A Sulfated Glycosaminoglycan Linkage Region Is a Novel Type of Human Natural Killer-1 (HNK-1) Epitope Expressed on Aggrecan in Perineuronal Nets
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{"title"=>"A sulfated glycosaminoglycan linkage region is a novel type of human natural killer-1 (HNK-1) epitope expressed on aggrecan in perineuronal nets", "type"=>"journal", "authors"=>[{"first_name"=>"Keiko", "last_name"=>"Yabuno", "scopus_author_id"=>"56041968900"}, {"first_name"=>"Jyoji", "last_name"=>"Morise", "scopus_author_id"=>"45661637000"}, {"first_name"=>"Yasuhiko", "last_name"=>"Kizuka", "scopus_author_id"=>"8528697000"}, {"first_name"=>"Noritaka", "last_name"=>"Hashii", "scopus_author_id"=>"8205709700"}, {"first_name"=>"Nana", "last_name"=>"Kawasaki", "scopus_author_id"=>"7103017475"}, {"first_name"=>"Satoru", "last_name"=>"Takahashi", "scopus_author_id"=>"56132080000"}, {"first_name"=>"Shinji", "last_name"=>"Miyata", "scopus_author_id"=>"36789887800"}, {"first_name"=>"Tomomi", "last_name"=>"Izumikawa", "scopus_author_id"=>"6603604898"}, {"first_name"=>"Hiroshi", "last_name"=>"Kitagawa", "scopus_author_id"=>"7402625590"}, {"first_name"=>"Hiromu", "last_name"=>"Takematsu", "scopus_author_id"=>"7005425236"}, {"first_name"=>"Shogo", "last_name"=>"Oka", "scopus_author_id"=>"7201600782"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"607910304", "doi"=>"10.1371/journal.pone.0144560", "sgr"=>"84955483153", "scopus"=>"2-s2.0-84955483153", "pmid"=>"26659409"}, "id"=>"4e621ea2-b038-3bf5-9c14-7a57fb57fbfe", "abstract"=>"Human natural killer-1 (HNK-1) carbohydrate (HSO3-3GlcAβ1-3Galβ1-4GlcNAc-R) is highly expressed in the brain and required for learning and neural plasticity. We previously demonstrated that expression of the HNK-1 epitope is mostly abolished in knockout mice for GlcAT-P (B3gat1), a major glucuronyltransferase required for HNK-1 biosynthesis, but remained in specific regions such as perineuronal nets (PNNs) in these mutant mice. Considering PNNs are mainly composed of chondroitin sulfate proteoglycans (CSPGs) and regulate neural plasticity, GlcAT-P-independent expression of HNK-1 in PNNs is suggested to play a role in neural plasticity. However, the function, structure, carrier glycoprotein and biosynthetic pathway for GlcAT-P-irrelevant HNK-1 epitope remain unclear. In this study, we identified a unique HNK-1 structure on aggrecan in PNNs. To determine the biosynthetic pathway for the novel HNK-1, we generated knockout mice for GlcAT-S (B3gat2), the other glucuronyltransferase required for HNK-1 biosynthesis. However, GlcAT-P and GlcAT-S double-knockout mice did not exhibit reduced HNK-1 expression compared with single GlcAT-P-knockout mice, indicating an unusual biosynthetic pathway for the HNK-1 epitope in PNNs. Aggrecan was purified from cultured cells in which GlcAT-P and -S are not expressed and we determined the structure of the novel HNK-1 epitope using liquid chromatography/mass spectrometry (LC/MS) as a sulfated linkage region of glycosaminoglycans (GAGs), HSO3-GlcA-Gal-Gal-Xyl-R. Taken together, we propose a hypothetical model where GlcAT-I, the sole glucuronyltransferase required for synthesis of the GAG linkage, is also responsible for biosynthesis of the novel HNK-1 on aggrecan. These results could lead to discovery of new roles of the HNK-1 epitope in neural plasticity.", "link"=>"http://www.mendeley.com/research/sulfated-glycosaminoglycan-linkage-region-novel-type-human-natural-killer1-hnk1-epitope-expressed-ag", "reader_count"=>14, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>5, "Student > Master"=>1, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>1, "Student > Ph. D. Student"=>5, "Student > Master"=>1, "Student > Bachelor"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>5, "Neuroscience"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Netherlands"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2605020"], "description"=>"<p>(A) PA-labeled <i>O</i>-linked glycans were prepared from aggrecan-Fc co-expressed with HNK-1ST in COS-1 cells. The base peak chromatogram of the glycans was obtained using selected ion monitoring (SIM) (<i>m/z</i> 782.5–832.5) in the negative ion mode (<i>upper panel</i>). An extracted ion chromatogram (EIC) of the ion at <i>m/z</i> 807.0–807.4 (<i>lower panel</i>). (B) MS/MS spectra (<i>upper panel</i>) of the ion [M-H]<sup>-</sup> (<i>m/z</i> 807.2) detected in peak A and MS/MS/MS spectra (<i>lower panel</i>) of the predominant product ion (<i>m/z</i> 727.2) in the MS/MS. S, sulfate group; HexA, hexuronic acid; Hex, hexose; Xyl-PA, xylose labeled with 2-aminopyridine.