FGF Signaling Regulates the Number of Posterior Taste Papillae by Controlling Progenitor Field Size
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{"title"=>"FGF signaling regulates the number of posterior taste papillae by controlling progenitor field size", "type"=>"journal", "authors"=>[{"first_name"=>"Camille I.", "last_name"=>"Petersen", "scopus_author_id"=>"46062484100"}, {"first_name"=>"Andrew H.", "last_name"=>"Jheon", "scopus_author_id"=>"6602620953"}, {"first_name"=>"Pasha", "last_name"=>"Mostowfi", "scopus_author_id"=>"37039864800"}, {"first_name"=>"Cyril", "last_name"=>"Charles", "scopus_author_id"=>"56258554900"}, {"first_name"=>"Saunders", "last_name"=>"Ching", "scopus_author_id"=>"46061859500"}, {"first_name"=>"Shoba", "last_name"=>"Thirumangalathu", "scopus_author_id"=>"15754931100"}, {"first_name"=>"Linda A.", "last_name"=>"Barlow", "scopus_author_id"=>"7004651861"}, {"first_name"=>"Ophir D.", "last_name"=>"Klein", "scopus_author_id"=>"8917319700"}], "year"=>2011, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537390", "scopus"=>"2-s2.0-79959853521", "sgr"=>"79959853521", "pui"=>"362058282", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"21655085", "doi"=>"10.1371/journal.pgen.1002098"}, "id"=>"6b182355-45f3-3359-8e66-97f3da37ea66", "abstract"=>"The sense of taste is fundamental to our ability to ingest nutritious substances and to detect and avoid potentially toxic ones. Sensory taste buds are housed in papillae that develop from epithelial placodes. Three distinct types of gustatory papillae reside on the rodent tongue: small fungiform papillae are found in the anterior tongue, whereas the posterior tongue contains the larger foliate papillae and a single midline circumvallate papilla (CVP). Despite the great variation in the number of CVPs in mammals, its importance in taste function, and its status as the largest of the taste papillae, very little is known about the development of this structure. Here, we report that a balance between Sprouty (Spry) genes and Fgf10, which respectively antagonize and activate receptor tyrosine kinase (RTK) signaling, regulates the number of CVPs. Deletion of Spry2 alone resulted in duplication of the CVP as a result of an increase in the size of the placode progenitor field, and Spry1(-/-);Spry2(-/-) embryos had multiple CVPs, demonstrating the redundancy of Sprouty genes in regulating the progenitor field size. By contrast, deletion of Fgf10 led to absence of the CVP, identifying FGF10 as the first inductive, mesenchyme-derived factor for taste papillae. Our results provide the first demonstration of the role of epithelial-mesenchymal FGF signaling in taste papilla development, indicate that regulation of the progenitor field size by FGF signaling is a critical determinant of papilla number, and suggest that the great variation in CVP number among mammalian species may be linked to levels of signaling by the FGF pathway.", "link"=>"http://www.mendeley.com/research/fgf-signaling-regulates-number-posterior-taste-papillae-controlling-progenitor-field-size", "reader_count"=>35, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>11, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>3, "Student > Master"=>3, "Student > Bachelor"=>3, "Lecturer"=>2, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>11, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>3, "Student > Master"=>3, "Student > Bachelor"=>3, "Lecturer"=>2, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>21, "Medicine and Dentistry"=>5, "Neuroscience"=>4, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1, "Australia"=>1, "Germany"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/769319"], "description"=>"<p>(A–C) Expression of <i>Spry1</i>, <i>Spry2</i>, and <i>Spry4</i> in the CV placode of wild-type mice. (D,E) Expression of <i>Etv5</i> in the CV placode of wild-type and <i>Spry2</i><sup>−/−</sup> mice. (F) qPCR analysis of the expression profiles of <i>Etv5</i> and Sprouty genes in the posterior tongue of wild-type and <i>Spry2</i><sup>−/−</sup> mice at E12.5. Scale bar, 20 µm. **, p<0.001.