Allergy-induced systemic inflammation impairs tendon quality

Summary: Background: Treatment of degenerating tendons still presents a major challenge, since the aetiology of tendinopathies remains poorly understood. Besides mechanical overuse, further known predisposing factors include rheumatoid arthritis, diabetes, obesity or smoking all of which combine wi...

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Main Authors: Christine Lehner, Gabriel Spitzer, Patrick Langthaler, Dominika Jakubecova, Barbara Klein, Nadja Weissenbacher, Andrea Wagner, Renate Gehwolf, Eugen Trinka, Bernhard Iglseder, Bernhard Paulweber, Ludwig Aigner, Sebastien Couillard-Després, Richard Weiss, Herbert Tempfer, Andreas Traweger
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:EBioMedicine
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352396421005727
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author Christine Lehner
Gabriel Spitzer
Patrick Langthaler
Dominika Jakubecova
Barbara Klein
Nadja Weissenbacher
Andrea Wagner
Renate Gehwolf
Eugen Trinka
Bernhard Iglseder
Bernhard Paulweber
Ludwig Aigner
Sebastien Couillard-Després
Richard Weiss
Herbert Tempfer
Andreas Traweger
author_facet Christine Lehner
Gabriel Spitzer
Patrick Langthaler
Dominika Jakubecova
Barbara Klein
Nadja Weissenbacher
Andrea Wagner
Renate Gehwolf
Eugen Trinka
Bernhard Iglseder
Bernhard Paulweber
Ludwig Aigner
Sebastien Couillard-Després
Richard Weiss
Herbert Tempfer
Andreas Traweger
author_sort Christine Lehner
collection DOAJ
description Summary: Background: Treatment of degenerating tendons still presents a major challenge, since the aetiology of tendinopathies remains poorly understood. Besides mechanical overuse, further known predisposing factors include rheumatoid arthritis, diabetes, obesity or smoking all of which combine with a systemic inflammation. Methods: To determine whether the systemic inflammation accompanying these conditions contributes to the onset of tendinopathy, we studied the effect of a systemic inflammation induced by an allergic episode on tendon properties. To this end, we induced an allergic response in mice by exposing them to a timothy grass pollen allergen and subsequently analysed both their flexor and Achilles tendons. Additionally, we analysed data from a health survey comprising data from more than 10.000 persons for an association between the occurrence of an allergy and tendinopathy. Findings: Biomechanical testing and histological analysis revealed that tendons from allergic mice not only showed a significant reduction of both elastic modulus and tensile stress, but also alterations of the tendon matrix. Moreover, treatment of 3D tendon-like constructs with sera from allergic mice resulted in a matrix-remodelling expression profile and the expression of macrophage-associated markers and matrix metalloproteinase 2 (MMP2) was increased in allergic Achilles tendons. Data from the human health study revealed that persons suffering from an allergy have an increased propensity to develop a tendinopathy. Interpretation: Our study demonstrates that the presence of a systemic inflammation accompanying an allergic condition negatively impacts on tendon structure and function. Funding: This study was financially supported by the Fund for the Advancement of Scientific Research at Paracelsus Medical University (PMU-FFF E-15/22/115-LEK), by the Land Salzburg, the Salzburger Landeskliniken (SALK, the Health Care Provider of the University Hospitals Landeskrankenhaus and Christian Doppler Klinik), the Paracelsus Medical University, Salzburg and by unrestricted grants from Bayer, AstraZeneca, Sanofi-Aventis, Boehringer-Ingelheim.
