Less is more: Improving proteostasis by translation slow down

Trends in Biochemical Sciences

Volumn 38, Issue 12, 2013, Pages 585-591

  Sherman, Michael Y ^a   Qian, Shu Bing ^b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

Aging; Co translational folding; Degradation; Proteostasis; Translation inhibitors

Indexed keywords

ALKALOID; ANDROGEN RECEPTOR; CHAPERONE; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EMETINE; EVEROLIMUS; HEAT SHOCK PROTEIN 104; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; HUNTINGTIN; HYPURISTANOL; INITIATION FACTOR 2; INITIATION FACTOR 2ALPHA; INITIATION FACTOR 4E BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; PF 4708671; POLYGLUTAMINE; PROTEIN SERINE THREONINE KINASE; RAPAMYCIN; RIDAFOROLIMUS; S6 KINASE; SOMATOMEDIN C; SUPEROXIDE DISMUTASE; TAU PROTEIN; TEMSIROLIMUS; TRANSFER RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AGING; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANTINEOPLASTIC ACTIVITY; AUTOPHAGY; CYSTIC FIBROSIS; DRUG EFFECT; DRUG TOLERABILITY; ENZYME INHIBITION; GENE MUTATION; HUMAN; HUNTINGTON CHOREA; KENNEDY DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA TRANSLATION; SIGNAL TRANSDUCTION; STRESS; TRANSLATION INITIATION; TRANSLATION REGULATION;

AGING; CO-TRANSLATIONAL FOLDING; DEGRADATION; PROTEOSTASIS; TRANSLATION INHIBITORS;

HOMEOSTASIS; PROTEIN BIOSYNTHESIS; PROTEINS;

EID: 84888136766     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2013.09.003     Document Type: Review

References (87)