</p>", "links"=>[], "tags"=>["co-expressed", "cv", "placode", "fgf", "signaling"], "article_id"=>439680, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g004", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spry1_and_Spry2_are_co_expressed_in_the_CV_placode_and_increased_FGF_signaling_is_detected_in_Spry2_mutants_/439680", "title"=>"<i>Spry1</i> and <i>Spry2</i> are co-expressed in the CV placode and increased FGF signaling is detected in <i>Spry2</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:41:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/769232"], "description"=>"<p>(A–H) Dorsal view of the expression of <i>Sox2</i>, <i>Shh</i>, <i>Bmp7</i>, and <i>Wnt10b</i> in wild-type and <i>Spry2</i><sup>−/−</sup> littermates. Scale bar, 50 µm. (A'–H') Coronal sections of A–H. Scale bar, 50 µm. (I,J) Sagittal views of the CV placodes stained with E-cadherin show an expansion of the placode in the anterior(A)-posterior(P) orientation in <i>Spry2</i><sup>−/−</sup> mice. Scale bar, 20 µm. (K) Quantification of the total number of cells in the CV placode. (L,M) Proliferating cells were detected by PCNA staining in coronal view. Scale bar, 20 µm. (N) The percentage of PCNA-positive cells in the CV placode at E12.5. * p<0.01. WT, wild-type; <i>S2</i><sup>−/−</sup>, <i>Spry2</i><sup>−/−</sup>.</p>", "links"=>[], "tags"=>["cv", "progenitor", "expanded"], "article_id"=>439601, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_CV_progenitor_field_at_E12_5_is_expanded_in_Spry2_8722_8722_mice_/439601", "title"=>"The CV progenitor field at E12.5 is expanded in <i>Spry2</i><sup>−/−</sup> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:40:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/769475"], "description"=>"<p>(A,B,F,G) Dorsal views of the expression patterns of <i>Etv5</i> and <i>Sox2</i> in <i>Spry1<sup>+/−</sup></i>;<i>Spry2<sup>+/−</sup></i> (DHet) and DKO mice. (C,H) Multiple CVPs in the anterio-posterior direction were observed in DKO mice visualized by E-cadherin immunofluorescence staining (<i>arrowheads</i>). Scale bar, 50 µm. (D,I) H&E staining of coronal sections through the CVP as indicated by dashed lines in C and H. Scale bar, 25 µm. (E,J) Multiple, presumptive CVPs visualized by SEM are indicated by dashed circles. Scale bar, 50 µm.</p>", "links"=>[], "tags"=>["cvps"], "article_id"=>439844, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g006", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Formation_of_multiple_CVPs_in_Spry1_8722_8722_Spry2_8722_8722_DKO_mice_/439844", "title"=>"Formation of multiple CVPs in <i>Spry1<sup>−/−</sup></i>;<i>Spry2<sup>−/−</sup></i> (DKO) mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:44:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/769379"], "description"=>"<p>(A–B') Expression of <i>Fgf10</i> in the CV placode of wild-type mice (arrowhead). Dashed line depicts the coronal plane of section for A' and B'. (C–F) Expression of FGF receptors (<i>Fgfr1-4</i>) in coronal sections. (G–I”) Genetic rescue of the loss of CVP phenotype in <i>Fgf10<sup>−/−</sup></i> mice (H) by deletion of <i>Spry2</i> (I) as visualized by E-cadherin immunofluorescence staining. (G'–I') Higher magnification views of boxed areas. (G”–I”) H&E staining of coronal sections through the CVP. Scale bars, 25 µm.</p>", "links"=>[], "tags"=>["cvp", "antagonized"], "article_id"=>439750, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g005", "stats"=>{"downloads"=>4, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fgf10_is_required_for_CVP_development_and_is_antagonized_by_Spry2_/439750", "title"=>"<i>Fgf10</i> is required for CVP development and is antagonized by <i>Spry2</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:42:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/386517", "https://ndownloader.figshare.com/files/386550", "https://ndownloader.figshare.com/files/386580", "https://ndownloader.figshare.com/files/386597", "https://ndownloader.figshare.com/files/386618", "https://ndownloader.figshare.com/files/386644", "https://ndownloader.figshare.com/files/386687"], "description"=>"<div><p>The sense of taste is fundamental to our ability to ingest nutritious substances and to detect and avoid potentially toxic ones. Sensory taste buds are housed in papillae that develop from epithelial placodes. Three distinct types of gustatory papillae reside on the rodent tongue: small fungiform papillae are found in the anterior tongue, whereas the posterior tongue contains the larger foliate papillae and a single midline circumvallate papilla (CVP). Despite the great variation in the number of CVPs in mammals, its