bims-glecem Biomed News
on Glycogen metabolism in exercise, cancer and energy metabolism
Issue of 2022–09–18
twelve papers selected by
Dipsikha Biswas, Københavns Universitet



  1. Front Mol Biosci. 2022 ;9 957549
      Introduction: The AMP-activated protein kinase (AMPK) is a master regulator of energy homeostasis that becomes activated by exercise and binds glycogen, an important energy store required to meet exercise-induced energy demands. Disruption of AMPK-glycogen interactions in mice reduces exercise capacity and impairs whole-body metabolism. However, the mechanisms underlying these phenotypic effects at rest and following exercise are unknown. Furthermore, the plasma metabolite responses to an acute exercise challenge in mice remain largely uncharacterized. Methods: Plasma samples were collected from wild type (WT) and AMPK double knock-in (DKI) mice with disrupted AMPK-glycogen binding at rest and following 30-min submaximal treadmill running. An untargeted metabolomics approach was utilized to determine the breadth of plasma metabolite changes occurring in response to acute exercise and the effects of disrupting AMPK-glycogen binding. Results: Relative to WT mice, DKI mice had reduced maximal running speed (p < 0.0001) concomitant with increased body mass (p < 0.01) and adiposity (p < 0.001). A total of 83 plasma metabolites were identified/annotated, with 17 metabolites significantly different (p < 0.05; FDR<0.1) in exercised (↑6; ↓11) versus rested mice, including amino acids, acylcarnitines and steroid hormones. Pantothenic acid was reduced in DKI mice versus WT. Distinct plasma metabolite profiles were observed between the rest and exercise conditions and between WT and DKI mice at rest, while metabolite profiles of both genotypes converged following exercise. These differences in metabolite profiles were primarily explained by exercise-associated increases in acylcarnitines and steroid hormones as well as decreases in amino acids and derivatives following exercise. DKI plasma showed greater decreases in amino acids following exercise versus WT. Conclusion: This is the first study to map mouse plasma metabolomic changes following a bout of acute exercise in WT mice and the effects of disrupting AMPK-glycogen interactions in DKI mice. Untargeted metabolomics revealed alterations in metabolite profiles between rested and exercised mice in both genotypes, and between genotypes at rest. This study has uncovered known and previously unreported plasma metabolite responses to acute exercise in WT mice, as well as greater decreases in amino acids following exercise in DKI plasma. Reduced pantothenic acid levels may contribute to differences in fuel utilization in DKI mice.
    Keywords:  AMP-activated protein kinase; acylcarnitines; amino acids; exercise metabolism; glycogen; metabolomics; pantothenic acid; plasma metabolite
    DOI:  https://doi.org/10.3389/fmolb.2022.957549
  2. J Inherit Metab Dis. 2022 Sep 16.
      Pompe disease is an inherited metabolic myopathy caused by deficiency of acid α-glucosidase (GAA), resulting in lysosomal glycogen accumulation. Residual GAA enzyme activity affects disease onset and severity, although other factors, including dysregulation of cytoplasmic glycogen metabolism, are suspected to modulate the disease course. In this study, performed in mice and patient biopsies, we found elevated protein levels of enzymes involved in glucose uptake and cytoplasmic glycogen synthesis in skeletal muscle from mice with Pompe disease, including glycogenin (GYG1), glycogen synthase (GS), glucose transporter 4 (GLUT4), glycogen branching enzyme (GBE1), and UDP-glucose pyrophosphorylase (UGP2). Expression levels were elevated before the loss of muscle mass and function. For first time, quantitative mass spectrometry in skeletal muscle biopsies from five adult patients with Pompe disease showed increased expression of glycogen branching enzyme protein relative to healthy controls at the group level. Paired analysis of individual patients who responded well to treatment with enzyme replacement therapy (ERT) showed reduction of glycogen synthase, glycogenin, and glycogen branching enzyme 1 in all patients after start of ERT compared to baseline. These results indicate that metabolic changes precede muscle wasting in Pompe disease, and imply a positive feedforward loop in Pompe disease, in which lysosomal glycogen accumulation promotes cytoplasmic glycogen synthesis and glucose uptake, resulting in aggravation of the disease phenotype.
