Dephosphorylation of Translation Initiation Factor 2α Enhances Glucose Tolerance and Attenuates Hepatosteatosis in Mice

Cell Metabolism

Volumn 7, Issue 6, 2008, Pages 520-532

  Oyadomari, Seiichi ^a   Harding, Heather P ^a   Zhang, Yuhong ^a   Oyadomari, Miho ^a   Ron, David ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HUMDISEASE

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; CCAAT ENHANCER BINDING PROTEIN BETA; GLYCOGEN; INITIATION FACTOR 2ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FATTY LIVER; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLYCOGEN LIVER LEVEL; HYPOGLYCEMIA; LIPID DIET; LIVER CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUTRIENT; OBESITY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; BLOOD GLUCOSE; CELL LINE; DIET; EUKARYOTIC INITIATION FACTOR-2; FATTY LIVER; GLUCOSE INTOLERANCE; LIVER; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PPAR GAMMA;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 44349163999     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2008.04.011     Document Type: Article

References (51)

1. Allen-Jennings A.E., Hartman M.G., Kociba G.J., and Hai T. The roles of ATF3 in liver dysfunction and the regulation of phosphoenolpyruvate carboxykinase gene expression. J. Biol. Chem. 277 (2002) 20020-20025
2. Batchvarova N., Wang X.-Z., and Ron D. Inhibition of adipogenesis by the stress-induced protein CHOP (GADD153). EMBO J. 14 (1995) 4654-4661
3. Bernales S., Papa F.R., and Walter P. Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol. 22 (2006) 487-508
4. Calkhoven C.F., Muller C., and Leutz A. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev. 14 (2000) 1920-1932
5. Chen C., Dudenhausen E.E., Pan Y.X., Zhong C., and Kilberg M.S. Human CCAAT/enhancer-binding protein beta gene expression is activated by endoplasmic reticulum stress through an unfolded protein response element downstream of the protein coding sequence. J. Biol. Chem. 279 (2004) 27948-27956
6. Delepine M., Nicolino M., Barrett T., Golamaully M., Lathrop G.M., and Julier C. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25 (2000) 406-409
7. Deng J., Lu P.D., Zhang Y., Scheuner D., Kaufman R.J., Sonenberg N., Harding H.P., and Ron D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol. Cell. Biol. 24 (2004) 10161-10168
8. Dhahbi J.M., Mote P.L., Tillman J.B., Walford R.L., and Spindler S.R. Dietary energy tissue-specifically regulates endoplasmic reticulum chaperone gene expression in the liver of mice. J. Nutr. 127 (1997) 1758-1764
9. Farmer S.R. Transcriptional control of adipocyte formation. Cell Metab. 4 (2006) 263-273
10. Gavrilova O., Haluzik M., Matsusue K., Cutson J.J., Johnson L., Dietz K.R., Nicol C.J., Vinson C., Gonzalez F.J., and Reitman M.L. Liver peroxisome proliferator-activated receptor gamma contributes to hepatic steatosis, triglyceride clearance, and regulation of body fat mass. J. Biol. Chem. 278 (2003) 34268-34276
11. Guo F., and Cavener D.R. The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab. 5 (2007) 103-114
12. Hao S., Sharp J.W., Ross-Inta C.M., McDaniel B.J., Anthony T.G., Wek R.C., Cavener D.R., McGrath B.C., Rudell J.B., Koehnle T.J., and Gietzen D.W. Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 307 (2005) 1776-1778
13. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., and Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6 (2000) 1099-1108
14. Harding H.P., Zeng H., Zhang Y., Jungreis R., Chung P., Plesken H., Sabatini D.D., and Ron D. Diabetes mellitus and exocrine pancreatic dysfunction in Perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7 (2001) 1153-1163
15. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11 (2003) 619-633
16. Hinnebusch A.G., and Natarajan K. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1 (2002) 22-32
17. Hu C.C., Qing K., and Chen Y. Diet-induced changes in stearoyl-CoA desaturase 1 expression in obesity-prone and -resistant mice. Obes. Res. 12 (2004) 1264-1270
18. Jiang H.Y., Wek S.A., McGrath B.C., Scheuner D., Kaufman R.J., Cavener D.R., and Wek R.C. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol. Cell. Biol. 23 (2003) 5651-5663
19. Jiang H.Y., Wek S.A., McGrath B.C., Lu D., Hai T., Harding H.P., Wang X., Ron D., Cavener D.R., and Wek R.C. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24 (2004) 1365-1377
20. Kleiner D.E., Brunt E.M., Van Natta M., Behling C., Contos M.J., Cummings O.W., Ferrell L.D., Liu Y.C., Torbenson M.S., Unalp-Arida A., et al. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41 (2005) 1313-1321
21. Lee A.H., Chu G.C., Iwakoshi N.N., and Glimcher L.H. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24 (2005) 4368-4380
22. Liu S., Croniger C., Arizmendi C., Harada-Shiba M., Ren J., Poli V., Hanson R.W., and Friedman J.E. Hypoglycemia and impaired hepatic glucose production in mice with a deletion of the C/EBPbeta gene. J. Clin. Invest. 103 (1999) 207-213
23. Lu P.D., Harding H.P., and Ron D. Translation re-initiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167 (2004) 27-33
