Altered versican cleavage in ADAMTS5 deficient mice; A novel etiology of myxomatous valve disease
In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for ‘...
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| Published in | Developmental biology Vol. 357; no. 1; pp. 152 - 164 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.09.2011
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| Subjects | |
| Online Access | Get full text |
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| Abstract | In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for ‘remodeling’ the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5−/− mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5−/− valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5−/− valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5−/− mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease.
► ADAMTS5 deficient mice develop enlarged cardiac valves by late fetal stages. ► Valve mesenchyme in Adamts5-/- mice display increased proliferation and intercellular space. ► In vivo reduction of the ADAMTS5 substrate versican rescues the valve phenotype in Adamts5-/- mice. ► Endothelial expression of ADAMTS5 is required for differentiation of cardiac valve mesenchyme. ► BMP2 and Sox9 expression is not down-regulated in Adamts5-/- cardiac valve cusps. |
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| AbstractList | In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for ‘remodeling’ the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5−/− mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5−/− valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5−/− valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5−/− mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease.
► ADAMTS5 deficient mice develop enlarged cardiac valves by late fetal stages. ► Valve mesenchyme in Adamts5-/- mice display increased proliferation and intercellular space. ► In vivo reduction of the ADAMTS5 substrate versican rescues the valve phenotype in Adamts5-/- mice. ► Endothelial expression of ADAMTS5 is required for differentiation of cardiac valve mesenchyme. ► BMP2 and Sox9 expression is not down-regulated in Adamts5-/- cardiac valve cusps. In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for ‘remodeling’ the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5⁻/⁻ mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5⁻/⁻ valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5⁻/⁻ valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5⁻/⁻ mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease. In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for ‘remodeling’ the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, ( A D isintegrin-like A nd M etalloprotease domain with T hrombo S pondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves contained a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5 −/− mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5 −/− valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5 −/− valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardium to mesenchymal signaling in late fetal valve development. Although adult Adamts5 −/− mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease. In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for 'remodeling' the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5(-/-) mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5(-/-) valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5(-/-) valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5(-/-) mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease. In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for 'remodeling' the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5(-/-) mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5(-/-) valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5(-/-) valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5(-/-) mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease.In fetal valve maturation the mechanisms by which the relatively homogeneous proteoglycan-rich extracellular matrix (ECM) of endocardial cushions is replaced by a specialized and stratified ECM found in mature valves are not understood. Therefore, we reasoned that uncovering proteases critical for 'remodeling' the proteoglycan rich (extracellular matrix) ECM may elucidate novel mechanisms of valve development. We have determined that mice deficient in ADAMTS5, (A Disintegrin-like And Metalloprotease domain with ThromboSpondin-type 1 motifs) which we demonstrated is expressed predominantly by valvular endocardium during cardiac valve maturation, exhibited enlarged valves. ADAMTS5 deficient valves displayed a reduction in cleavage of its substrate versican, a critical cardiac proteoglycan. In vivo reduction of versican, in Adamts5(-/-) mice, achieved through Vcan heterozygosity, substantially rescued the valve anomalies. An increase in BMP2 immunolocalization, Sox9 expression and mesenchymal cell proliferation were observed in Adamts5(-/-) valve mesenchyme and correlated with expansion of the spongiosa (proteoglycan-rich) region in Adamts5(-/-) valve cusps. Furthermore, these data suggest that ECM remodeling via ADAMTS5 is required for endocardial to mesenchymal signaling in late fetal valve development. Although adult Adamts5(-/-) mice are viable they do not recover from developmental valve anomalies and have myxomatous cardiac valves with 100% penetrance. Since the accumulation of proteoglycans is a hallmark of myxomatous valve disease, based on these data we hypothesize that a lack of versican cleavage during fetal valve development may be a potential etiology of adult myxomatous valve disease. |
| Author | McGarity, Jessica D. Weber, Deidra Diminich, A. Megan Apte, Suneel S. McCulloch, Daniel R. Bahan, Alexandria Nelson, Courtney M. Dupuis, Loren E. Wessels, Andy Kern, Christine B. |
| AuthorAffiliation | Department of Regenerative Medicine and Cell Biology, 171 Ashley Avenue, Medical University of South Carolina, Charleston, SC 29425, USA |
| AuthorAffiliation_xml | – name: Department of Regenerative Medicine and Cell Biology, 171 Ashley Avenue, Medical University of South Carolina, Charleston, SC 29425, USA |
| Author_xml | – sequence: 1 givenname: Loren E. surname: Dupuis fullname: Dupuis, Loren E. – sequence: 2 givenname: Daniel R. surname: McCulloch fullname: McCulloch, Daniel R. – sequence: 3 givenname: Jessica D. surname: McGarity fullname: McGarity, Jessica D. – sequence: 4 givenname: Alexandria surname: Bahan fullname: Bahan, Alexandria – sequence: 5 givenname: Andy surname: Wessels fullname: Wessels, Andy – sequence: 6 givenname: Deidra surname: Weber fullname: Weber, Deidra – sequence: 7 givenname: A. Megan surname: Diminich fullname: Diminich, A. Megan – sequence: 8 givenname: Courtney M. surname: Nelson fullname: Nelson, Courtney M. – sequence: 9 givenname: Suneel S. surname: Apte fullname: Apte, Suneel S. – sequence: 10 givenname: Christine B. surname: Kern fullname: Kern, Christine B. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21749862$$D View this record in MEDLINE/PubMed |
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| Issue | 1 |
| Keywords | PV Myxomatous valves ADAMTS MV EMT ECM AVC VIC PA ADAMTS5 AV αSMA Endocardial cushions Extracellular matrix OFT SLV WT Versican |
| Language | English |
| License | http://www.elsevier.com/open-access/userlicense/1.0 https://www.elsevier.com/tdm/userlicense/1.0 https://www.elsevier.com/open-access/userlicense/1.0 Copyright © 2011 Elsevier Inc. All rights reserved. |
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| SubjectTerms | ADAM Proteins - genetics ADAM Proteins - metabolism ADAMTS5 ADAMTS5 Protein adults Animals Bone Morphogenetic Protein 2 - genetics Bone Morphogenetic Protein 2 - metabolism Cell Proliferation Endocardial cushions Endocardium - metabolism etiology Extracellular matrix Gene Expression Regulation, Developmental heart Heart - embryology Heart Valve Diseases - etiology Heart Valve Diseases - genetics Heart Valves - embryology Heart Valves - metabolism heterozygosity Mesoderm - metabolism metalloproteinases Mice Mice, Transgenic Myxomatous valves penetrance proteoglycans Versican Versicans - metabolism |
| Title | Altered versican cleavage in ADAMTS5 deficient mice; A novel etiology of myxomatous valve disease |
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