Angelman Syndrome Protein UBE3A Interacts with Primary Microcephaly Protein ASPM, Localizes to Centrosomes and Regulates Chromosome Segregation
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{"title"=>"Angelman syndrome protein UBE3A interacts with primary microcephaly protein ASPM, localizes to centrosomes and regulates chromosome segregation", "type"=>"journal", "authors"=>[{"first_name"=>"Pooja", "last_name"=>"Singhmar", "scopus_author_id"=>"57189531495"}, {"first_name"=>"Arun", "last_name"=>"Kumar", "scopus_author_id"=>"55547117257"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21633703", "sgr"=>"79957465439", "doi"=>"10.1371/journal.pone.0020397", "scopus"=>"2-s2.0-79957465439", "pui"=>"361822305", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"19326203"}, "id"=>"43b7f485-224f-3286-b059-9f6408115f1b", "abstract"=>"Many proteins associated with the phenotype microcephaly have been localized to the centrosome or linked to it functionally. All the seven autosomal recessive primary microcephaly (MCPH) proteins localize at the centrosome. Microcephalic osteodysplastic primordial dwarfism type II protein PCNT and Seckel syndrome (also characterized by severe microcephaly) protein ATR are also centrosomal proteins. All of the above findings show the importance of centrosomal proteins as the key players in neurogenesis and brain development. However, the exact mechanism as to how the loss-of-function of these proteins leads to microcephaly remains to be elucidated. To gain insight into the function of the most commonly mutated MCPH gene ASPM, we used the yeast two-hybrid technique to screen a human fetal brain cDNA library with an ASPM bait. The analysis identified Angelman syndrome gene product UBE3A as an ASPM interactor. Like ASPM, UBE3A also localizes to the centrosome. The identification of UBE3A as an ASPM interactor is not surprising as more than 80% of Angelman syndrome patients have microcephaly. However, unlike in MCPH, microcephaly is postnatal in Angelman syndrome patients. Our results show that UBE3A is a cell cycle regulated protein and its level peaks in mitosis. The shRNA knockdown of UBE3A in HEK293 cells led to many mitotic abnormalities including chromosome missegregation, abnormal cytokinesis and apoptosis. Thus our study links Angelman syndrome protein UBE3A to ASPM, centrosome and mitosis for the first time. We suggest that a defective chromosome segregation mechanism is responsible for the development of microcephaly in Angelman syndrome.", "link"=>"http://www.mendeley.com/research/angelman-syndrome-protein-ube3a-interacts-primary-microcephaly-protein-aspm-localizes-centrosomes-re", "reader_count"=>54, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>3, "Student > Bachelor"=>5, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>13, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>3, "Student > Bachelor"=>5, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>27, "Medicine and Dentistry"=>6, "Neuroscience"=>7, "Chemical Engineering"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>7}, "Social Sciences"=>{"Social Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>27}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>3}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "China"=>1, "United Kingdom"=>1, "Portugal"=>2}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/772989"], "description"=>"<p>Examples of cells attempting to divide with missegregated (clone T, anaphase) and lagging chromosomes (clone U, telophase) (arrows). Also note cells with chromosomes hanging at the equatorial plane (clone U, anaphase and clone T, telophase) (arrows). Note the cells have disorganized mitotic spindles (all four panels) and bundling of microtubules at the central spindle (clone U, telophase) and at MTOC (clone T, anaphase). Scale = 2 µm.</p>", "links"=>[], "tags"=>["segregation", "defects", "abnormal", "spindles", "ube3a", "shrna", "knockdown"], "article_id"=>443360, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g007", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chromosome_segregation_defects_associated_with_abnormal_spindles_in_UBE3A_shRNA_knockdown_clones_/443360", "title"=>"Chromosome segregation defects associated with abnormal spindles in UBE3A shRNA knockdown clones.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:56:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/772607"], "description"=>"<p>Indirect immunofluorescence of HEK293 cells at interphase and different phases of mitosis stained with antibodies against ASPM and UBE3A (anti-UBE3A-sc-12380). Note anti-UBE3A-sc-12380 antibody (arrowheads) also shows a centrosomal staining pattern as observed with anti-UBE3A-sc-8926 antibody. Scale bar = 2 µm.