Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf

Aging Cell

Volumn 8, Issue 5, 2009, Pages 524-541

  Oliveira, Riva P ^a,c   Abate, Jess Porter ^a   Dilks, Kieran ^b   Landis, Jessica ^b   Ashraf, Jasmine ^b   Murphy, Coleen T ^b   Blackwell, T Keith ^a  

^a HARVARD STEM CELL INSTITUTE   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c FEDERAL UNIVERSITY OF OURO PRETO   (Brazil)

Author keywords

Aging; Caenorhabditis elegans; Detoxification; Insulin signaling; Oxidative stress; SKN 1

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF; TRANSCRIPTION FACTOR SKN 1; UNCLASSIFIED DRUG; ARSENIC TRIOXIDE; ARSENOUS ACID DERIVATIVE; CAENORHABDITIS ELEGANS PROTEIN; DNA BINDING PROTEIN; HELMINTH DNA; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SKN 1 PROTEIN, C ELEGANS; SKN-1 PROTEIN, C ELEGANS; TERT BUTYL HYDROPEROXIDE; TRANSCRIPTION FACTOR NRF1;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DETOXIFICATION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE TARGETING; GENETIC REGULATION; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION; ANIMAL; DNA MICROARRAY; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; ARSENITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA, HELMINTH; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION; LONGEVITY; NF-E2-RELATED FACTOR 1; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA, MESSENGER; TERT-BUTYLHYDROPEROXIDE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 70350625466     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00501.x     Document Type: Article

References (64)

