Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica

Rosanne D Reitsema; William F Jiemy; Lieske Wekema; Annemieke M H Boots; Peter Heeringa; Minke G Huitema; Wayel H Abdulahad; Yannick van Sleen; Maria Sandovici; Caroline Roozendaal; Arjan Diepstra; Thomas Kwee; Bhaskar Dasgupta; Elisabeth Brouwer; Kornelis S M van der Geest

doi:10.3389/fimmu.2022.943574

Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica

Rosanne D Reitsema, William F Jiemy, Lieske Wekema, Annemieke M H Boots, Peter Heeringa, Minke G Huitema, Wayel H Abdulahad, Yannick van Sleen, Maria Sandovici, Caroline Roozendaal, Arjan Diepstra, Thomas Kwee, Bhaskar Dasgupta, Elisabeth Brouwer, Kornelis S M van der Geest^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

Background: Although polymyalgia rheumatica (PMR) is a very common rheumatic inflammatory disease, current insight into the pathobiology of PMR is limited and largely based on studies in blood. We investigated T helper 1 (TH1) and T helper 17 (TH17) cell responses in blood, synovial fluid and bursa tissue of patients with PMR.

Materials and methods: Blood samples were collected from 18 patients with new-onset PMR and 32 healthy controls. Synovial fluid was aspirated from the inflamed shoulder bursae or biceps tendon sheath of 13 patients. Ultrasound-guided biopsies of the subacromial-subdeltoid (SASD) bursa were obtained from 11 patients. T cells were examined by flow cytometry, immunohistochemistry and immunofluorescence staining.

Results: Besides an increase of TH17 (CD4+IL-17+IFN-γ-) cells and T cytotoxic 17 (TC17; CD8+IL-17+IFN-γ-) cells, no other major changes were noted in the circulating T cell compartment of patients with PMR. Absolute numbers of CD4+ and CD8+ T cells were similar in blood and synovial fluid of patients with PMR. Synovial fluid T cells showed an effector-memory (CD45RO+CCR7-) phenotype. Percentages of TH1 (CD4+IFN-γ+IL-17-) cells and TH1/TH17 (CD4+IFN-γ+IL-17+) cells, but not TH17 or TC17 cells, were increased in the synovial fluid. Bursa tissue biopsies contained a small number of T cells, which were mostly CD8 negative. The majority of bursa tissue T cells produced IFN-γ but not IL-17. For comparison, B cells were scarcely detected in the bursa tissue.

Conclusion: Although the circulating TH17 cell pool is expanded in patients with PMR, our findings indicate that TH1 cells are involved in the inflammation of bursae and tendon sheaths in this condition. Our study points towards the TH1 cell pathway as a potential target for therapy in PMR.

Original language	English
Article number	943574
Number of pages	11
Journal	Frontiers in Immunology
Volume	13
DOIs	https://doi.org/10.3389/fimmu.2022.943574
Publication status	Published - 11-Aug-2022

Keywords

Bursitis
CD8-Positive T-Lymphocytes
Giant Cell Arteritis
Humans
Polymyalgia Rheumatica
Tenosynovitis

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Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumaticaFinal publisher's version, 9.95 MBLicence: CC BY

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Reitsema, R. D., Jiemy, W. F., Wekema, L., Boots, A. M. H., Heeringa, P., Huitema, M. G., Abdulahad, W. H., van Sleen, Y., Sandovici, M., Roozendaal, C., Diepstra, A., Kwee, T., Dasgupta, B., Brouwer, E., & van der Geest, K. S. M. (2022). Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica. Frontiers in Immunology, 13, Article 943574. https://doi.org/10.3389/fimmu.2022.943574

