eGFP-tagged Wnt-3a enables functional analysis of Wnt trafficking and signaling and kinetic assessment of Wnt binding to full-length Frizzled
The Wingless/Int1 (Wnt) signaling system plays multiple, essential roles in embryonic development, tissue homeostasis, and human diseases. Although many of the underlying signaling mechanisms are becoming clearer, the binding mode, kinetics, and selectivity of 19 mammalian WNTs to their receptors of...
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| Veröffentlicht in: | The Journal of biological chemistry 2020-06, Vol.295 (26), p.8759-8774 |
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| creator | Wesslowski, Janine Kozielewicz, Pawel Wang, Xianxian Cui, Haijun Schihada, Hannes Kranz, Dominique Karuna M, Pradhipa Levkin, Pavel Gross, Julia Christina Boutros, Michael Schulte, Gunnar Davidson, Gary |
| description | The Wingless/Int1 (Wnt) signaling system plays multiple, essential roles in embryonic development, tissue homeostasis, and human diseases. Although many of the underlying signaling mechanisms are becoming clearer, the binding mode, kinetics, and selectivity of 19 mammalian WNTs to their receptors of the class Frizzled (FZD1–10) remain obscure. Attempts to investigate Wnt-FZD interactions are hampered by the difficulties in working with Wnt proteins and their recalcitrance to epitope tagging. Here, we used a fluorescently tagged version of mouse Wnt-3a for studying Wnt-FZD interactions. We observed that the enhanced GFP (eGFP)-tagged Wnt-3a maintains properties akin to wild-type (WT) Wnt-3a in several biologically relevant contexts. The eGFP-tagged Wnt-3a was secreted in an evenness interrupted (EVI)/Wntless-dependent manner, activated Wnt/β-catenin signaling in 2D and 3D cell culture experiments, promoted axis duplication in Xenopus embryos, stimulated low-density lipoprotein receptor-related protein 6 (LRP6) phosphorylation in cells, and associated with exosomes. Further, we used conditioned medium containing eGFP-Wnt-3a to visualize its binding to FZD and to quantify Wnt-FZD interactions in real time in live cells, utilizing a recently established NanoBRET-based ligand binding assay. In summary, the development of a biologically active, fluorescent Wnt-3a reported here opens up the technical possibilities to unravel the intricate biology of Wnt signaling and Wnt-receptor selectivity. |
| doi_str_mv | 10.1074/jbc.RA120.012892 |
| format | Article |
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Although many of the underlying signaling mechanisms are becoming clearer, the binding mode, kinetics, and selectivity of 19 mammalian WNTs to their receptors of the class Frizzled (FZD1–10) remain obscure. Attempts to investigate Wnt-FZD interactions are hampered by the difficulties in working with Wnt proteins and their recalcitrance to epitope tagging. Here, we used a fluorescently tagged version of mouse Wnt-3a for studying Wnt-FZD interactions. We observed that the enhanced GFP (eGFP)-tagged Wnt-3a maintains properties akin to wild-type (WT) Wnt-3a in several biologically relevant contexts. The eGFP-tagged Wnt-3a was secreted in an evenness interrupted (EVI)/Wntless-dependent manner, activated Wnt/β-catenin signaling in 2D and 3D cell culture experiments, promoted axis duplication in Xenopus embryos, stimulated low-density lipoprotein receptor-related protein 6 (LRP6) phosphorylation in cells, and associated with exosomes. Further, we used conditioned medium containing eGFP-Wnt-3a to visualize its binding to FZD and to quantify Wnt-FZD interactions in real time in live cells, utilizing a recently established NanoBRET-based ligand binding assay. In summary, the development of a biologically active, fluorescent Wnt-3a reported here opens up the technical possibilities to unravel the intricate biology of Wnt signaling and Wnt-receptor selectivity.