ER stress potentiates insulin resistance through PERK-mediated FOXO phosphorylation

Genes and Development

Volumn 27, Issue 4, 2013, Pages 441-449

  Zhang, Wei ^a,b   Hietakangas, Ville ^c   Wee, Sheena ^a   Lim, Siew Choo ^a   Gunaratne, Jayantha ^a   Cohen, Stephen M ^a,b  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Diabetes; Drosophila; ER stress; PERK kinase; Unfolded protein response

Indexed keywords

INSULIN RECEPTOR; MEMBRANE PROTEIN; PROTEIN KINASE B; PROTEIN PERK; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; INSULIN RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CELL NUCLEUS; EIF-2 KINASE; ENDOPLASMIC RETICULUM STRESS; FORKHEAD TRANSCRIPTION FACTORS; HEP G2 CELLS; HUMANS; INSULIN RESISTANCE; MCF-7 CELLS; ONCOGENE PROTEIN V-AKT; PHOSPHORYLATION; PROTEIN TRANSPORT;

EID: 84874268065     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.201731.112     Document Type: Article

References (34)

1. Alon U. 2007. Network motifs: Theory and experimental approaches. Nat Rev Genet 8: 450-461.
2. Baumeister P., Luo S, Skarnes WC, Sui G, Seto E, Shi Y, Lee AS. 2005. Endoplasmic reticulum stress induction of the Grp78/BiP promoter: Activating mechanisms mediated by YY1 and its interactive chromatin modifiers. Mol Cell Biol 25: 4529-4540.
3. Bobrovnikova-Marjon E, Pytel D, Riese MJ, Vaites LP, Singh N, Koretzky GA., Witze ES, Diehl JA. 2012. PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation. Mol Cell Biol 32: 2268-2278.
4. Carvalho P., Goder V, Rapoport TA. 2006. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126: 361-373.
5. Greer EL., Brunet A. 2005. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24: 7410-7425.
6. Hamanaka RB., Bennett BS, Cullinan SB, Diehl JA. 2005. PERK and GCN2 contribute to eIF2a phosphorylation and cell cycle arrest after activation of the unfolded protein response pathway. Mol Biol Cell 16: 5493-5501.
7. Hietakangas V., Cohen SM. 2007. Re-evaluating AKT regulation: Role of TOR complex 2 in tissue growth. Genes Dev 21: 632-637.
8. Huang H., Tindall DJ. 2007. Dynamic FoxO transcription factors. J Cell Sci 120: 2479-2487.
9. Huang H., Regan KM, Lou Z, Chen J, Tindall DJ. 2006. CDK2-dependent phosphorylation of FOXO1 as an apoptotic response to DNA damage. Science 314: 294-297.
10. Junger MA., Rintelen F, Stocker H, Wasserman JD, Vegh M, Radimerski T., Greenberg ME, Hafen E. 2003. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2: 20.
11. Kim JJ., Li P, Huntley J, Chang JP, Arden KC, Olefsky JM. 2009. FoxO1 haploinsufficiency protects against high-fat dietinduced insulin resistance with enhanced peroxisome proliferator-activated receptor g activation in adipose tissue. Diabetes 58: 1275-1282.
12. Lehtinen MK., Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S., de la Iglesia N, Gygi S, Blackwell TK, et al. 2006. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001.
13. Malhi H., Gores GJ. 2008. Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin Liver Dis 28: 360-369.
14. Malhi H., Kaufman RJ. 2011. Endoplasmic reticulum stress in liver disease. J Hepatol 54: 795-809.
15. Martinez-Gac L, Marques M, Garcia Z, Campanero MR, Carrera AC. 2004. Control of cyclin G2 mRNA expression by forkhead transcription factors: Novel mechanism for cell cycle control by phosphoinositide 3-kinase and forkhead. Mol Cell Biol 24: 2181-2189.
16. Mattila J., Kallijarvi J, Puig O. 2008. RNAi screening for kinases and phosphatases identifies FoxO regulators. Proc Natl Acad Sci 105: 14873-14878.
17. Medema RH., Kops GJ, Bos JL, Burgering BM. 2000. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404: 782-787.
18. Mounir Z., Krishnamoorthy JL, Wang S, Papadopoulou B, Campbell S., Muller WJ, Hatzoglou M, Koromilas AE. 2011. Akt determines cell fate through inhibition of the PERK-eIF2a phosphorylation pathway. Sci Signal 4: ra62.
19. Nakae J., Biggs WH III, Kitamura T, Cavenee WK, Wright CV, Arden KC., Accili D. 2002. Regulation of insulin action and pancreatic b-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1. Nat Genet 32: 245-253.
20. Nakae J., Kitamura T, Kitamura Y, Biggs WH III, Arden KC, Accili D. 2003. The forkhead transcription factor Foxo1 regulates adipocyte differentiation. Dev Cell 4: 119-129.
21. Nakatsukasa K., Brodsky JL. 2008. The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic 9: 861-870.
22. Ozcan U., Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G., Gorgun C, Glimcher LH, Hotamisligil GS. 2004. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461.
23. Ozcan U., Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO., Gorgun CZ, Hotamisligil GS. 2006. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313: 1137-1140.
24. Puig O., Tjian R. 2005. Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev 19: 2435-2446.
25. Puig O., Marr MT, Ruhf ML, Tjian R. 2003. Control of cell number by Drosophila FOXO: Downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17: 2006-2020.
26. Shevchenko A., Tomas H, Havlis J, Olsen JV, Mann M. 2006. Ingel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860.
27. Smith MH., Ploegh HL, Weissman JS. 2011. Road to ruin: Targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086-1090.
28. Teleman AA., Hietakangas V, Sayadian AC, Cohen SM. 2008. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7: 21-32.
29. Urano F., Bertolotti A, Ron D. 2000. IRE1 and efferent signaling from the endoplasmic reticulum. J Cell Sci 113: 3697-3702.
30. Wu J., Kaufman RJ. 2006. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 13: 374-384.
31. Xiao C., Giacca A, Lewis GF. 2011. Sodium phenylbutyrate, a drug with known capacity to reduce endoplasmic reticulum stress, partially alleviates lipid-induced insulin resistance and b-cell dysfunction in humans. Diabetes 60: 918-924.
32. Yuan Z., Becker EB, Merlo P, Yamada T, DiBacco S, Konishi Y, Schaefer EM., Bonni A. 2008. Activation of FOXO1 by Cdk1 in cycling cells and postmitotic neurons. Science 319: 1665-1668.
33. Zhang W., Thompson BJ, Hietakangas V, Cohen SM. 2011. MAPK/ERK signaling regulates insulin sensitivity to control glucose metabolism in Drosophila. PLoS Genet 7: e1002429.
34. Zhao Y., Yang J, LiaoW, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L., Zhu WG. 2010. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 12: 665-675.