Induction of autophagy improves hepatic lipid metabolism in glucose-6-phosphatase deficiency

Journal of Hepatology

Volumn 64, Issue 2, 2016, Pages 370-379

  Farah, Benjamin L ^a   Landau, Dustin J ^b   Sinha, Rohit A ^a   Brooks, Elizabeth D ^b   Wu, Yajun ^c   Fung, Suet Yin Sarah ^a   Tanaka, Tomohiro ^d   Hirayama, Masahiro ^d   Bay, Boon Huat ^c   Koeberl, Dwight D ^b,e   Yen, Paul M ^a,b  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d TOHOKU UNIVERSITY   (Japan)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; Glucose 6 phosphatase; Glucose 6 phosphate; Glycogen; GSDIa; Hepatic steatosis; Lipophagy; Rapamycin; ULK1; von Gierkes disease

Indexed keywords

CELL PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; RAPAMYCIN; TRIACYLGLYCEROL; UNC51 LIKE KINASE 1; UNCLASSIFIED DRUG; GLUCOSE 6 PHOSPHATASE; IMMUNOSUPPRESSIVE AGENT; SERINE THREONINE PROTEIN KINASE ULK1; TARGET OF RAPAMYCIN KINASE; ULK1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL CULTURE; CELL STIMULATION; CONTROLLED STUDY; DOG; ENZYME INHIBITION; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; GLYCOGEN ANALYSIS; HEPATIC CLEARANCE; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LIPID STORAGE; LIVER CELL; LIVER FUNCTION; LIVER INJURY; LIVER METABOLISM; LIVER SIZE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; GLYCOGEN STORAGE DISEASE TYPE 1; LIVER; METABOLISM; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN-1 HOMOLOG; DOGS; GLUCOSE-6-PHOSPHATASE; GLYCOGEN STORAGE DISEASE TYPE I; HEPATOCYTES; IMMUNOSUPPRESSIVE AGENTS; LIPID METABOLISM; LIVER; MICE; ORGAN SIZE; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRIGLYCERIDES;

EID: 84954375734     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.10.008     Document Type: Article

References (44)