1. Powers E.T., Balch W.E. Diversity in the origins of proteostasis networks - a driver for protein function in evolution. Nat. Rev. Mol. Cell Biol. 2013, 14:237-248.
2. Ravikumar B., Rubinsztein D.C. Role of autophagy in the clearance of mutant huntingtin: a step towards therapy?. Mol. Aspects Med. 2006, 27:520-527.
3. Rubinsztein D.C., et al. Potential therapeutic applications of autophagy. Nat. Rev. Drug Discov. 2007, 6:304-312.
4. Sarkar S., Rubinsztein D.C. Small molecule enhancers of autophagy for neurodegenerative diseases. Mol. Biosyst. 2008, 4:895-901.
5. Sarkar S., et al. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine-expanded huntingtin and related proteinopathies. Cell Death Differ. 2009, 16:46-56.
6. Wang A.M., et al. Activation of Hsp70 reduces neurotoxicity by promoting polyglutamine protein degradation. Nat. Chem. Biol. 2013, 9:112-118.
7. O'Leary J.C., et al. Phenothiazine-mediated rescue of cognition in tau transgenic mice requires neuroprotection and reduced soluble tau burden. Mol. Neurodegener. 2010, 5:45.
8. Abisambra J., et al. Allosteric heat shock protein 70 inhibitors rapidly rescue synaptic plasticity deficits by reducing aberrant tau. Biol. Psychiatry 2013, 74:367-374.
9. Miyata Y., et al. Synthesis and initial evaluation of YM-08, a blood-brain barrier permeable derivative of the heat shock protein 70 (Hsp70) inhibitor MKT-077, which reduces tau levels. ACS Chem. Neurosci. 2013, 4:930-939.
10. Lee B.H., et al. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature 2012, 467:179-184.
11. Putcha P., et al. Brain-permeable small-molecule inhibitors of Hsp90 prevent alpha-synuclein oligomer formation and rescue alpha-synuclein-induced toxicity. J. Pharmacol. Exp. Ther. 2010, 332:849-857.
12. Paris D., et al. Reduction of beta-amyloid pathology by celastrol in a transgenic mouse model of Alzheimer's disease. J. Neuroinflammation 2010, 7:17.
13. Chafekar S.M., et al. Pharmacological tuning of heat shock protein 70 modulates polyglutamine toxicity and aggregation. ACS Chem. Biol. 2012, 7:1556-1564.
14. Kilpatrick K., et al. Chemical induction of Hsp70 reduces alpha-synuclein aggregation in neuroglioma cells. ACS Chem. Biol. 2013, 10.1021/cb400017.
15. Mu T.W., et al. Chemical and biological approaches synergize to ameliorate protein-folding diseases. Cell 2008, 134:769-781.
16. Pechmann S., et al. The ribosome as a hub for protein quality control. Mol. Cell 2013, 49:411-421.
17. Sosnick T.R., Barrick D. The folding of single domain proteins - have we reached a consensus?. Curr. Opin. Struct. Biol. 2011, 21:12-24.
18. Kramer G., et al. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16:589-597.
19. Komar A.A. A pause for thought along the co-translational folding pathway. Trends Biochem. Sci. 2009, 34:16-24.
20. Klinge S., et al. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 2011, 334:941-948.
21. Fedyukina D.V., Cavagnero S. Protein folding at the exit tunnel. Annu. Rev. Biophys. 2011, 40:337-359.
22. Wilson D.N., Beckmann R. The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr. Opin. Struct. Biol. 2011, 21:274-282.
23. Han Y., et al. Monitoring cotranslational protein folding in mammalian cells at codon resolution. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12467-12472.
24. Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 2001, 70:603-647.
25. Kampinga H.H., Craig E.A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 2010, 11:579-592.
26. del Alamo M., et al. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 2011, 9:e1001100.
27. Willmund F., et al. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 2013, 152:196-209.
28. Albanese V., et al. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 2006, 124:75-88.
29. Albanese V., et al. A ribosome-anchored chaperone network that facilitates eukaryotic ribosome biogenesis. J. Cell Biol. 2010, 189:69-81.
30. Schubert U., et al. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000, 404:770-774.
31. Vabulas R.M., Hartl F.U. Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 2005, 310:1960-1963.
32. Yewdell J.W., Nicchitta C.V. The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol. 2006, 27:368-373.
33. Duttler S., et al. Principles of cotranslational ubiquitination and quality control at the ribosome. Mol. Cell 2013, 50:379-393.
34. Wang F., et al. A cotranslational ubiquitination pathway for quality control of misfolded proteins. Mol. Cell 2013, 50:368-378.
35. Turner G.C., Varshavsky A. Detecting and measuring cotranslational protein degradation in vivo. Science 2000, 289:2117-2120.
36. Medicherla B., Goldberg A.L. Heat shock and oxygen radicals stimulate ubiquitin-dependent degradation mainly of newly synthesized proteins. J. Cell Biol. 2008, 182:663-673.
37. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
38. Holcik M., Sonenberg N. Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol. 2005, 6:318-327.
39. Ma X.M., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 2009, 10:307-318.
40. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
41. Liu B., et al. Cotranslational response to proteotoxic stress by elongation pausing of ribosomes. Mol. Cell 2013, 49:453-463.
42. Shalgi R., et al. Widespread regulation of translation by elongation pausing in heat shock. Mol. Cell 2013, 49:439-452.
43. Gingold H., Pilpel Y. Determinants of translation efficiency and accuracy. Mol. Syst. Biol. 2011, 7:481.
44. Abraham A.K., Pihl A. Effect of protein synthesis inhibitors on the fidelity of translation in eukaryotic systems. Biochim. Biophys. Acta 1983, 741:197-203.
45. Zaher H.S., Green R. Fidelity at the molecular level: lessons from protein synthesis. Cell 2009, 136:746-762.
