Mutations in the Human naked cuticle Homolog NKD1 Found in Colorectal Cancer Alter Wnt/Dvl/β-Catenin Signaling
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{"title"=>"Mutations in the human naked cuticle homolog NKD1 found in colorectal cancer alter Wnt/Dvl/β-catenin signaling", "type"=>"journal", "authors"=>[{"first_name"=>"Jianhui", "last_name"=>"Guo", "scopus_author_id"=>"7404483916"}, {"first_name"=>"Tolga", "last_name"=>"Cagatay", "scopus_author_id"=>"6602615854"}, {"first_name"=>"Guangjin", "last_name"=>"Zhou", "scopus_author_id"=>"57199877509"}, {"first_name"=>"Chih Chiang", "last_name"=>"Chan", "scopus_author_id"=>"14625839200"}, {"first_name"=>"Shelby", "last_name"=>"Blythe", "scopus_author_id"=>"26640240600"}, {"first_name"=>"Kaye", "last_name"=>"Suyama", "scopus_author_id"=>"7102249673"}, {"first_name"=>"Li", "last_name"=>"Zheng", "scopus_author_id"=>"57199126262"}, {"first_name"=>"Kaifeng", "last_name"=>"Pan", "scopus_author_id"=>"57197438560"}, {"first_name"=>"Chiping", "last_name"=>"Qian", "scopus_author_id"=>"7202310660"}, {"first_name"=>"Richard", "last_name"=>"Hamelin", "scopus_author_id"=>"7006877253"}, {"first_name"=>"Stephen N.", "last_name"=>"Thibodeau", "scopus_author_id"=>"34573421500"}, {"first_name"=>"Peter S.", "last_name"=>"Klein", "scopus_author_id"=>"7402598214"}, {"first_name"=>"Keith A.", "last_name"=>"Wharton", "scopus_author_id"=>"7005784459"}, {"first_name"=>"Wanguo", "last_name"=>"Liu", "scopus_author_id"=>"7407338830"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-71049160060", "sgr"=>"71049160060", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0007982", "pmid"=>"19956716", "isbn"=>"1932-6203", "pui"=>"355735302"}, "id"=>"bb1fa746-9e28-37f0-9adf-ae7845296e8b", "abstract"=>"BACKGROUND: Mutation of Wnt signal antagonists Apc or Axin activates beta-catenin signaling in many cancers including the majority of human colorectal adenocarcinomas. The phenotype of apc or axin mutation in the fruit fly Drosophila melanogaster is strikingly similar to that caused by mutation in the segment-polarity gene, naked cuticle (nkd). Nkd inhibits Wnt signaling by binding to the Dishevelled (Dsh/Dvl) family of scaffold proteins that link Wnt receptor activation to beta-catenin accumulation and TCF-dependent transcription, but human NKD genes have yet to be directly implicated in cancer.\n\nMETHODOLOGY/PRINCIPAL FINDINGS: We identify for the first time mutations in NKD1--one of two human nkd homologs--in a subset of DNA mismatch repair-deficient colorectal tumors that are not known to harbor mutations in other Wnt-pathway genes. The mutant Nkd1 proteins are defective at inhibiting Wnt signaling; in addition, the mutant Nkd1 proteins stabilize beta-catenin and promote cell proliferation, in part due to a reduced ability of each mutant Nkd1 protein to bind and destabilize Dvl proteins.\n\nCONCLUSIONS/SIGNIFICANCE: Our data raise the hypothesis that specific NKD1 mutations promote Wnt-dependent tumorigenesis in a subset of DNA mismatch-repair-deficient colorectal adenocarcinomas and possibly other Wnt-signal driven human cancers.", "link"=>"http://www.mendeley.com/research/mutations-human-naked-cuticle-homolog-nkd1-found-colorectal-cancer-alter-wntdvl%CE%B2catenin-signaling", "reader_count"=>25, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>6, "Student > Ph. D. Student"=>4, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>6, "Student > Ph. D. Student"=>4, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/874238"], "description"=>"<p>(A) Wild-type, <i>axin, apc</i>, and <i>nkd Drosophila</i> cuticles. Wild type has alternating denticle bands (arrow) and naked cuticle (arrowhead), with each mutant lacking denticle bands. (B) <i>NKD1</i> locus has 10 exons. Nkd1 schematic (orange) includes N-terminal myristoylation, EFX, 30aa (blue), and carboxy-terminal His-rich motifs. Exon 10 sequences around poly-(C) tracts (red) above