Fgf9 and Wnt4 Act as Antagonistic Signals to Regulate Mammalian Sex Determination
Publication Date
May 23, 2006
Journal
PLOS Biology
Authors
Yuna Kim, Akio Kobayashi, Ryohei Sekido, Leo Di Napoli, et al
Volume
4
Issue
6
Pages
e187
DOI
http://doi.org/10.1371/journal.pbio.0040187
Publisher URL
http://journals.plos.org/plosbiology/article?id=10.1371%2Fjournal.pbio.0040187
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/16700629
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1463023
Europe PMC
http://europepmc.org/abstract/MED/16700629
Web of Science
000238249600013
Scopus
33746907822
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Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/959551"], "description"=>"<div><p>(A–F) Whole-mount in situ hybridization for genes in the male pathway downstream of \n\t\t\t\t\t\t\t<i>Sox9, Dhh,</i> and \n\t\t\t\t\t\t\t<i>Amh</i>. \n\t\t\t\t\t\t\t<i>Dhh</i> expression is disrupted in XY \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> gonads (g) at 11.5 dpc (A and B). \n\t\t\t\t\t\t\t<i>Amh</i> expression is severely reduced in XY \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> gonads at 12.5 dpc (E and F).\n\t\t\t\t\t\t</p>\n <p>(G and H) Analysis of cell death in \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> XY gonads using an apoptotic marker, active caspase-3 (red). No increased apoptosis is observed in XY \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> gonads (g) compared with control XY gonads, although apoptotic cells are increased around mesonephric tubules (m) of the mutant gonads (arrow in H). Semitransparent dotted line indicates boundary between mesonephros and gonad. (PECAM, green).\n\t\t\t\t\t\t</p>\n <p>(I–K) Whole-mount in situ hybridization for \n\t\t\t\t\t\t\t<i>Wnt4,</i> an ovary marker. \n\t\t\t\t\t\t\t<i>Wnt4</i> is expressed in \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> XY gonads at 12.5 dpc (K) similar to the level in XX \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>+/−</sup> controls (I) but not in XY controls (J). The scale bars represent 50 μm.\n\t\t\t\t\t\t</p>\n <p>g, gonad; m, mesonephros.</p></div>", "links"=>[], "tags"=>["precursors", "pathway"], "article_id"=>629568, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sertoli_Cell_Precursors_Switch_from_Expression_of_Male_to_Female_Pathway_Genes_/629568", "title"=>"Sertoli Cell Precursors Switch from Expression of Male to Female Pathway Genes", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:43:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/960045"], "description"=>"<p>In both XX and XY gonads at 11.25 dpc (15 tail-somite stage), \n\t\t\t\t\t\t<i>Fgf9</i> transcripts (white arrows) are detected near the gonad surface (A and B), whereas \n\t\t\t\t\t\t<i>Wnt4</i> transcripts are detected near the gonad mesonephric boundary (C and D). We propose a model in which the fate of the gonad is balanced between these competing signals. A genetic or environmental switch initiates the male pathway by creating an imbalance between these signals. In mammals, this imbalance occurs through the up-regulation of \n\t\t\t\t\t\t<i>Sox9</i>. \n\t\t\t\t\t\t<i>Sox9</i> up-regulates \n\t\t\t\t\t\t<i>Fgf9,</i> and \n\t\t\t\t\t\t<i>Fgf9</i> maintains \n\t\t\t\t\t\t<i>Sox9,</i> forming a positive feed-forward loop in XY gonads. In this situation, the balance between FGF9 and WNT4 signals is shifted in favor of FGF9, and the dominance of the male pathway is established. In the absence of a feed-forward loop between SOX9 and FGF9 (e.g., in XX gonads), WNT4 blocks \n\t\t\t\t\t\t<i>Fgf9,</i> initiating the female pathway.