Strain-dependent oxidant release in articular cartilage originates from mitochondria
Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from th...
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Published in | Biomechanics and modeling in mechanobiology Vol. 13; no. 3; pp. 565 - 572 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
Berlin/Heidelberg
Springer Berlin Heidelberg
01.06.2014
Springer Nature B.V |
Subjects | |
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Abstract | Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium, an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains (
r
2
=
0.87
,
p
<
0.05
), and significant cell death was observed at strains
>
40 %. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell-permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology. |
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AbstractList | (ProQuest: ... denotes formulae and/or non-USASCII text omitted; see image).Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium, an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains (...), and significant cell death was observed at strains ...40 %. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell-permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology. Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult, and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically-induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium (DHE), an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains (r 2 = 0.83, p < 0.05), and significant cell death was observed at strains > 40%. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride (MnTMPyP) significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology. Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium, an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains ( r 2 = 0.87 , p < 0.05 ), and significant cell death was observed at strains > 40 %. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell-permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology. (ProQuest: ... denotes formulae and/or non-USASCII text omitted; see image) Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium, an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains (...), and significant cell death was observed at strains ...40 %. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell-permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology.[PUBLICATION ABSTRACT] Mechanical loading is essential for articular cartilage homeostasis and plays a central role in the cartilage pathology, yet the mechanotransduction processes that underlie these effects remain unclear. Previously, we showed that lethal amounts of reactive oxygen species (ROS) were liberated from the mitochondria in response to mechanical insult and that chondrocyte deformation may be a source of ROS. To this end, we hypothesized that mechanically induced mitochondrial ROS is related to the magnitude of cartilage deformation. To test this, we measured axial tissue strains in cartilage explants subjected to semi-confined compressive stresses of 0, 0.05, 0.1, 0.25, 0.5, or 1.0 MPa. The presence of ROS was then determined by confocal imaging with dihydroethidium, an oxidant sensitive fluorescent probe. Our results indicated that ROS levels increased linearly relative to the magnitude of axial strains (r(2) = 0.87, p < 0.05), and significant cell death was observed at strains >40%. By contrast, hydrostatic stress, which causes minimal tissue strain, had no significant effect. Cell-permeable superoxide dismutase mimetic Mn(III)tetrakis (1-methyl-4-pyridyl) porphyrin pentachloride significantly decreased ROS levels at 0.5 and 0.25 MPa. Electron transport chain inhibitor, rotenone, and cytoskeletal inhibitor, cytochalasin B, significantly decreased ROS levels at 0.25 MPa. Our findings strongly suggest that ROS and mitochondrial oxidants contribute to cartilage mechanobiology. |
Author | Ramakrishnan, P. S. Martin, J. A. Wagner, V. M. Brouillette, M. J. Sauter, E. E. Journot, B. J. McKinley, T. O. |
AuthorAffiliation | 2 Department of Biomedical Engineering, University of Iowa, Iowa City 1 Department of Orthopaedics and Rehabilitation, University of Iowa, Iowa City |
AuthorAffiliation_xml | – name: 1 Department of Orthopaedics and Rehabilitation, University of Iowa, Iowa City – name: 2 Department of Biomedical Engineering, University of Iowa, Iowa City |
Author_xml | – sequence: 1 givenname: M. J. surname: Brouillette fullname: Brouillette, M. J. email: marc-brouillette@uiowa.edu organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa – sequence: 2 givenname: P. S. surname: Ramakrishnan fullname: Ramakrishnan, P. S. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa – sequence: 3 givenname: V. M. surname: Wagner fullname: Wagner, V. M. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa – sequence: 4 givenname: E. E. surname: Sauter fullname: Sauter, E. E. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa – sequence: 5 givenname: B. J. surname: Journot fullname: Journot, B. J. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa – sequence: 6 givenname: T. O. surname: McKinley fullname: McKinley, T. O. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa – sequence: 7 givenname: J. A. surname: Martin fullname: Martin, J. A. organization: Ignacio Ponseti Orthopaedic Cell Biology Lab, Department of Orthopaedics and Rehabilitation, University of Iowa, Department of Biomedical Engineering, University of Iowa |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23896937$$D View this record in MEDLINE/PubMed |
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Keywords | Cartilage Chondrocyte Mechanical loading Reactive oxygen species (ROS) Cytoskeleton Superoxide Static stress Hydrostatic stress |
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SubjectTerms | Animals Biological and Medical Physics Biomedical Engineering and Bioengineering Biophysics Cartilage Cartilage, Articular - drug effects Cartilage, Articular - metabolism Cartilage, Articular - physiopathology Cattle Cytochalasin B - pharmacology Engineering Fluorescent Dyes Homeostasis In Vitro Techniques Microscopy, Confocal Mitochondria Mitochondria - metabolism Original Paper Oxidants - metabolism Oxidizing agents Reactive Oxygen Species - metabolism Rotenone Rotenone - pharmacology Strain Strain rate Stress, Mechanical Theoretical and Applied Mechanics |
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Title | Strain-dependent oxidant release in articular cartilage originates from mitochondria |
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