Adenovirus Protein E4-ORF1 Activation of PI3 Kinase Reveals Differential Regulation of Downstream Effector Pathways in Adipocytes

Cell Reports - Tập 17 - Trang 3305-3318 - 2016
Natasha Chaudhary1, Eva Gonzalez1, Sung-Hee Chang2, Fuqiang Geng2, Shahin Rafii2, Nasser K. Altorki3,4, Timothy E. McGraw1,3,4
1Department of Biochemistry, Weill Cornell Medicine, New York, NY 10065, USA
2Department of Medicine, Weill Cornell Medicine, New York, NY 10065, USA
3Department of Cardiothoracic Surgery, Weill Cornell Medicine, New York, NY, 10065, USA
4Lung Cancer Program, Meyer Cancer Center, Weill Cornell Medicine, New York, NY 10065, USA

Tài liệu tham khảo

Abel, 2001, Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver, Nature, 409, 729, 10.1038/35055575 Alessi, 1996, Mechanism of activation of protein kinase B by insulin and IGF-1, EMBO J., 15, 6541, 10.1002/j.1460-2075.1996.tb01045.x Bai, 2007, Dissecting multiple steps of GLUT4 trafficking and identifying the sites of insulin action, Cell Metab., 5, 47, 10.1016/j.cmet.2006.11.013 Bose, 2002, Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c, Nature, 420, 821, 10.1038/nature01246 Bruno, 2016, SEC16A is a RAB10 effector required for insulin-stimulated GLUT4 trafficking in adipocytes, J. Cell Biol., 214, 61, 10.1083/jcb.201509052 Chakrabarti, 2009, FoxO1 controls insulin-dependent adipose triglyceride lipase (ATGL) expression and lipolysis in adipocytes, J. Biol. Chem., 284, 13296, 10.1074/jbc.C800241200 Cheatham, 1994, Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation, Mol. Cell. Biol., 14, 4902, 10.1128/MCB.14.7.4902 Chung, 2007, A new crucial protein interaction element that targets the adenovirus E4-ORF1 oncoprotein to membrane vesicles, J. Virol., 81, 4787, 10.1128/JVI.02855-06 Costa, 2015, Measurement of PIP3 levels reveals an unexpected role for p110β in early adaptive responses to p110α-specific inhibitors in luminal breast cancer, Cancer Cell, 27, 97, 10.1016/j.ccell.2014.11.007 Dawson, 2001, Insulin-regulated trafficking of dual-labeled glucose transporter 4 in primary rat adipose cells, Biochem. Biophys. Res. Commun., 287, 445, 10.1006/bbrc.2001.5620 Dhurandhar, 2011, E4orf1: A novel ligand that improves glucose disposal in cell culture, PLoS ONE, 6, e23394, 10.1371/journal.pone.0023394 Dubuisson, 2011, PPARgamma-independent increase in glucose uptake and adiponectin abundance in fat cells, Endocrinology, 152, 3648, 10.1210/en.2011-0225 Eguez, 2005, Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein, Cell Metab., 2, 263, 10.1016/j.cmet.2005.09.005 Frese, 2003, Selective PDZ protein-dependent stimulation of phosphatidylinositol 3-kinase by the adenovirus E4-ORF1 oncoprotein, Oncogene, 22, 710, 10.1038/sj.onc.1206151 Frese, 2006, Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor, EMBO J., 25, 1406, 10.1038/sj.emboj.7601030 Gonzalez, 2009, Insulin-modulated Akt subcellular localization determines Akt isoform-specific signaling, Proc. Natl. Acad. Sci. USA, 106, 7004, 10.1073/pnas.0901933106 Gonzalez, 2011, Hyperinsulinemia leads to uncoupled insulin regulation of the GLUT4 glucose transporter and the FoxO1 transcription factor, Proc. Natl. Acad. Sci. USA, 108, 10162, 10.1073/pnas.1019268108 Graham, 2007, Tissue-specific alterations of glucose transport and molecular mechanisms of intertissue communication in obesity and type 2 diabetes, Horm. Metab. Res., 39, 717, 10.1055/s-2007-985879 Hart, 2011, Phosphorylation of AKT: A mutational analysis, Oncotarget, 2, 467, 10.18632/oncotarget.293 Hill, 1999, A role for protein kinase Bbeta/Akt2 in insulin-stimulated GLUT4 translocation in