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      Skeletal stem cell‐mediated suppression on inflammatory osteoclastogenesis occurs via concerted action of cell adhesion molecules and osteoprotegerin

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          Abstract

          In the current study, we investigated how skeletal stem cells (SSCs) modulate inflammatory osteoclast (OC) formation and bone resorption. Notably, we found that intercellular adhesion molecule‐1 (ICAM‐1), vascular cell adhesion molecule‐1 (VCAM‐1), and osteoprotegerin (OPG) play a synergistic role in SSC‐mediated suppression of inflammatory osteoclastogenesis. The effect of SSCs on inflammatory osteoclastogenesis was investigated using a lipopolysaccharide‐induced mouse osteolysis model in vivo and human osteoarthritis synovial fluid (OASF) in vitro. OC formation was determined by tartrate‐resistant acid phosphatase staining. Bone resorption was evaluated by microcomputerized tomography, serum C‐terminal telopeptide assay, and pit formation assay. The expression of ICAM‐1, VCAM‐1, and OPG in SSCs and their contribution to the suppression of osteoclastogenesis were determined by flow cytometry or enzyme linked immunosorbent assay. Gene modification, neutralization antibodies, and tumor necrosis factor‐α knockout mice were used to further explore the mechanism. The results demonstrated that SSCs remarkably inhibited inflammatory osteoclastogenesis in vivo and in vitro. Mechanistically, inflammatory OASF stimulated ICAM‐1 and VCAM‐1 expression as well as OPG secretion by SSCs. In addition, ICAM‐1 and VCAM‐1 recruited CD11b + OC progenitors to proximity with SSCs, which strengthened the inhibitory effects of SSC‐derived OPG on osteoclastogenesis. Furthermore, it was revealed that tumor necrosis factor α is closely involved in the suppressive effects. In summary, SSCs express a higher level of ICAM‐1 and VCAM‐1 and produce more OPG in inflammatory microenvironments, which are sufficient to inhibit osteoclastogenesis in a “capture and educate” manner. These results may represent a synergistic mechanism to prevent bone erosion during joint inflammation by SSCs.

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          Whole-Organ Magnetic Resonance Imaging Score (WORMS) of the knee in osteoarthritis.

          C Peterfy, A Guermazi, S Zaim … (2004)
          To describe a semi-quantitative scoring method for multi-feature, whole-organ evaluation of the knee in osteoarthritis (OA) based on magnetic resonance imaging (MRI) findings. To determine the inter-observer agreement of this scoring method. To examine associations among the features included in the scoring method. Nineteen knees of 19 patients with knee OA were imaged with MRI using conventional pulse sequences and a clinical 1.5 T MRI system. Images were independently analyzed by two musculoskeletal radiologists using a whole-organ MRI scoring method (WORMS) that incorporated 14 features: articular cartilage integrity, subarticular bone marrow abnormality, subarticular cysts, subarticular bone attrition, marginal osteophytes, medial and lateral meniscal integrity, anterior and posterior cruciate ligament integrity, medial and lateral collateral ligament integrity, synovitis/effusion, intraarticular loose bodies, and periarticular cysts/bursitis. Intraclass correlation coefficients (ICC) were determined for each feature as a measure of inter-observer agreement. Associations among the scores for different features were expressed as Spearman Rho. All knees showed structural abnormalities with MRI. Cartilage loss and osteophytes were the most prevalent features (98% and 92%, respectively). One of the least common features was ligament abnormality (8%). Inter-observer agreement for WORMS scores was high (most ICC values were >0.80). The individual features showed strong inter-associations. The WORMS method described in this report provides multi-feature, whole-organ assessment of the knee in OA using conventional MR images, and shows high inter-observer agreement among trained readers. This method may be useful in epidemiological studies and clinical trials of OA.
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            Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression.

            Guangwen Ren, Xin Zhao, Liying Zhang … (2010)
            Cell-cell adhesion mediated by ICAM-1 and VCAM-1 is critical for T cell activation and leukocyte recruitment to the inflammation site and, therefore, plays an important role in evoking effective immune responses. However, we found that ICAM-1 and VCAM-1 were critical for mesenchymal stem cell (MSC)-mediated immunosuppression. When MSCs were cocultured with T cells in the presence of T cell Ag receptor activation, they significantly upregulated the adhesive capability of T cells due to the increased expression of ICAM-1 and VCAM-1. By comparing the immunosuppressive effect of MSCs toward various subtypes of T cells and the expression of these adhesion molecules, we found that the greater expression of ICAM-1 and VCAM-1 by MSCs, the greater the immunosuppressive capacity that they exhibited. Furthermore, ICAM-1 and VCAM-1 were found to be inducible by the concomitant presence of IFN-gamma and inflammatory cytokines (TNF-alpha or IL-1). Finally, MSC-mediated immunosuppression was significantly reversed in vitro and in vivo when the adhesion molecules were genetically deleted or functionally blocked, which corroborated the importance of cell-cell contact in immunosuppression by MSCs. Taken together, these findings reveal a novel function of adhesion molecules in immunoregulation by MSCs and provide new insights for the clinical studies of antiadhesion therapies in various immune disorders.
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              Discovery of a periosteal stem cell mediating intramembranous bone formation

