Nutrient signaling in protein homeostasis: An increase in quantity at the expense of quality

Science Signaling

Volumn 6, Issue 271, 2013, Pages

  Conn, Crystal S ^a   Qian, Shu Bing ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; POLYPEPTIDE; PROTEASOME; RAPAMYCIN; RHEB PROTEIN; S6 KINASE;

ARTICLE; CELL ELONGATION; DOWNSTREAM PROCESSING; EMBRYO; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; NUTRIENT; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS; PROTEIN STABILITY; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSLATION; SIGNAL TRANSDUCTION; STRESS; TRANSLATION REGULATION;

ANIMALS; CELL LINE; DNA PRIMERS; HOMEOSTASIS; HUMANS; IMMUNOBLOTTING; LUCIFERASES; MICE; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

MAMMALIA;

EID: 84876574053     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2003520     Document Type: Article

References (52)

1. S. Wullschleger, R. Loewith, M. N. Hall, TOR signaling in growth and metabolism. Cell 124, 471-484 (2006).
2. M. Laplante, D. M. Sabatini, mTOR signaling in growth control and disease. Cell 149, 274-293 (2012).
3. X. M. Ma, J. Blenis, Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318 (2009).
4. N. Sonenberg, A. G. Hinnebusch, Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136, 731-745 (2009).
5. K. Inoki, K. L. Guan, Complexity of the TOR signaling network. Trends Cell Biol. 16, 206-212 (2006).
6. J. Huang, B. D. Manning, The TSC1-TSC2 complex: A molecular switchboard controlling cell growth. Biochem. J. 412, 179-190 (2008).
7. D. J. Kwiatkowski, B. D. Manning, Tuberous sclerosis: A GAP at the crossroads of multiple signaling pathways. Hum. Mol. Genet. 14, R251-R258 (2005).
8. J. Goto, D. M. Talos, P. Klein, W. Qin, Y. I. Chekaluk, S. Anderl, I. A. Malinowska, A. Di Nardo, R. T. Bronson, J. A. Chan, H. V. Vinters, S. G. Kernie, F. E. Jensen, M. Sahin, D. J. Kwiatkowski, Regulable neural progenitor-specific Tsc1 loss yields giant cells with organellar dysfunction in a model of tuberous sclerosis complex. Proc. Natl. Acad. Sci. U.S.A. 108, E1070-E1079 (2011).
9. R. Zoncu, A. Efeyan, D. M. Sabatini, mTOR: From growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35 (2011).
10. C. Kenyon, The plasticity of aging: Insights from long-lived mutants. Cell 120, 449-460 (2005).
11. E. Cohen, J. F. Paulsson, P. Blinder, T. Burstyn-Cohen, D. Du, G. Estepa, A. Adame, H. M. Pham, M. Holzenberger, J. W. Kelly, E. Masliah, A. Dillin, Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139, 1157-1169 (2009).
12. L. Fontana, The scientific basis of caloric restriction leading to longer life. Curr. Opin. Gastroenterol. 25, 144-150 (2009).
13. P. Kapahi, D. Chen, A. N. Rogers, S. D. Katewa, P. W. Li, E. L. Thomas, L. Kockel, With TOR, less is more: A key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 11, 453-465 (2010).
14. P. Kapahi, B. M. Zid, T. Harper, D. Koslover, V. Sapin, S. Benzer, Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr. Biol. 14, 885-890 (2004).
15. M. Kaeberlein, R. W. Powers III, K. K. Steffen, E. A. Westman, D. Hu, N. Dang, E. O. Kerr, K. T. Kirkland, S. Fields, B. K. Kennedy, Regulation of yeast replicative life span by TOR and Sch9 in response to nutrients. Science 310, 1193-1196 (2005).
16. D. E. Harrison, R. Strong, Z. D. Sharp, J. F. Nelson, C. M. Astle, K. Flurkey, N. L. Nadon, J. E. Wilkinson, K. Frenkel, C. S. Carter, M. Pahor, M. A. Javors, E. Fernandez, R. A. Miller, Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460, 392-395 (2009).
17. K. Z. Pan, J. E. Palter, A. N. Rogers, A. Olsen, D. Chen, G. J. Lithgow, P. Kapahi, Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6, 111-119 (2007).
18. M. Hansen, S. Taubert, D. Crawford, N. Libina, S. J. Lee, C. Kenyon, Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6, 95-110 (2007).
19. P. Syntichaki, K. Troulinaki, N. Tavernarakis, eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445, 922-926 (2007).
20. W. E. Balch, R. I. Morimoto, A. Dillin, J. W. Kelly, Adapting proteostasis for disease intervention. Science 319, 916-919 (2008).
21. R. I. Morimoto, Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427-1438 (2008).
22. B. Bukau, J. Weissman, A. Horwich, Molecular chaperones and protein quality control. Cell 125, 443-451 (2006).
23. J. Sun, C. S. Conn, Y. Han, V. Yeung, S. B. Qian, PI3K-mTORC1 attenuates stress response by inhibiting cap-independent Hsp70 translation. J. Biol. Chem. 286, 6791-6800 (2011).
24. R. J. Jackson, C. U. Hellen, T. V. Pestova, The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113-127 (2010).
25. S. G. Dann, A. Selvaraj, G. Thomas, mTOR Complex1-S6K1 signaling: At the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13, 252-259 (2007).