1. An JH, Blackwell TK (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev. 17, 1882-1893.
2. An JH, Vranas K, Lucke M, Inoue H, Hisamoto N, Matsumoto K, Blackwell TK (2005) Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc. Natl. Acad. Sci. USA 102, 16275-16280.
3. Banerjee R, Zou CG (2005) Redox regulation and reaction mechanism of human cystathionine-beta-synthase: a PLP-dependent hemesensor protein. Arch. Biochem. Biophys. 433, 144-156.
4. Bishop NA, Guarente L (2007a) Genetic links between diet and lifespan: shared mechanisms from yeast to humans. Nat. Rev. Genet. 8, 835-844.
5. Bishop NA, Guarente L (2007b) Two neurons mediate diet-restriction induced longevity in C. elegans. Nature 447, 545-549.
6. Blackwell TK, Bowerman B, Priess JR, Weintraub H (1994) Formation of a monomeric DNA binding domain by Skn-1 bZIP and homeodomain elements. Science 266, 621-628.
7. Blanc G, Font B, Eichenberger D, Moreau C, Ricard-Blum S, Hulmes DJ, Moali C (2007) Insights into how CUB domains can exert specific functions while sharing a common fold: conserved and specific features of the CUB1 domain contribute to the molecular basis of procollagen C-proteinase enhancer-1 activity. J. Biol. Chem. 282, 16924-16933.
8. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
9. Browne J, Tunnacliffe A, Burnell A (2002) Anhydrobiosis: plant desiccation gene found in a nematode. Nature 416, 38.
10. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190.
11. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3.
12. Dong MQ, Venable JD, Au N, Xu T, Park SK, Cociorva D, Johnson JR, Dillin A, Yates JR III (2007) Quantitative mass spectrometry identifies insulin signaling targets in C. elegans. Science 317, 660-663.
13. Droge W (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82, 47-95.
14. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863-14868.
15. Guarente L (2007) Sirtuins in aging and disease. Cold Spring Harb. Symp. Quant. Biol. 72, 483-488.
16. Hasegawa K, Miwa S, Isomura K, Tsutsumiuchi K, Taniguchi H, Miwa J (2008) Acrylamide-responsive genes in the nematode Caenorhabditis elegans. Toxicol Sci. 101, 215-225.
17. Hertweck M, Gobel C, Baumeister R (2004) C. elegans SGK-1 is the critical component in the Akt/PKB kinase complex to control stress response and life span. Dev Cell. 6, 577-588.
18. de Hoon MJ, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20, 1453-1454.
19. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol. Lett. 133, 1-16.
20. Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K (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.
21. Jasper H (2008) SKNy worms and long life. Cell 132, 915-916.
22. 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.
23. Kamath RS, Ahringer J (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
24. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2000) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, research0002.1-0002.10.
25. Kaplan J, De Domenico I, Ward DM (2008) Chediak-Higashi syndrome. Curr. Opin. Hematol. 15, 22-29.
26. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120, 449-460.
27. Kenyon C, Murphy CT (2006) Enrichment of regulatory motifs upstream of predicted DAF-16 targets. Nat. Genet. 38, 397-398; author reply 398.
28. Kobayashi M, Yamamoto M (2006) Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv. Enzyme Regul. 46, 113-140.
29. Kophengnavong T, Carroll AS, Blackwell TK (1999) The SKN-1 amino terminal arm is a DNA specificity segment. Mol. Cell. Biol. 19, 3039-3050.
30. Kubagawa HM, Watts JL, Corrigan C, Edmonds JW, Sztul E, Browse J, Miller MA (2006) Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat. Cell Biol. 8, 1143-1148.
31. Kwak MK, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler TW (2003) Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J. Biol. Chem. 278, 8135-8145.
32. Lee JM, Calkins MJ, Chan K, Kan YW, Johnson JA (2003a) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis. J. Biol. Chem. 278, 12029-12038.
33. Lee SS, Kennedy S, Tolonen AC, Ruvkun G (2003b) DAF-16 target genes that control C. elegans life-span and metabolism. Science 300, 644-647.
34. Leung L, Kwong M, Hou S, Lee C, Chan JY (2003) Deficiency of the Nrf1 and Nrf2 transcription factors results in early embryonic lethality and severe oxidative stress. J. Biol. Chem. 278, 48021-48029.
35. Lithgow GJ, Walker GA (2002) Stress resistance as a determinate of C. elegans lifespan. Mech. Ageing Dev. 123, 765-771.
36. Mathews WR, Guido DM, Fisher MA, Jaeschke H (1994) Lipid peroxidation as molecular mechanism of liver cell injury during reperfusion after ischemia. Free Radic. Biol. Med. 16, 763-770.
37. McElwee JJ, Schuster E, Blanc E, Piper MD, Thomas JH, Patel DS, Selman C, Withers DJ, Thornton JM, Partridge L, Gems D (2007) Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol. 8, R132.
38. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424, 277-283.
39. Murphy CT, Lee SJ, Kenyon C (2007) Tissue entrainment by feedback regulation of insulin gene expression in the endoderm of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 104, 19046-19050.
40. Nguyen T, Sherratt PJ, Pickett CB (2003) Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43, 233-260.
41. Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, Tissenbaum HA (2006) Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat. Genet. 38, 251-257.
42. Olahova M, Taylor SR, Khazaipoul S, Wang J, Morgan BA, Matsumoto K, Blackwell TK, Veal EA (2008) A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc. Natl. Acad. Sci. USA 105, 19839-19844.
43. Paradis S, Ruvkun G (1998) Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev. 12, 2488-2498.
44. Pavesi G, Mereghetti P, Mauri G, Pesole G (2004) Weeder Web: discovery of transcription factor binding sites in a set of sequences from co-regulated genes. Nucleic Acids Res. 32, W199-W203.
45. Rual JF, Ceron J, Koreth J, Hao T, Nicot AS, Hirozane-Kishikawa T, Vandenhaute J, Orkin SH, Hill DE, van den Heuvel S, Vidal M (2004) Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14, 2162-2168.
46. Rupert PB, Daughdrill GW, Bowerman B, Matthews BW (1998) The binding domain of Skn-1 in complex with DNA: a new DNA-binding motif. Nat. Struct. Biol. 5, 484-491.
47. Samuelson AV, Carr CE, Ruvkun G (2007) Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Genes Dev. 21, 2976-2994.
48. Sarkadi B, Homolya L, Szakacs G, Varadi A (2006) Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol. Rev. 86, 1179-1236.
49. Schwarz EM, Antoshechkin I, Bastiani C, Bieri T, Blasiar D, Canaran P, Chan J, Chen N, Chen WJ, Davis P, Fiedler TJ, Girard L, Harris TW, Kenny EE, Kishore R, Lawson D, Lee R, Muller HM, Nakamura C, Ozersky P, Petcherski A, Rogers A, Spooner W, Tuli MA, Van Auken K, Wang D, Durbin R, Spieth J, Stein LD, Sternberg PW (2006) WormBase: better software, richer content. Nucleic Acids Res. 34, D475-D478.
50. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, Plasterk RH, Fire A (2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476.
51. Taubert S, Van Gilst MR, Hansen M, Yamamoto KR (2006) A Mediator subunit, MDT-15, integrates regulation of fatty acid metabolism by NHR-49-dependent and -independent pathways in C. elegans. Genes Dev. 20, 1137-1149.
52. Taubert S, Hansen M, Van Gilst MR, Cooper SB, Yamamoto KR (2008) The Mediator subunit MDT-15 confers metabolic adaptation to ingested material. PLoS Genet. 4, e1000021.
53. Thakur JK, Arthanari H, Yang F, Pan SJ, Fan X, Breger J, Frueh DP, Gulshan K, Li DK, Mylonakis E, Struhl K, Moye-Rowley WS, Cormack BP, Wagner G, Naar AM (2008) A nuclear receptor-like pathway regulating multidrug resistance in fungi. Nature 452, 604-609.
54. Thomas-Chollier M, Sand O, Turatsinze JV, Janky R, Defrance M, Vervisch E, Brohee S, van Helden J (2008) RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 36, W119-W127.
55. Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
56. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet. 2, e183.
57. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK (2008) Direct inhibition of the longevitypromoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132, 1025-1038.
58. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121.
59. Vatamaniuk OK, Bucher EA, Sundaram MV, Rea PA (2005) CeHMT-1, a putative phytochelatin transporter, is required for cadmium tolerance in Caenorhabditis elegans. J. Biol. Chem. 280, 23684-23690.
60. Walker AK, See R, Batchelder C, Kophengnavong T, Gronniger JT, Shi Y, Blackwell TK (2000) A conserved transcription motif suggesting functional parallels between C. elegans SKN-1 and Cap 'n' Collarrelated bZIP proteins. J. Biol. Chem. 275, 22166-22171.
61. 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.
62. Yang F, Vought BW, Satterlee JS, Walker AK, Jim Sun ZY, Watts JL, Debeaumont R, Mako Saito R, Hyberts SG, Yang S, Macol C, Iyer L, Tjian R, van den Heuvel S, Hart AC, Wagner G, Naar AM (2006) An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis. Nature 442, 700-704.
63. Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC (2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127, 747-757.
64. You YJ, Kim J, Raizen DM, Avery L (2008) Insulin, cGMP, and TGF-beta signals regulate food intake and quiescence in C. elegans: a model for satiety. Cell Metab. 7, 249-257.