Molecular pathways for glucose homeostasis, insulin signaling and autophagy in hepatitis C virus induced insulin resistance in a cellular model

Virology

Volumn 434, Issue 1, 2012, Pages 5-17

  Das, Gokul C ^a   Hollinger, F Blaine ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Atg conjugation; Autophagy; Glucose homeostasis; GSK 3 phosphorylation; Hepatitis C virus; Insulin signaling; IRS 1 phosphorylation

Indexed keywords

3 METHYLADENINE; AUTOPHAGY PROTEIN 5; BECLIN 1; BIOLOGICAL MARKER; GLUCOSE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3ALPHA; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INSULIN RECEPTOR SUBSTRATE 2; INTERFERON; PROTEIN KINASE B; SERINE;

ARTICLE; AUTOPHAGY; BIOLOGICAL MODEL; CELL GROWTH; CELL TRANSPORT; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INSULIN RESISTANCE; INSULIN SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRUS LOAD;

AMINO ACID SUBSTITUTION; AUTOPHAGY; CELL LINE; GLUCOSE; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASES; HEPACIVIRUS; HEPATOCYTES; HOMEOSTASIS; HUMANS; INSULIN; INSULIN RESISTANCE; MODELS, BIOLOGICAL; MUTANT PROTEINS; SIGNAL TRANSDUCTION;

HEPATITIS C VIRUS;

EID: 84868111785     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.07.003     Document Type: Article

References (95)

