Infrapatellar Fat Pad-Synovial Membrane Anatomo-Fuctional Unit: Microscopic Basis for Piezo1/2 Mechanosensors Involvement in Osteoarthritis Pain

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Abstract

The Infrapatellar Fat Pad (IFP) is a fibro-adipose tissue of the knee recently reconsidered as part of a single anatomo-functional unit (AFU) together with the synovial membrane (SM). Several evidence support the role of this unit in the mechanisms that trigger and perpetuate the onset and progression of osteoarthritis (OA) disease. Additionally, the contribution of IFP-SM AFU in OA-associated pain has also been supposed, but this assumption still needs to be fully elucidated. Within this context, the recent discovery of the mechanoceptive Piezo ion channels (i.e., Piezo1 and Piezo2) in mammals and consciousness on their role in mediating both mechanoceptive and inflammatory stimuli could shed some light on knee OA pain, as well as on the process leading from acute to chronic nociceptive responses. For this purpose, the IFP-SM AFUs of both healthy donors (non-OA IFP-SM AFUs, n = 10) and OA patients (OA IFP-SM AFUs, n = 10) were processed by histology and immunohistochemistry. After the attribution of a histopathological score to IFP-SM AFUs to confirm intrinsic differences between the two groups, the specimens were investigated for the expression and localization/distribution pattern of the mechanosensors Piezo1 and Piezo2. In addition, the presence of monocytes/macrophages (CD68), peripheral nerve endings (PGP9.5) and neoangiogenesis signs (YAP1) was evaluated for a broad tissue characterization. The study results lead to a better description of the IFP-SM AFU microscopic features in both healthy and pathological conditions, highlighting peculiar differences in the study cohort. Specifically, immunopositivity towards Piezo1/2, CD68 and YAP1 markers was detected at vessels level in the OA- IFP-SM AFUs compartments, differently from the non-OA-group. A correlation with pain was also inferred, paving the way for the identification of new and effective molecules in OA management.

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Most cited references 83

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Osteoarthritis: a disease of the joint as an organ.

Richard F. Loeser, Steven R. Goldring, Carla R. Scanzello … (2012)

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Osteoarthritis.

Johanne Martel-Pelletier, Andrew J Barr, Flavia Cicuttini … (2016)

Osteoarthritis (OA) is the most common joint disorder, is associated with an increasing socioeconomic impact owing to the ageing population and mainly affects the diarthrodial joints. Primary OA results from a combination of risk factors, with increasing age and obesity being the most prominent. The concept of the pathophysiology is still evolving, from being viewed as cartilage-limited to a multifactorial disease that affects the whole joint. An intricate relationship between local and systemic factors modulates its clinical and structural presentations, leading to a common final pathway of joint destruction. Pharmacological treatments are mostly related to relief of symptoms and there is no disease-modifying OA drug (that is, treatment that will reduce symptoms in addition to slowing or stopping the disease progression) yet approved by the regulatory agencies. Identifying phenotypes of patients will enable the detection of the disease in its early stages as well as distinguish individuals who are at higher risk of progression, which in turn could be used to guide clinical decision making and allow more effective and specific therapeutic interventions to be designed. This Primer is an update on the progress made in the field of OA epidemiology, quality of life, pathophysiological mechanisms, diagnosis, screening, prevention and disease management.

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The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis.

Jérémie Sellam, Francis Berenbaum (2010)

Osteoarthritis (OA), one of the most common rheumatic disorders, is characterized by cartilage breakdown and by synovial inflammation that is directly linked to clinical symptoms such as joint swelling, synovitis and inflammatory pain. The gold-standard method for detecting synovitis is histological analysis of samples obtained by biopsy, but the noninvasive imaging techniques MRI and ultrasonography might also perform well. The inflammation of the synovial membrane that occurs in both the early and late phases of OA is associated with alterations in the adjacent cartilage that are similar to those seen in rheumatoid arthritis. Catabolic and proinflammatory mediators such as cytokines, nitric oxide, prostaglandin E(2) and neuropeptides are produced by the inflamed synovium and alter the balance of cartilage matrix degradation and repair, leading to excess production of the proteolytic enzymes responsible for cartilage breakdown. Cartilage alteration in turn amplifies synovial inflammation, creating a vicious circle. As synovitis is associated with clinical symptoms and also reflects joint degradation in OA, synovium-targeted therapy could help alleviate the symptoms of the disease and perhaps also prevent structural progression.

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Aron Emmi: URI : https://loop.frontiersin.org/people/862227/overview

Elena Stocco: URI : https://loop.frontiersin.org/people/1256830/overview

Martina Contran: URI : https://loop.frontiersin.org/people/1258840/overview

Elisa Belluzzi: URI : https://loop.frontiersin.org/people/304657/overview

Roberta Ramonda: URI : https://loop.frontiersin.org/people/958230/overview

Andrea Porzionato: URI : https://loop.frontiersin.org/people/181414/overview

Pietro Ruggieri: URI : https://loop.frontiersin.org/people/1626529/overview

Raffaele De Caro: URI : https://loop.frontiersin.org/people/191378/overview

Veronica Macchi: URI : https://loop.frontiersin.org/people/191374/overview

Journal

Journal ID (nlm-ta): Front Cell Dev Biol

Journal ID (iso-abbrev): Front Cell Dev Biol

Journal ID (publisher-id): Front. Cell Dev. Biol.

Title: Frontiers in Cell and Developmental Biology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2296-634X

Publication date (Electronic): 28 June 2022

Publication date Collection: 2022

Volume: 10

Electronic Location Identifier: 886604

Affiliations

[1] ¹ Department of Neuroscience , Section of Human Anatomy , University of Padova , Padova, Italy

[2] ² Musculoskeletal Pathology and Oncology Laboratory , Department of Surgery , Oncology and Gastroenterology (DiSCOG) , University of Padova , Padova, Italy

[3] ³ Orthopedics and Orthopedic Oncology , Department of Surgery , Oncology and Gastroenterology (DiSCOG) , University of Padova , Padova, Italy

[4] ⁴ Rheumatology Unit , Department of Medicine-DIMED , University of Padova , Padova, Italy

[5] ⁵ Internal Medicine I , Cà Foncello Hospital , Treviso, Italy

Author notes

Edited by: Yi Zhang, Central South University, China

Reviewed by: Shufang Wu, Xian Jiaotong University, China

Alek Erickson, Karolinska Institutet (KI), Sweden

*Correspondence: Raffaele De Caro, rdecaro@ 123456unipd.it

[ † ]

These authors have contributed equally to this work and share first authorship

This article was submitted to Stem Cell Research, a section of the journal Frontiers in Cell and Developmental Biology

Article

Publisher ID: 886604

DOI: 10.3389/fcell.2022.886604

PMC ID: 9274201

PubMed ID: 35837327

SO-VID: 7935bb60-f9a1-4950-b71b-28b3bf8f144b

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Infrapatellar Fat Pad-Synovial Membrane Anatomo-Fuctional Unit: Microscopic Basis for Piezo1/2 Mechanosensors Involvement in Osteoarthritis Pain

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GLUT4 biology

Most cited references 83

Osteoarthritis: a disease of the joint as an organ.

Osteoarthritis.

The role of synovitis in pathophysiology and clinical symptoms of osteoarthritis.

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