26. C. G. Proud, mTOR signalling in health and disease. Biochem. Soc. Trans. 39, 431-436 (2011).
27. A.C.Hsieh,Y. Liu, M. P. Edlind,N. T. Ingolia, M. R. Janes, A.Sher,E.Y.Shi, C. R. Stumpf, C. Christensen, M. J. Bonham, S. Wang, P. Ren, M. Martin, K. Jessen, M. E. Feldman, J. S. Weissman, K. M. Shokat, C. Rommel, D. Ruggero, The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 485, 55-61 (2012).
28. C. C. Thoreen, L. Chantranupong, H. R. Keys, T. Wang, N. S. Gray, D. M. Sabatini, A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485, 109-113 (2012).
29. A. Y. Choo, S. O. Yoon, S. G. Kim, P. P. Roux, J. Blenis, Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc. Natl. Acad. Sci. U.S.A. 105, 17414-17419 (2008).
30. C. Selman, J. M. Tullet, D. Wieser, E. Irvine, S. J. Lingard, A. I. Choudhury, M. Claret, H. Al-Qassab, D. Carmignac, F. Ramadani, A. Woods, I. C. Robinson, E. Schuster, R. L. Batterham, S. C. Kozma, G. Thomas, D. Carling, K. Okkenhaug, J. M. Thornton, L. Partridge, D. Gems, D. J. Withers, Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326, 140-144 (2009).
31. J. Frydman, H. Erdjument-Bromage, P. Tempst, F. U. Hartl, Co-translational domain folding as the structural basis for the rapid de novo folding of firefly luciferase. Nat. Struct. Biol. 6, 697-705 (1999).
32. R. Gupta, P. Kasturi, A. Bracher, C. Loew, M. Zheng, A. Villella, D. Garza, F. U. Hartl, S. Raychaudhuri, Firefly luciferase mutants as sensors of proteome stress. Nat. Methods 8, 879-884 (2011).
33. S. B. Qian, D. E. Ott, U. Schubert, J. R. Bennink, J. W. Yewdell, Fusion proteins with COOH-terminal ubiquitin are stable and maintain dual functionality in vivo. J. Biol. Chem. 277, 38818-38826 (2002).
34. F. U. Hartl, A. Bracher, M. Hayer-Hartl, Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
35. M. Y. Sherman, A. L. Goldberg, Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron 29, 15-32 (2001).
36. A. N. Fedorov, T. O. Baldwin, Cotranslational protein folding. J. Biol. Chem. 272, 32715-32718 (1997).
37. A. A. Komar, A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 34, 16-24 (2009).
38. J. R. Buchan, I. Stansfield, Halting a cellular production line: Responses to ribosomal pausing during translation. Biol. Cell 99, 475-487 (2007).
39. M. Rakwalska, S. Rospert, The ribosome-bound chaperones RAC and Ssb1/2p are required for accurate translation in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 9186-9197 (2004).
40. S. Belin, A. Beghin, E. Solano-Gonzàlez, L. Bezin, S. Brunet-Manquat, J. Textoris, A. C. Prats, H. C. Mertani, C. Dumontet, J. J. Diaz, Dysregulation of ribosome biogenesis and translational capacity is associated with tumor progression of human breast cancer cells. PLoS One 4, e7147 (2009).
41. N. T. Ingolia, L. F. Lareau, J. S. Weissman, Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802 (2011).
42. X. Zhou, T. Ikenoue, X. Chen, L. Li, K. Inoki, K. L. Guan, Rheb controls misfolded protein metabolism by inhibiting aggresome formation and autophagy. Proc. Natl. Acad. Sci. U.S.A. 106, 8923-8928 (2009).
43. C. M. McCay, M. F. Crowell, L. A. Maynard, The effect of retarded growth upon the length of life span and upon the ultimate body size. 1935. Nutrition 5, 155-171 (1989).
44. R. W. Powers III, M. Kaeberlein, S. D. Caldwell, B. K. Kennedy, S. Fields, Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 20, 174-184 (2006).
45. A. R. Hipkiss, On why decreasing protein synthesis can increase lifespan. Mech. Ageing Dev. 128, 412-414 (2007).
46. B. M. Zid, A. N. Rogers, S. D. Katewa, M. A. Vargas, M. C. Kolipinski, T. A. Lu, S. Benzer, P. Kapahi, 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139, 149-160 (2009).
47. C. G. Proud, mTORC1 signalling and mRNA translation. Biochem. Soc. Trans. 37, 227-231 (2009).
48. R. J. Dowling, I. Topisirovic, T. Alain, M. Bidinosti, B. D. Fonseca, E. Petroulakis, X. Wang, O. Larsson, A. Selvaraj, Y. Liu, S. C. Kozma, G. Thomas, N. Sonenberg, mTORC1-mediated cell proliferation, but not cell growth, controlled by the 4E-BPs. Science 328, 1172-1176 (2010).
49. H. Gingold, Y. Pilpel, Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 7, 481 (2011).
50. G. Zhang, M. Hubalewska, Z. Ignatova, Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat. Struct. Mol. Biol. 16, 274-280 (2009).
51. E. Siller, D. C. DeZwaan, J. F. Anderson, B. C. Freeman, J. M. Barral, Slowing bacterial translation speed enhances eukaryotic protein folding efficiency. J. Mol. Biol. 396, 1310-1318 (2010).
52. T. L. Hamilton, M. Stoneley, K. A. Spriggs, M. Bushell, TOPs and their regulation. Biochem. Soc. Trans. 34, 12-16 (2006).