Corneal Antifibrotic Switch Identified in Genetic and Pharmacological Deficiency of Vimentin
The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice genetically deficient for the IF protein vimentin (Vim−/−) have impaired wound healing from deficits in myofibroblast development. We report a s...
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Published in | The Journal of biological chemistry Vol. 287; no. 2; pp. 989 - 1006 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
06.01.2012
American Society for Biochemistry and Molecular Biology |
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Abstract | The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice genetically deficient for the IF protein vimentin (Vim−/−) have impaired wound healing from deficits in myofibroblast development. We report a surprising finding made in Vim−/− mice that corneas are protected from fibrosis and instead promote regenerative healing after traumatic alkali injury. This reparative phenotype in Vim−/− corneas is strikingly recapitulated by the pharmacological agent withaferin A (WFA), a small molecule that binds to vimentin and down-regulates its injury-induced expression. Attenuation of corneal fibrosis by WFA is mediated by down-regulation of ubiquitin-conjugating E3 ligase Skp2 and up-regulation of cyclin-dependent kinase inhibitors p27Kip1 and p21Cip1. In cell culture models, WFA exerts G2/M cell cycle arrest in a p27Kip1- and Skp2-dependent manner. Finally, by developing a highly sensitive imaging method to measure corneal opacity, we identify a novel role for desmin overexpression in corneal haze. We demonstrate that desmin down-regulation by WFA via targeting the conserved WFA-ligand binding site shared among type III IFs promotes further improvement of corneal transparency without affecting cyclin-dependent kinase inhibitor levels in Vim−/− mice. This dissociates a direct role for desmin in corneal cell proliferation. Taken together, our findings illuminate a previously unappreciated pathogenic role for type III IF overexpression in corneal fibrotic conditions and also validate WFA as a powerful drug lead toward anti-fibrosis therapeutic development.
Background: Withaferin A (WFA) is a vimentin-targeting inhibitor that has potent anti-proliferative activity.
Results: WFA protects against corneal fibrosis by down-regulating injury-induced vimentin to exert epithelial cell cycle arrest and inhibit myofibroblast expression, which is a mechanism closely mimicked in vimentin-deficient mice during injury healing.
Conclusion: Vimentin is a novel fibrosis target.
Significance: Ocular fibrotic conditions that overexpress vimentin could be treatable with WFA. |
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AbstractList | The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice genetically deficient for the IF protein vimentin (Vim−/−) have impaired wound healing from deficits in myofibroblast development. We report a surprising finding made in Vim−/− mice that corneas are protected from fibrosis and instead promote regenerative healing after traumatic alkali injury. This reparative phenotype in Vim−/− corneas is strikingly recapitulated by the pharmacological agent withaferin A (WFA), a small molecule that binds to vimentin and down-regulates its injury-induced expression. Attenuation of corneal fibrosis by WFA is mediated by down-regulation of ubiquitin-conjugating E3 ligase Skp2 and up-regulation of cyclin-dependent kinase inhibitors p27Kip1 and p21Cip1. In cell culture models, WFA exerts G2/M cell cycle arrest in a p27Kip1- and Skp2-dependent manner. Finally, by developing a highly sensitive imaging method to measure corneal opacity, we identify a novel role for desmin overexpression in corneal haze. We demonstrate that desmin down-regulation by WFA via targeting the conserved WFA-ligand binding site shared among type III IFs promotes further improvement of corneal transparency without affecting cyclin-dependent kinase inhibitor levels in Vim−/− mice. This dissociates a direct role for desmin in corneal cell proliferation. Taken together, our findings illuminate a previously unappreciated pathogenic role for type III IF overexpression in corneal fibrotic conditions and also validate WFA as a powerful drug lead toward anti-fibrosis therapeutic development.
Background: Withaferin A (WFA) is a vimentin-targeting inhibitor that has potent anti-proliferative activity.
Results: WFA protects against corneal fibrosis by down-regulating injury-induced vimentin to exert epithelial cell cycle arrest and inhibit myofibroblast expression, which is a mechanism closely mimicked in vimentin-deficient mice during injury healing.
Conclusion: Vimentin is a novel fibrosis target.
