The laforin-malin complex negatively regulates glycogen synthesis by modulating cellular glucose uptake via glucose transporters

Molecular and Cellular Biology

Volumn 32, Issue 3, 2012, Pages 652-663

  Singh, Pankaj Kumar ^a   Singh, Sweta ^a   Ganesh, Subramaniam ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

[No Author keywords available]

Indexed keywords

5' AMP ACTIVATED PROTEIN KINASE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; GLUCOSE TRANSPORTER; LAFORIN; MALIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; GLUCOSE TRANSPORT; GLYCOGEN ANALYSIS; GLYCOGEN SYNTHESIS; HUMAN; HUMAN CELL; MYOCLONUS EPILEPSY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN STABILITY;

ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; COS CELLS; GLUCOSE; GLUCOSE TRANSPORT PROTEINS, FACILITATIVE; GLYCOGEN; HUMANS; INCLUSION BODIES; LAFORA DISEASE; MICE; PROTEIN TYROSINE PHOSPHATASES, NON-RECEPTOR;

ANIMALIA;

EID: 84863011221     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06353-11     Document Type: Article

References (53)

1. Becker M, Newman S, Ismail-Beigi F. 1996. Stimulation of GLUT1 glucose transporter expression in response to inhibition of oxidative phosphorylation: role of reduced sulfhydryl groups. Mol. Cell. Endocrinol. 121:165-170.
2. Bell B, Xing H, Yan K, Gautam N, Muslin AJ. 1999. KSR-1 binds to G-protein βγ subunits and inhibits βγ-induced mitogen-activated protein kinase activation. J. Biol. Chem. 274:7982-7986.
3. Boer P, Sperling O. 2004. Modulation of glycogen phosphorylase activity affects 5-phosphoribosyl-1-pyrophosphate availability in rat hepatocyte cultures. Nucleosides Nucleotides Nucleic Acids 23:1235-1239.
4. Carruthers A, DeZutter J, Ganguly A, Devaskar SU. 2009. Will the original glucose transporter isoform please stand up! Am. J. Physiol. 297: E836-E848.
5. Chan EM, et al. 2004. Laforin preferentially binds the neurotoxic starchlike polyglucosans, which form in its absence in progressive myoclonus epilepsy. Hum. Mol. Genet. 13:1117-1129.
6. Chan EM, et al. 2003. Mutations in NHLRC1 cause progressive myoclonus epilepsy. Nat. Genet. 35:125-127.
7. Cheng A, et al. 2007. A role for AGL ubiquitination in the glycogen storage disorders of Lafora and Cori's disease. Genes Dev. 21:2399 -2409.
8. Cid E, Cifuentes D, BaquÉ S, Ferrer JC, Guinovart JJ. 2005. Determinants of the nucleocytoplasmic shuttling of muscle glycogen synthase. FEBS J. 272:3197-3213.
9. Coore HG, Randle PJ. 1964. Inhibition of glucose phosphorylation by mannoheptulose. Biochem. J. 91:56 -59.
10. Davies SP, Carling D, Hardie DG. 1989. Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMPdependent protein kinase, studied using a specific and sensitive peptide assay. Eur. J. Biochem. 186:123-128.
11. DePaoli-Roach AA, et al. 2010. Genetic depletion of the malin E3 ubiquitin ligase in mice leads to Lafora bodies and the accumulation of insoluble laforin. J. Biol. Chem. 285:25372-25381.
12. Dombrowski L, Roy D, Marcotte B, Marette A. 1996. A new procedure for the isolation of plasma membranes, T tubules, and internal membranes from skeletal muscle. Am. J. Physiol. 270:E667-E676.
13. Dubey D, Ganesh S. 2008. Modulation of functional properties of laforin phosphatase by alternative splicing reveals a novel mechanism for the EPM2Agene in Lafora progressive myoclonus epilepsy. Hum. Mol. Genet. 17:3010 -3020.