@article{d38c92ad9ab14f51bca00413277e3955,

title = "Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica",

abstract = "Background: Although polymyalgia rheumatica (PMR) is a very common rheumatic inflammatory disease, current insight into the pathobiology of PMR is limited and largely based on studies in blood. We investigated T helper 1 (TH1) and T helper 17 (TH17) cell responses in blood, synovial fluid and bursa tissue of patients with PMR.Materials and methods: Blood samples were collected from 18 patients with new-onset PMR and 32 healthy controls. Synovial fluid was aspirated from the inflamed shoulder bursae or biceps tendon sheath of 13 patients. Ultrasound-guided biopsies of the subacromial-subdeltoid (SASD) bursa were obtained from 11 patients. T cells were examined by flow cytometry, immunohistochemistry and immunofluorescence staining.Results: Besides an increase of TH17 (CD4+IL-17+IFN-γ-) cells and T cytotoxic 17 (TC17; CD8+IL-17+IFN-γ-) cells, no other major changes were noted in the circulating T cell compartment of patients with PMR. Absolute numbers of CD4+ and CD8+ T cells were similar in blood and synovial fluid of patients with PMR. Synovial fluid T cells showed an effector-memory (CD45RO+CCR7-) phenotype. Percentages of TH1 (CD4+IFN-γ+IL-17-) cells and TH1/TH17 (CD4+IFN-γ+IL-17+) cells, but not TH17 or TC17 cells, were increased in the synovial fluid. Bursa tissue biopsies contained a small number of T cells, which were mostly CD8 negative. The majority of bursa tissue T cells produced IFN-γ but not IL-17. For comparison, B cells were scarcely detected in the bursa tissue.Conclusion: Although the circulating TH17 cell pool is expanded in patients with PMR, our findings indicate that TH1 cells are involved in the inflammation of bursae and tendon sheaths in this condition. Our study points towards the TH1 cell pathway as a potential target for therapy in PMR.",

keywords = "Bursitis, CD8-Positive T-Lymphocytes, Giant Cell Arteritis, Humans, Polymyalgia Rheumatica, Tenosynovitis",

author = "Reitsema, {Rosanne D} and Jiemy, {William F} and Lieske Wekema and Boots, {Annemieke M H} and Peter Heeringa and Huitema, {Minke G} and Abdulahad, {Wayel H} and {van Sleen}, Yannick and Maria Sandovici and Caroline Roozendaal and Arjan Diepstra and Thomas Kwee and Bhaskar Dasgupta and Elisabeth Brouwer and {van der Geest}, {Kornelis S M}",

note = "Copyright {\textcopyright} 2022 Reitsema, Jiemy, Wekema, Boots, Heeringa, Huitema, Abdulahad, van Sleen, Sandovici, Roozendaal, Diepstra, Kwee, Dasgupta, Brouwer and van der Geest.",

year = "2022",

month = aug,

day = "11",

doi = "10.3389/fimmu.2022.943574",

language = "English",

volume = "13",

journal = "Frontiers in Immunology",

issn = "1664-3224",

publisher = "Frontiers Media SA",

}

Reitsema, RD , Jiemy, WF , Wekema, L , Boots, AMH , Heeringa, P, Huitema, MG, Abdulahad, WH , van Sleen, Y , Sandovici, M , Roozendaal, C , Diepstra, A , Kwee, T, Dasgupta, B, Brouwer, E & van der Geest, KSM 2022, 'Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica', Frontiers in Immunology, vol. 13, 943574. https://doi.org/10.3389/fimmu.2022.943574