\n\t\t\t\t\t</p>", "links"=>[], "tags"=>["signals", "bipotential"], "article_id"=>630052, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g007", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Opposing_Signals_Regulate_Sex_Determination_in_the_Bipotential_Gonad_/630052", "title"=>"Opposing Signals Regulate Sex Determination in the Bipotential Gonad", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:47:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/474322"], "description"=>"<div><p>The genes encoding members of the wingless-related MMTV integration site (WNT) and fibroblast growth factor (FGF) families coordinate growth, morphogenesis, and differentiation in many fields of cells during development. In the mouse, <em>Fgf9</em> and <em>Wnt4</em> are expressed in gonads of both sexes prior to sex determination. Loss of <em>Fgf9</em> leads to XY sex reversal, whereas loss of <em>Wnt4</em> results in partial testis development in XX gonads. However, the relationship between these signals and the male sex-determining gene, <em>Sry,</em> was unknown. We show through gain- and loss-of-function experiments that fibroblast growth factor 9 (FGF9) and WNT4 act as opposing signals to regulate sex determination. In the mouse XY gonad, <em>Sry</em> normally initiates a feed-forward loop between <em>Sox9</em> and <em>Fgf9,</em> which up-regulates <em>Fgf9</em> and represses <em>Wnt4</em> to establish the testis pathway. Surprisingly, loss of <em>Wnt4</em> in XX gonads is sufficient to up-regulate <em>Fgf9</em> and <em>Sox9</em> in the absence of <em>Sry</em>. These data suggest that the fate of the gonad is controlled by antagonism between <em>Fgf9</em> and <em>Wnt4</em>. The role of the male sex-determining switch— <em>Sry</em> in the case of mammals—is to tip the balance between these underlying patterning signals. In principle, sex determination in other vertebrates may operate through any switch that introduces an imbalance between these two signaling pathways. </p> </div>", "links"=>[], "tags"=>["antagonistic", "signals", "mammalian"], "article_id"=>153445, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187", "stats"=>{"downloads"=>0, "page_views"=>35, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fgf9_and_Wnt4_Act_as_Antagonistic_Signals_to_Regulate_Mammalian_Sex_Determination_/153445", "title"=>"<em>Fgf9</em> and \n\t\t\t\t\t<em>Wnt4</em> Act as Antagonistic Signals to Regulate Mammalian Sex Determination", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2006-05-23 00:57:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/959885"], "description"=>"<div><p>(A–C) FGF9 (red) immunostaining shows that FGF9 is expressed in XX \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> gonads at 12.5 dpc (C) relative to littermate controls (A and B).\n\t\t\t\t\t\t</p>\n <p>(D–L) SOX9 (red) immunostaining shows that SOX9 is transiently up-regulated in XX \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> gonads. SOX9 expression is detected in \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> XX gonads at 11.5–12.0 dpc (F and I), albeit at reduced levels compared with XY gonad controls (E-H). SOX9 is not detected in control XX \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>+/−</sup> gonads (D-J) or \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> XX gonads at 12.5 dpc (L). The ectopic coelomic vessel in XX \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> gonads [<a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.0040187#pbio-0040187-b028\" target=\"_blank\">28</a>] is indicated by arrowheads. PECAM, green. The scale bars represent 50 μm.