Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts

Aims: To evaluate the role of autophagy in primary knee fibroblasts undergoing myofibroblast differentiation as an in vitro model of arthrofibrosis, a complication after total knee arthroplasty characterized by aberrant intra-articular scar tissue formation and limited range of motion. Methods: We...

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Main Authors: Oliver B. Dilger, Mason F. Carstens, Cole E. Bothun, Ashley N. Payne, Daniel J. Berry, Joaquin Sanchez-Sotelo, Mark E. Morrey, Roman Thaler, Amel Dudakovic, Matthew P. Abdel
Format: Article
Language:English
Published: The British Editorial Society of Bone & Joint Surgery 2025-04-01
Series:Bone & Joint Research
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Online Access:https://online.boneandjoint.org.uk/doi/epdf/10.1302/2046-3758.144.BJR-2024-0312.R1
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author Oliver B. Dilger
Mason F. Carstens
Cole E. Bothun
Ashley N. Payne
Daniel J. Berry
Joaquin Sanchez-Sotelo
Mark E. Morrey
Roman Thaler
Amel Dudakovic
Matthew P. Abdel
author_facet Oliver B. Dilger
Mason F. Carstens
Cole E. Bothun
Ashley N. Payne
Daniel J. Berry
Joaquin Sanchez-Sotelo
Mark E. Morrey
Roman Thaler
Amel Dudakovic
Matthew P. Abdel
author_sort Oliver B. Dilger
collection DOAJ
description Aims: To evaluate the role of autophagy in primary knee fibroblasts undergoing myofibroblast differentiation as an in vitro model of arthrofibrosis, a complication after total knee arthroplasty characterized by aberrant intra-articular scar tissue formation and limited range of motion. Methods: We conducted a therapeutic screen of autophagic-modulating therapies in primary human knee fibroblasts undergoing transforming growth factor-beta 1 (TGF-β1)-mediated myofibroblast differentiation. Autophagy was induced pharmacologically with rapamycin or by amino acid deprivation. Picrosirius red staining was performed to quantify collagen deposition. Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) and western blotting were conducted to evaluate fibrotic gene expression levels. Results: Rapamycin, an mTOR complex 1 (mTORC1) inhibitor and autophagy inducer, reduced TGF-β1-mediated collagen deposition. Interestingly, we simultaneously report that myofibrogenic genes, including ACTA2, were highly upregulated following rapamycin-TGF-β1 treatment. When autophagy was induced through amino acid deprivation, we demonstrated suppressed extracellular matrix levels, fibrotic gene expression (e.g. ACTA2), and SMAD2 phosphorylation levels in TGF-β1-stimulated fibroblasts. Conclusion: Our findings demonstrate that the induction of cellular autophagy suppresses TGF-β1-induced collagen deposition in primary human knee fibroblasts. Taken together, these data suggest that cellular autophagy may be prophylactic against the pathogenesis of arthrofibrosis. Cite this article: Bone Joint Res 2025;14(4):328–337.
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spelling doaj-art-de4ae838e2ae410baed47785ee2ca84e2025-08-20T03:53:23ZengThe British Editorial Society of Bone & Joint SurgeryBone & Joint Research2046-37582025-04-0114433134010.1302/2046-3758.144.BJR-2024-0312.R1Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblastsOliver B. Dilger0Mason F. Carstens1Cole E. Bothun2Ashley N. Payne3Daniel J. Berry4Joaquin Sanchez-Sotelo5Mark E. Morrey6Roman Thaler7Amel Dudakovic8Matthew P. Abdel9Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USADepartment of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota, USAAims: To evaluate the role of autophagy in primary knee fibroblasts undergoing myofibroblast differentiation as an in vitro model of arthrofibrosis, a complication after total knee arthroplasty characterized by aberrant intra-articular scar tissue formation and limited range of motion. Methods: We conducted a therapeutic screen of autophagic-modulating therapies in primary human knee fibroblasts undergoing transforming growth factor-beta 1 (TGF-β1)-mediated myofibroblast differentiation. Autophagy was induced pharmacologically with rapamycin or by amino acid deprivation. Picrosirius red staining was performed to quantify collagen deposition. Reverse transcription-quantitative polymerase chain reaction (RT-qPCR) and western blotting were conducted to evaluate fibrotic gene expression levels. Results: Rapamycin, an mTOR complex 1 (mTORC1) inhibitor and autophagy inducer, reduced TGF-β1-mediated collagen deposition. Interestingly, we simultaneously report that myofibrogenic genes, including ACTA2, were highly upregulated following rapamycin-TGF-β1 treatment. When autophagy was induced through amino acid deprivation, we demonstrated suppressed extracellular matrix levels, fibrotic gene expression (e.g. ACTA2), and SMAD2 phosphorylation levels in TGF-β1-stimulated fibroblasts. Conclusion: Our findings demonstrate that the induction of cellular autophagy suppresses TGF-β1-induced collagen deposition in primary human knee fibroblasts. Taken together, these data suggest that cellular autophagy may be prophylactic against the pathogenesis of arthrofibrosis. Cite this article: Bone Joint Res 2025;14(4):328–337.https://online.boneandjoint.org.uk/doi/epdf/10.1302/2046-3758.144.BJR-2024-0312.R1arthrofibrosisautophagytotal knee arthroplasty (tka)myofibroblastextracellular matrixfibroblastsautophagytransforming growth factor-beta 1kneewestern blottingarthrofibrosisamino acidscollagensquantitative polymerase chain reaction
spellingShingle Oliver B. Dilger
Mason F. Carstens
Cole E. Bothun
Ashley N. Payne
Daniel J. Berry
Joaquin Sanchez-Sotelo
Mark E. Morrey
Roman Thaler
Amel Dudakovic
Matthew P. Abdel
Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
Bone & Joint Research
arthrofibrosis
autophagy
total knee arthroplasty (tka)
myofibroblast
extracellular matrix
fibroblasts
autophagy
transforming growth factor-beta 1
knee
western blotting
arthrofibrosis
amino acids
collagens
quantitative polymerase chain reaction
title Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
title_full Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
title_fullStr Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
title_full_unstemmed Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
title_short Induction of cellular autophagy impairs TGF-β1-mediated extracellular matrix deposition in primary human knee fibroblasts
title_sort induction of cellular autophagy impairs tgf β1 mediated extracellular matrix deposition in primary human knee fibroblasts
topic arthrofibrosis
autophagy
total knee arthroplasty (tka)
myofibroblast
extracellular matrix
fibroblasts
autophagy
transforming growth factor-beta 1
knee
western blotting
arthrofibrosis
amino acids
collagens
quantitative polymerase chain reaction
url https://online.boneandjoint.org.uk/doi/epdf/10.1302/2046-3758.144.BJR-2024-0312.R1
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