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Expression profiling of ovarian BMP antagonists reveals the potential interaction between TWSG1 and the chordin subfamily in the ovary
The TGF-β superfamily members and their antagonists comprise an indispensable system that controls mammalian ovarian development in a sophisticated manner. In contrast to a plethora of studies on the ovary-expressed TGF-β superfamily members, knowledge regarding their antagonists, including their ex...
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| Published in: | Molecular and cellular endocrinology 2021-12, Vol.538, p.111457-111457, Article 111457 |
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| container_title | Molecular and cellular endocrinology |
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| creator | Wang, Ying-Wen Wu, Chia-Hsu Lin, Ting-Yu Luo, Ching-Wei |
| description | The TGF-β superfamily members and their antagonists comprise an indispensable system that controls mammalian ovarian development in a sophisticated manner. In contrast to a plethora of studies on the ovary-expressed TGF-β superfamily members, knowledge regarding their antagonists, including their expression profiles and antagonism preferences, is still lacking. Using quantitative PCR in rats and transcriptomic dataset comparisons in mice and humans, we set out to characterize the relative expression levels of most antagonists in the mammalian ovary. We found that Twsg1 and Nbl1 are the most abundant BMP antagonists expressed in the rodent and human ovaries, respectively. TWSG1 has been reported to have synergistic action with the chordin subfamily, including CHRD and CHRDL1, the genes of which also showed moderate expression in the mammalian ovary. Therefore, their ovarian expression profiles and antagonisms against the ovary-expressed TGF-β superfamily members were further characterized. Bioactivity tests indicated that TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7. In addition, it can further enhance the antagonizing ability of CHRD towards BMP2, BMP4, BMP7 and GDF5, or CHRDL1's antagonism towards BMP2, BMP4, GDF5 and activin A. In combination with their distinct transcript profiles in ovarian compartments, our findings suggest that TWSG1 may work coordinately with CHRD within theca/interstitial shells and also with CHRDL1 in developing granulosa cells; these interactions would modulate the intraovarian functions of the TGF-β superfamily members, such as the control of progesterone production.
•We provide a global view of BMP antagonist expression in the mammalian ovaries.•TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7.•TWSG1 selectively potentiates the antagonisms of CHRD and CHRDL1.•TWSG1 works synergistically with CHRDs to modulate ovarian progesterone levels.•TWSG1 and CHRDs form a new mechanism to coordinate intraovarian BMP activity. |
| doi_str_mv | 10.1016/j.mce.2021.111457 |
| format | article |
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•We provide a global view of BMP antagonist expression in the mammalian ovaries.•TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7.•TWSG1 selectively potentiates the antagonisms of CHRD and CHRDL1.•TWSG1 works synergistically with CHRDs to modulate ovarian progesterone levels.•TWSG1 and CHRDs form a new mechanism to coordinate intraovarian BMP activity.</description><identifier>ISSN: 0303-7207</identifier><identifier>EISSN: 1872-8057</identifier><identifier>DOI: 10.1016/j.mce.2021.111457</identifier><identifier>PMID: 34517078</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Animals ; BMP antagonists ; Bone Morphogenetic Proteins - antagonists & inhibitors ; Cell Cycle Proteins - genetics ; Chordin ; Databases, Genetic ; Eye Proteins - genetics ; Female ; Gene Expression Profiling - methods ; Glycoproteins - genetics ; Humans ; Intercellular Signaling Peptides and Proteins - genetics ; Mice ; Ovary ; Ovary - chemistry ; Progesterone ; Proteins - genetics ; Rats ; Signal Transduction ; TGF-β superfamily ; Transforming Growth Factor beta1 - genetics ; TWSG1</subject><ispartof>Molecular and cellular endocrinology, 2021-12, Vol.538, p.111457-111457, Article 111457</ispartof><rights>2021 Elsevier B.V.