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622176, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LC_MS_n_structural_analysis_of_HNK_1_epitope_on_aggrecan_/1622176", "title"=>"LC/MS<sup>n</sup> structural analysis of HNK-1 epitope on aggrecan.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605021"], "description"=>"<p>GlcAT-I is responsible for synthesis of a linkage region of GAG, which is usually further elongated into a long GAG chain (e.g., CS chain). HNK-1ST transfers a sulfate group to GlcA of the linkage region of aggrecan, which likely results in the expression of the linkage type HNK-1 epitope, HSO<sub>3</sub>-GlcA-Gal-Gal-Xyl, in PNNs. The expression of the HNK-1 epitope on aggrecan suppresses the CS polymerization that starts from GlcA of the linkage region.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622177, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g007", "stats"=>{"downloads"=>1, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Biosynthetic_model_for_HNK_1_epitope_on_aggrecan_in_PNNs_/1622177", "title"=>"Biosynthetic model for HNK-1 epitope on aggrecan in PNNs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605013"], "description"=>"<p>(A) Schematic diagram of the targeting construct. For targeted disruption of the mouse GlcAT-S gene (<i>B3gat2</i>), exon1 containing the initiation codon and transmembrane region were replaced with a neo/lacZ cassette. Hatched lines represent the fragments used for the construction of the targeting vector. PCR primers used for screening are shown in arrowheads. Black bars indicate probes for Southern blot analysis. (B) Southern blot analysis of targeted ES cell clones. Genomic DNA isolated from ES cell clones were digested with PstI or SpeI and EcoRV, blotted and then hybridized with the 3’ or 5’ probe, respectively. The expected sizes of the WT allele and targeted allele (KO) are indicated. The ES clones, 6, 29, 37, 62, 116, 127, 203 and 258 were positive when screening using PCR. ES clone 115 was used as a negative control. (C) Western blot analysis of SKO mice. The membrane proteins were prepared from 6-week-old mouse kidneys (WT; +/+, heterozygote; +/-, homozygote; -/-). A non-sulfated form of HNK-1 epitope was detected with M6749 mAb.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622169, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Generation_of_GlcAT_S_deficient_mice_/1622169", "title"=>"Generation of GlcAT-S-deficient mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605014"], "description"=>"<p>(A, B) Soluble fractions prepared from 2- and 6-week-old mouse brains (WT and GlcAT-P-deficient mice) were treated with chABC with or without PNGase F, subjected to SDS-PAGE and then blotted using anti-HNK-1 mAb, 6B4 mAb, Cat-315 mAb, phosphacan pAb and aggrecan pAb. To compare the molecular weight of HNK-1 immunoreactive band with aggrecan or phosphacan, an HNK-1 mAb blot of 6-week-old PKO mice treated with chABC and PNGase F is shown on the right of the aggrecan panel. (C) Using urea-soluble fractions from 6-week-old PKO mouse brains (input), aggrecan was immunoprecipitated using aggrecan pAb (IP: aggrecan) or normal rabbit IgG (IP: IgG). The precipitated aggrecan was subjected to SDS-PAGE and western blotting with HNK-1, 6B4, Cat-315 and aggrecan antibodies.