    Keywords:  Pompe disease; Skeletal muscle; glycogen metabolism; lysosomal storage disorder; metabolic myopathy
    DOI:  https://doi.org/10.1002/jimd.12560
  3. JIMD Rep. 2022 Sep;63(5): 453-461
      Glycogen storage disease type 1a (GSD1a) is an inborn error of glucose metabolism characterized by fasting hypoglycemia, hepatomegaly, and growth failure. Late complications include nephropathy and hepatic adenomas. We conducted a retrospective observational study on a cohort of Amish patients with GSD1a. A total of 15 patients cared for at a single center, with a median age of 9.9 years (range 0.25-24 years) were included. All patients shared the same founder variant in GCPC c.1039 C > T. The phenotype of this cohort demonstrated good metabolic control with median cohort triglyceride level slightly above normal, no need for continuous overnight feeds, and a higher quality of life compared to a previous GSD cohort. The most frequent complications were oral aversion, gross motor delay, and renal hyperfiltration. We discuss our unique care delivery at a single center that cares for Amish patients with inherited disorders.
    Keywords:  gross motor delay; hepatomegaly; hypertriglyceridemia; hypoglycemia; oral aversion; quality of life
    DOI:  https://doi.org/10.1002/jmd2.12310
  4. Rev Neurol. 2022 Sep 16. 75(6): 129-136
       INTRODUCTION: McArdle's disease is caused by a mutation in the PYGM gene, causing a muscle myophosphorylase deficiency, altering the release of glucose-1-P from glycogen. It usually manifests itself in childhood with early and excessive tiredness, myalgias, cramps and contractures or rhabdomyolysis, although it is not usually diagnosed until adulthood. Creatine kinase increases sharply during exercise. Four pediatric patients are presented, the pathophysiology is summarized, and a diagnostic algorithm is proposed.
    PATIENTS AND METHODS: Ages between 6 and 14 years, the anamnesis, physical examination, biochemistry, elec-tro-myogram, ischemia test and genetic study are described. Muscle biopsy in a single patient. The algorithm was developed from the ischemia test.
    RESULTS: In the three men, myalgias appeared after finishing each sports session. Phenomenon 'second wind' in one case. Ischemia test without lactate elevation and marked ammonia elevation in all. Only one muscle biopsy with glycogen deposits and absence of myophosphorylase. PYGM gene with homozygous mutations in all. Dietary treatment attenuated their symptoms during aerobic exercises.
    CONCLUSIONS: The ischemia test was very useful to demonstrate a dysfunction in anaerobic glycolysis. It is worth noting that oral glucose supplementation is very useful in McArdle disease, but is contraindicated in all six defects of anaerobic glycolysis. The algorithm also allows targeting the defect of 20 metabolic or structural myopathies, which are summarized.
    DOI:  https://doi.org/10.33588/rn.7506.2022212
  5. Front Genet. 2022 ;13 932760
      Background: Glycogen storage diseases (GSDs) are known as a group of disorders characterized by genetic errors leading to accumulation of glycogen in various tissues. Since different types of GSD can sometimes be clinically indistinguishable, next generation sequencing is becoming a powerful tool for clinical diagnosis. Methods: 12 patients with suspected GSDs and their parents were enrolled in this study. The clinical and laboratory data of the patients were reviewed. Causative gene variants were identified in the patients using whole exome sequencing (WES) and verified by Sanger sequencing. Results: Genetic testing and analysis showed that 7 patients were diagnosed with GSD II (Pompe disease), 2 patients with GSD III, 1 patient with GSD VI, and 2 patients with GSD IXα. A total number of 18 variants were identified in 12 patients including 11 variants in GAA gene, 3 variants in AGL gene, 2 variants in PYGL gene and 2 variants in PHKA2 gene, of which 9 variants were reported and 9 variants were novel. SIFT, Polyphen-2, Mutation Taster, and REVEL predicted the novel variants (except GAA c.1052_1075 + 47del) to be disease-causing. The 3D structures of wild/mutant type GAA protein were predicted indicating that variants p. Trp621Gly, p. Pro541Leu, p. Ser800Ile and p. Gly293Trp might affect the proteins function via destroying hydrogen bonds or conformational constraints. Neither liver size nor laboratory findings allow for a differentiation among GSD III, GSD VI and GSD IXα. Conclusion: Our study expanded the variation spectrum of genes associated with GSDs. WES, in combination with clinical, biochemical, and pathological hallmarks, could provide accurate results for diagnosing and sub-typing GSD and related diseases in clinical setting.
