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Synovial Tissue Macrophages: Friend Or Foe?

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Synovial Tissue Macrophages: Friend Or Foe? Rheumatoid arthritis RMD Open: first published as 10.1136/rmdopen-2017-000527 on 6 December 2017. Downloaded from REVIEW Synovial tissue macrophages: friend or foe? Mariola Kurowska-Stolarska,1,2 Stefano Alivernini3 To cite: Kurowska-Stolarska M, ABSTRACT Alivernini S. Synovial Healthy synovial tissue includes a lining layer of synovial Key messages tissue macrophages: fibroblasts and macrophages. The influx of leucocytes There are different macrophage subpopulations friend or foe?. RMD Open during active rheumatoid arthritis (RA) includes ► in the human synovium with the potential to 2017;3:e000527. doi:10.1136/ monocytes that differentiate locally into proinflammatory rmdopen-2017-000527 contribute either to joint homeostasis or to chronic macrophages, and these produce pathogenic tumour inflammation in rheumatoid arthritis (RA). necrosis factor. During sustained remission, the synovial Experimental models of arthritis support the ► Prepublication history for tissue macrophage numbers recede to normal. The ► this paper is available online. constitutive presence of tissue macrophages in the lining concept that synovial tissue macrophages have a To view these files, please visit layer of the synovial membrane in healthy donors and pivotal role in reinstating joint homeostasis. the journal online (http://dx. doi. in patients with RA during remission suggests that this ► Deeper understanding of the role of human synovial org/ 10. 1136/ rmdopen- 2017- macrophage population may have a role in maintaining tissue macrophages in the regulation of joint 000527). and reinstating synovial tissue homeostasis respectively. homeostasis offers the prospect of new therapeutic strategies for RA. Received 5 September 2017 Recent appreciation of the different origins and functions Revised 9 November 2017 of tissue-resident compared with monocyte-derived Accepted 12 November 2017 macrophages has improved the understanding of their relative involvement in organ homeostasis in mouse two layers: the first is a thin (eg, <2 mm in models of disease. In this review, informed by mouse 2 radiocarpal joints by ultrasound imaging) models and human data, we describe the presence of but highly cellular lining layer composed different functional subpopulations of human synovial of two cell types: synovial fibroblasts and tissue macrophages and discuss their distinct contribution 1 to joint homeostasis and chronic inflammation in RA. synovial macrophages, and the second is a supporting sublining layer containing loose connective tissue with sublining fibroblasts, http://rmdopen.bmj.com/ SYNOVIAL TISSUE HOMEOSTASIS a rich network of sympathetic and sensory Synovial joints link the musculoskeletal system, nerves and blood and lymphatic vasculature 1Institute of Infection, Immunity and the joint synovium facilitates movement. that provides oxygen/nutrients and immune- and Inflammation, University of 1 Glasgow, Glasgow, UK Bones are linked by the joint capsule and drainage. Synovial fibroblasts provide the 2Rheumatoid Arthritis collagenous ligaments, and the bone surface extracellular matrix (ECM) that supports the Pathogenesis Centre of is covered with articular cartilage that absorbs structure of the synovium and secrete hyal- Excellence (RACE), Universities impact. The joint capsule consists of an outer uronic acid and lubricin into the synovial of Glasgow, Birmingham 1 on September 25, 2021 by guest. Protected copyright. and Newcastle, Glasgow, fibrous membrane containing ligaments and fluid. Synovial tissue macrophages (STM) are Birmingham and Newcastle, UK proprioceptive sensory nerves that regulate constitutively resident in healthy synovium. 3Institute of Rheumatology, the posture and motion of the joint and an Their tissue-specific function remains unre- Fondazione Policlinico inner synovial membrane that produces solved, but this likely includes sentinel joint Universitario A Gemelli, Catholic synovial fluid that lubricates the joint during homeostasis. Other immune cells (lympho- University of the Sacred Heart, Rome, Italy movement and nourishes avascular cartilage. cytes, mast cells and dendritic cells) are scarce In healthy people, this complex joint struc- in the normal synovium and localise mainly in Correspondence to ture is self-regulated by homeostatic mecha- perivascular areas of the sublining layer.3 Dr Mariola Kurowska-Stolarska, nisms to maintain well-functioning articula- In patients with RA, the synovial membrane Institute of Infection, Immunity tion, and the synovial membrane is vital for becomes hypertrophic (eg, 2–5 mm in radio- and Inflammation, University 1 2 of Glasgow Glasgow UK maintaining joint homeostasis. In rheuma- carpal joints) due to synovial