importance in taste function, and its status as the largest of the taste papillae, very little is known about the development of this structure. Here, we report that a balance between Sprouty (Spry) genes and <em>Fgf10</em>, which respectively antagonize and activate receptor tyrosine kinase (RTK) signaling, regulates the number of CVPs. Deletion of <em>Spry2</em> alone resulted in duplication of the CVP as a result of an increase in the size of the placode progenitor field, and <em>Spry1<sup>−/−</sup></em>;<em>Spry2<sup>−/−</sup></em> embryos had multiple CVPs, demonstrating the redundancy of Sprouty genes in regulating the progenitor field size. By contrast, deletion of <em>Fgf10</em> led to absence of the CVP, identifying FGF10 as the first inductive, mesenchyme-derived factor for taste papillae. Our results provide the first demonstration of the role of epithelial-mesenchymal FGF signaling in taste papilla development, indicate that regulation of the progenitor field size by FGF signaling is a critical determinant of papilla number, and suggest that the great variation in CVP number among mammalian species may be linked to levels of signaling by the FGF pathway.</p> </div>", "links"=>[], "tags"=>["fgf", "signaling", "regulates", "posterior", "papillae", "controlling", "progenitor"], "article_id"=>136294, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002098.s001", "https://dx.doi.org/10.1371/journal.pgen.1002098.s002", "https://dx.doi.org/10.1371/journal.pgen.1002098.s003", "https://dx.doi.org/10.1371/journal.pgen.1002098.s004", "https://dx.doi.org/10.1371/journal.pgen.1002098.s005", "https://dx.doi.org/10.1371/journal.pgen.1002098.s006", "https://dx.doi.org/10.1371/journal.pgen.1002098.s007"], "stats"=>{"downloads"=>32, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/FGF_Signaling_Regulates_the_Number_of_Posterior_Taste_Papillae_by_Controlling_Progenitor_Field_Size/136294", "title"=>"FGF Signaling Regulates the Number of Posterior Taste Papillae by Controlling Progenitor Field Size", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-06-02 01:44:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/769028"], "description"=>"<p>(A) Cartoon showing location of gustatory papillae in the rodent tongue. (B,C) <i>In situ</i> hybridization staining of <i>Shh.</i> Wild-type mice possess a single CVP in the posterior tongue, whereas the CVP is duplicated in <i>Spry2<sup>−/−</sup></i> mice (<i>arrowheads</i>). (D,E) SEM images of the tongue at E14.5. Scale bar, 500 µm. (F,G) DAPI fluorescence staining shows that the two CVPs (<i>arrowheads</i>) persist into adulthood in <i>Spry2<sup>−/−</sup></i> mice. (D'-G') Higher magnification images of boxed areas. (D',E') Scale bar, 25 µm.</p>", "links"=>[], "tags"=>["leads", "duplication", "cvp", "posterior"], "article_id"=>439385, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_Spry2_leads_to_a_duplication_of_the_CVP_in_the_posterior_tongue_/439385", "title"=>"Deletion of <i>Spry2</i> leads to a duplication of the CVP in the posterior tongue.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:36:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/769131"], "description"=>"<p>(Inset) Cartoon depicting the planes of observation. (A–N) E-cadherin (E-CAD) immunofluorescence staining of CV placodes and papillae in wild-type (A–G) and <i>Spry2<sup>−/−</sup></i> (H-N) mice. (O–X) H&E stains of coronal sections of the single CV placode and papilla in wild-type and the proximal CV placode and papilla in <i>Spry2<sup>−/−</sup></i> mice. The size of the papilla was quantified between E13 to E14 (D–F, K–M; ×10<sup>−3</sup> um). <i>Arrowheads</i> indicate developing trenches. Scale bars, 50 µm.</p>", "links"=>[], "tags"=>["cvp", "wild-type"], "article_id"=>439497, "categories"=>["Developmental Biology", "Evolutionary Biology"], "users"=>["Camille I. Petersen", "Andrew H. Jheon", "Pasha Mostowfi", "Cyril Charles", "Saunders Ching", "Shoba Thirumangalathu", "Linda A. Barlow", "Ophir D. Klein"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002098.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Development_of_the_CVP_in_wild_type_and_Spry2_8722_8722_mice_/439497", "title"=>"Development of the CVP in wild-type and <i>Spry2<sup>−/−</sup></i> mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-06-02 02:38:17"}

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