    Keywords:  AGL gene; GAA gene; PHKA2 gene; PYGL gene; glycogen storage diseases; mutation; whole exome sequencing
    DOI:  https://doi.org/10.3389/fgene.2022.932760
  6. Equine Vet J. 2022 Aug 16.
       BACKGROUND: Both type 1 (PSSM1) and type 2 polysaccharide storage myopathy (PSSM2) are characterised by aggregates of abnormal polysaccharide in skeletal muscle. Whereas the genetic basis for PSSM1 is known (R309H GYS1), the cause of PSSM2 in Quarter Horses (PSSM2-QH) is unknown and glycogen concentrations not defined.
    OBJECTIVES: To characterise the histopathological and biochemical features of PSSM2-QH and determine if an associated monogenic variant exists in genes known to cause glycogenosis.
    STUDY DESIGN: Retrospective case control.
    METHODS: Sixty-four PSSM2-QH, 30 PSSM1-QH and 185 control-QH were identified from a biopsy repository and clinical data, histopathology scores (0-3), glycogen concentrations and selected glycolytic enzyme activities compared. Coding sequences of 12 genes associated with muscle glycogenoses were identified from whole genome sequences and compared between seven PSSM2-QH and five control-QH.
    RESULTS: Exertional rhabdomyolysis in PSSM2-QH occurred predominantly in barrel racing and working cow/roping performance types and improved with regular exercise and a low starch/fat-supplemented diet. Histopathological scores, including the amount of amylase-resistant polysaccharide (PSSM2-QH 1.4 ± 0.6, PSSM1-QH 2.1 ± 0.3, control-QH 0 ± 0, p < 0.001), and glycogen concentrations (PSSM2-QH 129 ± 62, PSSM1-QH 175 ± 9, control-QH 80 ± 27 mmol/kg, p < 0.0001) were intermediate in PSSM2-QH with significant differences among groups. In PSSM2-QH, abnormal polysaccharide had a less filamentous ultrastructure than PSSM1-QH and phosphorylase and phosphofructokinase activities were normal. Seventeen of 30 PSSM2-QH with available pedigrees descended from one of three stallions within four generations. Of the 29 predicted high or moderate impact genetic variants identified in candidate genes, none were present in only PSSM2-QH and absent in control-QH.
    MAIN LIMITATIONS: Analyses of PSSM2-QH and PSSM1-QH were performed on shipped samples, controls on frozen samples.
    CONCLUSIONS: PSSM2-QH is a novel glycogen storage disorder that is not the result of a mutation in genes currently known to cause muscle glycogenoses in other species.
    Keywords:  glycogen; glycogenolysis; glycolysis; horse; muscle disease; polyglucosan
    DOI:  https://doi.org/10.1111/evj.13876
  7. J Inherit Metab Dis. 2022 Sep 11.
      Value-based healthcare (VBHC) intends to achieve better outcomes for patients, to improve quality of patient care, with reduced costs. Four dimensions define a model of intimately related value-pillars: personal value, allocative value, technical value, and societal value. VBHC is mostly applied in common diseases, and there are fundamental challenges in applying VBHC strategies to low volume, high complex healthcare situations, such as rare diseases, including inherited metabolic disorders. This article summarizes current practices at various academical domains (i.e., research, healthcare, education and training) that (aim to) increase values at various value-pillars for persons with liver glycogen storage diseases or fatty acid oxidation disorders and their families. Future perspectives may include facilitating virtual networks to function as integrated practice units, improving measurement of outcomes, and creating information technology platforms to overcome the ethical, legal, societal, and technical challenges of data sharing for health care and research purposes. This article is protected by copyright. All rights reserved.
