Loss of Function Mutation in the Palmitoyl-Transferase HHAT Leads to Syndromic 46,XY Disorder of Sex Development by Impeding Hedgehog Protein Palmitoylation and Signaling
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{"title"=>"Loss of Function Mutation in the Palmitoyl-Transferase HHAT Leads to Syndromic 46,XY Disorder of Sex Development by Impeding Hedgehog Protein Palmitoylation and Signaling", "type"=>"journal", "authors"=>[{"first_name"=>"Patrick", "last_name"=>"Callier", "scopus_author_id"=>"15755398300"}, {"first_name"=>"Pierre", "last_name"=>"Calvel", "scopus_author_id"=>"16023900300"}, {"first_name"=>"Armine", "last_name"=>"Matevossian", "scopus_author_id"=>"53868220200"}, {"first_name"=>"Periklis", "last_name"=>"Makrythanasis", "scopus_author_id"=>"25635661200"}, {"first_name"=>"Pascal", "last_name"=>"Bernard", "scopus_author_id"=>"55729515700"}, {"first_name"=>"Hiroshi", "last_name"=>"Kurosaka", "scopus_author_id"=>"11839162500"}, {"first_name"=>"Anne", "last_name"=>"Vannier", "scopus_author_id"=>"56675985900"}, {"first_name"=>"Christel", "last_name"=>"Thauvin-Robinet", "scopus_author_id"=>"6601932328"}, {"first_name"=>"Christelle", "last_name"=>"Borel", "scopus_author_id"=>"7101710930"}, {"first_name"=>"Séverine", "last_name"=>"Mazaud-Guittot", "scopus_author_id"=>"8569649200"}, {"first_name"=>"Antoine", "last_name"=>"Rolland", "scopus_author_id"=>"16025538500"}, {"first_name"=>"Christèle", "last_name"=>"Desdoits-Lethimonier", "scopus_author_id"=>"36704698400"}, {"first_name"=>"Michel", "last_name"=>"Guipponi", "scopus_author_id"=>"6603864187"}, {"first_name"=>"Céline", "last_name"=>"Zimmermann", "scopus_author_id"=>"35729797600"}, {"first_name"=>"Isabelle", "last_name"=>"Stévant", "scopus_author_id"=>"55578147400"}, {"first_name"=>"Françoise", "last_name"=>"Kuhne", "scopus_author_id"=>"6701361814"}, {"first_name"=>"Béatrice", "last_name"=>"Conne", "scopus_author_id"=>"6602598914"}, {"first_name"=>"Federico", "last_name"=>"Santoni", "scopus_author_id"=>"55348710600"}, {"first_name"=>"Sandy", "last_name"=>"Lambert", "scopus_author_id"=>"37161765800"}, {"first_name"=>"Frederic", "last_name"=>"Huet", "scopus_author_id"=>"7102362043"}, {"first_name"=>"Francine", "last_name"=>"Mugneret", "scopus_author_id"=>"7003638547"}, {"first_name"=>"Jadwiga", "last_name"=>"Jaruzelska", "scopus_author_id"=>"7004109766"}, {"first_name"=>"Laurence", "last_name"=>"Faivre", "scopus_author_id"=>"56091934200"}, {"first_name"=>"Dagmar", "last_name"=>"Wilhelm", "scopus_author_id"=>"7006636008"}, {"first_name"=>"Bernard", "last_name"=>"Jégou", "scopus_author_id"=>"55953106900"}, {"first_name"=>"Paul A.", "last_name"=>"Trainor", "scopus_author_id"=>"7003894254"}, {"first_name"=>"Marilyn D.", "last_name"=>"Resh", "scopus_author_id"=>"7004407168"}, {"first_name"=>"Stylianos E.", "last_name"=>"Antonarakis", "scopus_author_id"=>"36049009800"}, {"first_name"=>"Serge", "last_name"=>"Nef", "scopus_author_id"=>"6603613020"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537404", "pui"=>"373197097", "pmid"=>"24784881", "isbn"=>"1553-7404 (Electronic) 1553-7390 (Linking)", "doi"=>"10.1371/journal.pgen.1004340", "sgr"=>"84901609380", "scopus"=>"2-s2.0-84901609380"}, "id"=>"4d49fcd4-c5d1-3042-8316-1723be9f3790", "abstract"=>"The Hedgehog (Hh) family of secreted proteins act as morphogens to control embryonic patterning and development in a variety of organ systems. Post-translational covalent attachment of cholesterol and palmitate to Hh proteins are critical for multimerization and long range signaling potency. However, the biological impact of lipid modifications on Hh ligand distribution and signal reception in humans remains unclear. In the present study, we report a unique case of autosomal recessive syndromic 46,XY Disorder of Sex Development (DSD) with testicular dysgenesis and chondrodysplasia resulting from a homozygous G287V missense mutation in the hedgehog acyl-transferase (HHAT) gene. This mutation occurred in the conserved membrane bound O-acyltransferase (MBOAT) domain and experimentally disrupted the ability of HHAT to palmitoylate Hh proteins such as DHH and SHH. Consistent with the patient phenotype, HHAT was found to be expressed in the somatic cells of both XX and XY gonads at the time of sex determination, and Hhat loss of function in mice recapitulates most of the testicular, skeletal, neuronal and growth defects observed in humans. In the developing testis, HHAT is not required for Sertoli cell commitment but plays a role in proper testis cord formation and the differentiation of fetal Leydig cells. Altogether, these results shed new light on the mechanisms of action of Hh proteins. Furthermore, they provide the first clinical evidence of the essential role played by lipid modification of Hh proteins in human testicular organogenesis and embryonic development.", "link"=>"http://www.mendeley.com/research/loss-function-mutation-palmitoyltransferase-hhat-leads-syndromic-46xy-disorder-sex-development-imped", "reader_count"=>33, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>10, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>2, "Student > Master"=>5, "Other"=>2, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>12, "Agricultural