bims-glecem Biomed News
on Glycogen metabolism in exercise, cancer and energy metabolism
Issue of 2022–06–05
thirteen papers selected by
Dipsikha Biswas, Københavns Universitet



  1. J Biol Chem. 2022 May 30. pii: S0021-9258(22)00534-8. [Epub ahead of print] 102093
      Autophagy is an essential cellular process involving degradation of superfluous or defective macromolecules and organelles as a form of homeostatic recycling. Initially proposed to be a 'bulk' degradation pathway, a more nuanced appreciation of selective autophagy pathways has developed in the literature in recent years. As a glycogen-selective autophagy process, 'glycophagy' is emerging as a key metabolic route of transport and delivery of glycolytic fuel substrate. Study of glycophagy is at an early stage. Enhanced understanding of this major non-canonical pathway of glycogen flux will provide important opportunities for new insights into cellular energy metabolism. In addition, glycogen metabolic mishandling is centrally involved in the pathophysiology of several metabolic diseases in a wide range of tissues, including liver, skeletal muscle, cardiac muscle, and brain. Thus, advances in this exciting new field are of broad multi-disciplinary interest relevant to many cell types and metabolic states. Here, we review the current evidence of glycophagy involvement in homeostatic cellular metabolic processes and of molecular mediators participating in glycophagy flux, We integrate information from a variety of settings including cell lines, primary cell culture systems, ex vivo tissue preparations, genetic disease models and clinical glycogen disease states.
    Keywords:  Atg8; Gabarapl1; Stbd1; autophagy; glycogen; glycophagy; lysosome
    DOI:  https://doi.org/10.1016/j.jbc.2022.102093
  2. Neuromuscul Disord. 2022 Mar 31. pii: S0960-8966(22)00100-6. [Epub ahead of print]
      Muscle Glycogenosis type 0 (GSD 0B) is an extremely rare disorder first recognized in 2007 in three siblings with childhood onset and severe cardiomyopathy. Since then, a few cases with severe cardiac involvement and premature death have been reported. We describe two unrelated cases presenting with an adult-onset myopathy with no heart involvement. Clinical features were quite similar in both patients, mainly characterized by early fatigability, myalgia and muscle weakness. Muscle biopsy revealed marked glycogen depletion in nearly all myofibers. Biochemical assay demonstrated a marked reduction of Glycogen Synthase (GS) activity. Sequence analysis of GYS1 revealed two new variants: a homozygous G to C substitution in the splice donor consensus site (c.678+1G>C) in patient1 and a homozygous missense variant c.630G>C in exon 3 (p. Asp145His) in patient 2. This study describes a new phenotype of muscle GSD 0B presenting with adult onset, proximal myopathy, no cardiac abnormalities and a quite benign disease course. This report highlights the importance of a systematic diagnostic approach that includes muscle morphology and enzymatic assay to facilitate the identification of adult patients with GSD0B.
    Keywords:  GSD0B; Metabolic myopathy; Muscle glycogenosis; Muscle morphologic studies; Muscle weakness
    DOI:  https://doi.org/10.1016/j.nmd.2022.03.008
  3. Front Cell Dev Biol. 2022 ;10 853003
      Glycogen synthase kinase-3β (GSK-3β) is a downstream target of oncogenic KRas and can accumulate in the nucleus in pancreatic ductal adenocarcinoma (PDA). To determine the interplay between oncogenic KRas and nuclear GSK-3β in PDA development, we generated Lox-STOP-Lox (LSL) nuclear-targeted GSK-3β animals and crossed them with LSL-KRasG12D mice under the control of the Pdx1-cre transgene-referred to as KNGC. Interestingly, 4-week-old KNGC animals show a profound loss of acinar cells, the expansion of ductal cells, and the rapid development of cystic-like lesions reminiscent of intraductal papillary mucinous neoplasm (IPMN). RNA-sequencing identified the expression of several ductal cell lineage genes including AQP5. Significantly, the Aqp5+ ductal cell pool was proliferative, phenotypically distinct from quiescent pancreatic ductal cells, and deletion of AQP5 limited expansion of the ductal pool. Aqp5 is also highly expressed in human IPMN along with GSK-3β highlighting the putative role of Aqp5+ ductal cells in human preneoplastic lesion development. Altogether, these data identify nGSK-3β and KRasG12D as an important signaling node promoting the retention of pancreatic ductal progenitor cells, which could be used to further characterize pancreatic ductal development as well as lineage biomarkers related to IPMN and PDA.
