Regeneration of Jaw Joint Cartilage in Adult Zebrafish
The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate da...
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Published in | Frontiers in cell and developmental biology Vol. 9; p. 777787 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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20.01.2022
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Abstract | The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate damaged joints, we developed a surgical injury model in which the zebrafish jaw joint is destabilized
transection of the major jaw joint ligament, the interopercular-mandibular (IOM). Unilateral transection of the IOM ligament in 1-year-old fish resulted in an initial reduction of jaw joint cartilage by 14 days, with full regeneration of joint cartilage by 28 days. Joint cartilage regeneration involves the re-entry of articular chondrocytes into the cell cycle and the upregulated expression of
, a marker of developing chondrocytes in the embryo that becomes restricted to a subset of joint chondrocytes in adults. Genetic ablation of these
-expressing chondrocytes shows that they are essential for joint cartilage regeneration. To uncover the potential source of new chondrocytes during joint regeneration, we performed single-cell RNA sequencing of the uninjured adult jaw joint and identified multiple skeletal, connective tissue, and fibroblast subtypes. In particular, we uncovered a joint-specific periosteal population expressing
and
, with the jaw joint chondrocytes marked by
expression during regeneration. Our findings demonstrate the capacity of zebrafish to regenerate adult joint cartilage and identify candidate cell types that can be tested for their roles in regenerative response. |
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AbstractList | The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate damaged joints, we developed a surgical injury model in which the zebrafish jaw joint is destabilized
via
transection of the major jaw joint ligament, the interopercular–mandibular (IOM). Unilateral transection of the IOM ligament in 1-year-old fish resulted in an initial reduction of jaw joint cartilage by 14 days, with full regeneration of joint cartilage by 28 days. Joint cartilage regeneration involves the re-entry of articular chondrocytes into the cell cycle and the upregulated expression of
sox10
, a marker of developing chondrocytes in the embryo that becomes restricted to a subset of joint chondrocytes in adults. Genetic ablation of these
sox10
-expressing chondrocytes shows that they are essential for joint cartilage regeneration. To uncover the potential source of new chondrocytes during joint regeneration, we performed single-cell RNA sequencing of the uninjured adult jaw joint and identified multiple skeletal, connective tissue, and fibroblast subtypes. In particular, we uncovered a joint-specific periosteal population expressing
coch
and
grem1a
, with the jaw joint chondrocytes marked by
grem1a
expression during regeneration. Our findings demonstrate the capacity of zebrafish to regenerate adult joint cartilage and identify candidate cell types that can be tested for their roles in regenerative response. The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate damaged joints, we developed a surgical injury model in which the zebrafish jaw joint is destabilized transection of the major jaw joint ligament, the interopercular-mandibular (IOM). Unilateral transection of the IOM ligament in 1-year-old fish resulted in an initial reduction of jaw joint cartilage by 14 days, with full regeneration of joint cartilage by 28 days. Joint cartilage regeneration involves the re-entry of articular chondrocytes into the cell cycle and the upregulated expression of , a marker of developing chondrocytes in the embryo that becomes restricted to a subset of joint chondrocytes in adults. Genetic ablation of these -expressing chondrocytes shows that they are essential for joint cartilage regeneration. To uncover the potential source of new chondrocytes during joint regeneration, we performed single-cell RNA sequencing of the uninjured adult jaw joint and identified multiple skeletal, connective tissue, and fibroblast subtypes. In particular, we uncovered a joint-specific periosteal population expressing and , with the jaw joint chondrocytes marked by expression during regeneration. Our findings demonstrate the capacity of zebrafish to regenerate adult joint cartilage and identify candidate cell types that can be tested for their roles in regenerative response. The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate many structures that show limited or no healing capacity in mammals, including the jawbone. To test whether zebrafish can also regenerate damaged joints, we developed a surgical injury model in which the zebrafish jaw joint is