native (black) and mutant (blue) residues are shown. (C) <i>NKD1</i> electropherograms showing wild-type (WT) poly-(C)<sub>7</sub>, cell line TC7 with C-deletion (C6), cell line RKO with C-insertion (C8), and cell line HCT15 with G>A mutation (arrow) 3′ of poly-(C)<sub>7</sub>. (D, E) α-Nkd1 blots of whole cell extracts (D) and Triton X-100 soluble and insoluble fractions (E) from cell lines with indicated <i>NKD1</i> mutation. Arrows designate Nkd1 proteins. β-actin is loading control in D. CCD841 has full length Nkd1, with a minor degradation product at ∼35 kDa also seen with transfected <i>NKD1</i> (e.g. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone-0007982-g001\" target=\"_blank\">Fig. 1E</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone-0007982-g005\" target=\"_blank\">5C</a>), whereas SW480 with more abundant but wild-type Nkd1 has several degradation products.</p>", "links"=>[], "tags"=>["mutations"], "article_id"=>544673, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g001", "stats"=>{"downloads"=>2, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nkd_mutations_in_fly_and_human_/544673", "title"=>"<i>Nkd</i> mutations in fly and human.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:42:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/874359"], "description"=>"<p>(A) % <i>Xenopus</i> embryos with indicated axis phenotype after injection of <i>XWnt8</i>+/−wild-type or mutant <i>NKD1</i>. (n) = # embryos injected. Panels at right show representative lateral (L) and dorsal (D) views of embryos scored as single axis (white), short A/P axis (light gray), partial axis duplication (dark gray), and full axis duplication (black) according to the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#s4\" target=\"_blank\">Materials and Methods</a>. In embryos with single axis in the left panels, note trunk (white arrow) and cement gland (black arrow). Arrowheads designate each axis in embryos with axis duplications (right panels). Embryos with partial axis duplication have duplicated trunk tissue but a single cement gland, while embryos with full axis duplication have duplicated trunk tissues and cement glands. (B) Normalized TOPflash luciferase activity (RLU) in HEK-293 cells transfected with reporter +/−Dvl2 +/− indicated Nkd1 construct.</p>", "links"=>[], "tags"=>["nkd1", "mutant", "inhibits"], "article_id"=>544787, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wild_type_Nkd1_but_not_mutant_Nkd1_inhibits_Wnt_946_catenin_signaling_/544787", "title"=>"Wild-type Nkd1 but not mutant Nkd1 inhibits Wnt/β-catenin signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:42:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/874752"], "description"=>"<p>(A) Y2H between Nkd1-baits and Dvl-prey assayed for growth on triple dropout (3D+3AT) or double dropout (2D) media. Bar graphs on right show ONPG units from quantitative Y2H assay. Western blot indicates that Nkd1 mutant proteins are of comparable abundance (not shown). (B) GST-pulldown assay of <i>in vitro</i> translated, <sup>35</sup>[S]-labelled Dvl1-3 with each GST-Nkd1 protein. Bar graph is quantitative band intensity. Coomassie-stained gel shows each GST-fusion protein, with arrowheads indicating full-length proteins. (C) Western blots of Flag-IPs from HEK-293 cell extracts with equal amounts of each HA/Flag-tagged Nkd1, and then probed with α-HA (upper) and α-Dvl3 (middle). β-actin is loading control (lower). Note that less Dvl3 is IP'd by Nkd1<sup>C6</sup> or Nkd1<sup>C8</sup> as compared to full-length Nkd1. No co-IP was observed between wild-type or mutant Nkd1s and Dvl1 or Dvl2, reminiscent of the lack of stable co-IP between <i>Drosophila</i> Nkd and Dsh <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone.0007982-Rousset1\" target=\"_blank\">[13]</a>.