Skeletal muscle-specific eukaryotic translation initiation factor 2α phosphorylation controls amino acid metabolism and fibroblast growth factor 21-mediated non-cell-autonomous energy metabolism

FASEB Journal

Volumn 30, Issue 2, 2016, Pages 798-812

  Miyake, Masato ^a   Nomura, Akitoshi ^a   Ogura, Atsushi ^a   Takehana, Kenji ^b   Kitahara, Yoshihiro ^b   Takahara, Kazuna ^a   Tsugawa, Kazue ^a   Miyamoto, Chinobu ^a   Miura, Naoko ^a   Sato, Ryosuke ^a   Kurahashi, Kiyoe ^a   Harding, Heather P ^c   Oyadomari, Miho ^a   Ron, David ^c   Oyadomari, Seiichi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b Research Center   (Japan)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

ATF4; ER stress; Glutathione; Obesity; Small molecule

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; AMINO ACID; FIBROBLAST GROWTH FACTOR 21; INITIATION FACTOR 2ALPHA; LIGAND; MESSENGER RNA; PROTEIN KINASE R; FIBROBLAST GROWTH FACTOR; INITIATION FACTOR 2;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENERGY CONSUMPTION; ENERGY METABOLISM; GENE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; SKELETAL MUSCLE; STRESS; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

AMINO ACIDS; ANIMALS; ENERGY METABOLISM; EUKARYOTIC INITIATION FACTOR-2; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; PHOSPHORYLATION; UNFOLDED PROTEIN RESPONSE;

EID: 84958811791     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-275990     Document Type: Article

References (45)