    Keywords:  AQP5; GSK-3β; KRAS; intraductal papillary mucinous neoplasm; pancreatic adenocarcinoma; progenitor cell
    DOI:  https://doi.org/10.3389/fcell.2022.853003
  4. Development. 2022 May 15. pii: dev200229. [Epub ahead of print]149(10):
      In most sexually reproducing animals, sperm entry provides the signal to initiate the final stages of female meiosis. In Caenorhabditis elegans, this signal is required for completion of female anaphase I and entry into meiosis II (MII). memi-1/2/3 (meiosis-to-mitosis) encode maternal components that facilitate this process; memi-1/2/3(RNAi) results in a skipped-MII phenotype. Previously, we used a gain-of-function mutation, memi-1(sb41), to identify genetic suppressors that represent candidates for the sperm-delivered signal. Herein, we characterize two suppressors of memi-1(sb41): gskl-1 and gskl-2. Both genes encode functionally redundant sperm glycogen synthase kinase, type 3 (GSK3) protein kinases. Loss of both genes causes defects in male spermatogenesis, sperm pseudopod treadmilling and paternal-effect embryonic lethality. The two kinases locate within the pseudopod of activated sperm, suggesting that they directly or indirectly regulate the sperm cytoskeletal polymer major sperm protein (MSP). The GSK3 genes genetically interact with another memi-1(sb41) suppressor, gsp-4, which encodes a sperm-specific PP1 phosphatase, previously proposed to regulate MSP dynamics. Moreover, gskl-2 gsp-4; gskl-1 triple mutants often skip female MII, similar to memi-1/2/3(RNAi). The GSK3 kinases and PP1 phosphatases perform similar sperm-related functions and work together for post-fertilization functions in the oocyte that involve MEMI.
    Keywords:   Caenorhabditis elegans ; Fertilization; GSK3; MSP; Meiosis; Sperm motility; Spermatogenesis
    DOI:  https://doi.org/10.1242/dev.200229
  5. J Dermatol Sci. 2022 May 11. pii: S0923-1811(22)00123-2. [Epub ahead of print]
       BACKGROUND: Glycogen synthase kinase-3 (GSK-3) inhibitors are considered to activate Wnt/β-Catenin, which remains a controversial topic in melanoma treatment.
    OBJECTIVE: Here, we have developed Pym-5, an attractive GSK-3 inhibitor. Using Pym-5 as a chemical tool to probe the GSK-3 biology, we aimed to investigate the potential of GSK-3 inhibition as a strategy of melanoma treatment and underlying mechanisms.
    METHODS: Using pigment B16 and B16BL6 murine melanoma model in vitro and a zebrafish pigmentation model in vivo, we investigated Pym-5-meditaed activation of Wnt/β-Catenin, melanogenesis and antitumor response in melanoma treatment.
    RESULTS: We found that Pym-5 delayed the growth and promoted melanogenesis of melanoma cells. Pym-5 activated the transcription of β-Catenin and responsive targets genes (AXIN2 and MITF), melanin biosynthesis genes (TYR, TYRP1 and TYRP2) and eventually elevated the production of melanin. Interestingly, genetic inactivation of GSK-3β, but not its paralogue GSK-3α, compromised Pym-5-mediated melanogenesis in B16 and B16BL6 cells.
    CONCLUSION: These data provide insight into the potential therapeutic benefits obtained from activation of Wnt/β-Catenin signaling pathway and how Pym-5 can regulate melanin production and the rationale for future clinical application of GSK-3 inhibitor in melanoma patients.
