RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition

PLoS Genetics

Volumn 6, Issue 8, 2010, Pages

  Wang, Jinling ^a   Robida Stubbs, Stacey ^a   Tullet, Jennifer M A ^a,d   Rual, Jean François ^b,c   Vidal, Marc ^b,c   Keith Blackwell, T ^a  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MESSENGER RNA; PROTEIN GCS 1; PROTEIN SKN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CELL METABOLISM; CONTROLLED STUDY; DETOXIFICATION; DIET RESTRICTION; ENERGY METABOLISM; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE REGULATORY NETWORK; GENE SILENCING; GENE TARGETING; LIFE EXTENSION; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RNA INTERFERENCE; RNA TRANSLATION; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; LONGEVITY; PROTEIN BIOSYNTHESIS; RNA INTERFERENCE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 77957583314     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001048     Document Type: Article

References (63)

1. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414: 813-820.
2. Lithgow GJ, Walker GA (2002) Stress resistance as a determinate of C. elegans lifespan. Mech Ageing Dev 123: 765-771.
3. Droge W(2002) Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95.
4. Gems D, McElwee JJ (2005) Broad spectrum detoxification: the major longevity assurance process regulated by insulin/IGF-1 signaling? Mech Ageing Dev 126: 381-387.
5. Kregel KC, Zhang HJ (2007) An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Regul Integr Comp Physiol 292: R18-R36.
6. Lenzen S (2008) Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 36: 343-347.
7. Xu C, Li CY, Kong AN (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28: 249-268.
8. Hayes JD, McMahon M (2001) Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett 174: 103-113.
9. Kobayashi M, Yamamoto M (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul 46: 113-140.
10. Sykiotis GP, Bohmann D (2010) Stress-activated cap'n'collar transcription factors in aging and human disease. Sci Signal 3: re3.
11. An JH, Blackwell TK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17: 1882-1893.
12. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J, et al. (2009) Conditionadapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8: 524-541.
13. Park SK, Tedesco PM, Johnson TE (2009) Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8: 258-269.
14. Olahova M, Taylor SR, Khazaipoul S, Wang J, Morgan BA, et al. (2008) A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc Natl Acad Sci U S A 105: 19839-19844.
15. Kenyon CJ (2010) The genetics of ageing. Nature 464: 504-512.
16. Antebi A (2007) Genetics of aging in Caenorhabditis elegans. PLoS Genet 3: e129. doi:10.1371/journal.pgen.0030129.
17. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, et al. (2008) Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132: 1025-1038.
18. Bishop NA, Guarente L (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545-549.
19. Kennedy BK, Kaeberlein M (2009) Hot topics in aging research: protein translation, 2009. Aging Cell 8: 617-623.
20. Bjedov I, Toivonen JM, Kerr F, Slack C, Jacobson J, et al. (2010) Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab 11: 35-46.
21. Zid BM, Rogers AN, Katewa SD, Vargas MA, Kolipinski MC, et al. (2009) 4EBP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139: 149-160.
22. Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, et al. (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6: 111-119.
23. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, et al. (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6: 95-110.
24. Selman C, Tullet JM, Wieser D, Irvine E, Lingard SJ, et al. (2009) Ribosomal protein S6 kinase 1 signaling regulates mammalian life span. Science 326: 140-144.
25. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, et al. (2004) Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14: 885-890.
26. Syntichaki P, Troulinaki K, Tavernarakis N (2007) eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans. Nature 445: 922-926.
27. Steffen KK, MacKay VL, Kerr EO, Tsuchiya M, Hu D, et al. (2008) Yeast life span extension by depletion of 60 s ribosomal subunits is mediated by Gcn4. Cell 133: 292-302.
28. Henderson ST, Bonafe M, Johnson TE (2006) daf-16 protects the nematode Caenorhabditis elegans during food deprivation. J Gerontol A Biol Sci Med Sci 61: 444-460.
29. Tohyama D, Yamaguchi A, Yamashita T (2008) Inhibition of a eukaryotic initiation factor (eIF2Bdelta/F11A3.2) during adulthood extends lifespan in Caenorhabditis elegans. Faseb J 22: 4327-4337.
