Genome-wide screening identifies new genes required for stress-induced phase 2 detoxification gene expression in animals

BMC Biology

Volumn 12, Issue 1, 2014, Pages

  Crook McMahon, Helen M ^a   Oláhová, Monika ^a   Button, Emma L ^a   Winter, Johnathan J ^a   Veal, Elizabeth A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

aging; arsenite; glutathione; Nrf2; p38; peroxiredoxin; signal transduction

Indexed keywords

ANIMALIA;

REACTIVE OXYGEN METABOLITE; XENOBIOTIC AGENT;

ANIMAL; CAENORHABDITIS ELEGANS; DRUG DETOXIFICATION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETICS; GENOME; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS;

ANIMALS; CAENORHABDITIS ELEGANS; GENE EXPRESSION REGULATION; GENOME, HELMINTH; GENOME-WIDE ASSOCIATION STUDY; METABOLIC DETOXICATION, PHASE II; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL; XENOBIOTICS;

EID: 84910077277     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/s12915-014-0064-6     Document Type: Article

References (35)

1. Liebler DC, Guengerich FP. Elucidating mechanisms of drug-induced toxicity. Nat Rev Drug Discov 2005, 4:410-420. 10.1038/nrd1720, 15864270.
2. Board PG, Menon D. Glutathione transferases, regulators of cellular metabolism and physiology. Biochim Biophys Acta 1830, 2013:3267-3288.
3. McElwee JJ, Schuster E, Blanc E, Piper MD, Thomas JH, Patel DS, Selman C, Withers DJ, Thornton JM, Partridge L, Gems D. Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol 2007, 8:R132. 10.1186/gb-2007-8-7-r132, 17612391.
4. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 2008, 132:1025-1038. 10.1016/j.cell.2008.01.030, 18358814.
5. Jaramillo MC, Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 2013, 27:2179-2191. 10.1101/gad.225680.113, 24142871.
6. Furfaro AL, Macay JR, Marengo B, Nitti M, Parodi A, Fenoglio D, Marinari UM, Pronzato MA, Domenicotti C, Traverso N. Resistance of neuroblastoma GI-ME-N cell line to glutathione depletion involves Nrf2 and heme oxygenase-1. Free Radic Biol Med 2012, 52:488-496. 10.1016/j.freeradbiomed.2011.11.007, 22142473.
7. Zhang DD. The Nrf2-Keap1-ARE signaling pathway: the regulation and dual function of Nrf2 in cancer. Antioxid Redox Signal 2010, 13:1623-1626. 10.1089/ars.2010.3301, 20486759.
8. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J, Murphy CT, Blackwell TK. Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 2009, 8:524-541. 10.1111/j.1474-9726.2009.00501.x, 19575768.
9. McMahon M, Lamont DJ, Beattie KA, Hayes JD. Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals. Proc Natl Acad Sci USA 2010, 107:18838-18843. 10.1073/pnas.1007387107, 20956331.
10. An JH, Blackwell TK. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 2003, 17:1882-1893. 10.1101/gad.1107803, 12869585.
11. Inoue H, Hisamoto N, An JH, Oliveira RP, Nishida E, Blackwell TK, Matsumoto K. The C. elegans p38 MAPK pathway regulates nuclear localization of the transcription factor SKN-1 in oxidative stress response. Genes Dev 2005, 19:2278-2283. 10.1101/gad.1324805, 16166371.
12. An JH, Vranas K, Lucke M, Inoue H, Hisamoto N, Matsumoto K, Blackwell TK. Regulation of the Caenorhabditis elegans oxidative stress defense protein SKN-1 by glycogen synthase kinase-3. Proc Natl Acad Sci USA 2005, 102:16275-16280. 10.1073/pnas.0508105102, 16251270.
13. Choe KP, Przybysz AJ, Strange K. 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 2009, 29:2704-2715. 10.1128/MCB.01811-08, 19273594.
14. Olahova M, Taylor SR, Khazaipoul S, Wang J, Morgan BA, Matsumoto K, Blackwell TK, Veal EA. A redox-sensitive peroxiredoxin that is important for longevity has tissue- and stress-specific roles in stress resistance. Proc Natl Acad Sci USA 2008, 105:19839-19844. 10.1073/pnas.0805507105, 19064914.
15. WormBase. []., www.wormbase.org
16. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, Fang L, Halfnight E, Lee D, Lin J, Lorch A, McKay S, Okada HM, Pan J, Schulz AK, Tu D, Wong K, Zhao Z, Alexeyenko A, Burglin T, Sonnhammer E, Schnabel R, Jones SJ, Marra MA, Baillie DL, Moerman DG. High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 2007, 5:e237. 10.1371/journal.pbio.0050237, 17850180.
17. Wang J, Robida-Stubbs S, Tullet JM, Rual JF, Vidal M, Blackwell TK. RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition. PLoS Genet 2010, 6:8.
18. van Haaften G, Romeijn R, Pothof J, Koole W, Mullenders LH, Pastink A, Plasterk RH, Tijsterman M. Identification of conserved pathways of DNA-damage response and radiation protection by genome-wide RNAi. Curr Biol 2006, 16:1344-1350. 10.1016/j.cub.2006.05.047, 16824923.
19. Samuelson AV, Carr CE, Ruvkun G. Gene activities that mediate increased life span of C. elegans insulin-like signaling mutants. Genes Dev 2007, 21:2976-2994. 10.1101/gad.1588907, 18006689.
20. Liao VH, Yu CW. Caenorhabditis elegans gcs-1 confers resistance to arsenic-induced oxidative stress. Biometals 2005, 18:519-528. 10.1007/s10534-005-2996-3, 16333752.
21. Leiers B, Kampkotter A, Grevelding CG, Link CD, Johnson TE, Henkle-Duhrsen K. A stress-responsive glutathione S-transferase confers resistance to oxidative stress in Caenorhabditis elegans. Free Radic Biol Med 2003, 34:1405-1415. 10.1016/S0891-5849(03)00102-3, 12757851.
22. Simmer F, Moorman C, van der Linden AM, Kuijk E, van den Berghe PV, Kamath RS, Fraser AG, Ahringer J, Plasterk RH. Genome-wide RNAi of C. elegans using the hypersensitive rrf-3 strain reveals novel gene functions. PLoS Biol 2003, 1:E12. 10.1371/journal.pbio.0000012, 14551910.
23. Merlet J, Burger J, Gomes JE, Pintard L. Regulation of cullin-RING E3 ubiquitin-ligases by neddylation and dimerization. Cell Mol Life Sci 2009, 66:1924-1938. 10.1007/s00018-009-8712-7, 19194658.
24. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, Inoue H, Tanaka-Hino M, Hisamoto N, Matsumoto K, Tan MW, Ausubel FM. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002, 297:623-626. 10.1126/science.1073759, 12142542.
25. Liberati NT, Fitzgerald KA, Kim DH, Feinbaum R, Golenbock DT, Ausubel FM. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc Natl Acad Sci USA 2004, 101:6593-6598. 10.1073/pnas.0308625101, 15123841.
26. Leung CK, Hasegawa K, Wang Y, Deonarine A, Tang L, Miwa J, Choe KP. A direct interaction between the WD40 repeat protein WDR-23 and SKN-1/Nrf inhibits binding to target DNA. Mol Cell Biol 2014, 34:3156-3167. 10.1128/MCB.00114-14, 24912676.
27. Chen D, Wilkinson CR, Watt S, Penkett CJ, Toone WM, Jones N, Bahler J. Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol Biol Cell 2008, 19:308-317. 10.1091/mbc.E07-08-0735, 18003976.
28. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 2003, 35:238-245. 10.1038/ng1248, 14517554.
29. van der Hoeven R, McCallum KC, Cruz MR, Garsin DA. Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog 2011, 7:e1002453. 10.1371/journal.ppat.1002453, 22216003.
30. Papp D, Csermely P, Soti C. A role for SKN-1/Nrf in pathogen resistance and immunosenescence in Caenorhabditis elegans. PLoS Pathog 2012, 8:e1002673. 10.1371/journal.ppat.1002673, 22577361.
31. Nystrom T, Yang J, Molin M. Peroxiredoxins, gerontogenes linking aging to genome instability and cancer. Genes Dev 2012, 26:2001-2008. 10.1101/gad.200006.112, 22987634.
32. Wu H, Pomeroy SL, Ferreira M, Teider N, Mariani J, Nakayama KI, Hatakeyama S, Tron VA, Saltibus LF, Spyracopoulos L, Leng RP. UBE4B promotes Hdm2-mediated degradation of the tumor suppressor p53. Nat Med 2011, 17:347-355. 10.1038/nm.2283, 21317885.
33. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94. 4366476.
34. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237. 10.1038/nature01278, 12529635.
35. Stat Trek. []., http://stattrek.com/Tables/Hypergeometric.aspx