</p>", "links"=>[], "tags"=>["nkd1", "proteins", "reduced"], "article_id"=>545185, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g005", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutant_Nkd1_proteins_exhibit_reduced_Dsh_Dvl_associations_/545185", "title"=>"Mutant Nkd1 proteins exhibit reduced Dsh/Dvl associations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:44:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/875021"], "description"=>"<p><i>NKD1, AXIN2, TCF7L2, CTNNB1</i>, and <i>APC</i> gene mutation status in 40 MSI-CRC tumors (top) and 11 cell lines (bottom). Key: −, no lesion; ins, nucleotide insertion; del, nucleotide deletion; /−, allelic deletion. For <i>NKD1</i> and <i>AXIN2</i>, mutation in indicated nucleotide is designated, while for <i>TCF7L2</i> the status of the poly(A) tract (A8–wild-type; A9–mutant) is designated. <i>CTNNB1</i> exon-3 was screened for activating mutations (M). For <i>APC</i>, tumors positive for protein-truncation (T) are indicated <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone.0007982-Powell1\" target=\"_blank\">[45]</a>. Presence (+) or absence (−) of <i>APC</i> and <i>CTNNB1</i> lesions in each cell line is as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone.0007982-Gayet1\" target=\"_blank\">[48]</a>.</p>", "links"=>[], "tags"=>["lesions", "msi", "colon", "tumors"], "article_id"=>545449, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.t001", "stats"=>{"downloads"=>3, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Wnt_pathway_genetic_lesions_in_MSI_colon_tumors_and_cell_lines_/545449", "title"=>"Wnt-pathway genetic lesions in MSI colon tumors and cell lines.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 03:46:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/874888"], "description"=>"<p>(A–A″) <i>71B-Gal4/UAS-Nkd<sup>GFP</sup></i> third-instar <i>Drosophila</i> salivary gland stained with α-Dsh and imaged for GFP (A) and Dsh (A′) distributions (merged image in A″). Quantitation of Dsh pixel intensity (white box in A′) reveals reduced staining in cell expressing more (right, green asterisk) Nkd<sup>GFP</sup> than in adjacent cell expressing less Nkd<sup>GFP</sup>. (B) Western blots of HEK-293 cells transfected with indicated Flag/HA-tagged Nkd1 and Dvl1, Dvl2, or Dvl3 constructs probed with α-HA, α-Dvl1-3, and α-βtubulin as a loading control. Each of the Dvl1-3 blots was loaded with equal amounts of extract, as confirmed by probing each blot with α-βtubulin. (C) HEK-293 cells co-expressing Nkd1<sup>GFP</sup> and Dvl1, stained with α-Dvl1, and imaged for GFP (green), Dvl1 (red), and DNA (blue) showing fine punctate Dvl1 distribution in cells expressing low to absent Nkd1<sup>GFP</sup> (white arrow). In adjacent cells expressing Nkd1<sup>GFP</sup>, Dvl1 is relocalized to Nkd1<sup>GFP</sup>/Dvl1 aggregates (yellow arrow), with loss of fine punctate Dvl1 staining (arrowheads). (D, E) Models of Nkd function in <i>Drosophila</i> (D) and <i>NKD1</i>-mutant CRC (E). Double lines: upper = plasma membrane; lower = nuclear membrane. (D) Fly Wg(Wnt) binds Fz/Arrow(Lrp5/6) receptors, which inhibits the Apc/Axin/CK1/GSK3β complex that promotes degradation of Arm(β-catenin). Arm complexes with Pan(TCF) to activate target genes including <i>nkd</i>. Nkd promotes Dsh turnover to partially inhibit signaling, and employs the nuclear import factor Imp-α3 to enter the nucleus and further inhibit signaling through unknown mechanisms <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0007982#pone.0007982-Chan3\" target=\"_blank\">[31]</a>. (E) In <i>NKD1</i>-mutant CRC, the mutant Nkd1 protein no longer binds and promotes Dvl turnover, stabilizing β-catenin and activating TCF-dependent transcription of target genes.