</rights><rights>Copyright © 2021 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c419t-b16f07adb694bbf73e1db7db7c342db0a698e369768835bd4392d62fedffe73f3</citedby><cites>FETCH-LOGICAL-c419t-b16f07adb694bbf73e1db7db7c342db0a698e369768835bd4392d62fedffe73f3</cites><orcidid>0000-0003-3956-2935 ; 0000-0002-0300-0386</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,786,790,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34517078$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Ying-Wen</creatorcontrib><creatorcontrib>Wu, Chia-Hsu</creatorcontrib><creatorcontrib>Lin, Ting-Yu</creatorcontrib><creatorcontrib>Luo, Ching-Wei</creatorcontrib><title>Expression profiling of ovarian BMP antagonists reveals the potential interaction between TWSG1 and the chordin subfamily in the ovary</title><title>Molecular and cellular endocrinology</title><addtitle>Mol Cell Endocrinol</addtitle><description>The TGF-β superfamily members and their antagonists comprise an indispensable system that controls mammalian ovarian development in a sophisticated manner. In contrast to a plethora of studies on the ovary-expressed TGF-β superfamily members, knowledge regarding their antagonists, including their expression profiles and antagonism preferences, is still lacking. Using quantitative PCR in rats and transcriptomic dataset comparisons in mice and humans, we set out to characterize the relative expression levels of most antagonists in the mammalian ovary. We found that Twsg1 and Nbl1 are the most abundant BMP antagonists expressed in the rodent and human ovaries, respectively. TWSG1 has been reported to have synergistic action with the chordin subfamily, including CHRD and CHRDL1, the genes of which also showed moderate expression in the mammalian ovary. Therefore, their ovarian expression profiles and antagonisms against the ovary-expressed TGF-β superfamily members were further characterized. Bioactivity tests indicated that TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7. In addition, it can further enhance the antagonizing ability of CHRD towards BMP2, BMP4, BMP7 and GDF5, or CHRDL1's antagonism towards BMP2, BMP4, GDF5 and activin A. In combination with their distinct transcript profiles in ovarian compartments, our findings suggest that TWSG1 may work coordinately with CHRD within theca/interstitial shells and also with CHRDL1 in developing granulosa cells; these interactions would modulate the intraovarian functions of the TGF-β superfamily members, such as the control of progesterone production.
•We provide a global view of BMP antagonist expression in the mammalian ovaries.•TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7.•TWSG1 selectively potentiates the antagonisms of CHRD and CHRDL1.•TWSG1 works synergistically with CHRDs to modulate ovarian progesterone levels.•TWSG1 and CHRDs form a new mechanism to coordinate intraovarian BMP activity.</description><subject>Animals</subject><subject>BMP antagonists</subject><subject>Bone Morphogenetic Proteins - antagonists & inhibitors</subject><subject>Cell Cycle Proteins - genetics</subject><subject>Chordin</subject><subject>Databases, Genetic</subject><subject>Eye Proteins - genetics</subject><subject>Female</subject><subject>Gene Expression Profiling - methods</subject><subject>Glycoproteins - genetics</subject><subject>Humans</subject><subject>Intercellular Signaling Peptides and Proteins - genetics</subject><subject>Mice</subject><subject>Ovary</subject><subject>Ovary - chemistry</subject><subject>Progesterone</subject><subject>Proteins - genetics</subject><subject>Rats</subject><subject>Signal Transduction</subject><subject>TGF-β superfamily</subject><subject>Transforming Growth Factor beta1 - genetics</subject><subject>TWSG1</subject><issn>0303-7207</issn><issn>1872-8057</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp9kF1PFDEUhhuCkQX9AdyYXnIzaz9mpjPxSgigCUYTMV42_TiFbmbate2u8gf43XZZ9JKkSS_6vE_PeRE6pWRJCe3fr5azgSUjjC4ppW0nDtCCDoI1A-nEIVoQTngjGBFH6DjnFSFEdGx4jY5421FBxLBAj5d_1gly9jHgdYrOTz7c4ehw3KrkVcDnX75hFYq6i8HnknGCLagp43IPeB0LhOLVhH0okJQpO42G8hsg4Nuf369pzdon1tzHZH3AeaOdmv30UDNPD7uPHt6gV65a4e3zfYJ-XF3eXnxqbr5ef774eNOYlo6l0bR3RCir-7HV2gkO1GpRj-Ets5qofhyA96Poh4F32rZ8ZLZnDqxzILjjJ-hs7627_tpALnL22cA0qQBxkyXrBOs4pZxWlO5Rk2LOCZxcJz_XWSUlcle_XMlav9zVL_f118y7Z_1Gz2D_J_71XYEPewDqklsPSWbjIRiwPoEp0kb_gv4vOPuYBg</recordid><startdate>20211201</startdate><enddate>20211201</enddate><creator>Wang, Ying-Wen</creator><creator>Wu, Chia-Hsu</creator><creator>Lin, Ting-Yu</creator><creator>Luo, Ching-Wei</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3956-2935</orcidid><orcidid>https://orcid.org/0000-0002-0300-0386</orcidid></search><sort><creationdate>20211201</creationdate><title>Expression profiling of ovarian BMP antagonists reveals the potential interaction between TWSG1 and the chordin subfamily in the ovary</title><author>Wang, Ying-Wen ; Wu, Chia-Hsu ; Lin, Ting-Yu ; Luo, Ching-Wei</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c419t-b16f07adb694bbf73e1db7db7c342db0a698e369768835bd4392d62fedffe73f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animals</topic><topic>BMP antagonists</topic><topic>Bone