24. Lu P.D., Jousse C., Marciniak S.J., Zhang Y., Novoa I., Scheuner D., Kaufman R.J., Ron D., and Harding H.P. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23 (2004) 169-179
25. Maurin A.C., Jousse C., Averous J., Parry L., Bruhat A., Cherasse Y., Zeng H., Zhang Y., Harding H., Ron D., and Fafournoux P. The GCN2 kinase biases feeding behavior to maintain amino-acid homeostasis in omnivores. Cell Metab. 1 (2005) 273-277
26. Millward C.A., Heaney J.D., Sinasac D.S., Chu E.C., Bederman I.R., Gilge D.A., Previs S.F., and Croniger C.M. Mice with a deletion in the gene for CCAAT/enhancer-binding protein beta are protected against diet-induced obesity. Diabetes 56 (2007) 161-167
27. Nakatani Y., Kaneto H., Kawamori D., Yoshiuchi K., Hatazaki M., Matsuoka T.A., Ozawa K., Ogawa S., Hori M., Yamasaki Y., and Matsuhisa M. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280 (2005) 847-851
28. Novoa I., Zeng H., Harding H., and Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153 (2001) 1011-1022
29. Novoa I., Zhang Y., Zeng H., Jungreis R., Harding H.P., and Ron D. Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22 (2003) 1180-1187
30. Oyadomari S., Yun C., Fisher E.A., Kreglinger N., Kreibich G., Oyadomari M., Harding H.P., Goodman A.G., Harant H., Garrison J.L., et al. Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126 (2006) 727-739
31. Ozawa K., Miyazaki M., Matsuhisa M., Takano K., Nakatani Y., Hatazaki M., Tamatani T., Yamagata K., Miyagawa J., Kitao Y., et al. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes 54 (2005) 657-663
32. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., Tuncman G., Gorgun C., Glimcher L.H., and Hotamisligil G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306 (2004) 457-461
33. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., and Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313 (2006) 1137-1140
34. Patil C.K., Li H., and Walter P. Gcn4p and novel upstream activating sequences regulate targets of the unfolded protein response. PLoS Biol. 2 (2004) E246
35. Rahman S.M., Schroeder-Gloeckler J.M., Janssen R.C., Jiang H., Qadri I., Maclean K.N., and Friedman J.E. CCAAT/enhancing binding protein beta deletion in mice attenuates inflammation, endoplasmic reticulum stress, and lipid accumulation in diet-induced nonalcoholic steatohepatitis. Hepatology 45 (2007) 1108-1117
36. Ron D., and Habener J.F. CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant negative inhibitor of gene transcription. Genes Dev. 6 (1992) 439-453
37. Ron D., and Harding H. eIF2a phosphorylation in cellular stress responses and disease. In: Sonenberg N., Hershey J., and Mathews M. (Eds). Translational Control (2007), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA 345-368
38. Rosen E.D., Walkey C.J., Puigserver P., and Spiegelman B.M. Transcriptional regulation of adipogenesis. Genes Dev. 14 (2000) 1293-1307
39. Rutkowski D.T., Arnold S.M., Miller C.N., Wu J., Li J., Gunnison K.M., Mori K., Sadighi Akha A.A., Raden D., and Kaufman R.J. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. 4 (2006) e374
40. Schadinger S.E., Bucher N.L., Schreiber B.M., and Farmer S.R. PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes. Am. J. Physiol. Endocrinol. Metab. 288 (2005) E1195-E1205
41. Scheuner D., Song B., McEwen E., Gillespie P., Saunders T., Bonner-Weir S., and Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7 (2001) 1165-1176
42. Scheuner D., Mierde D.V., Song B., Flamez D., Creemers J.W., Tsukamoto K., Ribick M., Schuit F.C., and Kaufman R.J. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat. Med. 11 (2005) 757-764
43. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
44. Schroder M., Chang J.S., and Kaufman R.J. The unfolded protein response represses nitrogen-starvation induced developmental differentiation in yeast. Genes Dev. 14 (2000) 2962-2975
45. Schroeder-Gloeckler J.M., Rahman S.M., Janssen R.C., Qiao L., Shao J., Roper M., Fischer S.J., Lowe E., Orlicky D.J., McManaman J.L., et al. CCAAT/enhancer-binding protein beta deletion reduces adiposity, hepatic steatosis, and diabetes in Lepr(db/db) mice. J. Biol. Chem. 282 (2007) 15717-15729
46. Shen X., Ellis R.E., Lee K., Liu C.-Y., Yang K., Solomon A., Yoshida H., Morimoto R., Kurnit D.M., Mori K., and Kaufman R.J. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107 (2001) 893-903
47. Vattem K.M., and Wek R.C. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101 (2004) 11269-11274
48. Wang N.D., Finegold M., Bradley A., Ou C., Abdelsayed S., Wilde M., Taylor L., Wilson D., and Darlington G. Impaired energy homeostasis in C/EBPα knockout mice. Science 269 (1995) 1108-1112
49. Wu J., Rutkowski D.T., Dubois M., Swathirajan J., Saunders T., Wang J., Song B., Yau G.D., and Kaufman R.J. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell 13 (2007) 351-364
50. Yamamoto K., Sato T., Matsui T., Sato M., Okada T., Yoshida H., Harada A., and Mori K. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell 13 (2007) 365-376
51. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., Gannon M., Ma K., McNaughton K., and Cavener D.R. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22 (2002) 3864-3874