46. Thompson R.C., Karim A.M. The accuracy of protein biosynthesis is limited by its speed: high fidelity selection by ribosomes of aminoacyl-tRNA ternary complexes containing GTPγS]. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:4922-4926.
47. Fluitt A., et al. Ribosome kinetics and aa-tRNA competition determine rate and fidelity of peptide synthesis. Comput. Biol. Chem. 2007, 31:335-346.
48. Hekman K.E., et al. A conserved eEF2 coding variant in SCA26 leads to loss of translational fidelity and increased susceptibility to proteostatic insult. Hum. Mol. Genet. 2012, 21:5472-5483.
49. Paredes J.A., et al. Low level genome mistranslations deregulate the transcriptome and translatome and generate proteotoxic stress in yeast. BMC Biol. 2012, 10:55.
50. Kim S.Y., Craig E.A. Broad sensitivity of Saccharomyces cerevisiae lacking ribosome-associated chaperone ssb or zuo1 to cations, including aminoglycosides. Eukaryot. Cell 2005, 4:82-89.
51. Ingolia N.T., et al. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 2011, 147:789-802.
52. Buchan J.R., Stansfield I. Halting a cellular production line: responses to ribosomal pausing during translation. Biol. Cell 2007, 99:475-487.
53. Kertesz M., et al. Genome-wide measurement of RNA secondary structure in yeast. Nature 2010, 467:103-107.
54. Plotkin J.B., Kudla G. Synonymous but not the same: the causes and consequences of codon bias. Nat. Rev. Genet. 2011, 12:32-42.
55. Zhang G., et al. Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat. Struct. Mol. Biol. 2009, 16:274-280.
56. Shabalina S.A., et al. Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity. Nucleic Acids Res. 2013, 41:2073-2094.
57. Xu Y., et al. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 2013, 495:116-120.
58. Zhou M., et al. Non-optimal codon usage affects expression, structure and function of clock protein FRQ. Nature 2013, 495:111-115.
59. Siller E., et al. Slowing bacterial translation speed enhances eukaryotic protein folding efficiency. J. Mol. Biol. 2010, 396:1310-1318.
60. Meriin A.B., et al. A novel approach to recovery of function of mutant proteins by slowing down translation. J. Biol. Chem. 2012, 287:34264-34272.
61. Meriin A.B., et al. Association of translation factor eEF1A with defective ribosomal products generates a signal for aggresome formation. J. Cell Sci. 2012, 125:2665-2674.
62. Tsaytler P., et al. Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science 2011, 332:91-94.
63. Hulleman J.D., et al. Translational attenuation differentially alters the fate of disease-associated fibulin proteins. FASEB J. 2013, 26:4548-4560.
64. Laplante M., Sabatini D.M. mTOR signaling in growth control and disease. Cell 2012, 149:274-293.
65. Conn C.S., Qian S.B. Nutrient signaling in protein homeostasis: an increase in quantity at the expense of quality. Sci. Signal. 2013, 6:ra24.
66. Jackson R.J., et al. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 2010, 11:113-127.
67. Choo A.Y., et al. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:17414-17419.
68. Mehta R., et al. Regulation of mRNA translation as a conserved mechanism of longevity control. Adv. Exp. Med. Biol. 2010, 694:14-29.
69. Tohyama D., et al. Inhibition of a eukaryotic initiation factor (eIF2Bdelta/F11A3.2) during adulthood extends lifespan in Caenorhabditis elegans. FASEB J. 2008, 22:4327-4337.
70. Hansen M., et al. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 2007, 6:95-110.
71. Hipkiss A.R. On why decreasing protein synthesis can increase lifespan. Mech. Ageing Dev. 2007, 128:412-414.
72. Silva M.C., et al. A genetic screening strategy identifies novel regulators of the proteostasis network. PLoS Genet. 2011, 7:e1002438.
73. Demontis F., Perrimon N. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 2010, 143:813-825.
74. Blagosklonny M.V. An anti-aging drug today: from senescence-promoting genes to anti-aging pill. Drug Discov. Today 2007, 12:218-224.
75. Wei Y., et al. Growth or longevity: the TOR's decision on lifespan regulation. Biogerontology 2013, 14:353-363.
76. Marie C., Petri W.A. Amoebic dysentery. Clin. Evid. (Online) 2013, 2013:pii: 0918.
77. Lamming D.W., et al. Rapalogs and mTOR inhibitors as anti-aging therapeutics. J. Clin. Invest. 2013, 123:980-989.
78. Blagosklonny M.V. Rapalogs in cancer prevention: anti-aging or anticancer?. Cancer Biol. Ther. 2013, 13:1349-1354.
79. Inoki K., et al. Signaling by target of rapamycin proteins in cell growth control. Microbiol. Mol. Biol. Rev. 2005, 69:79-100.
80. Proud C.G. Role of mTOR signalling in the control of translation initiation and elongation by nutrients. Curr. Top. Microbiol. Immunol. 2004, 279:215-244.
81. Das F., et al. TGFβ enforces activation of eukaryotic elongation factor-2 (eEF2) via inactivation of eEF2 kinase by p90 ribosomal S6 kinase (p90Rsk) to induce mesangial cell hypertrophy. FEBS Lett. 2010, 584:4268-4272.
82. Dennis M.D., et al. Role of p70S6K1-mediated phosphorylation of eIF4B and PDCD4 proteins in the regulation of protein synthesis. J. Biol. Chem. 2012, 287:42890-42899.
83. Pearce L.R., et al. Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem. J. 2011, 431:245-255.
84. Pavitt G.D., Ron D. New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb. Perspect. Biol. 2012, 4. pii: a012278.
85. Kojima E., et al. The function of GADD34 is a recovery from a shutoff of protein synthesis induced by ER stress: elucidation by GADD34-deficient mice. FASEB J. 2003, 17:1573-1575.
86. Boyce M., et al. A selective inhibitor of eIF2α dephosphorylation protects cells from ER stress. Science 2005, 307:935-939.
87. Sica D.A. Centrally acting antihypertensive agents: an update. J. Clin. Hypertens. (Greenwich) 2007, 9:399-405.