1. J.Y. Chou, H.S. Jun, and B.C. Mansfield Glycogen storage disease type I and G6Pase-beta deficiency: etiology and therapy Nat Rev Endocrinol 6 2010 676 688
2. R. Froissart, M. Piraud, A.M. Boudjemline, C. Vianey-Saban, F. Petit, A. Hubert-Buron, and et al. Glucose-6-phosphatase deficiency Orphanet J Rare Dis 6 2011 27
3. D.D. Koeberl, P.S. Kishnani, and Y.T. Chen Glycogen storage disease types I and II: treatment updates J Inherit Metab Dis 30 2007 159 164
4. L.M. Franco, V. Krishnamurthy, D. Bali, D.A. Weinstein, P. Arn, B. Clary, and et al. Hepatocellular carcinoma in glycogen storage disease type Ia: a case series J Inherit Metab Dis 28 2005 153 162
5. S.K. Reddy, P.S. Kishnani, J.A. Sullivan, D.D. Koeberl, D.M. Desai, M.A. Skinner, and et al. Resection of hepatocellular adenoma in patients with glycogen storage disease type Ia J Hepatol 47 2007 658 663
6. S. Barth, D. Glick, and K.F. Macleod Autophagy: assays and artifacts J Pathol 221 2010 117 124
7. N. Mizushima, and M. Komatsu Autophagy: renovation of cells and tissues Cell 147 2011 728 741
8. J. Ezaki, N. Matsumoto, M. Takeda-Ezaki, M. Komatsu, K. Takahashi, Y. Hiraoka, and et al. Liver autophagy contributes to the maintenance of blood glucose and amino acid levels Autophagy 7 2011 727 736
9. O.B. Kotoulas, S.A. Kalamidas, and D.J. Kondomerkos Glycogen autophagy Microsc Res Tech 64 2004 10 20
10. R. Singh, S. Kaushik, Y. Wang, Y. Xiang, I. Novak, M. Komatsu, and et al. Autophagy regulates lipid metabolism Nature 458 2009 1131 1135
11. Y. Fukuo, S. Yamashina, H. Sonoue, A. Arakawa, E. Nakadera, T. Aoyama, and et al. Abnormality of autophagic function and cathepsin expression in the liver from patients with non-alcoholic fatty liver disease Hepatol Res 44 2014 1026 1036
12. T. Kamimoto, S. Shoji, T. Hidvegi, N. Mizushima, K. Umebayashi, D.H. Perlmutter, and et al. Intracellular inclusions containing mutant alpha1-antitrypsin Z are propagated in the absence of autophagic activity J Biol Chem 281 2006 4467 4476
13. T.C. Tan, D.H. Crawford, L.A. Jaskowski, V.N. Subramaniam, A.D. Clouston, D.I. Crane, and et al. Excess iron modulates endoplasmic reticulum stress-associated pathways in a mouse model of alcohol and high-fat diet-induced liver injury Lab Invest 93 2013 1295 1312
14. N. Raben, V. Hill, L. Shea, S. Takikita, R. Baum, N. Mizushima, and et al. Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease Hum Mol Genet 17 2008 3897 3908
15. J. Duran, A. Gruart, M. Garcia-Rocha, J.M. Delgado-Garcia, and J.J. Guinovart Glycogen accumulation underlies neurodegeneration and autophagy impairment in Lafora disease Hum Mol Genet 23 2014 3147 3156
16. A. Takamura, M. Komatsu, T. Hara, A. Sakamoto, C. Kishi, S. Waguri, and et al. Autophagy-deficient mice develop multiple liver tumors Genes Dev 25 2011 795 800
17. C.W. Lin, H. Zhang, M. Li, X. Xiong, X. Chen, X. Chen, and et al. Pharmacological promotion of autophagy alleviates steatosis and injury in alcoholic and non-alcoholic fatty liver conditions in mice J Hepatol 58 2013 993 999
18. J. Zhou, B.L. Farah, R.A. Sinha, Y. Wu, B.K. Singh, B.H. Bay, and et al. Epigallocatechin-3-gallate (EGCG), a green tea polyphenol, stimulates hepatic autophagy and lipid clearance PLoS One 9 2014 e87161
19. R.A. Sinha, B.L. Farah, B.K. Singh, M.M. Siddique, Y. Li, Y. Wu, and et al. Caffeine stimulates hepatic lipid metabolism by the autophagy-lysosomal pathway in mice Hepatology 59 2014 1366 1380
20. P.L. Jeffrey, D.H. Brown, and B.I. Brown Studies of lysosomal alpha-glucosidase. II. Kinetics of action of the rat liver enzyme Biochemistry 9 1970 1416 1422
21. O.B. Kotoulas, S.A. Kalamidas, and D.J. Kondomerkos Glycogen autophagy in glucose homeostasis Pathol Res Pract 202 2006 631 638
22. C.H. Jung, C.B. Jun, S.H. Ro, Y.M. Kim, N.M. Otto, J. Cao, and et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery Mol Biol Cell 20 2009 1992 2003
23. D.F. Egan, D.B. Shackelford, M.M. Mihaylova, S. Gelino, R.A. Kohnz, W. Mair, and et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy Science 331 2011 456 461
24. A. Roczniak-Ferguson, C.S. Petit, F. Froehlich, S. Qian, J. Ky, B. Angarola, and et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis Sci Signal 5 2012 ra42