and Biological Sciences"=>8, "Medicine and Dentistry"=>8, "Chemistry"=>1, "Psychology"=>1, "Earth and Planetary Sciences"=>1, "Environmental Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>8}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Switzerland"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1481928"], "description"=>"<p>A) qRT-PCR analysis of <i>HHAT</i> and Hedgehog protein coding genes (<i>DHH</i>, <i>IHH</i> and <i>SHH</i>) expression in human fetal tissues at Gestation Week 9. B) qRT-PCR analysis reveals that HHAT is preferentially expressed in human Sertoli cells (SOX9-expressing cells) compared to Leydig cells (INSL3-expressing cells). C) Evaluation of the expression of <i>Hhat</i> (left panel) and Hedgehog genes (right panel) by qRT-PCR in mouse SF1<sup>+</sup> somatic cells from developing XY (blue bars) and XX (red bars) gonads. Legend: L, lung; H, Heart; I, Intestine; T, Tongue; K, Kidney; D, anterior limb digits.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "fetal", "post-natal"], "article_id"=>1013773, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.g002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/HHAT_is_widely_expressed_during_human_fetal_development_and_post_natal_life_/1013773", "title"=>"HHAT is widely expressed during human fetal development and post-natal life.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481927"], "description"=>"<p>A) The familial case presented here consists of two non-consanguineous individuals with two siblings affected with chondrodysplasia. The histological analysis of the dysgenetic gonads revealed the presence of few immature seminiferous tubules in both left (B) and right (C) gonads (arrowheads). D) Sanger sequencing of the proband and parental genomic DNA confirmed the parental origin of the G&gt;T substitution observed at position 860 of HHAT long isoform. E) The mutated Glycine 287 is conserved among vertebrates from zebrafish to humans, and is localized N-terminal to the 6th transmembrane domain of HHAT long isoform.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "mutation", "dsd"], "article_id"=>1013772, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.g001", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/HHAT_mutation_in_46_XY_DSD_with_chondrodysplasia_/1013772", "title"=>"HHAT mutation in 46,XY DSD with chondrodysplasia.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481936"], "description"=>"<p>MAF: Minimum Allele Frequency.</p><p>*Scores for the different pathogenicity prediction scores. For the splice variant NNSplice and ESEfinder were used instead of SIFT, PolyPhen2 and Mutation Taster.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "variants"], "article_id"=>1013781, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.t002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/List_of_variants_identified_for_the_different_models_tested_/1013781", "title"=>"List of variants identified for the different models tested.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481935"], "description"=>"<p>SNV: Single Nucleotide Variant.</p><p>*The target is the total protein coding sequence of the human genes according to RefSeq.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "variants"], "article_id"=>1013780, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.t001", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Number_of_reads_coverage_and_variants_identified_per_individual_/1013780", "title"=>"Number of reads, coverage and variants identified per individual.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481929"], "description"=>"<p>A) COS-1 cells were transfected with the indicated constructs and cell lysates were analyzed directly by Western blotting. B) COS-1 cells transfected with wild type or G287V HHAT-HA were fixed and processed for indirect immunofluoresence and stained with the antibodies indicated. C) COS-1 cells were transfected with the indicated HHAT construct and incubated in DMEM supplemented with 10% FBS, 100 µg/ml cyclohexamide, and 40 µg/ml chloramphenicol. At each indicated time point, cells were lysed and subjected to SDS-PAGE and Western blotting with anti-HA antibodies. The amount of HA signal at each time point was determined using GS-800 Calibrated Densitometer (BioRad). Experiments were carried out in duplicate and repeated three times. D) <i>In vitro</i> palmitoylation assay using SHH and membranes from cells expressing wild type or G287V HHAT. Top panel, incorporation of <sup>125</sup>I-iodopalmitate into SHH detected by phosphorimaging. Middle panel, Anti-SHH Western blot. Lower panel, Anti-HA Western blot. Experiments were carried out in duplicate and repeated three times. E) <i>In vitro</i> palmitoylation assay using DHH and membranes from cells expressing wild type or G287V HHAT. Top panel, incorporation of <sup>125</sup>I-iodopalmitate into DHH detected by phosphorimaging. Middle panel, Coomassie-staining of DHH. Lower panel, Anti-HA Western blot. Experiments were carried out in duplicate and repeated three times.