A Prevalent Variant in PPP1R3A Impairs Glycogen Synthesis and Reduces Muscle Glycogen Content in Humans and Mice
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{"title"=>"A prevalent variant in PPP1R3A impairs glycogen synthesis and reduces muscle glycogen content in humans and mice", "type"=>"journal", "authors"=>[{"first_name"=>"David B.", "last_name"=>"Savage", "scopus_author_id"=>"7202012451"}, {"first_name"=>"Lanmin", "last_name"=>"Zhai", "scopus_author_id"=>"7007168023"}, {"first_name"=>"Balasubramanian", "last_name"=>"Ravikumar", "scopus_author_id"=>"23486749200"}, {"first_name"=>"Soo Choi", "last_name"=>"Cheol", "scopus_author_id"=>"12761818500"}, {"first_name"=>"Johanna E.", "last_name"=>"Snaar", "scopus_author_id"=>"6603375891"}, {"first_name"=>"Amanda C.", "last_name"=>"McGuire", "scopus_author_id"=>"23485855900"}, {"first_name"=>"Sung Eun", "last_name"=>"Wou", "scopus_author_id"=>"23969709500"}, {"first_name"=>"Gemma", "last_name"=>"Medina-Gomez", "scopus_author_id"=>"8678999100"}, {"first_name"=>"Sheene", "last_name"=>"Kim", "scopus_author_id"=>"16833636900"}, {"first_name"=>"Cheryl B.", "last_name"=>"Bock", "scopus_author_id"=>"7102421136"}, {"first_name"=>"Dyann M.", "last_name"=>"Segvich", "scopus_author_id"=>"23486968900"}, {"first_name"=>"Antonio", "last_name"=>"Vidal-Puig", "scopus_author_id"=>"7003817501"}, {"first_name"=>"Nicholas J.", "last_name"=>"Wareham", "scopus_author_id"=>"7006224498"}, {"first_name"=>"Gerald I.", "last_name"=>"Shulman", "scopus_author_id"=>"7102613915"}, {"first_name"=>"Fredrik", "last_name"=>"Karpe", "scopus_author_id"=>"56243027200"}, {"first_name"=>"Roy", "last_name"=>"Taylor", "scopus_author_id"=>"7405756928"}, {"first_name"=>"Bartholomew A.", "last_name"=>"Pederson", "scopus_author_id"=>"6603801382"}, {"first_name"=>"Peter J.", "last_name"=>"Roach", "scopus_author_id"=>"7101866587"}, {"first_name"=>"Stephen", "last_name"=>"O'Rahilly", "scopus_author_id"=>"7101607650"}, {"first_name"=>"Anna A.", "last_name"=>"DePaoli-Roach", "scopus_author_id"=>"7005343394"}], "year"=>2008, "source"=>"PLoS Medicine", "identifiers"=>{"issn"=>"15491277", "pmid"=>"18232732", "pui"=>"351198266", "scopus"=>"2-s2.0-38849204124", "doi"=>"10.1371/journal.pmed.0050027", "isbn"=>"1549-1676 (Electronic)\r1549-1277 (Linking)", "sgr"=>"38849204124"}, "id"=>"442bc1c2-1fd3-3b2a-b9b4-3ec13e6ae198", "abstract"=>"BACKGROUND: Stored glycogen is an important source of energy for skeletal muscle. Human genetic disorders primarily affecting skeletal muscle glycogen turnover are well-recognised, but rare. We previously reported that a frameshift/premature stop mutation in PPP1R3A, the gene encoding RGL, a key regulator of muscle glycogen metabolism, was present in 1.36% of participants from a population of white individuals in the UK. However, the functional implications of the mutation were not known. The objective of this study was to characterise the molecular and physiological consequences of this genetic variant.\\n\\nMETHODS AND FINDINGS: In this study we found a similar prevalence of the variant in an independent UK white population of 744 participants (1.46%) and, using in vivo (13)C magnetic resonance spectroscopy studies, demonstrate that human carriers (n = 6) of the variant have low basal (65% lower, p = 0.002) and postprandial muscle glycogen levels. Mice engineered to express the equivalent mutation had similarly decreased muscle glycogen levels (40% lower in heterozygous knock-in mice, p < 0.05). In muscle tissue from these mice, failure of the truncated mutant to bind glycogen and colocalize with glycogen synthase (GS) decreased GS and increased glycogen phosphorylase activity states, which account for the decreased glycogen content.