1. Aguirre V., Werner E.D., Giraud J., Lee Y.H., Shoelson S.E., White M.F. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 2002, 277:1531-1537.
2. Ait-Goughoulte M., Kanda T., Meyer K., Ryerse J.S., Ray R.B., Ray R. Hepatitis C virus genotype 1a growth and induction of autophagy. J. Virol. 2008, 82:2241-2249.
3. Alessi D.R., Deak M., Casamayor A., Caudwell F.B., Morrice N., Norman D.G., Gaffney P., Reese C.B., MacDougall C.N., Harbison D., Ashworth A., Bownes M. 3-phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol. 1997, 7:776-789.
4. Alessi D.R., Pearce L.R., Garcia-Martinez J.M. New insights into mTOR signaling: mTORC2 and beyond. Sci. Signal 2009, 2:e27.
5. Aytug S., Reich D., Sapiro L.E., Bernstein D., Begum N. Impaired IRS-1/PI3-kinase signaling in patients with HCV: a mechanism for increased prevalence of type 2 diabetes. Hepatology 2003, 38:1384-1392.
6. Azoulay-Alfaguter I., Yaffe Y., Licht-Murava A., Urbanska M., Jaworski J., Pietrokovski S., Hirschberg K., Eldar-Finkelman H. Distinct molecular regulation of glycogen synthase kinase-3alpha isozyme controlled by its N-terminal region: functional role in calcium/calpain signaling. J. Biol. Chem. 2011, 286:13470-13480.
7. Banerjee S., Saito K., Ait-Goughoulte M., Meyer K., Ray R.B., Ray R. Hepatitis C virus core protein upregulates serine phosphorylation of insulin receptor substrate-1 and impairs the downstream akt/protein kinase B signaling pathway for insulin resistance. J. Virol. 2008, 82:2606-2612.
8. Blumer R.M., van Roomen C.P., Meijer A.J., Houben-Weerts J.H., Sauerwein H.P., Dubbelhuis P.F. Regulation of adiponectin secretion by insulin and amino acids in 3T3-L1 adipocytes. Metabolism 2008, 57:1655-1662.
9. Boden G. Effects of free fatty acids (FFA) on glucose metabolism: significance for insulin resistance and type 2 diabetes. Exp. Clin. Endocrinol. Diabetes 2003, 111:121-124.
10. Cai Z., Zhang C., Chang K.S., Jiang J., Ahn B.C., Wakita T., Liang T.J., Luo G. Robust production of infectious hepatitis C virus (HCV) from stably HCV cDNA-transfected human hepatoma cells. J. Virol. 2005, 79:13963-13973.
11. Chen C.H., Shaikenov T., Peterson T.R., Aimbetov R., Bissenbaev A.K., Lee S.W., Wu J., Lin H.K., Sarbassov d.D ER stress inhibits mTORC2 and Akt signaling through GSK-3beta-mediated phosphorylation of rictor. Sci. Signal 2011, 4:ra10.
12. Ciaraldi T.P., Abrams L., Nikoulina S., Mudaliar S., Henry R.R. Glucose transport in cultured human skeletal muscle cells. Regulation by insulin and glucose in nondiabetic and non-insulin-dependent diabetes mellitus subjects. J. Clin. Invest. 1995, 96:2820-2827.
13. Codogno P., Mehrpour M., Proikas-Cezanne T. Canonical and non-canonical autophagy: variations on a common theme of self-eating?. Nat. Rev. Mol. Cell Biol. 2012, 13:7-12.
14. Cohen P., Frame S. The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2001, 2:769-776.
15. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995, 378:785-789.
16. D'Souza R., Sabin C.A., Foster G.R. Insulin resistance plays a significant role in liver fibrosis in chronic hepatitis C and in the response to antiviral therapy. Am. J. Gastroenterol. 2005, 100:1509-1515.
17. Ding V.W., Chen R.H., McCormick F. Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J. Biol. Chem. 2000, 275:32475-32481.
18. Dong H., Czaja M.J. Regulation of lipid droplets by autophagy. Trends Endocrinol. Metab. 2011, 22:234-240.
19. Duseja A., Dhiman R.K., Chawla Y., Thumburu K.K., Kumar A., Das A., Bhadada S., Bhansali A. Insulin resistance is common in patients with predominantly genotype 3 chronic hepatitis C. Dig. Dis. Sci. 2009, 54:1778-1782.