</p>", "links"=>[], "tags"=>["colocalization", "ube3a", "aspm", "centrosome"], "article_id"=>442976, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g004", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Confirmation_of_colocalization_of_UBE3A_with_ASPM_at_the_centrosome_using_a_different_UBE3A_antibody_/442976", "title"=>"Confirmation of colocalization of UBE3A with ASPM at the centrosome using a different UBE3A antibody.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:49:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/387330"], "description"=>"<div><p>Many proteins associated with the phenotype microcephaly have been localized to the centrosome or linked to it functionally. All the seven autosomal recessive primary microcephaly (MCPH) proteins localize at the centrosome. Microcephalic osteodysplastic primordial dwarfism type II protein PCNT and Seckel syndrome (also characterized by severe microcephaly) protein ATR are also centrosomal proteins. All of the above findings show the importance of centrosomal proteins as the key players in neurogenesis and brain development. However, the exact mechanism as to how the loss-of-function of these proteins leads to microcephaly remains to be elucidated. To gain insight into the function of the most commonly mutated MCPH gene <em>ASPM</em>, we used the yeast two-hybrid technique to screen a human fetal brain cDNA library with an ASPM bait. The analysis identified Angelman syndrome gene product UBE3A as an ASPM interactor. Like ASPM, UBE3A also localizes to the centrosome. The identification of UBE3A as an ASPM interactor is not surprising as more than 80% of Angelman syndrome patients have microcephaly. However, unlike in MCPH, microcephaly is postnatal in Angelman syndrome patients. Our results show that UBE3A is a cell cycle regulated protein and its level peaks in mitosis. The shRNA knockdown of UBE3A in HEK293 cells led to many mitotic abnormalities including chromosome missegregation, abnormal cytokinesis and apoptosis. Thus our study links Angelman syndrome protein UBE3A to ASPM, centrosome and mitosis for the first time. We suggest that a defective chromosome segregation mechanism is responsible for the development of microcephaly in Angelman syndrome.</p> </div>", "links"=>[], "tags"=>["angelman", "ube3a", "interacts", "microcephaly", "localizes", "centrosomes", "regulates", "chromosome", "segregation"], "article_id"=>136482, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397", "stats"=>{"downloads"=>12, "page_views"=>52, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Angelman_Syndrome_Protein_UBE3A_Interacts_with_Primary_Microcephaly_Protein_ASPM_Localizes_to_Centrosomes_and_Regulates_Chromosome_Segregation/136482", "title"=>"Angelman Syndrome Protein UBE3A Interacts with Primary Microcephaly Protein ASPM, Localizes to Centrosomes and Regulates Chromosome Segregation", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 01:48:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/773253"], "description"=>"<p>Abbreviation: n = total number of mitotic cells observed.</p>", "links"=>[], "tags"=>["mitotic", "abnormalities", "scrambled", "ube3a", "shrna", "knockdown"], "article_id"=>443627, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.t001", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantitation_of_mitotic_abnormalities_in_scrambled_and_UBE3A_shRNA_knockdown_cells_/443627", "title"=>"Quantitation of mitotic abnormalities in scrambled and UBE3A shRNA knockdown cells.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-25 01:00:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/772349"], "description"=>"<p>(A) Indirect immunofluorescence of HEK293 cells stained with anti-γ-tubulin and raised anti-ASPM antibodies. Upper panel: Note ASPM (red) colocalizes with the centrosomal marker γ-tubulin (green). Lower panel: Pre-immune serum (PIS/normal IgG) does not show any signal. Scale bar = 2 µm. (B) Immunofluorescence images of HEK293 cells stained with anti-α-tubulin and raised anti-ASPM antibodies. Upper panel: note ASPM localizes at midbody during cytokinesis (arrow heads). Lower panel: note ASPM localizes at spindle poles during metaphase (arrow heads). Scale bar = 2 µm. (C) Expression profile of ASPM and UBE3A by Western blot analysis using lysates from human fetal brain, human fetal kidney, HEK293, A549, HeLa and HepG2. Anti-ASPM and anti-UBE3A (anti-UBE3A-sc-8926) antibodies recognize 410 kDa and 100 kDa bands, respectively. Note the ubiquitous expression of both proteins. (D) Co-immunoprecipitation of ASPM and UBE3A in human fetal kidney tissue. Upper panel: immunoprecipitation of ASPM co-precipitates UBE3A (100 kDa). Lower panel: immunoprecipitation of UBE3A co-precipitates ASPM (410 kDa). Input lane represents tissue lysate used in pulldown. None of these proteins coprecipitated with either normal IgG or PA/G beads. Abbreviations: IB, immunoblotting; and, IP, immunoprecipitation.