\\n\\nCONCLUSIONS: Thus, PPP1R3A C1984DeltaAG (stop codon 668) is, to our knowledge, the first prevalent mutation described that directly impairs glycogen synthesis and decreases glycogen levels in human skeletal muscle. The fact that it is present in approximately 1 in 70 UK whites increases the potential biomedical relevance of these observations.", "link"=>"http://www.mendeley.com/research/prevalent-variant-ppp1r3a-impairs-glycogen-synthesis-reduces-muscle-glycogen-content-humans-mice", "reader_count"=>29, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>2, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>11, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>2, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Medicine and Dentistry"=>7, "Agricultural and Biological Sciences"=>14, "Sports and Recreations"=>3, "Business, Management and Accounting"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Sports and Recreations"=>{"Sports and Recreations"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Cameroon"=>1, "United States"=>2, "Portugal"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/939103"], "description"=>"<p>(A) Muscle glycogen, (B) blood glucose, and (C) insulin levels in humans with the <i>PPP1R3A FS</i> mutation before and after two standardised meals (given at 60 and 240 min). Data from <i>PPP1R3A FS</i> carriers (<i>n</i> = 4; open circles) are compared with those from volunteers without diabetes (<i>n</i> = 9; solid squares) and from participants with type 2 diabetes (T2DM; <i>n</i> = 9; filled triangles). Mean data from two digenic participants (double heterozygotes for the <i>PPP1R3A FS</i> and <i>PPARG FS</i>) are included in graphs (A) and (B). Mean fasting insulin levels from the two digenic individuals were 199, 5,744, 9,534, 1,303, 13,689, and 10,291 pmol/l, too high to include in (C), at 0, 60, 120, 240, 360, and 480 minutes, respectively.</p>", "links"=>[], "tags"=>["Biochemistry", "diabetes and endocrinology"], "article_id"=>609531, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g001", "stats"=>{"downloads"=>4, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Human_PPP1R3A_FS_Carrier_Phenotype_/609531", "title"=>"Human <i>PPP1R3A FS</i> Carrier Phenotype", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:38:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/939407"], "description"=>"<div><p>(A) Western blots of protein phosphatase-1 catalytic subunit delta (PP1cδ) and GS in muscle extracts.</p>\n <p>(B) Western blots for R<sub>GL</sub> and GS following R<sub>GL</sub> immunoprecipitation with a R<sub>GL</sub> N-terminal antibody (Ab).</p>\n <p>(C) Western blots for R<sub>GL</sub> and GS following R<sub>GL</sub> immunoprecipitation with a R<sub>GL</sub> C-terminal antibody (Ab).</p></div>", "links"=>[], "tags"=>["wt", "knock-in", "truncated", "mutant", "gs", "skeletal", "extracts", "heterozygous", "kin", "homozygous"], "article_id"=>609828, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interactions_between_WT_R_GL_R_GL_Knock_In_Truncated_Mutant_R_GL_trunc_and_GS_in_Skeletal_Muscle_Extracts_from_WT_R_GL_Knock_In_Heterozygous_R_GL_kin_het_and_R_GL_Knock_In_Homozygous_R_GL_kin_hom_Mice_/609828", "title"=>"Interactions between WT R<sub>GL</sub>, R<sub>GL</sub> Knock-In Truncated Mutant (R<sub>GL</sub> trunc), and GS in Skeletal Muscle Extracts from WT, R<sub>GL</sub> Knock-In Heterozygous (R<sub>GL</sub> kin het) and R<sub>GL</sub> Knock-In Homozygous (R<sub>GL</sub> kin hom) Mice", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:43:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/939560"], "description"=>"<p>GS was pulled down with GST-glycogenin—GST-GN(297–333)—fusion protein before and after α-amylase digestion of glycogen in skeletal muscle extracts from wild type (R<sub>GL</sub> WT) and R<sub>GL</sub> knock-in homozygous (R<sub>GL</sub> kin hom) mice. (A) GST-GN(297–333) pulls down almost all GS, but (B) neither the WT nor the truncated R<sub>GL</sub> (R<sub>GL</sub> trunc) was pulled down by GST-GN(297–333).