proteases may influence HA degradation pathway.

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Funding

This work was supported by the Start-up Research Laboratory for Over-sea Talent Fund, China (Z391405) and Changzhou University Research Introduction Research Fund (ZMF14020066) to Prof. Xiaoying Zhou; Changzhou University Undergraduate Innovation and Entrepreneurship Fund, China (2019–02-C-96) to Yaming Guo; National Science Foundation of China (No: 81503136) to Nan Hu; and Jiangsu Province Graduate Student Scientific Research Innovation Scheme (201810292046Y) to Tao Wei.

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Authors and Affiliations

  1. School of Pharmacy, School of Medicine, Changzhou University, Changzhou, 213164, Jiangsu, China

    Yaming Guo, Tao Wei & Xiaoying Zhou

  2. Endocrine Department, Changzhou First People’s Hospital, Changzhou, 213003, China

    Nan Hu

  3. School of Medicine, the University of Southampton, Southampton, SO16 6YD, UK

    Xiaoying Zhou

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  1. Yaming Guo
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  2. Tao Wei
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Contributions

The corresponding author, Prof. Xiaoying Zhou, has made contributions to the funding, organizations, conception, design, interpretation of data, drafted/edited, and corrected the paperwork critically for intellectual content; co-first authors, Yaming Guo and Tao Wei, have made contributions to the funding, experimental works, technique operation, involved in animal model and cell model, data analysis, and preparation of the first draft and figures and corrections; Dr. Nan Hu has made contributions to experimental works, technique operation, data analysis, and drafting of corrections.

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Correspondence to Xiaoying Zhou.

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All procedures were undertaken with the approval of the Changzhou University Ethics Association (application approval number: CCZU20191022).

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Guo, Y., Wei, T., Hu, N. et al. Disrupted homeostasis of synovial hyaluronic acid and its associations with synovial mast cell proteases of rheumatoid arthritis patients and collagen-induced arthritis rats. Immunol Res 69, 584–593 (2021). https://doi.org/10.1007/s12026-021-09231-2

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