              Shawon Debnath, Alisha R. Yallowitz, Jason McCormick … (2018)
              Bone is comprised of separate inner endosteal and outer periosteal compartments, each with distinct contributions to bone physiology and each maintaining separate pools of cells due to physical separation by the bone cortex. While the skeletal stem cell giving rise to endosteal osteoblasts has been extensively studied, the identification of a periosteal stem cell has been elusive 1–5 . Here, we identify a periosteal stem cell (PSC) present in the long bones and calvarium of mice that displays clonal multipotency, self-renewal and sits at the apex of a differentiation hierarchy. Single cell and bulk transcriptional profiling show that PSCs display distinct transcriptional signatures in comparison with both other skeletal stem cells and mature mesenchymal cells. While other skeletal stem cells form bone via an initial cartilage template using the endochondral pathway 4 , PSCs form bone via a direct intramembranous route, providing a cellular basis for the divergence between intramembranous versus endochondral developmental pathways. However there is plasticity in this division, as PSCs acquire endochondral bone formation capacity in response to injury. Genetic blockade of the ability of PSCs to give rise to bone-forming osteoblasts results in selective impairments in cortical bone architecture and defects in fracture healing. A cell analogous to PSCs is present in the human periosteum, raising the possibility that PSCs are attractive targets for drug and cellular therapy for skeletal disorders. Moreover, the identification of PSCs provides evidence that bone contains multiple pools of stem cells, each with distinct physiologic functions.
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                Author and article information

                Contributors
                Li Ding: dingli7578@163.com
                Ning Mao: maoning3suo@126.com
                Heng Zhu:
                ORCID: https://orcid.org/0000-0002-8408-3821
                zhudingdingabc@163.com
                Journal
                Journal ID (nlm-ta): Stem Cells Transl Med
                Journal ID (iso-abbrev): Stem Cells Transl Med
                Journal ID (doi): 10.1002/(ISSN)2157-6580
                Journal ID (publisher-id): SCT3
                Title: Stem Cells Translational Medicine
                Publisher: John Wiley & Sons, Inc. (Hoboken, USA )
                ISSN (Print): 2157-6564
                ISSN (Electronic): 2157-6580
                Publication date (Electronic): 27 November 2019
                Publication date Collection: February 2020
                Volume: 9
                Issue: 2 ( doiID: 10.1002/sct3.v9.2 )
                Pages: 261-272
                Affiliations
                [ 1 ] Beijing Institute of Radiation Medicine Beijing People's Republic of China
                [ 2 ] Beijing Institute of Basic Medical Sciences Beijing People's Republic of China
                [ 3 ] Air Force Medical Center, PLA Beijing People's Republic of China
                [ 4 ] Jizhong Energy Xingtai MIG General Hospital Xingtai People's Republic of China
                [ 5 ] People's Liberation Army General Hospital Beijing People's Republic of China
                Author notes
                [*] [* ] Correspondence

                Heng Zhu, Beijing Institute of Radiation Medicine, Road Taiping 27, Beijing, 100850, People's Republic of China.

                Email: zhudingdingabc@ 123456163.com

                Ning Mao, Beijing Institute of Basic Medical Sciences, Road Taiping 27, Beijing, 100850, People's Republic of China.

                Email: maoning3suo@ 123456126.com

                Li Ding, Air Force Medical Center, PLA, Road Fucheng 30, Beijing, 100142, People's Republic of China.

                Email: dingli7578@ 123456163.com

                Author information
                https://orcid.org/0000-0002-8408-3821
                Article
                Publisher ID: SCT312627
                DOI: 10.1002/sctm.19-0300
                PMC ID: 6988769
                PubMed ID: 31774632
                SO-VID: 9cfa2a9e-83eb-42a9-bfb7-af4cc423fb8a
                Copyright © © 2019 The Authors. stem cells translational medicine published by Wiley Periodicals, Inc. on behalf of AlphaMed Press
                License:

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                Date received : 13 September 2019
                Date accepted : 04 October 2019
                Page count
                Figures: 6, Tables: 0, Pages: 12, Words: 8720
                Funding
                Funded by: Beijing Natural Sciences Grants
                Award ID: 7192203
                Award ID: 7182123
                Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;
                Award ID: 81101342
                Award ID: 81371945
                Award ID: 81500083
                Award ID: 81871771
                Award ID: 81572159
                Categories
                Subject: Tissue‐specific Progenitor and Stem Cells
                Subject: Tissue‐specific Progenitor and Stem Cells
                Custom metadata
                source-schema-version-number 2.0
                cover-date February 2020
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.5 mode:remove_FC converted:29.01.2020

                Keywords: cell adhesion molecules,inflammatory osteoclastogenesis,osteoprotegerin,skeletal stem cells
                Data availability:
                Keywords: cell adhesion molecules, inflammatory osteoclastogenesis, osteoprotegerin, skeletal stem cells

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