</p>", "links"=>[], "tags"=>["synthase"], "article_id"=>609989, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glycogen_Synthase_Pull_Down_/609989", "title"=>"Glycogen Synthase Pull Down", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:46:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/939722"], "description"=>"<p>Western blotting of high-speed supernatants and pellets of skeletal muscle extracts from WT, R<sub>GL</sub> knock-in heterozygous (het), and R<sub>GL</sub> knock-in homozygous (hom) mice. High speed (HS) ultracentrifugation at 100,0000<i>g</i> for 90 min was used to pellet glycogen. Western blots for R<sub>GL</sub>, GS, and GP were then performed on the supernatant and pellet fractions.</p>", "links"=>[], "tags"=>["blot", "skeletal"], "article_id"=>610150, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_R_GL_Western_Blot_Analysis_of_Skeletal_Muscle_Extracts_/610150", "title"=>"R<sub>GL</sub> Western Blot Analysis of Skeletal Muscle Extracts", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 00:02:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/939846"], "description"=>"<div><p>(A) Glucose tolerance following intraperitoneal glucose (2 mg/g body weight) administration in WT, R<sub>GL</sub> knock-in heterozygous (R<sub>GL</sub> kin het), and R<sub>GL</sub> kin homozygous (R<sub>GL</sub> kin hom) mice.</p>\n <p>(B) Plasma glucose response to intraperitoneal insulin (0.75 mU/g body weight) in WT-, R<sub>GL</sub> knock-in heterozygous (R<sub>GL</sub> kin het)-, and R<sub>GL</sub> knock-in homozygous (R<sub>GL</sub> kin hom) mice. Peripheral and hepatic insulin sensitivity were assessed by means of hyperinsulinemic-euglycemic clamps in WT and R<sub>GL</sub> kin het mice (C–G). Glucose infusion rates (C); peripheral glucose turnover (D); and basal (E) and suppressed (F) endogenous glucose production (EGP) during hyperinsulinemic-euglycemic clamps.</p>\n <p>(G) Whole body (WB) glycolysis and glycogen synthesis were measured during the clamps.</p>\n <p>Data are expressed as mean values ± SEM for 6–9 mice per treatment group.</p></div>", "links"=>[], "tags"=>["insulin", "knock-in"], "article_id"=>610281, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g006", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glucose_Tolerance_and_Insulin_Sensitivity_in_R_GL_Knock_in_Mice_/610281", "title"=>"Glucose Tolerance and Insulin Sensitivity in R<sub>GL</sub> Knock-in Mice", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 00:04:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/939250"], "description"=>"<div><p>(A) R<sub>GL</sub> Western blots of skeletal muscle extracts from WT, R<sub>GL</sub> knock-in heterozygous (R<sub>GL</sub> kin het), and R<sub>GL</sub> knock-in homozygous (R<sub>GL</sub> kin hom) mice. The predicted molecular weight (MW) of the truncated R<sub>GL</sub> (R<sub>GL</sub> trunc, 643 amino acids) is 72,000 but it migrates on SDS polyacrylamide gel electrophoresis with an apparent MW of 83,000.</p>\n <p>(B) GS activity was assayed in the absence (−) or presence (+) of G6P in extracts of skeletal muscle from WT, R<sub>GL</sub> knock-in heterozygous (R<sub>GL</sub> kin het), and R<sub>GL</sub> knock-in homozygous (R<sub>GL</sub> kin hom) mice not injected or injected intraperitoneally with 5 mU/g insulin for 10 min (plain and chequered bars, respectively).</p>\n <p>(C) Total GS activity (mU/mg) measured in the presence of 7.2 mM G6P.</p>\n <p>(D) Glycogen phosphorylase (Ph) activity was assayed in the absence (−) or presence (+) of 2 mM AMP.</p>\n <p>(E) Total glycogen phosphorylase (Ph) activity (U/mg) measured in the presence of 2 mM AMP.</p>\n <p>(F) Glycogen content in muscle.</p>\n <p><i>n</i> = 4–9 per group; * <i>p</i> < 0.05 versus WT basal; # <i>p</i> < 0.05 insulin versus basal.