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.RA120.012892</identifier><identifier>PMID: 32381507</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; bioluminescence resonance energy transfer (BRET) ; Cell Biology ; Frizzled ; Frizzled Receptors - analysis ; Frizzled Receptors - metabolism ; fusion protein ; G protein–coupled receptor (GPCR) ; Green Fluorescent Proteins - analysis ; Green Fluorescent Proteins - metabolism ; HEK293 Cells ; Humans ; ligand binding ; membrane protein ; Mice ; Microscopy, Confocal - methods ; NanoBiT ; NanoBRET ; Protein Interaction Maps ; Protein Transport ; trafficking ; Wnt signaling ; Wnt Signaling Pathway ; Wnt3A Protein - analysis ; Wnt3A Protein - metabolism ; Xenopus</subject><ispartof>The Journal of biological chemistry, 2020-06, Vol.295 (26), p.8759-8774</ispartof><rights>2020 © 2020 Wesslowski et al.</rights><rights>2020 Wesslowski et al.</rights><rights>2020 Wesslowski et al. 2020 Wesslowski et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c551t-509ebe9ba29b74c58c6301a94e55611088196c6b45b41b58ccfe3945135ed723</citedby><cites>FETCH-LOGICAL-c551t-509ebe9ba29b74c58c6301a94e55611088196c6b45b41b58ccfe3945135ed723</cites><orcidid>0000-0002-1889-1636 ; 0000-0002-2700-7013 ; 0000-0002-8939-5664 ; 0000-0003-1414-3566 ; 0000-0002-7934-7407 ; 0000-0002-9458-817X ; 0000-0002-2264-5518</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7324525/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7324525/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32381507$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:144151643$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Wesslowski, Janine</creatorcontrib><creatorcontrib>Kozielewicz, Pawel</creatorcontrib><creatorcontrib>Wang, Xianxian</creatorcontrib><creatorcontrib>Cui, Haijun</creatorcontrib><creatorcontrib>Schihada, Hannes</creatorcontrib><creatorcontrib>Kranz, Dominique</creatorcontrib><creatorcontrib>Karuna M, Pradhipa</creatorcontrib><creatorcontrib>Levkin, Pavel</creatorcontrib><creatorcontrib>Gross, Julia Christina</creatorcontrib><creatorcontrib>Boutros, Michael</creatorcontrib><creatorcontrib>Schulte, Gunnar</creatorcontrib><creatorcontrib>Davidson, Gary</creatorcontrib><title>eGFP-tagged Wnt-3a enables functional analysis of Wnt trafficking and signaling and kinetic assessment of Wnt binding to full-length Frizzled</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>The Wingless/Int1 (Wnt) signaling system plays multiple, essential roles in embryonic development, tissue homeostasis, and human diseases. Although many of the underlying signaling mechanisms are becoming clearer, the binding mode, kinetics, and selectivity of 19 mammalian WNTs to their receptors of the class Frizzled (FZD1–10) remain obscure. Attempts to investigate Wnt-FZD interactions are hampered by the difficulties in working with Wnt proteins and their recalcitrance to epitope tagging. Here, we used a fluorescently tagged version of mouse Wnt-3a for studying Wnt-FZD interactions. We observed that the enhanced GFP (eGFP)-tagged Wnt-3a maintains properties akin to wild-type (WT) Wnt-3a in several biologically relevant contexts. The eGFP-tagged Wnt-3a was secreted in an evenness interrupted (EVI)/Wntless-dependent manner, activated Wnt/β-catenin signaling in 2D and 3D cell culture experiments, promoted axis duplication in Xenopus embryos, stimulated low-density lipoprotein receptor-related protein 6 (LRP6) phosphorylation in cells, and associated with exosomes. Further, we used conditioned medium containing eGFP-Wnt-3a to visualize its binding to FZD and to quantify Wnt-FZD interactions in real time in live cells, utilizing a recently established NanoBRET-based ligand binding assay. In summary, the development of a biologically active, fluorescent Wnt-3a reported here opens up the technical possibilities to unravel the intricate biology of Wnt signaling and Wnt-receptor selectivity.