20. Eldar-Finkelman H., Argast G.M., Foord O., Fischer E.H., Krebs E.G. Expression and characterization of glycogen synthase kinase-3 mutants and their effect on glycogen synthase activity in intact cells. Proc. Nat. Acad. Sci. U.S.A. 1996, 93:10228-10233.
21. Erickson A.K., Seiwert S., Gale M. Antiviral potency analysis and functional comparison of consensus interferon, interferon-alpha2a and pegylated interferon-alpha2b against hepatitis C virus infection. Antiviral Ther. 2008, 13:851-862.
22. Furusaka A., Nishiyama M., Ohkawa K., Yamori T., Tsuruo T., Yonezawa K., Kasuga M., Hayashi S., Tanaka T. Expression of insulin receptor substrate-1 in hepatocytes: an investigation using monoclonal antibodies. Cancer Lett. 1994, 84:85-92.
23. Geng J., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep. 2008, 9:859-864.
24. Gonzalez C.D., Lee M.S., Marchetti P., Pietropaolo M., Towns R., Vaccaro M.I., Watada H., Wiley J.W. The emerging role of autophagy in the pathophysiology of diabetes mellitus. Autophagy 2011, 7:2-11.
25. Gopal K., Johnson T.C., Gopal S., Watfish A., Bang C.T., Suwandhi P., Pena-Sahdala H.N., Clain D.J., Bodenheimer H.C., Min A.D. Correlation between beta-lipoprotein levels and outcome of hepatitis C treatment. Hepatology 2006, 44:335-340.
26. He C., Bassik M.C., Moresi V., Sun K., Wei Y., Zou Z., An Z., Loh J., Fisher J., Sun Q., Korsmeyer S., Packer M., May H.I., Hill J.A., Virgin H.W., Gilpin C., Xiao G., Bassel-Duby R., Scherer P.E., Levine B. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 2012, 481:511-515.
27. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43:67-93.
28. Heaton N.S., Randall G. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe 2010, 8:422-432.
29. Herschkovitz A., Liu Y.F., Ilan E., Ronen D., Boura-Halfon S., Zick Y. Common inhibitory serine sites phosphorylated by IRS-1 kinases, triggered by insulin and inducers of insulin resistance. J. Biol. Chem. 2007, 282:18018-18027.
30. Hoeflich K.P., Luo J., Rubie E.A., Tsao M.S., Jin O., Woodgett J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000, 406:86-90.
31. Huynh K.K., Eskelinen E.L., Scott C.C., Malevanets A., Saftig P., Grinstein S. LAMP proteins are required for fusion of lysosomes with phagosomes. Embo J. 2007, 26:313-324.
32. Jacinto E., Facchinetti V., Liu D., Soto N., Wei S., Jung S.Y., Huang Q., Qin J., Su B. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 2006, 127:125-137.
33. Jope R.S., Yuskaitis C.J., Beurel E. Glycogen synthase kinase-3 (GSK3): inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32:577-595.
34. Julien L.A., Carriere A., Moreau J., Roux P.P. mTORC1-activated S6K1 phosphorylates rictor on threonine 1135 and regulates mTORC2 signaling. Mol. Cell. Biol. 2010, 30:908-921.
35. Jung H.S., Chung K.W., Won K.J., Kim J., Komatsu M., Tanaka K., Nguyen Y.H., Kang T.M., Yoon K.H., Kim J.W., Jeong Y.T., Han M.S., Lee M.K., Kim K.W., Shin J., Lee M.S. Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab. 2008, 8:318-324.
36. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J. 2000, 19:5720-5728.
37. Kanazawa T., Taneike I., Akaishi R., Yoshizawa F., Furuya N., Fujimura S., Kadowaki M. Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes. J. Biol. Chem. 2004, 279:8452-8459.
38. Kim K.W., Mutter R.W., Cao C., Albert J.M., Freeman M., Hallahan D.E., Lu B. Autophagy for cancer therapy through inhibition of pro-apoptotic proteins and mammalian target of rapamycin signaling. J. Biol. Chem. 2006, 281:36883-36890.
39. Lee Y.R., Lei H.Y., Liu M.T., Wang J.R., Chen S.H., Jiang-Shieh Y.F., Lin Y.S., Yeh T.M., Liu C.C., Liu H.S. Autophagic machinery activated by dengue virus enhances virus replication. Virology 2008, 374:240-248.