TY - JOUR

T1 - Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica

AU - Reitsema, Rosanne D

AU - Jiemy, William F

AU - Wekema, Lieske

AU - Boots, Annemieke M H

AU - Heeringa, Peter

AU - Huitema, Minke G

AU - Abdulahad, Wayel H

AU - van Sleen, Yannick

AU - Sandovici, Maria

AU - Roozendaal, Caroline

AU - Diepstra, Arjan

AU - Kwee, Thomas

AU - Dasgupta, Bhaskar

AU - Brouwer, Elisabeth

AU - van der Geest, Kornelis S M

PY - 2022/8/11

Y1 - 2022/8/11

N2 - Background: Although polymyalgia rheumatica (PMR) is a very common rheumatic inflammatory disease, current insight into the pathobiology of PMR is limited and largely based on studies in blood. We investigated T helper 1 (TH1) and T helper 17 (TH17) cell responses in blood, synovial fluid and bursa tissue of patients with PMR.Materials and methods: Blood samples were collected from 18 patients with new-onset PMR and 32 healthy controls. Synovial fluid was aspirated from the inflamed shoulder bursae or biceps tendon sheath of 13 patients. Ultrasound-guided biopsies of the subacromial-subdeltoid (SASD) bursa were obtained from 11 patients. T cells were examined by flow cytometry, immunohistochemistry and immunofluorescence staining.Results: Besides an increase of TH17 (CD4+IL-17+IFN-γ-) cells and T cytotoxic 17 (TC17; CD8+IL-17+IFN-γ-) cells, no other major changes were noted in the circulating T cell compartment of patients with PMR. Absolute numbers of CD4+ and CD8+ T cells were similar in blood and synovial fluid of patients with PMR. Synovial fluid T cells showed an effector-memory (CD45RO+CCR7-) phenotype. Percentages of TH1 (CD4+IFN-γ+IL-17-) cells and TH1/TH17 (CD4+IFN-γ+IL-17+) cells, but not TH17 or TC17 cells, were increased in the synovial fluid. Bursa tissue biopsies contained a small number of T cells, which were mostly CD8 negative. The majority of bursa tissue T cells produced IFN-γ but not IL-17. For comparison, B cells were scarcely detected in the bursa tissue.Conclusion: Although the circulating TH17 cell pool is expanded in patients with PMR, our findings indicate that TH1 cells are involved in the inflammation of bursae and tendon sheaths in this condition. Our study points towards the TH1 cell pathway as a potential target for therapy in PMR.

AB - Background: Although polymyalgia rheumatica (PMR) is a very common rheumatic inflammatory disease, current insight into the pathobiology of PMR is limited and largely based on studies in blood. We investigated T helper 1 (TH1) and T helper 17 (TH17) cell responses in blood, synovial fluid and bursa tissue of patients with PMR.Materials and methods: Blood samples were collected from 18 patients with new-onset PMR and 32 healthy controls. Synovial fluid was aspirated from the inflamed shoulder bursae or biceps tendon sheath of 13 patients. Ultrasound-guided biopsies of the subacromial-subdeltoid (SASD) bursa were obtained from 11 patients. T cells were examined by flow cytometry, immunohistochemistry and immunofluorescence staining.Results: Besides an increase of TH17 (CD4+IL-17+IFN-γ-) cells and T cytotoxic 17 (TC17; CD8+IL-17+IFN-γ-) cells, no other major changes were noted in the circulating T cell compartment of patients with PMR. Absolute numbers of CD4+ and CD8+ T cells were similar in blood and synovial fluid of patients with PMR. Synovial fluid T cells showed an effector-memory (CD45RO+CCR7-) phenotype. Percentages of TH1 (CD4+IFN-γ+IL-17-) cells and TH1/TH17 (CD4+IFN-γ+IL-17+) cells, but not TH17 or TC17 cells, were increased in the synovial fluid. Bursa tissue biopsies contained a small number of T cells, which were mostly CD8 negative. The majority of bursa tissue T cells produced IFN-γ but not IL-17. For comparison, B cells were scarcely detected in the bursa tissue.Conclusion: Although the circulating TH17 cell pool is expanded in patients with PMR, our findings indicate that TH1 cells are involved in the inflammation of bursae and tendon sheaths in this condition. Our study points towards the TH1 cell pathway as a potential target for therapy in PMR.

KW - Bursitis

KW - CD8-Positive T-Lymphocytes

KW - Giant Cell Arteritis

KW - Humans

KW - Polymyalgia Rheumatica

KW - Tenosynovitis

U2 - 10.3389/fimmu.2022.943574

DO - 10.3389/fimmu.2022.943574

M3 - Article

C2 - 36032100

SN - 1664-3224

VL - 13

JO - Frontiers in Immunology

JF - Frontiers in Immunology

M1 - 943574

ER -

Contribution of pathogenic T helper 1 and 17 cells to bursitis and tenosynovitis in polymyalgia rheumatica

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