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "mutation", "hhat"], "article_id"=>1013774, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.g003", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/G287V_mutation_results_in_loss_of_HHAT_activity_/1013774", "title"=>"G287V mutation results in loss of HHAT activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481937", "https://ndownloader.figshare.com/files/1481938", "https://ndownloader.figshare.com/files/1481939", "https://ndownloader.figshare.com/files/1481940"], "description"=>"<div><p>The Hedgehog (Hh) family of secreted proteins act as morphogens to control embryonic patterning and development in a variety of organ systems. Post-translational covalent attachment of cholesterol and palmitate to Hh proteins are critical for multimerization and long range signaling potency. However, the biological impact of lipid modifications on Hh ligand distribution and signal reception in humans remains unclear. In the present study, we report a unique case of autosomal recessive syndromic 46,XY Disorder of Sex Development (DSD) with testicular dysgenesis and chondrodysplasia resulting from a homozygous G287V missense mutation in the hedgehog acyl-transferase (<i>HHAT</i>) gene. This mutation occurred in the conserved membrane bound <i>O</i>-acyltransferase (MBOAT) domain and experimentally disrupted the ability of HHAT to palmitoylate Hh proteins such as DHH and SHH. Consistent with the patient phenotype, HHAT was found to be expressed in the somatic cells of both XX and XY gonads at the time of sex determination, and <i>Hhat</i> loss of function in mice recapitulates most of the testicular, skeletal, neuronal and growth defects observed in humans. In the developing testis, HHAT is not required for Sertoli cell commitment but plays a role in proper testis cord formation and the differentiation of fetal Leydig cells. Altogether, these results shed new light on the mechanisms of action of Hh proteins. Furthermore, they provide the first clinical evidence of the essential role played by lipid modification of Hh proteins in human testicular organogenesis and embryonic development.</p></div>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "mutation", "palmitoyl-transferase", "hhat", "leads", "syndromic", "impeding", "hedgehog", "palmitoylation"], "article_id"=>1013782, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>[nil, nil, nil, nil], "stats"=>{"downloads"=>33, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Loss_of_Function_Mutation_in_the_Palmitoyl_Transferase_HHAT_Leads_to_Syndromic_46_XY_Disorder_of_Sex_Development_by_Impeding_Hedgehog_Protein_Palmitoylation_and_Signaling/1013782", "title"=>"Loss of Function Mutation in the Palmitoyl-Transferase HHAT Leads to Syndromic 46,XY Disorder of Sex Development by Impeding Hedgehog Protein Palmitoylation and Signaling", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-05-01 03:54:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/1481933"], "description"=>"<p>A–F) H&amp;E staining of wild-type (WT) and <i>Hhat<sup>Creface/Creface</sup></i> mutant (Creface) XY gonads at E12.5 (A, B), E13.5 (C, D) and E15.5 (E, F). Note the reduction in testis size from E12.5 onward and the presence of dysgenetic testis cords (asterisk) with considerable variations in term of shape and size. Finally, the interstitial space (arrowhead) in the E13.5 and E15.5 mutant testes was abnormally dense and cellular in comparison of control mice testis. G–X) Expression of key testicular markers was assessed by double/single immunofluorescence at E12.5, E13.5 and E15.5 on both wild-type (WT) and <i>Hhat<sup>Creface/Creface</sup></i> mutant (Creface) XY gonads using either the Sertoli cell marker SOX9 (green) and the germ cell marker ECADH (red, G–L), the meiotic marker γH2AX (red) along with the germ cell marker MVH (green; M–R) or the Sertoli cell marker WT1 (green) with the Leydig cell marker CYP11A1 (red, S–X). Note the near complete absence of Leydig cells in mutant testes.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Sex determination", "Cell differentiation", "Cell fate determination", "genetics", "dysgenesis", "embryo", "lacking"], "article_id"=>1013778, "categories"=>["Biological Sciences"], "users"=>["Patrick Callier", "Pierre Calvel", "Armine Matevossian", "Periklis Makrythanasis", "Pascal Bernard", "Hiroshi Kurosaka", "Anne Vannier", "Christel Thauvin-Robinet", "Christelle Borel", "Séverine Mazaud-Guittot", "Antoine Rolland", "Christèle Desdoits-Lethimonier", "Michel Guipponi", "Céline Zimmermann", "Isabelle Stévant", "Françoise Kuhne", "Béatrice Conne", "Federico Santoni", "Sandy Lambert", "Fréderic Huet", "Francine Mugneret", "Jadwiga Jaruzelska", "Laurence Faivre", "Dagmar Wilhelm", "Bernard Jégou", "Paul A. Trainor", "Marilyn D. Resh", "Stylianos E. Antonarakis", "Serge Nef"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004340.g004", "stats"=>{"downloads"=>3, "page_views"=>49, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Testicular_dysgenesis_in_mouse_embryo_lacking_i_Hhat_i_/1013778", "title"=>"Testicular dysgenesis in mouse embryo lacking <i>Hhat</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-01 03:54:20"}

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