</description><subject>Animals</subject><subject>bioluminescence resonance energy transfer (BRET)</subject><subject>Cell Biology</subject><subject>Frizzled</subject><subject>Frizzled Receptors - analysis</subject><subject>Frizzled Receptors - metabolism</subject><subject>fusion protein</subject><subject>G protein–coupled receptor (GPCR)</subject><subject>Green Fluorescent Proteins - analysis</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>ligand binding</subject><subject>membrane protein</subject><subject>Mice</subject><subject>Microscopy, Confocal - methods</subject><subject>NanoBiT</subject><subject>NanoBRET</subject><subject>Protein Interaction Maps</subject><subject>Protein Transport</subject><subject>trafficking</subject><subject>Wnt signaling</subject><subject>Wnt Signaling Pathway</subject><subject>Wnt3A Protein - analysis</subject><subject>Wnt3A Protein - metabolism</subject><subject>Xenopus</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNp1UUtPFTEUboxGLsjelenSzVz7nIcLE0K8YEKiMSSya9rOmaHQ28G2FwP_gf9Mr3MhsrCLPs73aHs-hN5TsqSkEZ-ujF3-PKKMLAllbcdeoQUlLa-4pBev0YIQRquOyXYP7ad0RcoQHX2L9jjjLZWkWaAHOFn9qLIeR-jxr5ArrjEEbTwkPGyCzW4K2mNdprvkEp6GLQvnqIfB2WsXxoL1OLmxMJ5OpQzZWaxTgpTWUAQ7nXGh37LyVNy9rzyEMV_iVXT39x76d-jNoH2Cw916gM5XX8-PT6uz7yffjo_OKislzZUkHRjojGadaYSVra05oboTIGVNSwda2tW2NkIaQU2B7QC8E5JyCX3D-AGqZtv0B242Rt1Et9bxTk3aqV3puuxAiYaKWhT-l5lfkDX0tnwoav9C9hIJ7lKN061qOBOSyWLwcWcQp98bSFmtXbLgvQ4wbZJighDJG1Fv30Zmqo1TShGG52soUdvQVQld_Q1dzaEXyYd_n_cseEq5ED7PBCg9vXUQVbIOgoXeRbBZ9ZP7v_sjYQu_CQ</recordid><startdate>20200626</startdate><enddate>20200626</enddate><creator>Wesslowski, Janine</creator><creator>Kozielewicz, Pawel</creator><creator>Wang, Xianxian</creator><creator>Cui, Haijun</creator><creator>Schihada, Hannes</creator><creator>Kranz, Dominique</creator><creator>Karuna M, Pradhipa</creator><creator>Levkin, Pavel</creator><creator>Gross, Julia Christina</creator><creator>Boutros, Michael</creator><creator>Schulte, Gunnar</creator><creator>Davidson, Gary</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-1889-1636</orcidid><orcidid>https://orcid.org/0000-0002-2700-7013</orcidid><orcidid>https://orcid.org/0000-0002-8939-5664</orcidid><orcidid>https://orcid.org/0000-0003-1414-3566</orcidid><orcidid>https://orcid.org/0000-0002-7934-7407</orcidid><orcidid>https://orcid.org/0000-0002-9458-817X</orcidid><orcidid>https://orcid.org/0000-0002-2264-5518</orcidid></search><sort><creationdate>20200626</creationdate><title>eGFP-tagged Wnt-3a enables functional analysis of Wnt trafficking and signaling and kinetic assessment of Wnt binding to full-length Frizzled</title><author>Wesslowski, Janine ; Kozielewicz, Pawel ; Wang, Xianxian ; Cui, Haijun ; Schihada, Hannes ; Kranz, Dominique ; Karuna M, Pradhipa ; Levkin, Pavel ; Gross, Julia Christina ; Boutros, Michael ; Schulte, Gunnar ; Davidson, Gary</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c551t-509ebe9ba29b74c58c6301a94e55611088196c6b45b41b58ccfe3945135ed723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>bioluminescence resonance energy transfer (BRET)</topic><topic>Cell Biology</topic><topic>Frizzled</topic><topic>Frizzled Receptors - analysis</topic><topic>Frizzled Receptors - metabolism</topic><topic>fusion protein</topic><topic>G protein–coupled receptor (GPCR)</topic><topic>Green Fluorescent Proteins - analysis</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>HEK293 Cells</topic><topic>Humans</topic><topic>ligand binding</topic><topic>membrane protein</topic><topic>Mice</topic><topic>Microscopy, Confocal - methods</topic><topic>NanoBiT</topic><topic>NanoBRET</topic><topic>Protein Interaction Maps</topic><topic>Protein Transport</topic><topic>trafficking</topic><topic>Wnt signaling</topic><topic>Wnt Signaling Pathway</topic><topic>Wnt3A Protein - analysis</topic><topic>Wnt3A Protein - metabolism</topic><topic>Xenopus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wesslowski, Janine</creatorcontrib><creatorcontrib>Kozielewicz, Pawel</creatorcontrib><creatorcontrib>Wang, Xianxian</creatorcontrib><creatorcontrib>Cui, Haijun</creatorcontrib><creatorcontrib>Schihada, Hannes</creatorcontrib><creatorcontrib>Kranz, Dominique</creatorcontrib><creatorcontrib>Karuna