    Keywords:  GSK-3β; Melanogenesis; Melanoma; Pym-5
    DOI:  https://doi.org/10.1016/j.jdermsci.2022.05.003
  6. J Mol Graph Model. 2022 May 22. pii: S1093-3263(22)00104-8. [Epub ahead of print]115 108225
      Cancer malignancies require the application of advanced strategies leading to the development of novel theranostic. Quite often drugs target a variety of receptors in the cell signaling cascades that could be explored to combat aggressive tumors. Herein, two receptors that are over-expressed during the diagnosis of breast cancer are used as the primary drug targets, inclusively Glycogen Synthase kinase -3 beta (GSK-3Β) and Inhibitor of nuclear factor kappa kinase-beta (IKK-β). Dual-targeting inhibitors pave the way for a challenging pathway in the treatment of aberrant tumor progression. The present study involves the observation of similarities in the structure of the receptors, along with the designing of novel therapeutics that act on them by molecular docking followed by a pharmacokinetic screening approach. A 3D QSAR modeling study is performed to approach the functionality of the bioactive conformer molecules. Additionally, Molecular Dynamic Simulation parameters are used for the validation of the drug complexes. Already available inhibitors are used as reference compounds and a library of analogs generated for these compounds from the PubChem database has been used for in silico designing of novel inhibitors. Molecular Docking and ADME analysis narrowed down the vast library of compounds to two specific classes of chemical compounds. Molecular Dynamic simulation studies used for the selection of the novel moieties showed significant superiority in their stability studies and binding trajectories resulted in two novel molecules A6 and B3 that could inhibit the kinase receptors. The current work involves computational designing of therapeutics targeting two major oncogenic proteins.
    Keywords:  Dual targetting; GSK-3B; IKK-β; In silico drug designing; Molecular dynamics simulation
    DOI:  https://doi.org/10.1016/j.jmgm.2022.108225
  7. Food Chem. 2022 May 23. pii: S0308-8146(22)01256-0. [Epub ahead of print]393 133294
      Glycogen branching enzymes (GBEs) have been used to generate new branches in starches for producing slowly digestible starches. The aim of this study was to expand the knowledge about the mode of action of these enzymes by identifying structural aspects of starchy substrates affecting the products generated by different GBEs. The structures obtained from incubating five GBEs (three from glycoside hydrolase family (GH) 13 and two from GH57) on five different substrates exhibited minor but statistically significant correlations between the amount of longer chains (degree of polymerization (DP) 9-24) of the product and both the amylose content and the degree of branching of the substrate (Pearson correlation coefficient of ≤-0.773 and ≥0.786, respectively). GH57 GBEs mainly generated large products with long branches (100-700 kDa and DP 11-16) whereas GH13 GBEs produced smaller products with shorter branches (6-150 kDa and DP 3-10).
    Keywords:  Chain length distribution; Glycogen branching enzyme; Maltodextrin; Molecular size; Starch
    DOI:  https://doi.org/10.1016/j.foodchem.2022.133294
  8. Eur J Appl Physiol. 2022 Jun 01.
       PURPOSE: Studies have indicated upper body involvement during football, provoking long-term muscular adaptations. This study aimed at examining the acute metabolic response in upper and lower body skeletal muscle to football training organized as small-sided games (SSG).
    METHODS: Ten healthy male recreational football players [age 24 ± 1 (± SD) yrs; height 183 ± 4 cm; body mass 83.1 ± 9.7 kg; body fat 15.5 ± 5.4%] completed 1-h 5v5 SSG (4 × 12 min interspersed with 4-min recovery periods). Muscle biopsies were obtained from m. vastus lateralis (VL) and m. deltoideus (DE) pre- and post-SSG for muscle glycogen and metabolite analyses. Blood lactate samples were obtained at rest, middle and end of the SSG.