40. Liberman Z., Eldar-Finkelman H. Serine 332 phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 attenuates insulin signaling. J. Biol. Chem. 2005, 280:4422-4428.
41. Lindenbach B.D., Evans M.J., Syder A.J., Wolk B., Tellinghuisen T.L., Liu C.C., Maruyama T., Hynes R.O., Burton D.R., McKeating J.A., Rice C.M. Complete replication of hepatitis C virus in cell culture. Science 2005, 309:623-626.
42. Lindenbach B.D., Rice C.M. Unravelling hepatitis C virus replication from genome to function. Nature 2005, 436:933-938.
43. Liu C.L., Chen S., Dietrich D., Hu B.R. Changes in autophagy after traumatic brain injury. J. Cereb. Blood Flow Metab. 2008, 28:674-683.
44. Liu Y.F., Herschkovitz A., Boura-Halfon S., Ronen D., Paz K., LeRoith D., Zick Y. Serine phosphorylation proximal to its phosphotyrosine binding domain inhibits insulin receptor substrate 1 function and promotes insulin resistance. Mol. Cell Biol. 2004, 24:9668-9681.
45. Lok A.S., McMahon B.J. Chronic hepatitis B. Hepatology 2001, 34:1225-1241.
46. MacAulay K., Doble B.W., Patel S., Hansotia T., Sinclair E.M., Drucker D.J., Nagy A., Woodgett J.R. Glycogen synthase kinase 3alpha-specific regulation of murine hepatic glycogen metabolism. Cell Metab. 2007, 6:329-337.
47. Mai S., Muster B., Bereiter-Hahn J., Jendrach M. Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence lifespan. Autophagy 2012, 8.
48. Matsuda T., Zhai P., Maejima Y., Hong C., Gao S., Tian B., Goto K., Takagi H., Tamamori-Adachi M., Kitajima S., Sadoshima J. Distinct roles of GSK-3alpha and GSK-3beta phosphorylation in the heart under pressure overload. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:20900-20905.
49. Mehta S.H., Brancati F.L., Sulkowski M.S., Strathdee S.A., Szklo M., Thomas D.L. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann. Intern. Med. 2000, 133:592-599.
50. Meijer A.J., Codogno P. Macroautophagy: protector in the diabetes drama?. Autophagy 2007, 3:523-526.
51. Miquilena-Colina M.E., Lima-Cabello E., Sanchez-Campos S., Garcia-Mediavilla M.V., Fernandez-Bermejo M., Lozano-Rodriguez T., Vargas-Castrillon J., Buque X., Ochoa B., Aspichueta P., Gonzalez-Gallego J., Garcia-Monzon C. Hepatic fatty acid translocase CD36 upregulation is associated with insulin resistance, hyperinsulinaemia and increased steatosis in non-alcoholic steatohepatitis and chronic hepatitis C. Gut 2011.
52. Mizui T., Yamashina S., Tanida I., Takei Y., Ueno T., Sakamoto N., Ikejima K., Kitamura T., Enomoto N., Sakai T., Kominami E., Watanabe S. Inhibition of hepatitis C virus replication by chloroquine targeting virus-associated autophagy. J. Gastroenterol 2009.
53. Mizushima N., Noda T., Yoshimori T., Tanaka Y., Ishii T., George M.D., Klionsky D.J., Ohsumi M., Ohsumi Y. A protein conjugation system essential for autophagy. Nature 1998, 395:395-398.
54. Mizushima N., Yamamoto A., Hatano M., Kobayashi Y., Kabeya Y., Suzuki K., Tokuhisa T., Ohsumi Y., Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J. Cell Biol. 2001, 152:657-668.
55. Mora A., Sakamoto K., McManus E.J., Alessi D.R. Role of the PDK1-PKB-GSK3 pathway in regulating glycogen synthase and glucose uptake in the heart. FEBS Lett. 2005, 579:3632-3638.
56. Nehrbass D., Klimek F., Bannasch P. Overexpression of insulin receptor substrate-1 emerges early in hepatocarcinogenesis and elicits preneoplastic hepatic glycogenosis. Am. J. Pathol. 1998, 152:341-345.
57. Park S.H., Chi G.Y., Eom H.S., Kim G.Y., Hyun J.W., Kim W.J., Lee S.J., Yoo Y.H., Choi Y.H. Role of autophagy in apoptosis induction by methylene chloride extracts of Mori cortex in NCI-H460 human lung carcinoma cells. Int. J. Oncol. 2012, 40:1929-1940.
58. Patel S., Doble B.W., MacAulay K., Sinclair E.M., Drucker D.J., Woodgett J.R. Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol. Cell Biol. 2008, 28:6314-6328.