    Keywords:  fatty acid oxidation; glycogen storage disease; inborn errors of metabolism; value-based healthcare
    DOI:  https://doi.org/10.1002/jimd.12555
  8. Proteins. 2022 Sep 14.
      As drug-binding kinetics has become an important factor to be considered in modern drug discovery, this work evaluated the ability of the Milestoning method in computing the absolute dissociation rate of a ligand from the serine-threonine kinase glycogen synthase kinase 3β, which is a target for designing drugs to treat diseases such as neurodegenerative disorders and diabetes. We found that the Milestoning method gave good agreement with experiment with modest computational costs. Although the time scale for dissociation lasted tens of seconds, the collective molecular dynamics simulations total less than 1 μs. Computing the committor function helped to identify the transition states, in which the ligand moved substantially away from the binding pocket. The glycine-rich loop with a serine residue attaching to its tips was found to undergo large movement from the bound to the transition states and might play a role in controlling drug-dissociation kinetics. This article is protected by copyright. All rights reserved.
    Keywords:  Milestoning simulation; absolute drug-dissociation rate; glycogen synthase kinase 3β (GSK3β); transition-state structures
    DOI:  https://doi.org/10.1002/prot.26423
  9. J Hematol Oncol. 2022 Sep 14. 15(1): 134
       BACKGROUND: Glycogen synthase kinase-3 (GSK-3) is a serine/threonine kinase with multiple roles in tumour growth, cell invasion and metastasis. We have previously established GSK-3 as an upstream regulator of PD-1 gene expression in CD8 + T cells and demonstrated that GSK-3 inhibition is as effective as anti-PD-1 mAb blockade in controlling tumour growth. Elraglusib (9-ING-41) is a specific small-molecule inhibitor of GSK-3β with clinical activity in patients with advanced cancers, including a patient with refractory melanoma whose response provided the rationale for the current study.
    METHODS: The B16 melanoma mouse model was used to observe the effect of elraglusib on tumour growth either as a single agent or in combination (simultaneously and sequentially) with anti-PD-1 mAb treatment. B16 tumour cells were implanted in either the flank, brain or both locations, and Kaplan-Meier plots were used to depict survival and significance determined using log rank tests. Expression of the immune checkpoint molecules, TIGIT, LAG-3 and PD-1, was evaluated using flow cytometry alongside expression of the chemokine receptor, CXCR3. Further evaluation of PD-1 expression was determined through RT-qPCR and immunohistochemistry.
    RESULTS: We demonstrated that elraglusib has a suppressive effect against melanoma as a single agent and enhanced anti-PD-1 therapy. There was a synergistic effect when elraglusib was used in combination with anti-PD-1 mAb, and an even greater effect when used as sequential therapy. Suppression of tumour growth was associated with a reduced expression of immune checkpoint molecules, PD-1, TIGIT and LAG-3 with upregulation of CXCR3 expression.
    CONCLUSIONS: These data highlight the potential of elraglusib as an immune-modulatory agent and demonstrate the benefit of a sequential approach with immune checkpoint inhibition followed by GSK-3β inhibition in melanoma and provide a rationale for clinical investigation of elraglusib combined with immune checkpoint inhibitory molecules, including those targeting PD-1, TIGIT and LAG-3. This has several potential implications for current immunotherapy regimes, including possibly reducing the intensity of anti-PD-1 mAb treatment needed for response in patients receiving elraglusib, especially given the benign adverse event profile of elraglusib observed to date. Based on these data, a clinical study of elraglusib, an anti-PD-1 mAb and chemotherapy is ongoing (NCT NCT05239182).
