A role for SKN-1/Nrf in pathogen resistance and immunosenescence in caenorhabditis elegans

PLoS Pathogens

Volumn 8, Issue 4, 2012, Pages

  Papp, Diána ^a,b   Csermely, Péter ^a   Soti, Csaba ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; HYDROGEN PEROXIDE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE P38; SOMATOMEDIN; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; TRANSCRIPTION FACTOR SKN 1; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; SKN 1 PROTEIN, C ELEGANS; SKN-1 PROTEIN, C ELEGANS; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL IMMUNITY; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; GENE ACTIVATION; GENE TARGETING; GENETIC TRANSCRIPTION; IMMUNOREGULATION; INNATE IMMUNITY; INTESTINE CELL; LONGEVITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA; RNA INTERFERENCE; SENESCENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; XENOBIOTIC STRESS; AGING; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM;

CAENORHABDITIS ELEGANS; ENTEROCOCCUS FAECALIS; NEGIBACTERIA; POSIBACTERIA; PSEUDOMONAS AERUGINOSA;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA-BINDING PROTEINS; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PSEUDOMONAS AERUGINOSA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84861215311     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002673     Document Type: Article

References (53)

1. Bolm M, Jansen WT, Schnabel R, Chhatwal GS, (2004) Hydrogen peroxide-mediated killing of Caenorhabditis elegans: a common feature of different streptococcal species. Infect Immun 72: 1192-1194.
2. Jansen WT, Bolm M, Balling R, Chhatwal GS, Schnabel R, (2002) Hydrogen peroxide-mediated killing of Caenorhabditis elegans by Streptococcus pyogenes. Infect Immun 70: 5202-5207.
3. Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM, (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96: 47-56.
4. Chavez V, Mohri-Shiomi A, Garsin DA, (2009) Ce-Duox1/BLI-3 generates reactive oxygen species as a protective innate immune mechanism in Caenorhabditis elegans. Infect Immun 77: 4983-4989.
5. Mohri-Shiomi A, Garsin DA, (2008) Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J Biol Chem 283: 194-201.
6. Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, et al. (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300: 1921.
7. Singh V, Aballay A, (2006) Heat-shock transcription factor (HSF)-1 pathway required for Caenorhabditis elegans immunity. Proc Natl Acad Sci U S A 103: 13092-13097.
8. Richardson CE, Kooistra T, Kim DH, (2010) An essential role for XBP-1 in host protection against immune activation in C. elegans. Nature 463: 1092-1095.
9. Chavez V, Mohri-Shiomi A, Maadani A, Vega LA, Garsin DA, (2007) Oxidative stress enzymes are required for DAF-16-mediated immunity due to generation of reactive oxygen species by Caenorhabditis elegans. Genetics 176: 1567-1577.
10. Singh V, Aballay A, (2009) Regulation of DAF-16-mediated Innate Immunity in Caenorhabditis elegans. J Biol Chem 284: 35580-35587.
11. Kim DH, Feinbaum R, Alloing G, Emerson FE, Garsin DA, et al. (2002) A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297: 623-626.
12. Dong C, Davis RJ, Flavell RA, (2002) MAP kinases in the immune response. Annu Rev Immunol 20: 55-72.
13. Schulenburg H, Hoeppner MP, Weiner J 3rd, Bornberg-Bauer E, (2008) Specificity of the innate immune system and diversity of C-type lectin domain (CTLD) proteins in the nematode Caenorhabditis elegans. Immunobiology 213: 237-250.
14. Alper S, McBride SJ, Lackford B, Freedman JH, Schwartz DA, (2007) Specificity and complexity of the Caenorhabditis elegans innate immune response. Mol Cell Biol 27: 5544-5553.
15. 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.
16. 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.
17. Bishop NA, Guarente L, (2007) Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature 447: 545-549.
18. 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.
19. 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.
20. 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.
21. Hoeven R, McCallum KC, Cruz MR, Garsin DA, (2011) Ce-Duox1/BLI-3 generated reactive oxygen species trigger protective SKN-1 activity via p38 MAPK signaling during infection in C. elegans. PLoS Pathog 7: e1002453.
22. Shapira M, Hamlin BJ, Rong J, Chen K, Ronen M, et al. (2006) A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc Natl Acad Sci U S A 103: 14086-14091.