59. Pazienza V., Clement S., Pugnale P., Conzelman S., Foti M., Mangia A., Negro F. The hepatitis C virus core protein of genotypes 3a and 1b downregulates insulin receptor substrate 1 through genotype-specific mechanisms. Hepatology 2007, 45:1164-1171.
60. Pearce N.J., Arch J.R., Clapham J.C., Coghlan M.P., Corcoran S.L., Lister C.A., Llano A., Moore G.B., Murphy G.J., Smith S.A., Taylor C.M., Yates J.W., Morrison A.D., Harper A.J., Roxbee-Cox L., Abuin A., Wargent E., Holder J.C. Development of glucose intolerance in male transgenic mice over expressing human glycogen synthase kinase-3beta on a muscle-specific promoter. Metabolism 2004, 53:1322-1330.
61. Roach P.J. Glycogen and its metabolism. Curr. Mol. Med. 2002, 2:101-120.
62. Romero-Gomez M., Viloria M.D., Andrade R.J., Salmeron J., Diago M., Fernandez-Rodriguez C.M., Corpas R., Cruz M., Grande L., Vazquez L., Munoz-De-Rueda P., Lopez-Serrano P., Gila A., Gutierrez M.L., Perez C., Ruiz-Extremera A., Suarez E., Castillo J. Insulin resistance impairs sustained response rate to peginterferon plus ribavirin in chronic hepatitis C patients. Gastroenterology 2005, 128:636-641.
63. Rondinone C.M., Carvalho E., Wesslau C., Smith U.P. Impaired glucose transport and protein kinase B activation by insulin, but not okadaic acid, in adipocytes from subjects with type II diabetes mellitus. Diabetologia 1999, 42:819-825.
64. Salic A., Mitchison T.J. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Nat. Acad. Sci. U.S.A. 2008, 105:2415-2420.
65. Sarbassov D.D., Ali S.M., Sabatini D.M. Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 2005, 17:596-603.
66. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
67. Shah O.J., Hunter T. Turnover of the active fraction of IRS1 involves raptor-mTOR- and S6K1-dependent serine phosphorylation in cell culture models of tuberous sclerosis. Mol. Cell Biol. 2006, 26:6425-6434.
68. Shao Y., Gao Z., Feldman T., Jiang X. Stimulation of ATG12-ATG5 conjugation by ribonucleic acid. Autophagy 2007, 3:10-16.
69. Shintani Y., Fujie H., Miyoshi H., Tsutsumi T., Tsukamoto K., Kimura S., Moriya K., Koike K. Hepatitis C virus infection and diabetes: direct involvement of the virus in the development of insulin resistance. Gastroenterology 2004, 126:840-848.
70. Shivakumar C.V., Das G.C. Interaction of human polyomavirus BK with the tumor-suppressor protein p53. Oncogene 1996, 13:323-332.
71. Sinha S., Colbert C.L., Becker N., Wei Y., Levine B. Molecular basis of the regulation of Beclin 1-dependent autophagy by the gamma-herpesvirus 68 Bcl-2 homolog M11. Autophagy 2008, 4:989-997.
72. Sir D., Chen W.L., Choi J., Wakita T., Yen T.S., Ou J.H. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 2008, 48:1054-1061.
73. Skurat A.V., Roach P.J. Phosphorylation of sites 3a and 3b (Ser640 and Ser644) in the control of rabbit muscle glycogen synthase. J. Biol. Chem. 1995, 270:12491-12497.
74. Street A., Macdonald A., Crowder K., Harris M. The Hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase-dependent survival signaling cascade. J. Biol. Chem. 2004, 279:12232-12241.
75. Summers S.A., Yin V.P., Whiteman E.L., Garza L.A., Cho H., Tuttle R.L., Birnbaum M.J. Signaling pathways mediating insulin-stimulated glucose transport. Ann. N.Y. Acad. Sci. 1999, 892:169-186.
76. Sutherland C., Leighton I.A., Cohen P. Inactivation of glycogen synthase kinase-3 beta by phosphorylation: new kinase connections in insulin and growth-factor signalling. Biochem. J. 1993, 296(Pt 1):15-19.
77. Tanaka S., Wands J.R. Insulin receptor substrate 1 overexpression in human hepatocellular carcinoma cells prevents transforming growth factor beta1-induced apoptosis. Cancer Res. 1996, 56:3391-3394.