    Keywords:  9-ING-41; Elraglusib; Glycogen synthase kinase-3; LAG-3: lymphocyte activation gene-3; Melanoma; PD-1: programmed cell death protein 1; T cells; TIGIT: T cell immunoreceptor with immunoglobulin and ITIM domains; Tbet/Tbx21
    DOI:  https://doi.org/10.1186/s13045-022-01352-x
  10. Future Med Chem. 2022 Sep 15.
      Background: Owing to the chronic nature of Type 2 diabetes mellitus, antidiabetic drugs must have long-lasting efficacy. Compound 1 has a good inhibitory effect on acute hyperglycemia, but its long-term hypoglycemic effect has not been evaluated. Results: Preliminary prediction and in vitro experimental pharmacokinetic results support the use of compound 1 for long-term in vivo experiments. Long-term experiments demonstrated that compound 1 significantly reduces blood glucose, improves the oral glucose tolerance of obese mice and has a positive effect on body weight, free fatty acid, hepatocyte steatosis and inflammatory cell infiltration. Conclusion: These findings lay a good foundation for the further exploration and development of novel glycogen phosphorylase inhibitors.
    Keywords:  benzazepinone derivative; glycogen phosphorylase inhibitor; long-term hypoglycemic; obese Type 2 diabetes mellitus; pharmacokinetic; pharmacological
    DOI:  https://doi.org/10.4155/fmc-2022-0115
  11. Bioorg Chem. 2022 Sep 03. pii: S0045-2068(22)00526-0. [Epub ahead of print]129 106120
      The purpose of this study was to evaluate the effect of GP inhibitor as a potential pharmaceutical target on MI/R injury. Four different structural types of novel compounds (I, II, III, and IV) were designed and synthesized, obtaining 31 novel GP inhibitors. SAR studies revealed that the conjugates of 5-chloroindole with benzo six-membered heterocyclic were found to elevate the activity. In particular, compound IIIh (IC50 = 0.21 ± 0.03 µM) emerged as a potent derivative against RMGPa, being approximately 2-fold less potent than that of PSN-357. In order to screen out a compound for in vivo activity test, we further conducted an experiment of inhibition against three different subtypes of GPa (HLGPa, HMGPa and HBGPa) and the corresponding affinity experiment. As a result, compound IIIh showed strong inhibitory activity against the above three subtypes of GP, especially on HBGPa (IC50 = 0.09 ± 0.002 µM), which was relatively close to that of positive control ingliforib (IC50 = 0.16 ± 0.02 µM). The affinity of compound IIIh to HBGPa was 4.3 times higher than that of HLGPa, and 1.1 times higher than that of HMGPa. This fact further proved that compound IIIh has a higher inhibitory effect on HMGPa than the other two subtypes. Besides, in vivo activity evaluation demonstrated that compound IIIh exhibited obviously cardioprotective effect on MI/R injury mice. The discovery of compound IIIh provides a new strategy for developing novel GP inhibitors with myocardial ischemia protection.
    Keywords:  Glycogen phosphorylase inhibitors; Heterocyclic derivatives; Myocardial ischemia injury; Structure-activity relationship
    DOI:  https://doi.org/10.1016/j.bioorg.2022.106120
  12. Exp Biol Med (Maywood). 2022 Sep 15. 15353702221117128
      The aim of this study was to explore effects of naringin (Nar) on antifatigue ability; the weight-loaded and non-loading swimming tests were performed. Compared with the control group, dietary supplementation of Nar significantly prolonged the weight-loaded swimming time to exhaustion of mice (P < 0.01). Nar significantly reduced the serum lactic acid (LD) level (P < 0.05) and lactate dehydrogenase (LDH) activity (P < 0.001), while increased the serum non-esterified free fatty acids (NEFA) level (P < 0.001). In addition, Nar significantly increased the liver glycogen and muscle glycogen contents (P < 0.05) and the phosphoenolpyruvate carboxykinase (PEPCK) (P < 0.01) and glucokinase (GCK) mRNA levels (P < 0.001) in liver and gastrocnemius (GAS) muscle. Furthermore, Nar significantly improved the antioxidant capacity, mitochondrial function, and muscle mitochondrial fatty acid β-oxidation (P < 0.05), and decreased inflammation and muscle damage-related gene expression (P < 0.05). These findings suggested that Nar can improve antifatigue effect by enhancing antioxidant capacity and mitochondrial function and preventing muscle damage.
    Keywords:  Naringin; antifatigue; antioxidant capacity; mitochondrial function; muscle damage
    DOI:  https://doi.org/10.1177/15353702221117128