    RESULTS: Muscle glycogen in VL decreased (P < 0.01) by 21% and tended (P = 0.08) to decrease in DE by 13%. Muscle lactate increased in VL (117%; P < 0.001) and DE (81%; P < 0.001) during the game, while blood lactate rose threefold. Muscle ATP and PCr were unaltered, but intermuscular differences were detected for ATP at both time points (P < 0.001) and for PCr at pre-SSG (P < 0.05) with VL demonstrating higher values than DE, while muscle creatine rose in VL (P < 0.001) by 41% and by 22% in DE (P = 0.02). Baseline citrate synthase maximal activity was higher (P < 0.05) in VL compared to DE, whereas baseline muscle lactate concentration was higher (P < 0.05) in DE than VL.
    CONCLUSION: The upper body may be extensively involved during football play, but besides a rise in muscle lactate in the deltoideus muscle similar to the leg muscles, the present study did not demonstrate acute metabolic changes of an order that may explain the previously reported training effect of football play in the upper extremities.
    Keywords:  Lower body; Muscle glycogen; Muscle lactate; Muscle metabolites; Oxidative capacity; Soccer; Upper body
    DOI:  https://doi.org/10.1007/s00421-022-04970-y
  9. MicroPubl Biol. 2022 ;2022
      Excess triglycerides from the diet are stored in structures called lipid droplets in adipose tissue. Genome-wide RNAi screens have identified mRNA splicing factors as important for lipid droplet formation; however, the full complement of splicing factors that regulate lipid storage is not known. Here, we characterize the role of snRNP-U1-70K , the gene encoding for a splicing protein involved in recognizing the 5' splice site in introns, in regulating lipid and carbohydrate storage in the Drosophila fat body. Decreasing snRNP-U1-70K specifically in the fly fat body resulted in less triglyceride, glycogen, and glucose in each fat body cell. Consistent with these decreased nutrient storage phenotypes, snRNP-U1-70K-RNAi flies ate less, providing a potential cause for less lipid and carbohydrate storage in these flies. These data further support the role of mRNA processing in regulating metabolic homeostasis in Drosophila .
    DOI:  https://doi.org/10.17912/micropub.biology.000580
  10. Braz J Med Biol Res. 2022 ;pii: S0100-879X2022000100304. [Epub ahead of print]55 e11795
      There is a high incidence of non-obese type 2 diabetes mellitus (non-obese-T2DM) cases, particularly in Asian countries, for which the pathogenesis remains mainly unclear. Interestingly, Goto-Kakizaki (GK) rats spontaneously develop insulin resistance (IR) and non-obese-T2DM, making them a lean diabetes model. Physical exercise is a non-pharmacological therapeutic approach to reduce adipose tissue mass, improving peripheral IR, glycemic control, and quality of life in obese animals or humans with T2DM. In this narrative review, we selected and analyzed the published literature on the effects of physical exercise on the metabolic features associated with non-obese-T2DM. Only randomized controlled trials with regular physical exercise training, freely executed physical activity, or skeletal muscle stimulation protocols in GK rats published after 2008 were included. The results indicated that exercise reduces plasma insulin levels, increases skeletal muscle glycogen content, improves exercise tolerance, protects renal and myocardial function, and enhances blood oxygen flow in GK rats.