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622170, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HNK_1_carbohydrate_epitope_expressed_in_GlcAT_P_deficient_mice_/1622170", "title"=>"HNK-1 carbohydrate epitope expressed in GlcAT-P-deficient mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605015"], "description"=>"<p>Sagittal sections of cerebral cortex from 6-week-old WT (A-C) and PKO mice (D-L) were singly (for WT) or doubly (for PKO) immunostained with HNK-1 mAb (A, D), 6B4 mAb (B, G), or Cat-315 mAb (C, J), and aggrecan pAb (E, H, K). F, I and L are overlaid images. High magnification images of HNK-1-, 6B4- or Cat-315- and aggrecan-positive PNNs are shown in the insets. Scale bars, 200 μm (A-C), 100 μm (D-L) and 20 μm (insets).</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622171, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HNK_1_carbohydrate_and_aggrecan_are_expressed_in_the_PNNs_/1622171", "title"=>"HNK-1 carbohydrate and aggrecan are expressed in the PNNs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605017"], "description"=>"<p>(A) Soluble fractions from 6-week-old GlcAT-P-deficient mice (PKO) and GlcAT-P and -S double deficient mice (DKO) were treated with chABC and PNGase F, subjected to SDS-PAGE and blotted using HNK-1 mAb, 6B4 mAb, Cat-315 mAb, aggrecan pAb, phosphacan pAb, H28 (NCAM mAb) or actin mAb. The effect of PNGase F treatment was confirmed by western blotting with H28 mAb. Actin was used as the loading control. (B) Using soluble fractions from 6-week-old DKO mouse brains (input), aggrecan and phosphacan were immunoprecipitated with aggrecan pAb (IP: aggrecan), normal rabbit IgG (IP: IgG) or phosphacan pAb (IP: phosphacan). The precipitated aggrecan and phosphacan were subjected to SDS-PAGE and western blotting with HNK-1, aggrecan and phosphacan antibodies. (C-N) Sagittal sections of cerebral cortex from 6-week-old PKO (C-E) and DKO mice (F-N) were double-immunostained with HNK-1 mAb, 6B4 mAb or Cat-315 mAb (<i>red</i>) and WFA lectin (<i>green</i>). Scale bar, 100 μm.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622173, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HNK_1_carbohydrate_expressed_in_PKO_and_DKO_mice_/1622173", "title"=>"HNK-1 carbohydrate expressed in PKO and DKO mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2605019"], "description"=>"<p>(A) Schematic diagram of the Fc-tagged short aggrecan used in this study. (B) Aggrecan-Fc with or without HNK-1ST was heterologously expressed into COS-1 cells. Aggrecan-Fc in the culture medium was purified using a Protein G Sepharose column and digested with 100 μU/ml chABC and then blotted with anti-Fc pAb, HNK-1 mAb and anti-CS antibodies (CS56 and clone IIH6). (C) Aggrecan-Fc and/or phosphacan-myc-Fc were transiently expressed with HNK-1ST-EGFP into COS-1 cells. Aggrecan-Fc and phosphacan-myc-Fc in the culture medium were precipitated with ethanol and digested with 200 μU/ml chABC, subjected to SDS-PAGE and then blotted with anti-Fc pAb, HNK-1 mAb, aggrecan pAb and phosphacan pAb.</p>", "links"=>[], "tags"=>["gag", "cspg", "novel HNK", "Knockout mice", "epitope", "Sulfated Glycosaminoglycan Linkage Region", "sulfated linkage region", "hso", "Perineuronal Nets Human", "Human Natural Killer", "chondroitin sulfate proteoglycans", "biosynthetic pathway", "B 3gat", "lc", "pnn"], "article_id"=>1622175, "categories"=>["Biological Sciences"], "users"=>["Keiko Yabuno", "Jyoji Morise", "Yasuhiko Kizuka", "Noritaka Hashii", "Nana Kawasaki", "Satoru Takahashi", "Shinji Miyata", "Tomomi Izumikawa", "Hiroshi Kitagawa", "Hiromu Takematsu", "Shogo Oka"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0144560.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_a_novel_HNK_1_epitope_on_aggrecan_in_COS_1_cells_/1622175", "title"=>"Expression of a novel HNK-1 epitope on aggrecan in COS-1 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-12-10 10:30:15"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"7", "full-text"=>"8", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"12", "full-text"=>"15", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"7", "full-text"=>"5", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"14", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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