adipocytes, Mol. Cell. Biol., 19, 7771, 10.1128/MCB.19.11.7771 Kaestner, 2000, Unified nomenclature for the winged helix/forkhead transcription factors, Genes Dev., 14, 142, 10.1101/gad.14.2.142 Kajno, 2015, Development of a new model system to dissect isoform specific Akt signalling in adipocytes, Biochem. J., 468, 425, 10.1042/BJ20150191 Karylowski, 2004, GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes, Mol. Biol. Cell, 15, 870, 10.1091/mbc.E03-07-0517 Knight, 2006, A pharmacological map of the PI3-K family defines a role for p110alpha in insulin signaling, Cell, 125, 733, 10.1016/j.cell.2006.03.035 Kohn, 1996, Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation, J. Biol. Chem., 271, 31372, 10.1074/jbc.271.49.31372 Kong, 2014, The human adenovirus E4-ORF1 protein subverts discs large 1 to mediate membrane recruitment and dysregulation of phosphatidylinositol 3-kinase, PLoS Pathog., 10, e1004102, 10.1371/journal.ppat.1004102 Krishnapuram, 2011, Template to improve glycemic control without reducing adiposity or dietary fat, Am. J. Physiol. Endocrinol. Metab., 300, E779, 10.1152/ajpendo.00703.2010 Kusminski, 2015, E4orf1 induction in adipose tissue promotes insulin-independent signaling in the adipocyte, Mol. Metab., 4, 653, 10.1016/j.molmet.2015.07.004 Lampson, 2000, Demonstration of insulin-responsive trafficking of GLUT4 and vpTR in fibroblasts, J. Cell Sci., 113, 4065, 10.1242/jcs.113.22.4065 Lampson, 2001, Insulin-regulated release from the endosomal recycling compartment is regulated by budding of specialized vesicles, Mol. Biol. Cell, 12, 3489, 10.1091/mbc.12.11.3489 Larance, 2005, Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking, J. Biol. Chem., 280, 37803, 10.1074/jbc.M503897200 Lawrence, 1992, GLUT4 facilitates insulin stimulation and cAMP-mediated inhibition of glucose transport, Proc. Natl. Acad. Sci. USA, 89, 3493, 10.1073/pnas.89.8.3493 Lee, 1997, Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein, Proc. Natl. Acad. Sci. USA, 94, 6670, 10.1073/pnas.94.13.6670 Leto, 2012, Regulation of glucose transport by insulin: Traffic control of GLUT4, Nat. Rev. Mol. Cell Biol., 13, 383, 10.1038/nrm3351 Lizunov, 2005, Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells, J. Cell Biol., 169, 481, 10.1083/jcb.200412069 Maianu, 2001, Adipocytes exhibit abnormal subcellular distribution and translocation of vesicles containing glucose transporter 4 and insulin-regulated aminopeptidase in type 2 diabetes mellitus: Implications regarding defects in vesicle trafficking, J. Clin. Endocrinol. Metab., 86, 5450, 10.1210/jcem.86.11.8053 Martin, 2000, Effects of insulin on intracellular GLUT4 vesicles in adipocytes: Evidence for a secretory mode of regulation, J. Cell Sci., 113, 3427, 10.1242/jcs.113.19.3427 Martin, 2006, GLUT4 distribution between the plasma membrane and the intracellular compartments is maintained by an insulin-modulated bipartite dynamic mechanism, J. Biol. Chem., 281, 484, 10.1074/jbc.M505944200 Nakae, 2002, Regulation of insulin action and pancreatic beta-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1, Nat. Genet., 32, 245, 10.1038/ng890 Nakae, 2008, Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure, Diabetes, 57, 563, 10.2337/db07-0698 Ng, 2008, Rapid activation of Akt2 is sufficient to stimulate GLUT4 translocation in 3T3-L1 adipocytes, Cell Metab., 7, 348, 10.1016/j.cmet.2008.02.008 O’Shea, 2005, Adenoviral proteins mimic nutrient/growth signals to activate the mTOR pathway for viral replication, EMBO J., 24, 1211, 10.1038/sj.emboj.7600597 Olson, 1996, Structure, function, and regulation of the mammalian facilitative