14. Fernández-Sánchez ME, et al. 2003. Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glycogen accumulation. Hum. Mol. Genet. 12:3161-3171.
15. Ganesh S, et al. 2000. Laforin, defective in the progressive myoclonus epilepsy of Lafora type, is a dual-specificity phosphatase associated with polyribosomes. Hum. Mol. Genet. 9:2251-2261.
16. Ganesh S, et al. 2002. Targeted disruption of the Epm2a gene causes formation of Lafora inclusion bodies, neurodegeneration, ataxia, myoclonus epilepsy and impaired behavioral response in mice. Hum. Mol. Genet. 11:1251-1262.
17. Ganesh S, Puri R, Singh S, Mittal S, Dubey D. 2006. Recent advances in the molecular basis of Lafora's progressive myoclonus epilepsy. J. Hum. Genet. 51:1- 8.
18. Ganesh S, et al. 2004. The carbohydrate-binding domain of Lafora disease protein targets Lafora polyglucosan bodies. Biochem. Biophys. Res. Commun. 313:1101-1109.
19. Garyali P, et al. 2009. The laforin-malin complex suppresses the cellular toxicity of misfolded proteins by promoting their degradation through the ubiquitin-proteasome system. Hum. Mol. Genet. 18:688 -700.
20. Gentry MS, Worby CA, Dixon JE. 2005. Insights into Lafora disease: malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin. Proc. Natl. Acad. Sci. U. S. A. 102:8501- 8506.
21. Guinez C, et al. 2008. Protein ubiquitination is modulated by O-GlcNAc glycosylation. FASEB J. 22:2901-2911.
22. Hardie DG. 2007. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 8:774 -785.
23. Hawley SA, Gadalla AE, Olsen GS, Hardie DG. 2002. The antidiabetic drug metformin activates the AMP-activated protein kinase cascade via an adenine nucleotide-independent mechanism. Diabetes 51:2420 -2425.
24. Hresko RC, Heimberg H, Chi MM, Mueckler M. 1998. Glucosamineinduced insulin resistance in 3T3-L1 adipocytes is caused by depletion of intracellular ATP. J. Biol. Chem. 273:20658 -20668.
25. James LR, et al. 2002. Flux through the hexosamine pathway is a determinant of nuclear factor _B-dependent promoter activation. Diabetes 51: 1146-1156.
26. Johnston M. 1999. Feasting, fasting and fermenting. Glucose sensing in yeast and other cells. Trends Genet. 15:29 -33.
27. Liu Y, Wang Y, Wu C, Liu Y, Zheng P. 2006. Dimerization of laforin is required for its optimal phosphatase activity, regulation of GSK3_ phosphorylation, and Wnt signaling. J. Biol. Chem. 28:34768 -34774.
28. Luiken JJ, et al. 2004. Regulation of cardiac long-chain fatty acid and glucose uptake by translocation of substrate transporters. Pflugers Arch. 448:1-15.
29. Luo B, et al. 2007. Chronic hexosamine flux stimulates fatty acid oxidation by activating AMP-activated protein kinase in adipocytes. J. Biol. Chem. 282:7172-7180.
30. Marshall S, Nadeau O, Yamasaki K. 2005. Glucosamine-induced activation of glycogen biosynthesis in isolated adipocytes. Evidence for a rapid allosteric control mechanism within the hexosamine biosynthesis pathway. J. Biol. Chem. 280:11018 -11024.
31. Medina RA, Owen GI. 2002. Glucose transporters: expression, regulation and cancer. Biol. Res. 35:9 -26.
32. Minassian BA, et al. 1998. Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat. Genet. 20:171-174.
33. Mittal S, Dubey D, Yamakawa K, Ganesh S. 2007. Lafora disease proteins malin and laforin are recruited to aggresomes in response to proteasomal impairment. Hum. Mol. Genet. 16:753-762.
34. Munekata K, Sakamoto K. 2009. Forkhead transcription factor Foxo1 is essential for adipocyte differentiation. In Vitro Cell. Dev. Biol. Anim. 45: 642-651.