    DOI:  https://doi.org/10.1590/1414-431X2022e11795
  11. Biochim Biophys Acta Mol Cell Res. 2022 May 27. pii: S0167-4889(22)00092-1. [Epub ahead of print] 119300
      Exercise-induced physical endurance enhancement and skeletal muscle remodeling can prevent and delay the development of multiple diseases, especially metabolic syndrome. Herein, the study explored the association between glucagon-like peptide-1 (GLP-1) secretion and exercise, and its effect on skeletal muscle remodeling to enhance endurance capacity. We found both acute exercise and short-term endurance training significantly increased the secretion of GLP-1 in mice. Recombinant adeno-associated virus (AAV) encoding Gcg (proglucagon) was used to induce the overexpression of GLP-1 in skeletal muscle of mice. Overexpression of GLP-1 in skeletal muscle enhanced endurance capacity. Meanwhile, glycogen synthesis, glucose uptake, type I fibers proportion, and mitochondrial biogenesis were augmented in GLP-1-AAV skeletal muscle. Furthermore, the in vitro experiment showed that exendin-4 (a GLP-1 receptor agonist) treatment remarkably promoted glucose uptake, type I fibers formation, and mitochondrial respiration. Mechanistically, the knockdown of AMPK could reverse the effects imposed by GLP-1R activation in vitro. Taken together, these results verify that GLP-1 regulates skeletal muscle remodeling to enhance exercise endurance possibly via GLP-1R signaling-mediated phosphorylation of AMPK.
    Keywords:  Endurance capacity; GLP-1; Glycogen storage; Mitochondrial biogenesis; Muscle fiber type
    DOI:  https://doi.org/10.1016/j.bbamcr.2022.119300
  12. PLoS Genet. 2022 Jun;18(6): e1010228
      NGLY1 deficiency, a rare disease with no effective treatment, is caused by autosomal recessive, loss-of-function mutations in the N-glycanase 1 (NGLY1) gene and is characterized by global developmental delay, hypotonia, alacrima, and seizures. We used a Drosophila model of NGLY1 deficiency to conduct an in vivo, unbiased, small molecule, repurposing screen of FDA-approved drugs to identify therapeutic compounds. Seventeen molecules partially rescued lethality in a patient-specific NGLY1 deficiency model, including multiple serotonin and dopamine modulators. Exclusive dNGLY1 expression in serotonin and dopamine neurons, in an otherwise dNGLY1 deficient fly, was sufficient to partially rescue lethality. Further, genetic modifier and transcriptomic data supports the importance of serotonin signaling in NGLY1 deficiency. Connectivity Map analysis identified glycogen synthase kinase 3 (GSK3) inhibition as a potential therapeutic mechanism for NGLY1 deficiency, which we experimentally validated with TWS119, lithium, and GSK3 knockdown. Strikingly, GSK3 inhibitors and a serotonin modulator rescued size defects in dNGLY1 deficient larvae upon proteasome inhibition, suggesting that these compounds act through NRF1, a transcription factor that is regulated by NGLY1 and regulates proteasome expression. This study reveals the importance of the serotonin pathway in NGLY1 deficiency, and serotonin modulators or GSK3 inhibitors may be effective therapeutics for this rare disease.
    DOI:  https://doi.org/10.1371/journal.pgen.1010228
  13. Redox Biol. 2022 May 17. pii: S2213-2317(22)00111-2. [Epub ahead of print]53 102339
      Cervical cancer is one of the most common gynecological malignancies with poor prognosis due to constant chemoresistance and repeated relapse. Ciclopirox olamine (CPX), a synthetic antifungal agent, has recently been identified to be a promising anti-cancer candidate. However, the detailed mechanisms related to its anti-cancer effects remain unclear and need to be further elucidated. In this study, we found that CPX could induce proliferation inhibition in cervical cancer cells by targeting PARK7. Further results demonstrated that CPX could induce cytoprotective autophagy by downregulating the expression of PARK7 to activate PRKAA1 or by PARK7-independent accumulation of ROS to inhibit mTOR signaling. Meanwhile, CPX treatment increased the glycogen clustering and glycophagy in cervical cancer cells. The presence of N-acetyl-l-cysteine (NAC), a ROS scavenger, led to further clustering of glycogen in cells by reducing autophagy and enhancing glycophagy, which promoted CPX-induced inhibition of cervical cancer cell proliferation. Together, our study provides new insights into the molecular mechanisms of CPX in the anti-cancer therapy and opens new avenues for the glycophagy in cancer therapeutics.
    Keywords:  CPX; Cervical cancer; Glycophagy; PARK7/DJ-1; ROS
    DOI:  https://doi.org/10.1016/j.redox.2022.102339