Morphogenetic Proteins - antagonists & inhibitors</topic><topic>Cell Cycle Proteins - genetics</topic><topic>Chordin</topic><topic>Databases, Genetic</topic><topic>Eye Proteins - genetics</topic><topic>Female</topic><topic>Gene Expression Profiling - methods</topic><topic>Glycoproteins - genetics</topic><topic>Humans</topic><topic>Intercellular Signaling Peptides and Proteins - genetics</topic><topic>Mice</topic><topic>Ovary</topic><topic>Ovary - chemistry</topic><topic>Progesterone</topic><topic>Proteins - genetics</topic><topic>Rats</topic><topic>Signal Transduction</topic><topic>TGF-β superfamily</topic><topic>Transforming Growth Factor beta1 - genetics</topic><topic>TWSG1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Ying-Wen</creatorcontrib><creatorcontrib>Wu, Chia-Hsu</creatorcontrib><creatorcontrib>Lin, Ting-Yu</creatorcontrib><creatorcontrib>Luo, Ching-Wei</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular and cellular endocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Ying-Wen</au><au>Wu, Chia-Hsu</au><au>Lin, Ting-Yu</au><au>Luo, Ching-Wei</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Expression profiling of ovarian BMP antagonists reveals the potential interaction between TWSG1 and the chordin subfamily in the ovary</atitle><jtitle>Molecular and cellular endocrinology</jtitle><addtitle>Mol Cell Endocrinol</addtitle><date>2021-12-01</date><risdate>2021</risdate><volume>538</volume><spage>111457</spage><epage>111457</epage><pages>111457-111457</pages><artnum>111457</artnum><issn>0303-7207</issn><eissn>1872-8057</eissn><notes>ObjectType-Article-2</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-1</notes><notes>content type line 23</notes><abstract>The TGF-β superfamily members and their antagonists comprise an indispensable system that controls mammalian ovarian development in a sophisticated manner. In contrast to a plethora of studies on the ovary-expressed TGF-β superfamily members, knowledge regarding their antagonists, including their expression profiles and antagonism preferences, is still lacking. Using quantitative PCR in rats and transcriptomic dataset comparisons in mice and humans, we set out to characterize the relative expression levels of most antagonists in the mammalian ovary. We found that Twsg1 and Nbl1 are the most abundant BMP antagonists expressed in the rodent and human ovaries, respectively. TWSG1 has been reported to have synergistic action with the chordin subfamily, including CHRD and CHRDL1, the genes of which also showed moderate expression in the mammalian ovary. Therefore, their ovarian expression profiles and antagonisms against the ovary-expressed TGF-β superfamily members were further characterized. Bioactivity tests indicated that TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7. In addition, it can further enhance the antagonizing ability of CHRD towards BMP2, BMP4, BMP7 and GDF5, or CHRDL1's antagonism towards BMP2, BMP4, GDF5 and activin A. In combination with their distinct transcript profiles in ovarian compartments, our findings suggest that TWSG1 may work coordinately with CHRD within theca/interstitial shells and also with CHRDL1 in developing granulosa cells; these interactions would modulate the intraovarian functions of the TGF-β superfamily members, such as the control of progesterone production.
•We provide a global view of BMP antagonist expression in the mammalian ovaries.•TWSG1 alone can directly inhibit the signaling of BMP6 or BMP7.•TWSG1 selectively potentiates the antagonisms of CHRD and CHRDL1.•TWSG1 works synergistically with CHRDs to modulate ovarian progesterone levels.•TWSG1 and CHRDs form a new mechanism to coordinate intraovarian BMP activity.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>34517078</pmid><doi>10.1016/j.mce.2021.111457</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-3956-2935</orcidid><orcidid>https://orcid.org/0000-0002-0300-0386</orcidid></addata></record> |
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| subjects | Animals BMP antagonists Bone Morphogenetic Proteins - antagonists & inhibitors Cell Cycle Proteins - genetics Chordin Databases, Genetic Eye Proteins - genetics Female Gene Expression Profiling - methods Glycoproteins - genetics Humans Intercellular Signaling Peptides and Proteins - genetics Mice Ovary Ovary - chemistry Progesterone Proteins - genetics Rats Signal Transduction TGF-β superfamily Transforming Growth Factor beta1 - genetics TWSG1 |
| title | Expression profiling of ovarian BMP antagonists reveals the potential interaction between TWSG1 and the chordin subfamily in the ovary |
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