Significance: Ocular fibrotic conditions that overexpress vimentin could be treatable with WFA. Background: Withaferin A (WFA) is a vimentin-targeting inhibitor that has potent anti-proliferative activity. Results: WFA protects against corneal fibrosis by down-regulating injury-induced vimentin to exert epithelial cell cycle arrest and inhibit myofibroblast expression, which is a mechanism closely mimicked in vimentin-deficient mice during injury healing. Conclusion: Vimentin is a novel fibrosis target. Significance: Ocular fibrotic conditions that overexpress vimentin could be treatable with WFA. The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice genetically deficient for the IF protein vimentin ( Vim −/− ) have impaired wound healing from deficits in myofibroblast development. We report a surprising finding made in Vim −/− mice that corneas are protected from fibrosis and instead promote regenerative healing after traumatic alkali injury. This reparative phenotype in Vim −/− corneas is strikingly recapitulated by the pharmacological agent withaferin A (WFA), a small molecule that binds to vimentin and down-regulates its injury-induced expression. Attenuation of corneal fibrosis by WFA is mediated by down-regulation of ubiquitin-conjugating E3 ligase Skp2 and up-regulation of cyclin-dependent kinase inhibitors p27 Kip1 and p21 Cip1 . In cell culture models, WFA exerts G 2 /M cell cycle arrest in a p27 Kip1 - and Skp2-dependent manner. Finally, by developing a highly sensitive imaging method to measure corneal opacity, we identify a novel role for desmin overexpression in corneal haze. We demonstrate that desmin down-regulation by WFA via targeting the conserved WFA-ligand binding site shared among type III IFs promotes further improvement of corneal transparency without affecting cyclin-dependent kinase inhibitor levels in Vim −/− mice. This dissociates a direct role for desmin in corneal cell proliferation. Taken together, our findings illuminate a previously unappreciated pathogenic role for type III IF overexpression in corneal fibrotic conditions and also validate WFA as a powerful drug lead toward anti-fibrosis therapeutic development. The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice genetically deficient for the IF protein vimentin (Vim(-/-)) have impaired wound healing from deficits in myofibroblast development. We report a surprising finding made in Vim(-/-) mice that corneas are protected from fibrosis and instead promote regenerative healing after traumatic alkali injury. This reparative phenotype in Vim(-/-) corneas is strikingly recapitulated by the pharmacological agent withaferin A (WFA), a small molecule that binds to vimentin and down-regulates its injury-induced expression. Attenuation of corneal fibrosis by WFA is mediated by down-regulation of ubiquitin-conjugating E3 ligase Skp2 and up-regulation of cyclin-dependent kinase inhibitors p27(Kip1) and p21(Cip1). In cell culture models, WFA exerts G(2)/M cell cycle arrest in a p27(Kip1)- and Skp2-dependent manner. Finally, by developing a highly sensitive imaging method to measure corneal opacity, we identify a novel role for desmin overexpression in corneal haze. We demonstrate that desmin down-regulation by WFA via targeting the conserved WFA-ligand binding site shared among type III IFs promotes further improvement of corneal transparency without affecting cyclin-dependent kinase inhibitor levels in Vim(-/-) mice. This dissociates a direct role for desmin in corneal cell proliferation. Taken together, our findings illuminate a previously unappreciated pathogenic role for type III IF overexpression in corneal fibrotic conditions and also validate WFA as a powerful drug lead toward anti-fibrosis therapeutic development. |
Author | Zhan, Chang-Guo Nakayama, Keiichi I. Lee, Do-Min Bargagna-Mohan, Paola Hamza, Adel Mohan, Royce Paranthan, Riya R. Lau, Daniel L. Kim, Kyung Bo Srinivasan, Cidambi Nakayama, Keiko Herrmann, Harald |
Author_xml | – sequence: 1 givenname: Paola surname: Bargagna-Mohan fullname: Bargagna-Mohan, Paola organization: Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030 – sequence: 2 givenname: Riya R. surname: Paranthan fullname: Paranthan, Riya R. organization: Department of Ophthalmology and Visual Sciences, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 3 givenname: Adel surname: Hamza fullname: Hamza, Adel organization: Department of Pharmaceutical Sciences, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 4 givenname: Chang-Guo surname: Zhan fullname: Zhan, Chang-Guo organization: Department of Pharmaceutical Sciences, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 5 givenname: Do-Min surname: Lee fullname: Lee, Do-Min organization: Department of Pharmaceutical Sciences, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 6 givenname: Kyung Bo surname: Kim fullname: Kim, Kyung Bo organization: Department of Pharmaceutical Sciences, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 7 givenname: Daniel L. surname: Lau fullname: Lau, Daniel L. organization: Department of Computer and Electrical Engineering, University of Kentucky, Lexington, Kentucky, 40503 – sequence: 8 givenname: Cidambi surname: Srinivasan fullname: Srinivasan, Cidambi organization: Department of Statistics, University of Kentucky, Lexington, Kentucky 40503 – sequence: 9 givenname: Keiko surname: Nakayama fullname: Nakayama, Keiko organization: Division of Developmental Genetics, Tohoku University Graduate School of Medicine, Sendai, Miyagi 980-8575, Japan – sequence: 10 givenname: Keiichi I. surname: Nakayama fullname: Nakayama, Keiichi I. organization: Department of Molecular and Cellular Biology, Medical Institute of Bioregulation, Kyushu University, Fukuoka 812-8582, Japan – sequence: 11 givenname: Harald surname: Herrmann fullname: Herrmann, Harald organization: Functional Architecture of the Cell Group, German Cancer Research Center (DKFZ), D-69120 Heidelberg, Germany – sequence: 12 givenname: Royce surname: Mohan fullname: Mohan, Royce email: Mohan@UCHC.edu organization: Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030 |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22117063$$D View this record in MEDLINE/PubMed |
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Keywords | Vimentin Withaferin A Pharmacogenetics Tissue Repair Cell Cycle Fibrosis Cytoskeleton Drug Discovery Skp2 Desmin |
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Snippet | The type III intermediate filaments (IFs) are essential cytoskeletal elements of mechanosignal transduction and serve critical roles in tissue repair. Mice... Background: Withaferin A (WFA) is a vimentin-targeting inhibitor that has potent anti-proliferative activity. Results: WFA protects against corneal fibrosis by... |
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SubjectTerms | Animals Cell Cycle Cell Differentiation - drug effects Cell Differentiation - genetics Cell Proliferation - drug effects Cornea - metabolism Cornea - pathology Corneal Diseases - drug therapy Corneal Diseases - genetics Corneal Diseases - metabolism Corneal Diseases - pathology Cytoskeleton Desmin Desmin - genetics Desmin - metabolism Drug Discovery Fibrosis Gene Expression Regulation - drug effects Gene Expression Regulation - genetics Humans Mice Mice, Knockout Molecular Bases of Disease Pharmacogenetics S-Phase Kinase-Associated Proteins - genetics S-Phase Kinase-Associated Proteins - metabolism Skp2 Tissue Repair Vimentin Vimentin - antagonists & inhibitors Vimentin - genetics Vimentin - metabolism Withaferin A Withanolides - pharmacology Wound Healing - drug effects Wound Healing - genetics |
Title | Corneal Antifibrotic Switch Identified in Genetic and Pharmacological Deficiency of Vimentin |
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