23. Kim DH, Liberati NT, Mizuno T, Inoue H, Hisamoto N, et al. (2004) Integration of Caenorhabditis elegans MAPK pathways mediating immunity and stress resistance by MEK-1 MAPK kinase and VHP-1 MAPK phosphatase. Proc Natl Acad Sci U S A 101: 10990-10994.
24. Liberati NT, Fitzgerald KA, Kim DH, Feinbaum R, Golenbock DT, et al. (2004) Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc Natl Acad Sci U S A 101: 6593-6598.
25. Couillault C, Pujol N, Reboul J, Sabatier L, Guichou JF, et al. (2004) TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat Immunol 5: 488-494.
26. Laws TR, Harding SV, Smith MP, Atkins TP, Titball RW, (2004) Age influences resistance of Caenorhabditis elegans to killing by pathogenic bacteria. FEMS Microbiol Lett 234: 281-287.
27. Youngman MJ, Rogers ZN, Kim DH, (2011) A decline in p38 MAPK signaling underlies immunosenescence in Caenorhabditis elegans. PLoS Genet 7: e1002082.
28. Tan MW, Mahajan-Miklos S, Ausubel FM, (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96: 715-720.
29. Oliveira RP, Porter Abate J, Dilks K, Landis J, Ashraf J, et al. (2009) Condition-adapted stress and longevity gene regulation by Caenorhabditis elegans SKN-1/Nrf. Aging Cell 8: 524-541.
30. Park SK, Tedesco PM, Johnson TE, (2009) Oxidative stress and longevity in Caenorhabditis elegans as mediated by SKN-1. Aging Cell 8: 258-269.
31. Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, et al. (2012) WormBase 2012: more genomes, more data, new website. Nucleic Acids Res 40: D735-741.
32. Cypser JR, Johnson TE, (2002) Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J Gerontol A Biol Sci Med Sci 57: B109-114.
33. Talalay P, Dinkova-Kostova AT, Holtzclaw WD, (2003) Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv Enzyme Regul 43: 121-134.
34. An JH, Blackwell TK, (2003) SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 17: 1882-1893.
35. Motohashi H, Yamamoto M, (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549-557.
36. Kim J, Cha YN, Surh YJ, (2010) A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res 690: 12-23.
37. Nagai N, Thimmulappa RK, Cano M, Fujihara M, Izumi-Nagai K, et al. (2009) Nrf2 is a critical modulator of the innate immune response in a model of uveitis. Free Radic Biol Med 47: 300-306.
38. Harvey CJ, Thimmulappa RK, Sethi S, Kong X, Yarmus L, et al. (2011) Targeting Nrf2 signaling improves bacterial clearance by alveolar macrophages in patients with COPD and in a mouse model. Sci Transl Med 3: 78ra32.
39. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, et al. (2006) Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 116: 984-995.
40. Shivers RP, Pagano DJ, Kooistra T, Richardson CE, Reddy KC, et al. (2010) Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet 6: e1000892.
41. Evans EA, Kawli T, Tan MW, (2008) Pseudomonas aeruginosa suppresses host immunity by activating the DAF-2 insulin-like signaling pathway in Caenorhabditis elegans. PLoS Pathog 4: e1000175.
42. Ono K, Han J, (2000) The p38 signal transduction pathway: activation and function. Cell Signal 12: 1-13.
43. Carty M, Goodbody R, Schroder M, Stack J, Moynagh PN, et al. (2006) The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat Immunol 7: 1074-1081.
44. Aw D, Silva AB, Palmer DB, (2007) Immunosenescence: emerging challenges for an ageing population. Immunology 120: 435-446.
45. Alper S, (2010) Model systems to the rescue: The relationship between aging and innate immunity. Commun Integr Biol 3: 409-414.
46. Kirkwood TB, (2008) Understanding ageing from an evolutionary perspective. J Intern Med 263: 117-127.
47. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R, (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366: 461-464.
48. Singh V, Aballay A, (2006) Heat shock and genetic activation of HSF-1 enhance immunity to bacteria. Cell Cycle 5: 2443-2446.
49. Schuster E, McElwee JJ, Tullet JM, Doonan R, Matthijssens F, et al. (2010) DamID in C. elegans reveals longevity-associated targets of DAF-16/FoxO. Mol Syst Biol 6: 399.
50. Ewbank JJ, Zugasti O, (2011) C. elegans: model host and tool for antimicrobial drug discovery. Dis Model Mech 4: 300-304.
51. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
52. Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, et al. (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98: 10892-10897.
53. Powell JR, Ausubel FM, (2008) Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Meth Mol Biol 415: 403-427.