</p>", "links"=>[], "tags"=>["nkd1s", "abundance"], "article_id"=>545323, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g006", "stats"=>{"downloads"=>2, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutant_Nkd1s_do_not_limit_the_abundance_of_Dsh_Dvl_as_well_as_wild_type_Nkd1_/545323", "title"=>"Mutant Nkd1s do not limit the abundance of Dsh/Dvl as well as wild type Nkd1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:45:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/874462"], "description"=>"<p>(A) Western blot of cytosolic and nuclear extracts of cells with wild-type (CCD841) or mutant (Co115) <i>NKD1</i>. GAPDH and HDAC2 were probed as loading controls. (B–B″, C–C″) β-catenin (red) and DNA (blue) distribution in CCD841 cells (B–B″) and Co115 (C–C″) cells. Arrows designate nuclei. Merged images in B″ and C″. (D) Western blot of cytosolic extracts of HEK-293 cells transfected with <i>lacZ</i> control (-), wild type Nkd1 (WT), or indicated mutant Nkd1 construct, and probed for β-catenin, Nkd1, and loading control GAPDH. Note that each mutant Nkd1 but not wild type Nkd1 increases β-catenin levels. (E) Relative cell number as a function of days post retroviral infection of CCD841 cells with empty vector control, wild type Nkd1, or indicated Nkd1 mutant (p = 0.016, 0.012, and 0.0091 for C6, C8, and R288H mutants as compared to control) (F) Relative cell number as a function of days post retroviral infection of Co115 cells with control or wild-type Nkd1 (p = 0.022). α-Nkd1 western blots of cell extracts, with GAPDH or β-actin loading control, are shown below each plot in E and F.</p>", "links"=>[], "tags"=>["cell biology/cell signaling", "developmental biology/pattern formation", "oncology/gastrointestinal cancers"], "article_id"=>544887, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_NKD1_mutations_on_catenin_and_cell_proliferation_/544887", "title"=>"Effect of <i>NKD1</i>-mutations on β-catenin and cell proliferation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:43:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/874595"], "description"=>"<p>(A, B) HEK-293 cells expressing HA/Flag-tagged Nkd1 (A) or Nkd1<sup>C8</sup> (B) stained with α-HA (green). Nkd1 accumulates in puncta (arrows), while Nkd1<sup>C8</sup> is diffusely distributed in the cytoplasm. Nkd1<sup>C6</sup> distributed in a pattern similar to Nkd1<sup>C8</sup> (not shown). (C, D) Cells co-expressing Dvl3 and wild-type (C) or C8 (D) Nkd1<sup>GFP</sup> constructs. Nkd1-GFP (green, C) shows near complete colocalization (arrows) with Dvl3 (red, C′), while Nkd1<sup>C8</sup>-GFP (D) accumulates in cytoplasmic aggregates surrounded by Dvl3 (arrows). Merged images are in C″, D″, DNA is blue in A–D. Similar results were observed in cells coexpressing Nkd1<sup>C8</sup>-GFP and Dvl1 or Dvl2, and in cells expressing Nkd1<sup>C6</sup>-GFP and Dvl1, Dvl2, or Dvl3 (not shown). (E) Salivary gland from wild-type third instar <i>Drosophila</i> larva stained with α-Dsh (red) showing diffuse and punctate staining. (F–F″) <i>A8-Gal4/UAS-Nkd<sup>GFP</sup></i> salivary gland stained with α-Dsh and imaged for GFP (F) and Dsh (F′; merged in F″). Fly Nkd<sup>GFP</sup> relocalizes Dsh to perinuclear aggregates (arrows) similar to those observed with Nkd1<sup>GFP</sup>/Dvl3 in C.</p>", "links"=>[], "tags"=>["truncation", "alters", "subcellular", "localization", "dvl"], "article_id"=>545022, "categories"=>["Cancer", "Cell Biology", "Developmental Biology"], "users"=>["Jianhui Guo", "Tolga Cagatay", "Guangjin Zhou", "Chih-Chiang Chan", "Shelby Blythe", "Kaye Suyama", "Li Zheng", "Kaifeng Pan", "Chiping Qian", "Richard Hamelin", "Stephen N. Thibodeau", "Peter S. Klein", "Keith A. Wharton Jr", "Wanguo Liu"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0007982.g004", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nkd1_truncation_alters_subcellular_localization_and_Dvl_colocalization_/545022", "title"=>"Nkd1 truncation alters subcellular localization and Dvl colocalization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 03:44:02"}

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Relative Metric

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