1. Walter, P., and Ron, D. (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081-1086
2. Back, S.H., and Kaufman, R. J. (2012) Endoplasmic reticulumstress and type 2 diabetes. Annu. Rev. Biochem. 81, 767-793
3. Hotamisligil, G. S. (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917
4. Samuel, V. T., and Shulman, G. I. (2012) Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871
5. Harding, H. P., Zhang, Y., Zeng, H., Novoa, I., Lu, P. D., Calfon, M., Sadri, N., Yun, C., Popko, B., Paules, R., Stojdl, D. F., Bell, J. C., Hettmann, T., Leiden, J.M., and Ron, D. (2003)An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633
6. Lu, P.D., Harding, H. P., and Ron, D. (2004)Translationreinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167, 27-33
7. Vattem, K.M., andWek, R.C. (2004)Reinitiationinvolvingupstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101, 11269-11274
8. Baird, T. D., and Wek, R. C. (2012) Eukaryotic initiation factor 2 phosphorylation and translational control inmetabolism. Adv. Nutr. 3, 307-321
9. Harding, H. P., Calfon, M., Urano, F., Novoa, I., and Ron, D. (2002) Transcriptional and translational control in the Mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18, 575-599
10. Wu, J., Ruas, J. L., Estall, J. L., Rasbach, K. A., Choi, J. H., Ye, L., Boström, P., Tyra, H.M., Crawford, R.W., Campbell, K. P., Rutkowski, D. T., Kaufman, R. J., and Spiegelman, B. M. (2011) The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1a/ATF6a complex. Cell Metab. 13, 160-169
11. Iwawaki, T., Akai, R., Kohno, K., and Miura, M. (2004) A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat. Med. 10, 98-102
12. Acosta-Alvear, D., Zhou, Y., Blais, A., Tsikitis, M., Lents, N. H., Arias, C., Lennon, C. J., Kluger, Y., and Dynlacht, B. D. (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell 27, 53-66
13. Ebert, S. M., Monteys, A.M., Fox, D.K., Bongers, K. S., Shields, B. E., Malmberg, S. E., Davidson, B. L., Suneja, M., and Adams, C. M. (2010) The transcription factor ATF4 promotes skeletal myofiber atrophy during fasting. Mol. Endocrinol. 24, 790-799
14. Nakanishi, K., Sudo, T., and Morishima, N. (2005) Endoplasmic reticulum stress signaling transmitted by ATF6 mediates apoptosis during muscle development. J. Cell Biol. 169, 555-560
15. Oyadomari, S., Harding, H. P., Zhang, Y., Oyadomari, M., and Ron, D. (2008) Dephosphorylation of translation initiation factor 2alpha enhances glucose tolerance and attenuates hepatosteatosis in mice. Cell Metab. 7, 520-532
16. Brennan, K. J., and Hardeman, E. C. (1993) Quantitative analysis of the human alpha-skeletal actin gene in transgenicmice. J. Biol. Chem. 268, 719-725
17. Oyadomari, S., Yun, C., Fisher, E. A., Kreglinger, N., Kreibich, G., Oyadomari, M., Harding, H. P., Goodman, A. G., Harant, H., Garrison, J. L., Taunton, J., Katze, M. G., and Ron, D. (2006) Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126, 727-739
18. Goodman, C. A., Mabrey, D. M., Frey, J. W., Miu, M. H., Schmidt, E.K., Pierre, P., and Hornberger, T.A. (2011)Novel insights into the regulation of skeletal muscle protein synthesis as revealed by a new nonradioactive in vivo technique. FASEB J. 25, 1028-1039
19. Kim, H. J., Jamart, C., Deldicque, L., An, G. L., Lee, Y.H., Kim, C. K., Raymackers, J.M., and Francaux, M. (2011) Endoplasmic reticulum stress markers and ubiquitin-proteasome pathway activity in response to a 200-km run. Med. Sci. Sports Exerc. 43, 18-25
20. Lu, P. D., Jousse, C., Marciniak, S. J., Zhang, Y., Novoa, I., Scheuner, D., Kaufman, R. J., Ron, D., and Harding, H. P. (2004) Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23, 169-179
21. Lewerenz, J., and Maher, P. (2009) Basal levels of eIF2alpha phosphorylation determine cellular antioxidant status by regulating ATF4 and xCT expression. J. Biol. Chem. 284, 1106-1115
22. Ji, L. L. (2008)Modulation of skeletalmuscle antioxidant defense by exercise: role of redox signaling. Free Radic. Biol. Med. 44, 142-152
23. Mailloux, R. J., Adjeitey, C. N., Xuan, J. Y., and Harper, M. E. (2012) Crucial yet divergent roles of mitochondrial redox state in skeletal muscle vs. brown adipose tissue energetics. FASEB J. 26, 363-375
24. Mar?, M., Morales, A., Colell, A., Garc?a-Ruiz, C., andFernandez-Checa, J. C. (2009) Mitochondrial glutathione, a key survival antioxidant. Antioxid. Redox Signal. 11, 2685-2700
25. Adams, A. C., and Kharitonenkov, A. (2012) FGF21: The center of a transcriptional nexus in metabolic regulation. Curr. Diabetes Rev. 8, 285-293
26. Potthoff, M. J., Kliewer, S. A., and Mangelsdorf, D. J. (2012) Endocrine fibroblast growth factors 15/19 and 21: from feast to famine. Genes Dev. 26, 312-324