\n\t\t\t\t\t\t</p></div>", "links"=>[], "tags"=>["sox9", "xx"], "article_id"=>629896, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g006", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ectopic_Expression_of_Male_Factors_SOX9_and_FGF9_in_XX__Wnt4_8722_8722_Gonads_/629896", "title"=>"Ectopic Expression of Male Factors, SOX9 and FGF9, in XX \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>−/−</sup> Gonads", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:46:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/959726"], "description"=>"<div><p>(A–C) \n\t\t\t\t\t\t\t<i>Wnt4</i> whole-mount in situ hybridization on gonad cultures. Adding exogenous FGF9 in gonad cultures results in the down-regulation of \n\t\t\t\t\t\t\t<i>Wnt4</i> expression in cultured XX gonads (C). Controls (A and B) were cultured without FGF9 peptide.\n\t\t\t\t\t\t</p>\n <p>(D–G) Reduction in the dose of \n\t\t\t\t\t\t\t<i>Wnt4</i> allows FGF9 to induce SOX9 in XX gonads. Immunostaining of SOX9 (red) shows that addition of FGF9 up-regulates SOX9 expression in heterozygous \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>+/−</sup> XX gonads (G), but not in \n\t\t\t\t\t\t\t<i>Wnt4</i><sup>+/+</sup> XX gonads (F). PECAM, green. The scale bars represent 50 μm.\n\t\t\t\t\t\t</p></div>", "links"=>[], "tags"=>["antagonism"], "article_id"=>629742, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g005", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutual_Antagonism_between__Fgf9_and__Wnt4_/629742", "title"=>"Mutual Antagonism between \n\t\t\t\t\t\t\t<i>Fgf9</i> and \n\t\t\t\t\t\t\t<i>Wnt4</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:44:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/959218"], "description"=>"<div><p>(A–D) \n\t\t\t\t\t\t\t<i>Sry</i> expression is not dependent on \n\t\t\t\t\t\t\t<i>Fgf9</i>. \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>+/−</sup> (A) and \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> (B) XY gonads at 11.5 dpc expressing GFP (green) from the \n\t\t\t\t\t\t\t<i>Sry</i> promoter (polygonal cells, arrows). Blood cells show background fluorescence (doughnut-shaped cells). \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>+/−</sup> (C) and \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> (D) XY gonads at 11.5 dpc expressing SRY<sup>MYC</sup> protein (red, arrowheads). Inset shows nuclear counterstain (green, Syto13) colocalizing with SRY<sup>MYC</sup>. PECAM (blue) marks endothelial and germ cells. Scale bars represent 25 μm.\n\t\t\t\t\t\t</p>\n <p>(E–K) Exogenous FGF9 can up-regulate SOX9 expression in XX gonads. Immunostaining of SOX9 (green) in primary cultures of gonadal cells. XX cells (E) and XY cells (G) cultured with exogenous FGF9 show induction of SOX9 expression (F and H, respectively). Cells were counterstained using the nuclear marker, Syto13 (red). Immunostaining of SOX9 (red) in gonad explants cultured with BSA- or FGF9-coated beads. SOX9 is expressed in XY gonads and cells contacting FGF9-coated beads (dotted circle labeled “F”) in XX gonads (I and K) but not in XX cells contacting BSA-coated control beads (“B”) (J). PECAM (blue) marks endothelial and germ cells. Scale bars (I–K) represent 50 μm.</p></div>", "links"=>[], "tags"=>["cell biology", "developmental biology"], "article_id"=>629240, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Epistatic_Relationship_of__Sry_Fgf9_and__Sox9_/629240", "title"=>"Epistatic Relationship of \n\t\t\t\t\t\t\t<i>Sry, Fgf9,</i> and \n\t\t\t\t\t\t\t<i>Sox9</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:41:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/959048"], "description"=>"<div><p>(A–F) Detection of FGF9 protein (red) at different stages of gonad development. FGF9 is up-regulated in XY gonads at 11.5 (B), 12.5 (D), and 13.5 dpc (F) while it is down-regulated in XX after 11.5 dpc (A, C, and E). No signal was detected in XY \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> gonads (unpublished data).