destabilized via transection of the major jaw joint ligament, the interopercular–mandibular (IOM). Unilateral transection of the IOM ligament in 1-year-old fish resulted in an initial reduction of jaw joint cartilage by 14 days, with full regeneration of joint cartilage by 28 days. Joint cartilage regeneration involves the re-entry of articular chondrocytes into the cell cycle and the upregulated expression of sox10, a marker of developing chondrocytes in the embryo that becomes restricted to a subset of joint chondrocytes in adults. Genetic ablation of these sox10-expressing chondrocytes shows that they are essential for joint cartilage regeneration. To uncover the potential source of new chondrocytes during joint regeneration, we performed single-cell RNA sequencing of the uninjured adult jaw joint and identified multiple skeletal, connective tissue, and fibroblast subtypes. In particular, we uncovered a joint-specific periosteal population expressing coch and grem1a, with the jaw joint chondrocytes marked by grem1a expression during regeneration. Our findings demonstrate the capacity of zebrafish to regenerate adult joint cartilage and identify candidate cell types that can be tested for their roles in regenerative response. |
Author | Crump, J Gage Fabian, Peter Smeeton, Joanna Anderson, Troy Natarajan, Natasha Tseng, Kuo-Chang |
AuthorAffiliation | 2 Department of Genetics and Development , Columbia Stem Cell Initiative , Columbia University Irving Medical Center , Columbia University , New York , NY , United States 3 Department of Stem Cell Biology and Regenerative Medicine , Keck School of Medicine , University of Southern California , Los Angeles , CA , United States 1 Department of Rehabilitation and Regenerative Medicine , Columbia Stem Cell Initiative , Columbia University Irving Medical Center , Columbia University , New York , NY , United States |
AuthorAffiliation_xml | – name: 1 Department of Rehabilitation and Regenerative Medicine , Columbia Stem Cell Initiative , Columbia University Irving Medical Center , Columbia University , New York , NY , United States – name: 2 Department of Genetics and Development , Columbia Stem Cell Initiative , Columbia University Irving Medical Center , Columbia University , New York , NY , United States – name: 3 Department of Stem Cell Biology and Regenerative Medicine , Keck School of Medicine , University of Southern California , Los Angeles , CA , United States |
Author_xml | – sequence: 1 givenname: Joanna surname: Smeeton fullname: Smeeton, Joanna organization: Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States – sequence: 2 givenname: Natasha surname: Natarajan fullname: Natarajan, Natasha organization: Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States – sequence: 3 givenname: Troy surname: Anderson fullname: Anderson, Troy organization: Department of Genetics and Development, Columbia Stem Cell Initiative, Columbia University Irving Medical Center, Columbia University, New York, NY, United States – sequence: 4 givenname: Kuo-Chang surname: Tseng fullname: Tseng, Kuo-Chang organization: Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States – sequence: 5 givenname: Peter surname: Fabian fullname: Fabian, Peter organization: Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States – sequence: 6 givenname: J Gage surname: Crump fullname: Crump, J Gage organization: Department of Stem Cell Biology and Regenerative Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, United States |
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Copyright | Copyright © 2022 Smeeton, Natarajan, Anderson, Tseng, Fabian and Crump. Copyright © 2022 Smeeton, Natarajan, Anderson, Tseng, Fabian and Crump. 2022 Smeeton, Natarajan, Anderson, Tseng, Fabian and Crump |
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Keywords | joint zebrafish regeneration osteoarthritis cartilage |
Language | English |
License | Copyright © 2022 Smeeton, Natarajan, Anderson, Tseng, Fabian and Crump. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Chrissy L. Hammond, University of Bristol, United Kingdom Edited by: Brian Frank Eames, University of Saskatchewan, Canada This article was submitted to Molecular and Cellular Pathology, a section of the journal Frontiers in Cell and Developmental Biology Jianquan Chen, Soochow University, China |
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Snippet | The poor intrinsic repair capacity of mammalian joint cartilage likely contributes to the high incidence of arthritis worldwide. Adult zebrafish can regenerate... |
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SubjectTerms | cartilage Cell and Developmental Biology joint osteoarthritis regeneration zebrafish |
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Title | Regeneration of Jaw Joint Cartilage in Adult Zebrafish |
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