</p></div>", "links"=>[], "tags"=>["glycogen", "metabolism", "knock-in", "wild-type"], "article_id"=>609674, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>"https://dx.doi.org/10.1371/journal.pmed.0050027.g002", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Muscle_Glycogen_Metabolism_in_R_GL_Knock_in_and_Wild_Type_Mice_/609674", "title"=>"Muscle Glycogen Metabolism in R<sub>GL</sub> Knock-in and Wild-Type Mice", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-01-29 02:41:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/475373", "https://ndownloader.figshare.com/files/475432", "https://ndownloader.figshare.com/files/475501", "https://ndownloader.figshare.com/files/475557", "https://ndownloader.figshare.com/files/475606"], "description"=>"<div><h3>Background</h3><p>Stored glycogen is an important source of energy for skeletal muscle. Human genetic disorders primarily affecting skeletal muscle glycogen turnover are well-recognised, but rare. We previously reported that a frameshift/premature stop mutation in <em>PPP1R3A</em>, the gene encoding R<sub>GL</sub>, a key regulator of muscle glycogen metabolism, was present in 1.36% of participants from a population of white individuals in the UK. However, the functional implications of the mutation were not known. The objective of this study was to characterise the molecular and physiological consequences of this genetic variant.</p> <h3>Methods and Findings</h3><p>In this study we found a similar prevalence of the variant in an independent UK white population of 744 participants (1.46%) and, using in vivo <sup>13</sup>C magnetic resonance spectroscopy studies, demonstrate that human carriers (<em>n</em> = 6) of the variant have low basal (65% lower, <em>p</em> = 0.002) and postprandial muscle glycogen levels. Mice engineered to express the equivalent mutation had similarly decreased muscle glycogen levels (40% lower in heterozygous knock-in mice, <em>p</em> < 0.05). In muscle tissue from these mice, failure of the truncated mutant to bind glycogen and colocalize with glycogen synthase (GS) decreased GS and increased glycogen phosphorylase activity states, which account for the decreased glycogen content.</p> <h3>Conclusions</h3><p>Thus, <em>PPP1R3A</em> C1984ΔAG (stop codon 668) is, to our knowledge, the first prevalent mutation described that directly impairs glycogen synthesis and decreases glycogen levels in human skeletal muscle. The fact that it is present in ∼1 in 70 UK whites increases the potential biomedical relevance of these observations.</p> </div>", "links"=>[], "tags"=>["prevalent", "variant", "impairs", "glycogen", "synthesis", "reduces", "humans", "mice"], "article_id"=>153654, "categories"=>["Chemistry", "Biochemistry"], "users"=>["David B Savage", "Lanmin Zhai", "Balasubramanian Ravikumar", "Cheol Soo Choi", "Johanna E Snaar", "Amanda C McGuire", "Sung-Eun Wou", "Gemma Medina-Gomez", "Sheene Kim", "Cheryl B Bock", "Dyann M Segvich", "Antonio Vidal-Puig", "Nicholas J Wareham", "Gerald I Shulman", "Fredrik Karpe", "Roy Taylor", "Bartholomew A Pederson", "Peter J Roach", "Stephen O'Rahilly", "Anna A DePaoli-Roach"], "doi"=>["https://dx.doi.org/10.1371/journal.pmed.0050027.sg001", "https://dx.doi.org/10.1371/journal.pmed.0050027.sg002", "https://dx.doi.org/10.1371/journal.pmed.0050027.sg003", "https://dx.doi.org/10.1371/journal.pmed.0050027.sg004", "https://dx.doi.org/10.1371/journal.pmed.0050027.sd001"], "stats"=>{"downloads"=>27, "page_views"=>47, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Prevalent_Variant_in_PPP1R3A_Impairs_Glycogen_Synthesis_and_Reduces_Muscle_Glycogen_Content_in_Humans_and_Mice/153654", "title"=>"A Prevalent Variant in <em>PPP1R3A</em> Impairs Glycogen Synthesis and Reduces Muscle Glycogen Content in Humans and Mice", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-01-29 01:00:54"}

PMC Usage Stats | Further Information

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Relative Metric

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