M, Pradhipa</creatorcontrib><creatorcontrib>Levkin, Pavel</creatorcontrib><creatorcontrib>Gross, Julia Christina</creatorcontrib><creatorcontrib>Boutros, Michael</creatorcontrib><creatorcontrib>Schulte, Gunnar</creatorcontrib><creatorcontrib>Davidson, Gary</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><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><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wesslowski, Janine</au><au>Kozielewicz, Pawel</au><au>Wang, Xianxian</au><au>Cui, Haijun</au><au>Schihada, Hannes</au><au>Kranz, Dominique</au><au>Karuna M, Pradhipa</au><au>Levkin, Pavel</au><au>Gross, Julia Christina</au><au>Boutros, Michael</au><au>Schulte, Gunnar</au><au>Davidson, Gary</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>eGFP-tagged Wnt-3a enables functional analysis of Wnt trafficking and signaling and kinetic assessment of Wnt binding to full-length Frizzled</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2020-06-26</date><risdate>2020</risdate><volume>295</volume><issue>26</issue><spage>8759</spage><epage>8774</epage><pages>8759-8774</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>The Wingless/Int1 (Wnt) signaling system plays multiple, essential roles in embryonic development, tissue homeostasis, and human diseases. Although many of the underlying signaling mechanisms are becoming clearer, the binding mode, kinetics, and selectivity of 19 mammalian WNTs to their receptors of the class Frizzled (FZD1–10) remain obscure. Attempts to investigate Wnt-FZD interactions are hampered by the difficulties in working with Wnt proteins and their recalcitrance to epitope tagging. Here, we used a fluorescently tagged version of mouse Wnt-3a for studying Wnt-FZD interactions. We observed that the enhanced GFP (eGFP)-tagged Wnt-3a maintains properties akin to wild-type (WT) Wnt-3a in several biologically relevant contexts. The eGFP-tagged Wnt-3a was secreted in an evenness interrupted (EVI)/Wntless-dependent manner, activated Wnt/β-catenin signaling in 2D and 3D cell culture experiments, promoted axis duplication in Xenopus embryos, stimulated low-density lipoprotein receptor-related protein 6 (LRP6) phosphorylation in cells, and associated with exosomes. Further, we used conditioned medium containing eGFP-Wnt-3a to visualize its binding to FZD and to quantify Wnt-FZD interactions in real time in live cells, utilizing a recently established NanoBRET-based ligand binding assay. In summary, the development of a biologically active, fluorescent Wnt-3a reported here opens up the technical possibilities to unravel the intricate biology of Wnt signaling and Wnt-receptor selectivity.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>32381507</pmid><doi>10.1074/jbc.RA120.012892</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-1889-1636</orcidid><orcidid>https://orcid.org/0000-0002-2700-7013</orcidid><orcidid>https://orcid.org/0000-0002-8939-5664</orcidid><orcidid>https://orcid.org/0000-0003-1414-3566</orcidid><orcidid>https://orcid.org/0000-0002-7934-7407</orcidid><orcidid>https://orcid.org/0000-0002-9458-817X</orcidid><orcidid>https://orcid.org/0000-0002-2264-5518</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals bioluminescence resonance energy transfer (BRET) Cell Biology Frizzled Frizzled Receptors - analysis Frizzled Receptors - metabolism fusion protein G protein–coupled receptor (GPCR) Green Fluorescent Proteins - analysis Green Fluorescent Proteins - metabolism HEK293 Cells Humans ligand binding membrane protein Mice Microscopy, Confocal - methods NanoBiT NanoBRET Protein Interaction Maps Protein Transport trafficking Wnt signaling Wnt Signaling Pathway Wnt3A Protein - analysis Wnt3A Protein - metabolism Xenopus |
| title | eGFP-tagged Wnt-3a enables functional analysis of Wnt trafficking and signaling and kinetic assessment of Wnt binding to full-length Frizzled |
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