30. Chen D, Pan KZ, Palter JE, Kapahi P (2007) Longevity determined by developmental arrest genes in Caenorhabditis elegans. Aging Cell 6: 525-533.
31. Curran SP, Ruvkun G (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet 3: e56. doi:10.1371/journal.pgen.0030056.
32. An JH, Vranas K, Lucke M, Inoue H, Hisamoto N, et al. (2005) Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc Natl Acad Sci U S A 102: 16275-16280.
33. Kamath RS, Ahringer J (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
34. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, et al. (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14: 2162-2168.
35. Choe KP, Przybysz AJ, Strange K (2009) The WD40 repeat protein WDR-23 functions with the CUL4/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans. Mol Cell Biol 29: 2704-2715.
36. Cope GA, Deshaies RJ (2003) COP9 signalosome: a multifunctional regulator of SCF and other cullin-based ubiquitin ligases. Cell 114: 663-671.
37. Pick E, Pintard L (2009) In the land of the rising sun with the COP9 signalosome and related Zomes. Symposium on the COP9 signalosome, Proteasome and eIF3. EMBO reports 10: 343-348.
38. Chamovitz DA (2009) Revisiting the COP9 signalosome as a transcriptional regulator. EMBO reports 10: 352-358.
39. Luke-Glaser S, Roy M, Larsen B, Le Bihan T, Metalnikov P, et al. (2007) CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol Cell Biol 27: 4526-4540.
40. Kahn NW, Rea SL, Moyle S, Kell A, Johnson TE (2008) Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans. Biochem J 409: 205-213.
41. Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, et al. (2005) The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev 19: 2278-2283.
42. Honda Y, Honda S (1999) The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. Faseb J 13: 1385-1393.
43. Hamilton B, Dong Y, Shindo M, Liu W, Odell I, et al. (2005) A systematic RNAi screen for longevity genes in C. elegans. Genes Dev 19: 1544-1555.
44. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
45. Lee SJ, Murphy CT, Kenyon C (2009) Glucose shortens the life span of C. elegans by downregulating DAF-16/FOXO activity and aquaporin gene expression. Cell Metab 10: 379-391.
46. Porter Abate J, Blackwell TK (2009) Life is short, if sweet. Cell Metab 10: 338-339.
47. Sykiotis GP, Bohmann D (2008) Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell 14: 76-85.
48. Fisher AL, Page KE, Lithgow GJ, Nash L (2008) The Caenorhabditis elegans K10C2.4 gene encodes a member of the fumarylacetoacetate hydrolase family: a Caenorhabditis elegans model of type I tyrosinemia. J Biol Chem 283: 9127-9135.
49. Loh K, Deng H, Fukushima A, Cai X, Boivin B, et al. (2009) Reactive oxygen species enhance insulin sensitivity. Cell Metab 10: 260-272.
50. Sevier CS, Kaiser CA (2008) Ero1 and redox homeostasis in the endoplasmic reticulum. Biochim Biophys Acta 1783: 549-556.
51. Radhakrishnan SK, Lee CS, Young P, Beskow A, Chan JY, et al. (2010) Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol Cell 38: 17-28.
52. Mair W, Dillin A (2008) Aging and survival: the genetics of life span extension by dietary restriction. Annu Rev Biochem 77: 727-754.
53. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, Orosz L, et al. (2003) Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 426: 620.
54. Sheaffer KL, Updike DL, Mango SE (2008) The Target of Rapamycin pathway antagonizes pha-4/FoxA to control development and aging. Curr Biol 18: 1355-1364.
55. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, et al. (2009) Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462: 522-526.
56. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774.
57. Turner GC, Varshavsky A (2000) Detecting and measuring cotranslational protein degradation in vivo. Science 289: 2117-2120.
58. Fielenbach N, Antebi A (2008) C. elegans dauer formation and the molecular basis of plasticity. Genes Dev 22: 2149-2165.
59. Bowerman B, Eaton BA, Priess JR (1992) skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68: 1061-1075.
60. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, et al. (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389: 994-999.
61. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2001) Effectiveness of specific RNA-mediated interference through ingested doublestranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.
62. Link CD, Johnson CJ (2002) Reporter transgenes for study of oxidant stress in Caenorhabditis elegans. Methods Enzymol 353: 497-505.
63. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, et al. (2005) Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184.