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spelling doaj.art-a9a60de349324be0abf71be6980c04b12022-12-22T04:04:06ZengElsevierEBioMedicine2352-39642022-01-0175103778Allergy-induced systemic inflammation impairs tendon qualityChristine Lehner0Gabriel Spitzer1Patrick Langthaler2Dominika Jakubecova3Barbara Klein4Nadja Weissenbacher5Andrea Wagner6Renate Gehwolf7Eugen Trinka8Bernhard Iglseder9Bernhard Paulweber10Ludwig Aigner11Sebastien Couillard-Després12Richard Weiss13Herbert Tempfer14Andreas Traweger15Institute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, Austria; Corresponding author at: Institute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria.Institute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaDepartment of Neurology, Christian Doppler University Hospital, Paracelsus Medical University and Centre for Cognitive Neuroscience, Affiliated member of the European Reference Network EpiCARE, Austria; Department of Mathematics, Paris Lodron University of Salzburg, Salzburg, Austria; Team Biostatistics and Big Medical Data, IDA Lab Salzburg, Paracelsus Medical University, Salzburg, AustriaInstitute of Experimental Neuroregeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Salzburg, AustriaInstitute of Molecular Regenerative Medicine, Spinal Cord Injury and Tissue Regeneration Center Salzburg, Paracelsus Medical University, Salzburg, AustriaInstitute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaInstitute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaInstitute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaDepartment of Neurology, Christian Doppler University Hospital, Paracelsus Medical University and Centre for Cognitive Neuroscience, Affiliated member of the European Reference Network EpiCARE, Austria; Department of Public Health, Health Services Research and Health Technology Assessment, UMIT–University for Health Sciences, Medical Informatics and Technology, Hall in Tirol, Austria; Neuroscience Institute, Christian Doppler University Hospital, Paracelsus Medical University and Centre for Cognitive Neuroscience Salzburg, AustriaDepartment of Geriatric Medicine, Christian Doppler University Hospital, Paracelsus Medical University, Salzburg, AustriaDepartment of Internal Medicine, St. Johanns University Hospital, Paracelsus Medical University, Salzburg, AustriaAustrian Cluster for Tissue Regeneration, Vienna, Austria; Institute of Molecular Regenerative Medicine, Spinal Cord Injury and Tissue Regeneration Center Salzburg, Paracelsus Medical University, Salzburg, AustriaAustrian Cluster for Tissue Regeneration, Vienna, Austria; Institute of Experimental Neuroregeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Salzburg, AustriaDepartment of Biosciences, Paris Lodron University of Salzburg, Salzburg, AustriaInstitute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaInstitute of Tendon and Bone Regeneration, Spinal Cord Injury & Tissue Regeneration Center Salzburg, Paracelsus Medical University, Strubergasse 22, Salzburg 5020, Austria; Austrian Cluster for Tissue Regeneration, Vienna, AustriaSummary: Background: Treatment of degenerating tendons still presents a major challenge, since the aetiology of tendinopathies remains poorly understood. Besides mechanical overuse, further known predisposing factors include rheumatoid arthritis, diabetes, obesity or smoking all of which combine with a systemic inflammation. Methods: To determine whether the systemic inflammation accompanying these conditions contributes to the onset of tendinopathy, we studied the effect of a systemic inflammation induced by an allergic episode on tendon properties. To this end, we induced an allergic response in mice by exposing them to a timothy grass pollen allergen and subsequently analysed both their flexor and Achilles tendons. Additionally, we analysed data from a health survey comprising data from more than 10.000 persons for an association between the occurrence of an allergy and tendinopathy. Findings: Biomechanical testing and histological analysis revealed that tendons from allergic mice not only showed a significant reduction of both elastic modulus and tensile stress, but also alterations of the tendon matrix. Moreover, treatment of 3D tendon-like constructs with sera from allergic mice resulted in a matrix-remodelling expression profile and the expression of macrophage-associated markers and matrix metalloproteinase 2 (MMP2) was increased in allergic Achilles tendons. Data from the human health study revealed that persons suffering from an allergy have an increased propensity to develop a tendinopathy. Interpretation: Our study demonstrates that the presence of a systemic inflammation accompanying an allergic condition negatively impacts on tendon structure and function. Funding: This study was financially supported by the Fund for the Advancement of Scientific Research at Paracelsus Medical University (PMU-FFF E-15/22/115-LEK), by the Land Salzburg, the Salzburger Landeskliniken (SALK, the Health Care Provider of the University Hospitals Landeskrankenhaus and Christian Doppler Klinik), the Paracelsus Medical University, Salzburg and by unrestricted grants from Bayer, AstraZeneca, Sanofi-Aventis, Boehringer-Ingelheim.http://www.sciencedirect.com/science/article/pii/S2352396421005727AllergyTendinopathySystemic inflammationTendon
spellingShingle Christine Lehner
Gabriel Spitzer
Patrick Langthaler
Dominika Jakubecova
Barbara Klein
Nadja Weissenbacher
Andrea Wagner
Renate Gehwolf
Eugen Trinka
Bernhard Iglseder
Bernhard Paulweber
Ludwig Aigner
Sebastien Couillard-Després
Richard Weiss
Herbert Tempfer
Andreas Traweger
Allergy-induced systemic inflammation impairs tendon quality
EBioMedicine
Allergy
Tendinopathy
Systemic inflammation
Tendon
title Allergy-induced systemic inflammation impairs tendon quality
title_full Allergy-induced systemic inflammation impairs tendon quality
title_fullStr Allergy-induced systemic inflammation impairs tendon quality
title_full_unstemmed Allergy-induced systemic inflammation impairs tendon quality
title_short Allergy-induced systemic inflammation impairs tendon quality
title_sort allergy induced systemic inflammation impairs tendon quality
topic Allergy
Tendinopathy
Systemic inflammation
Tendon
url http://www.sciencedirect.com/science/article/pii/S2352396421005727
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