</p>", "links"=>[], "tags"=>["aspm", "ube3a"], "article_id"=>442727, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g002", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_ASPM_and_interaction_of_ASPM_with_UBE3A_in_vivo_/442727", "title"=>"Localization of ASPM and interaction of ASPM with UBE3A <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:45:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/772217"], "description"=>"<p>(A) Schematic representation of putative domains and motifs in ASPM. A C–terminal region of ASPM, named CTR (amino acids 3,276–3,477) used as a bait in Y2H analysis is shown. An N-terminal region (amino acids 544–1,059) encompassing the predicted microtubule binding domain and a part of calponin homology domain used for antibody generation is also shown. (B) Y2H screening of transformants by nutritional selection and X-α-gal plate assay. Note growth and blue color for transformants harboring pVA3+pTD1 (positive control) and pACT2-UBE3A+pGBKT7-CTR. As expected, no growth and blue color were observed for transformants harboring pLam5′+pTD1, pACT2+pGBKT7, pACT2+pGBKT7-CTR and pACT2-UBE3A+pGBKT7. (C) Schematic representation of UBE3A protein. The ASPM interacting region of UBE3A (amino acids 639–875) is located within the HECT domain (amino acids 545 to 875). The numbers represent amino acid positions.</p>", "links"=>[], "tags"=>["aspm", "ube3a", "y2h"], "article_id"=>442601, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_interaction_between_ASPM_and_UBE3A_by_Y2H_analysis_/442601", "title"=>"Identification of interaction between ASPM and UBE3A by Y2H analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:43:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/773153"], "description"=>"<p>(A) Note cells undergoing cytokinesis with elongated nuclear morphology giving rise to abnormal number of nuclei. An extended midbody (arrowheads) and micronuclei (arrows) can be seen in all the panels. ASPM was found to be diffusely present at the midbody. Scale = 2 µm. (B) Quantitation of apoptosis by <i>in vivo</i> detection of caspase-3 activity. Note UBE3A shRNA clones showed a significant increase in apoptotic cells as compared to scrambled clones. Cells were analyzed by flow cytometry using FL-1 channel (10,000 cells were measured for each sample). Mean ± SEM values for the samples is as follows: scrambled clone P = 6.150±0.2972, scrambled clone K = 4.920±0.0986, UBE3AshRNA clone T = 7.700±0.2663, and UBE3AshRNA clone U = 14.99±0.2929. Data are representative of three independent experiments. Unpaired Student's t-test was used to determine the significance of difference between scrambled and UBE3A knockdown clones.</p>", "links"=>[], "tags"=>["cytokinesis", "apoptosis", "ube3a", "knockdown"], "article_id"=>443527, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Abnormal_cytokinesis_and_apoptosis_in_UBE3A_knockdown_cells_/443527", "title"=>"Abnormal cytokinesis and apoptosis in UBE3A knockdown cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:58:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/772489"], "description"=>"<p>(A) Indirect immunofluorescence of HEK293 cells at interphase and different phases of mitosis stained with antibodies against ASPM and UBE3A (anti-UBE3A-sc-8926). Note colocalization of UBE3A with ASPM at the centrosome throughout mitosis (arrowheads). Note weak centrosomal staining of UBE3A in an interphase cell (arrow). (B) Indirect immunofluorescence of A549 cells stained with antibodies against UBE3A (anti-UBE3A-sc-8926) and ASPM at metaphase and telophase. Note colocalization of UBE3A with ASPM at the centrosome (arrowheads). Scale bar = 2 µm.