glucose transporter gene family, Annu. Rev. Nutr., 16, 235, 10.1146/annurev.nu.16.070196.001315 Piper, 1991, Differential sorting of two glucose transporters expressed in insulin-sensitive cells, Am. J. Physiol., 260, C570, 10.1152/ajpcell.1991.260.3.C570 Rogers, 2008, Human adenovirus Ad-36 induces adipogenesis via its E4 orf-1 gene, Int. J. Obes., 32, 397, 10.1038/sj.ijo.0803748 Rogers, 2008, Metabolically favorable remodeling of human adipose tissue by human adenovirus type 36, Diabetes, 57, 2321, 10.2337/db07-1311 Sadacca, 2013, Specialized sorting of GLUT4 and its recruitment to the cell surface are independently regulated by distinct Rabs, Mol. Biol. Cell, 24, 2544, 10.1091/mbc.E13-02-0103 Saltiel, 2002, Insulin signaling pathways in time and space, Trends Cell Biol., 12, 65, 10.1016/S0962-8924(01)02207-3 Saltiel, 2003, Insulin signaling in microdomains of the plasma membrane, Traffic, 4, 711, 10.1034/j.1600-0854.2003.00119.x Sano, 2003, Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation, J. Biol. Chem., 278, 14599, 10.1074/jbc.C300063200 Sano, 2007, Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane, Cell Metab., 5, 293, 10.1016/j.cmet.2007.03.001 Satoh, 1993, Use of bismannose photolabel to elucidate insulin-regulated GLUT4 subcellular trafficking kinetics in rat adipose cells. Evidence that exocytosis is a critical site of hormone action, J. Biol. Chem., 268, 17820, 10.1016/S0021-9258(17)46778-0 Shewan, 2003, GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: Involvement of an acidic targeting motif, Mol. Biol. Cell, 14, 973, 10.1091/mbc.E02-06-0315 Tengholm, 2002, A PI3-kinase signaling code for insulin-triggered insertion of glucose transporters into the plasma membrane, Curr. Biol., 12, 1871, 10.1016/S0960-9822(02)01223-X Thai, 2014, Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication, Cell Metab., 19, 694, 10.1016/j.cmet.2014.03.009 Vazirani, 2016, Disruption of Adipose Rab10-Dependent Insulin Signaling Causes Hepatic Insulin Resistance, Diabetes, 65, 1577, 10.2337/db15-1128 Wang, 1999, Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts, Mol. Cell. Biol., 19, 4008, 10.1128/MCB.19.6.4008 Wang, 2008, Human adenovirus type 36 enhances glucose uptake in diabetic and nondiabetic human skeletal muscle cells independent of insulin signaling, Diabetes, 57, 1805, 10.2337/db07-1313 Weiland, 1990, Development of the hormone-sensitive glucose transport activity in differentiating 3T3-L1 murine fibroblasts. Role of the two transporter species and their subcellular localization, Biochem. J., 270, 331, 10.1042/bj2700331 Weiss, 1997, A carboxy-terminal region required by the adenovirus type 9 E4 ORF1 oncoprotein for transformation mediates direct binding to cellular polypeptides, J. Virol., 71, 7873, 10.1128/JVI.71.10.7873-7880.1997 Xiong, 2010, GLUT4 is sorted to vesicles whose accumulation beneath and insertion into the plasma membrane are differentially regulated by insulin and selectively affected by insulin resistance, Mol. Biol. Cell, 21, 1375, 10.1091/mbc.E09-08-0751 Xu, 2002, Translocation of small preformed vesicles is responsible for the insulin activation of glucose transport in adipose cells. Evidence from the in vitro reconstitution assay, J. Biol. Chem., 277, 47972, 10.1074/jbc.C200486200 Zeigerer, 2002, GLUT4 retention in adipocytes requires two intracellular insulin-regulated transport steps, Mol. Biol. Cell, 13, 2421, 10.1091/mbc.E02-02-0071 Zeigerer, 2004, Insulin stimulation of GLUT4 exocytosis, but not its inhibition of endocytosis, is dependent on RabGAP AS160, Mol. Biol. Cell, 15, 4406, 10.1091/mbc.E04-04-0333