fibroblast and Rheumatoid Arthritis toid arthritis (RA), this normal joint structure proliferation, increased blood/lymphatic Pathogenesis Centre of is progressively compromised due to inflam- vasculature and an inflammatory influx of Excellence (RACE) Universities mation of the synovial membrane that fails immune cells from the circulation. The prod- of Glasgow, Birmingham and to resolve, and this ultimately leads to loss of ucts of these activated cells lead to destruc- Newcastle Glasgow, Birmingham and Newcastle UK ; joint function. tion of cartilage and bone, pain and loss of 4 Mariola. Kurowska- Stolarska@ The synovial membrane is a highly special- joint function. These changes appear conse- glasgow. ac. uk ised, multifunctional structure consisting of quential to aberrant homeostatic mechanisms Kurowska-Stolarska M, Alivernini S. RMD Open 2017;3:e000527. doi:10.1136/rmdopen-2017-000527 1 RMD Open RMD Open: first published as 10.1136/rmdopen-2017-000527 on 6 December 2017. Downloaded from that fail to resolve inflammatory synovitis. Understanding reinstated in RA. Therefore, understanding homeostatic synovial homeostasis may offer the prospect of new therapeutic mechanisms in these patients could help to develop ther- strategies for RA. apeutic strategies to reinstate synovial homeostasis in RA. Experimental models of arthritis support the concept that STMs have a pivotal role in this process.15 SYNOVIAL TISSUE INFLAMMATION AND RESOLUTION IN RA RA is the most common inflammatory arthropathy, STM SUBPOPULATIONS affecting approximately 0.4 million people in the UK,5 The functions of macrophages in joint synovial tissue of causing morbidity and reduced quality of life and healthy subjects are poorly described. In RA, most knowl- represents a substantial socioeconomic and healthcare edge of synovial myeloid cells is derived from studies of burden. An interplay between genetics (>100 loci), envi- monocytes from RA synovial fluid that contribute to local ronmental factors (eg, cigarette smoking and occupa- production of inflammatory and joint-degrading media- tional exposure to silica) and alterations in the mucosal tors.16–18 However, monocytes are not present in the syno- microbiome can contribute to the development of RA.6 7 vial fluid from healthy subjects19 and from patients with Clinical RA is preceded by an asymptomatic preclinical RA in remission.20 breach of tolerance to citrullinated self-peptides, activa- STMs are the most common resident immune cells tion of autoreactive T cells and production of anticitrulli- in the healthy synovial membrane,21 and dendritic cells nated peptide-specific antibodies (ACPA). Joint injury or and lymphocytes are scarce. In active RA with myeloid other poorly defined events can then lead to activation and lymphoid synovitis, the synovial membrane is leuco- of the synovial tissue vasculature permitting localisation cyte-rich, including an increased number of proinflam- of ACPA immune complexes in the synovium. These matory macrophages that likely differentiate locally from complexes activate synovial tissue fibroblasts and bone blood monocytes attracted to synovial tissue and fluid by cells (osteoclasts) and perpetuate the influx of leuco- local chemokines,22 and these macrophages are the main cytes, for example, neutrophils, monocytes, Th1/Th17 producers of pathogenic TNF.4 11 17 In remission, most and B cells. These cells are activated by local stimuli (eg, of the synovial inflammation resolves, but STMs in the endogenous Toll-like receptors (TLR) ligands, proinflam- lining layer persist.11 It would be important to establish matory cytokines and hypoxia), further modulated by if these macrophages have the same phenotype as those genetic and epigenetic modifications of gene expression in healthy synovium. The constitutive presence of tissue to propagate the synovitis. Depending on the dominant macrophages in healthy synovial tissue and the sustained cellular component and distinct molecular pathogenic presence in patients with RA during remission suggests pathways, RA synovitis can be characterised as myeloid that these subpopulations of STMs may have a role in (macrophage rich), lymphoid (containing T/B cell folli- 11 4 8 synovial homeostasis. cles) and fibroid (leucocyte low) (comprehensive reviews http://rmdopen.bmj.com/ on mechanisms and type of synovitis). Emerging data suggest that this underlying cellular heterogeneity in RA may THE CONCEPT OF TISSUE-RESIDENT AND MONOCYTE-DERIVED influence the clinical outcome to therapies targeting MACROPHAGES different biological pathways.9 Mouse models show that most healthy organs contain Recent advances in RA therapies mainly target the medi- tissue-resident macrophages that originate from ators of inflammation (eg, tumour necrosis factor (TNF), prenatal precursors and are essential for maintaining
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