25. X. Luo, G. Hall, S. Li, A. Bird, P.J. Lavin, M.P. Winn, and et al. Hepatorenal correction in murine glycogen storage disease type I with a double-stranded adeno-associated virus vector Mol Ther 19 2011 1961 1970
26. D.D. Koeberl, B.D. Sun, T.V. Damodaran, T. Brown, D.S. Millington, D.K. Benjamin Jr, and et al. Early, sustained efficacy of adeno-associated virus vector-mediated gene therapy in glycogen storage disease type Ia Gene Ther 13 2006 1281 1289
27. P.S. Kishnani, Y. Bao, J.Y. Wu, A.E. Brix, J.L. Lin, and Y.T. Chen Isolation and nucleotide sequence of canine glucose-6-phosphatase mRNA: identification of mutation in puppies with glycogen storage disease type Ia Biochem Mol Med 61 1997 168 177
28. A. Demaster, X. Luo, S. Curtis, K.D. Williams, D.J. Landau, E.J. Drake, and et al. Long-term efficacy following readministration of an adeno-associated virus vector in dogs with glycogen storage disease type Ia Hum Gene Ther 23 2012 407 418
29. B.L. Farah, R.A. Sinha, Y. Wu, B.K. Singh, J. Zhou, B.H. Bay, and et al. Beta-Adrenergic agonist and antagonist regulation of autophagy in HepG2 cells, primary mouse hepatocytes, and mouse liver PLoS One 9 2014 e98155
30. D.J. Klionsky, F.C. Abdalla, H. Abeliovich, R.T. Abraham, A. Acevedo-Arozena, K. Adeli, and et al. Guidelines for the use and interpretation of assays for monitoring autophagy Autophagy 8 2012 445 544
31. K.J. Lei, H. Chen, C.J. Pan, J.M. Ward, B. Mosinger Jr., E.J. Lee, and et al. Glucose-6-phosphatase dependent substrate transport in the glycogen storage disease type-1a mouse Nat Genet 13 1996 203 209
32. P.S. Kishnani, E. Faulkner, S. VanCamp, M. Jackson, T. Brown, A. Boney, and et al. Canine model and genomic structural organization of glycogen storage disease type Ia (GSD Ia) Vet Pathol 38 2001 83 91
33. B. Sun, S. Li, L. Yang, T. Damodaran, D. Desai, A.M. Diehl, and et al. Activation of glycolysis and apoptosis in glycogen storage disease type Ia Mol Genet Metab 97 2009 267 271
34. M. Komatsu, S. Kageyama, and Y. Ichimura P62/SQSTM1/A170: physiology and pathology Pharmacol Res 66 2012 457 462
35. H. Abrahamsen, H. Stenmark, and H.W. Platta Ubiquitination and phosphorylation of Beclin 1 and its binding partners: tuning class III phosphatidylinositol 3-kinase activity and tumor suppression FEBS Lett 586 2012 1584 1591
36. R.H. Bandsma, C.H. Wiegman, A.W. Herling, H.J. Burger, A. ter Harmsel, A.J. Meijer, and et al. Acute inhibition of glucose-6-phosphate translocator activity leads to increased de novo lipogenesis and development of hepatic steatosis without affecting VLDL production in rats Diabetes 50 2001 2591 2597
37. T.P. Neufeld Contribution of Atg1-dependent autophagy to TOR-mediated cell growth and survival Autophagy 3 2007 477 479
38. A. McBride, S. Ghilagaber, A. Nikolaev, and D.G. Hardie The glycogen-binding domain on the AMPK beta subunit allows the kinase to act as a glycogen sensor Cell Metab 9 2009 23 34
39. D.J. Roberts, V.P. Tan-Sah, E.Y. Ding, J.M. Smith, and S. Miyamoto Hexokinase-II positively regulates glucose starvation-induced autophagy through TORC1 inhibition Mol Cell 53 2014 521 533
40. G. Marino, F. Pietrocola, T. Eisenberg, Y. Kong, S.A. Malik, A. Andryushkova, and et al. Regulation of autophagy by cytosolic acetyl-coenzyme a Mol Cell 53 2014 710 725
41. J.A. Martina, Y. Chen, M. Gucek, and R. Puertollano MTORC1 functions as a transcriptional regulator of autophagy by preventing nuclear transport of TFEB Autophagy 8 2012 903 914
42. S.J. Ricoult, and B.D. Manning The multifaceted role of mTORC1 in the control of lipid metabolism EMBO Rep 14 2013 242 251
43. T. Hidvegi, M. Ewing, P. Hale, C. Dippold, C. Beckett, C. Kemp, and et al. An autophagy-enhancing drug promotes degradation of mutant alpha1-antitrypsin Z and reduces hepatic fibrosis Science 329 2010 229 232
44. Y.M. Lee, H.S. Jun, C.J. Pan, S.R. Lin, L.H. Wilson, B.C. Mansfield, and et al. Prevention of hepatocellular adenoma and correction of metabolic abnormalities in murine glycogen storage disease type Ia by gene therapy Hepatology 56 2012 1719 1729