27. Kharitonenkov, A., Shiyanova, T. L., Koester, A., Ford, A. M., Micanovic, R., Galbreath, E. J., Sandusky, G. E., Hammond, L. J., Moyers, J. S., Owens, R. A., Gromada, J., Brozinick, J. T., Hawkins, E. D., Wroblewski, V. J., Li, D. S., Mehrbod, F., Jaskunas, S. R., and Shanafelt, A. B. (2005) FGF-21 as a novelmetabolic regulator. J. Clin. Invest. 115, 1627-1635
28. Badman, M. K., Koester, A., Flier, J. S., Kharitonenkov, A., and Maratos-Flier, E. (2009) Fibroblast growth factor 21-deficient mice demonstrate impaired adaptation to ketosis. Endocrinology 150, 4931-4940
29. Bai, H., Chen, T., Ming, J., Sun, H., Cao, P., Fusco, D.N., Chung, R. T., Chorev, M., Jin, Q., and Aktas, B.H. (2013)Dual activators of protein kinase R (PKR) and protein kinase R-like kinase PERK identify common and divergent catalytic targets. Chem Bio Chem14, 1255-1262
30. Boyce, M., Bryant, K. F., Jousse, C., Long, K., Harding, H. P., Scheuner, D., Kaufman, R. J., Ma, D., Coen, D.M., Ron, D., and Yuan, J. (2005) A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307, 935-939
31. Tsaytler, P., Harding, H. P., Ron, D., and Bertolotti, A. (2011) Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science 332, 91-94
32. Sidrauski, C., Acosta-Alvear, D., Khoutorsky, A., Vedantham, P., Hearn, B. R., Li, H., Gamache, K., Gallagher, C. M., Ang, K. K., Wilson, C., Okreglak, V., Ashkenazi, A., Hann, B., Nader, K., Arkin, M. R., Renslo, A. R., Sonenberg, N., and Walter, P. (2013) Pharmacological brake-release of mRNA translation enhances cognitive memory. eLife 2, e00498
33. Inagaki, T., Lin, V. Y., Goetz, R., Mohammadi, M., Mangelsdorf, D. J., and Kliewer, S. A. (2008) Inhibition of growth hormone signaling by the fasting-induced hormone FGF21. Cell Metab. 8, 77-83
34. Dutchak, P. A., Katafuchi, T., Bookout, A. L., Choi, J. H., Yu, R. T., Mangelsdorf, D. J., and Kliewer, S. A. (2012) Fibroblast growth factor-21 regulates PPARg activity and the antidiabetic actions of thiazolidinediones. Cell 148, 556-567
35. Fon Tacer, K., Bookout, A. L., Ding, X., Kurosu, H., John, G. B., Wang, L., Goetz, R., Mohammadi, M., Kuro-o, M., Mangelsdorf, D. J., and Kliewer, S. A. (2010) Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol. Endocrinol. 24, 2050-2064
36. Kim, K.H., Jeong, Y.T., Oh, H., Kim, S.H., Cho, J.M., Kim, Y.N., Kim, S.S., Kim, H., Hur, K.Y., Kim, H.K., Ko, T., Han, J., Kim, H.L., Kim, J., Back, S.H., Komatsu, M., Chen, H., Chan, D.C., Konishi, M., Itoh, N., Choi, C. S., and Lee, M. S. (2013) Autophagy deficiency leads to protection fromobesity and insulin resistance by inducing Fgf21 as a mitokine. Nat. Med. 19, 83-92
37. Bchir, W., Maurin, A. C., Carraro, V., Averous, J., Jousse, C., Muranishi, Y., Parry, L., Stepien, G., Fafournoux, P., and Bruhat, A. (2013) The eIF2a/ATF4 pathway is essential for stress-induced autophagy gene expression. Nucleic Acids Res. 41, 7683-7699
38. Lew, H., Pyke, S., and Quintanilha, A. (1985) Changes in the glutathione status of plasma, liver and muscle following exhaustive exercise in rats. FEBS Lett. 185, 262-266
39. Sen, C. K., Atalay, M., and Hanninen, O. (1994) Exercise-induced oxidative stress: glutathione supplementation and deficiency. J. Appl. Physiol. 77, 2177-2187
40. Nguyen, D., Samson, S. L., Reddy, V. T., Gonzalez, E. V., and Sekhar, R. V. (2013) Impaired mitochondrial fatty acid oxidation and insulin resistance in aging:novel protective role of glutathione.Aging Cell 12, 415-425
41. Inagaki, T., Dutchak, P., Zhao, G., Ding, X., Gautron, L., Parameswara, V., Li, Y., Goetz, R., Mohammadi, M., Esser, V., Elmquist, J. K., Gerard, R. D., Burgess, S. C., Hammer, R. E., Mangelsdorf, D. J., and Kliewer, S.A. (2007)Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 5, 415-425
42. Fisher, F. M., Kleiner, S., Douris, N., Fox, E. C., Mepani, R. J., Verdeguer, F., Wu, J., Kharitonenkov, A., Flier, J. S., Maratos-Flier, E., and Spiegelman, B. M. (2012) FGF21 regulates PGC-1a and browning of white adipose tissues in adaptive thermogenesis. GenesDev. 26, 271-281
43. Nelson, B. T., Ding, X., Boney-Montoya, J., Gerard, R. D., Kliewer, S. A., and Andrews, M. T. (2013) Metabolic hormone FGF21 is induced in ground squirrels during hibernation but its overexpression is not sufficient to cause torpor. PLoS One 8, e53574
44. Mamady, H., and Storey, K. B. (2008) Coping with the stress: expression of ATF4, ATF6, and downstream targets in organs of hibernating ground squirrels. Arch. Biochem. Biophys. 477, 77-85
45. Frerichs, K. U., Smith, C. B., Brenner, M., DeGracia, D. J., Krause, G. S., Marrone, L., Dever, T. E., and Hallenbeck, J. M. (1998) Suppressionofproteinsynthesis inbrainduringhibernationinvolves inhibition of protein initiation and elongation. Proc. Natl. Acad. Sci. USA 95, 14511-14516