\n\t\t\t\t\t\t</p>\n <p>(G–J) Serial sections of wild-type XX and compound heterozygous \n\t\t\t\t\t\t\t<i>Kit</i><sup>W/Wv</sup> XY gonads stained for alkaline phosphatase (purple; G and I) and FGF9 (red; H and J). Testis cords are formed in the absence of germ cells in XY \n\t\t\t\t\t\t\t<i>Kit</i><sup>W/Wv</sup> mutant gonads at 12.5 dpc (arrowhead in J). Expression of FGF9 is present in the mutant gonads where Sertoli cells are the only remaining cell type in the cords (J). Semitransparent dotted line indicates the boundary between gonad and mesonephroi. PECAM (green) marks germ cells and vascular endothelial cells (C–F, H, and J). The scale bars represent 25 μm.\n\t\t\t\t\t\t</p>\n <p>g, gonad; m, mesonephroi.</p></div>", "links"=>[], "tags"=>["cell-specific", "fgf9", "embryonic"], "article_id"=>629080, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g001", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Stage_and_Cell_Specific_Expression_of_FGF9_in_Embryonic_Gonads_/629080", "title"=>"Stage- and Cell-Specific Expression of FGF9 in Embryonic Gonads", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:40:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/959382"], "description"=>"<div><p>(A–F) Immunostaining of SOX9 (red) in \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>+/−</sup> and \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> XY gonads shows that \n\t\t\t\t\t\t\t<i>Fgf9</i> is required for maintenance of SOX9. The up-regulation of SOX9 in Sertoli precursor cells appears normal in \n\t\t\t\t\t\t\t<i>Fgf9</i><sup>−/−</sup> gonads at 11.5 dpc (D) compared with heterozygous littermate controls (A). However, SOX9 is detected in fewer cells in mutant gonads at 12.0 dpc (B and E), and is lost by 12.5 dpc (C and F).\n\t\t\t\t\t\t</p>\n <p>(G–J) mRNA whole-mount in situ hybridization for \n\t\t\t\t\t\t\t<i>Sry</i> and \n\t\t\t\t\t\t\t<i>Fgf9</i> in \n\t\t\t\t\t\t\t<i>Sox9</i><sup>flox/Δ</sup> and \n\t\t\t\t\t\t\t<i>Sox9</i><sup>Δ/Δ</sup> XY gonads shows that \n\t\t\t\t\t\t\t<i>Sox9</i> is required for \n\t\t\t\t\t\t\t<i>Fgf9</i> expression. \n\t\t\t\t\t\t\t<i>Sry</i> expression is detected in both \n\t\t\t\t\t\t\t<i>Sox9</i><sup>flox/Δ</sup> and \n\t\t\t\t\t\t\t<i>Sox9</i><sup>Δ/Δ</sup> gonads at 11.5 dpc (G and H), whereas \n\t\t\t\t\t\t\t<i>Fgf9</i> expression is markedly decreased or absent in \n\t\t\t\t\t\t\t<i>Sox9</i><sup>Δ/Δ</sup> gonads at 11.5 dpc (I and J).\n\t\t\t\t\t\t</p>\n <p>(K–O) Comparison of cell proliferation in \n\t\t\t\t\t\t\t<i>Sox9</i><sup>Δ/Δ</sup> versus \n\t\t\t\t\t\t\t<i>Sox9</i><sup>flox/Δ</sup> gonads at 11.5 dpc using immunostaining for phosphorylated histone H3. XY-specific proliferation at the gonad surface (K) is reduced in the absence of \n\t\t\t\t\t\t\t<i>Sox9</i> (L). Bar graph (O) shows quantitation of proliferation obtained by counting positive cells in the cortical region of each gonad (right brace) and normalizing to the number obtained from XY \n\t\t\t\t\t\t\t<i>Sox9</i><sup>flox/Δ</sup> gonads. \n\t\t\t\t\t\t\t<i>n</i> = 30, with five sections of each gonad and three pairs of gonads for each genotype. PECAM, green (A–F and K–N). The scale bars represent 25 μm.\n\t\t\t\t\t\t</p></div>", "links"=>[], "tags"=>["cell biology", "developmental biology"], "article_id"=>629403, "categories"=>["Cell Biology", "Developmental Biology"], "users"=>["Yuna Kim", "Akio Kobayashi", "Ryohei Sekido", "Leo DiNapoli", "Jennifer Brennan", "Marie-Christine Chaboissier", "Francis Poulat", "Richard R Behringer", "Robin Lovell-Badge", "Blanche Capel"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.0040187.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interdependent_Relationship_between__Fgf9_and__Sox9_/629403", "title"=>"Interdependent Relationship between \n\t\t\t\t\t\t\t<i>Fgf9</i> and \n\t\t\t\t\t\t\t<i>Sox9</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 08:42:29"}

PMC Usage Stats | Further Information

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Relative Metric

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