</p>", "links"=>[], "tags"=>["colocalizes", "aspm"], "article_id"=>442860, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_UBE3A_colocalizes_with_ASPM_at_the_centrosome_/442860", "title"=>"UBE3A colocalizes with ASPM at the centrosome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:47:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/772710"], "description"=>"<p>(A) Flow cytometric analysis of cells to confirm synchronization in different cell cycle phases. Note the cells in G1 phase show a 2n peak, cells in M phase with a 4n peak and cells in S phase fall in between 2n-4n peaks, suggesting cell cycle arrest at these phases. UN: unsynchronized cells. (B) HEK293 cells synchronized at different cell cycle phases were analyzed for UBE3A and ASPM expression by Western blot analysis. Note the expression of UBE3A was found to peak in M phase as compared to its levels in G1 and S phases. The level of ASPM peaks during G1 and M phases. Erk1/2 was used a loading control. The level of Erk1/2 is known to remain unaffected during different phases of cell cycle. (C) Western blot analysis of lysates from HEK293 cells transfected with an increasing concentration of the pCMV4-HA-UBE3A construct. Note UBE3A overexpression fails to degrade ASPM. Overexpression of UBE3A was determined by probing the blot with anti-HA antibody. β-Actin was used as a loading control. (D) Immunofluorescence analysis of HEK293 cells overexpressing the pCMV4-HA-UBE3A construct. UBE3A and ASPM staining were examined by anti-HA and anti-ASPM antibodies respectively. Note overexpression of UBE3A does not alter ASPM localization or protein level (compare ASPM signals in upper and lower panels). Also note colocalization of UBE3A with ASPM at the centrosome (upper panel). Cells transfected with the pCMV-HA vector were also stained with anti-HA antibody as a control (lower panel).</p>", "links"=>[], "tags"=>["fails", "degrade"], "article_id"=>443088, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g005", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_UBE3A_is_a_cell_cycle_dependent_protein_and_it_fails_to_degrade_ASPM_/443088", "title"=>"UBE3A is a cell cycle dependent protein and it fails to degrade ASPM.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:51:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/772858"], "description"=>"<p>(A) HEK293 cells transfected with a HuSH 29mer shRNA construct against UBE3A and puromycin resistant clones (B, T and U) were examined for knockdown by Western blot analysis. As a control, clones (C, P and K) transfected with scrambled shRNA were also generated. Note reduced expression of UBE3A in clones B, T and U as compared to scrambled clones C, P and K. (B) Densitometric analysis of blot in panel A. UBE3A knockdown clones T and U showed approximately 80% knockdown as compared to the scrambled clone P and K. Bars represent average values from densitometric analysis of the bands obtained in three separate experiments. (C) Representative images of scrambled and UBE3A shRNA knockdown prometaphase cells showing UBE3A staining. Note a reduced UBE3A signal (arrowheads) at the centrosome in an UBE3A shRNA knockdown cell as compared to a scrambled cell. γ-tubulin was used for centrosomal staining (arrows). (D) Western blot analysis of lysates from scrambled clones P and K, and UBE3A knockdown clones T and U with anti-ASPM antibody. Note that the ASPM protein level remains unaffected in UBE3A knockdown clones as compared to scrambled clones. β-Actin was used as a loading control. (E) Representative images of mitotic cells at different stages from scrambled clone P showing normal chromosome alignment and mitotic spindles. Arrows point to ASPM staining and arrowhead marks the midbody. Scale = 2 µm. (F) Cells from UBE3A knockdown clone T showing misalignment of chromosomes and multipolarity at metaphase. Note an arrow points to misaligned chromosomes which lie outside the spindle poles (upper panel). Note in two multipolar cells (lower panel), the different poles are marked with arrowheads for lower right cell and marked with “*” for upper left cell. Scale = 2 µm.</p>", "links"=>[], "tags"=>["ube3a", "shrna", "knockdown", "clones", "mitotic"], "article_id"=>443231, "categories"=>["Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Pooja Singhmar", "Arun Kumar"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020397.g006", "stats"=>{"downloads"=>2, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Generation_of_stable_UBE3A_shRNA_knockdown_clones_and_analysis_of_mitotic_stages_/443231", "title"=>"Generation of stable UBE3A shRNA knockdown clones and analysis of mitotic stages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-25 00:53:51"}

PMC Usage Stats | Further Information

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