35. Polekhina G, et al. 2003. AMPK beta subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13:867- 871.
36. Puri R, Suzuki T, Yamakawa K, Ganesh S. 2009. Hyperphosphorylation and aggregation of tau in laforin-deficient mice, an animal model for Lafora disease. J. Biol. Chem. 284:22657-22663.
37. Romá-Mateo C, et al. 2011.Laforin, a dual-specificity protein phosphatase involved in Lafora disease, is phosphorylated at Ser25 by AMPactivated protein kinase. Biochem. J. 439:265-275.
38. Salt IP, Johnson G, Ashcroft SJ, Hardie DG. 1998. AMP-activated protein kinase is activated by low glucose in cell lines derived from pancreatic beta cells, and may regulate insulin release. Biochem. J. 335:533- 539.
39. Sengupta S, Badwar I, Upadhyay M, Singh S, Ganesh S. 2011. Malin and laforin are essential components of a protein complex that protects cells from the thermal stress. J. Cell Sci. 124:2277-2286.
40. Shin BC, McKnight RA, Devaskar SU. 2004. Glucose transporter GLUT8 translocation in neurons is not insulin responsive. J. Neurosci. Res. 75: 835-844.
41. Singh S, Ganesh S. 2009. Lafora progressive myoclonus epilepsy: a metaanalysis of reported mutations in the first decade following the discovery of the EPM2A and NHLRC1 genes. Hum. Mutat. 30:715-723.
42. Solaz-Fuster MC, et al. 2008. Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMP-activated protein kinase pathway. Hum. Mol. Genet. 17:667- 678.
43. Tagliabracci VS, et al. 2007. Laforin is a glycogen phosphatase, deficiency of which leads to elevated phosphorylation of glycogen in vivo. Proc. Natl. Acad. Sci. U. S. A. 104:19262-19266.
44. Tagliabracci VS, et al. 2008. Abnormal metabolism of glycogen phosphate as a cause for Lafora disease. J. Biol. Chem. 283:33816 -33825.
45. Tagliabracci VS, et al. 2011. Phosphate incorporation during glycogen synthesis and Lafora disease. Cell. Metab. 13:274 -282.
46. Vernia S, et al. 2009. AMP-activated protein kinase phosphorylates R5/PTG, the glycogen targeting subunit of the R5/PTG-protein phosphatase 1 holoenzyme, and accelerates its down-regulation by the laforin-malin complex. J. Biol. Chem. 284:8247- 8255.
47. Vernia S, et al. 2011. Laforin, a dual specificity phosphatase involved in Lafora disease, regulates insulin response and whole-body energy balance in mice. Hum. Mol. Genet. 20:2571-2584.
48. Vilchez D, et al. 2007. Mechanism suppressing glycogen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat. Neurosci. 10:1407-1413.
49. Wang J, Stuckey JA, Wishart M, Dixon JE. 2002. A unique carbohydrate binding domain targets the Lafora disease phosphatase to glycogen. J. Biol. Chem. 277:2377-2380.
50. Wolfsdorf JI, Holm IA, Weinstein DA. 1999. Glycogen storage diseases: phenotypic, genetic, and biochemical characteristics, and therapy. Endocrinol. Metab. Clin. North. Am. 4:801- 823.
51. Yokoi S, Austin J, Witmer F, Sakai M. 1968. Studies in myoclonus epilepsy (Lafora body form). I. Isolation and preliminary characterization of Lafora bodies in two cases. Arch. Neurol. 19:15-33.
52. Yokoi S, Nakayama H, Negishi T. 1975. Biochemical studies on tissues from a patient with Lafora disease. Clin. Chim Acta 62:415- 423.
53. Zhong D, et al. 2008. 2-Deoxyglucose induces Akt phosphorylation via a mechanism independent of LKB1/AMP-activated protein kinase signaling activation or glycolysis inhibition. Mol. Cancer Ther. 4:809-817.