78. Uddin S., Fish E.N., Sher D.A., Gardziola C., White M.F., Platanias L.C. Activation of the phosphatidylinositol 3-kinase serine kinase by IFN-alpha. J. Immunol. 1997, 158:2390-2397.
79. Uddin S., Majchrzak B., Wang P.C., Modi S., Khan M.K., Fish E.N., Platanias L.C. Interferon-dependent activation of the serine kinase PI 3'-kinase requires engagement of the IRS pathway but not the Stat pathway. Biochem. Biophys. Res. Commun. 2000, 270:158-162.
80. Uddin S., Yenush L., Sun X.J., Sweet M.E., White M.F., Platanias L.C. Interferon-alpha engages the insulin receptor substrate-1 to associate with the phosphatidylinositol 3'-kinase. J. Biol. Chem. 1995, 270:15938-15941.
81. Vanhaesebroeck B., Alessi D.R. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 2000, 346(Pt 3):561-576.
82. Vescovo T., Romagnoli A., Perdomo A.B., Corazzari M., Ciccosanti F., Alonzi T., Nardacci R., Ippolito G., Tripodi M., Garcia-Monzon C., Lo I.O., Piacentini M., Fimia G.M. Autophagy protects cells from HCV-induced defects in lipid metabolism. Gastroenterology 2012, 142:644-653.
83. Wakita T., Pietschmann T., Kato T., Date T., Miyamoto M., Zhao Z.J., Murthy K., Habermann A., Krausslich H.G., Mizokami M., Bartenschlager R., Liang T.J. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 2005, 11:791-796.
84. Wang P., Guan Y.F., Du H., Zhai Q.W., Su D.F., Miao C.Y. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 2012, 8:77-87.
85. Wang Q.M., Park I.K., Fiol C.J., Roach P.J., DePaoli-Roach A.A. Isoform differences in substrate recognition by glycogen synthase kinases 3 alpha and 3 beta in the phosphorylation of phosphatase inhibitor 2. Biochemistry 1994, 33:143-147.
86. Waris G., Felmlee D.J., Negro F., Siddiqui A. Hepatitis C virus induces proteolytic cleavage of sterol regulatory element binding proteins and stimulates their phosphorylation via oxidative stress. J. Virol. 2007, 81:8122-8130.
87. Welsh G.I., Miyamoto S., Price N.T., Safer B., Proud C.G. T-cell activation leads to rapid stimulation of translation initiation factor eIF2B and inactivation of glycogen synthase kinase-3. J. Biol. Chem. 1996, 271:11410-11413.
88. Xie Z., Klionsky D.J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 2007, 9:1102-1109.
89. Yang J., Takahashi Y., Cheng E., Liu J., Terranova P.F., Zhao B., Thrasher J.B., Wang H.G., Li B. GSK-3beta promotes cell survival by modulating Bif-1-dependent autophagy and cell death. J. Cell Sci. 2010, 123:861-870.
90. Yang L., Li P., Fu S., Calay E.S., Hotamisligil G.S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010, 11:467-478.
91. Yuan H., Mao J., Li L., Wu D. Suppression of glycogen synthase kinase activity is not sufficient for leukemia enhancer factor-1 activation. J. Biol. Chem. 1999, 274:30419-30423.
92. Zhao L., Zhu Y., Wang D., Chen M., Gao P., Xiao W., Rao G., Wang X., Jin H., Xu L., Sui N., Chen Q. Morphine induces Beclin 1- and ATG5-dependent autophagy in human neuroblastoma SH-SY5Y cells and in the rat hippocampus. Autophagy 2010, 6:386-394.
93. Zhong J., Gastaminza P., Cheng G.F., Kapadia S., Kato T., Burton D.R., Wieland S.F., Uprichard S.L., Wakita T., Chisari F.V. Robust hepatitis C virus infection in vitro. Proc. Nat. Acad. Sci. U.S.A. 2005, 102:9294-9299.
94. Zick Y. Insulin resistance: a phosphorylation-based uncoupling of insulin signaling. Trends Cell Biol. 2001, 11:437-441.
95. Zou M., Lu N., Hu C., Liu W., Sun Y., Wang X., You Q., Gu C., Xi T., Guo Q. Beclin 1-mediated autophagy in hepatocellular carcinoma cells: implication in anticancer efficiency of oroxylin A via inhibition of mTOR signaling. Cell Signal 2012, 24:1722-1732.