WWP-1 is a novel modulator of the DAF-2 insulin-like signaling network involved in pore-forming toxin cellular defenses in Caenorhabditis elegans

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Chen, Chang Shi ^a   Bellier, Audrey ^b   Kao, Cheng Yuan ^b   Yang, Ya Luen ^a   Chen, Huan Da ^a   Los, Ferdinand C O ^b   Aroian, Raffi V ^b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; PORE FORMING CYTOTOXIC PROTEIN; PROTEIN; PROTEIN DAF 2; PROTEIN WWP 1; SOMATOMEDIN C; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; DAF 2 PROTEIN, C ELEGANS; DAF-2 PROTEIN, C ELEGANS; INSULIN; INSULIN RECEPTOR; UBIQUITIN PROTEIN LIGASE; VIRULENCE FACTOR; WWP1 PROTEIN, C ELEGANS;

ARTICLE; BACILLUS THURINGIENSIS; CAENORHABDITIS ELEGANS; CELLULAR IMMUNITY; CONTROLLED STUDY; INNATE IMMUNITY; LIFESPAN; NONHUMAN; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; AGING; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GRAM POSITIVE INFECTION; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY;

BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); CAENORHABDITIS ELEGANS; PSEUDOMONAS AERUGINOSA;

AGING; ANIMALS; BACILLUS THURINGIENSIS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE EXPRESSION REGULATION; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; INSULIN; MODELS, BIOLOGICAL; MUTATION; RECEPTOR, INSULIN; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; VIRULENCE FACTORS;

EID: 77949765104     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009494     Document Type: Article

References (47)

1. Alouf JE (2003) Molecular features of the cytolytic pore-forming bacterial protein toxins. Folia Microbiol (Praha) 48: 5-16.
2. Parker MW, Feil SC (2005) Pore-forming protein toxins: from structure to function. Prog Biophys Mol Biol 88: 91-142.
3. Iacovache I, van der Goot FG, Pernot L (2008) Pore formation: an ancient yet complex form of attack. Biochim Biophys Acta 1778: 1611-1623.
4. de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37: 409-433.
5. Bravo A, Gill SS, Soberon M (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon 49: 423-435.
6. Marroquin LD, Elyassnia D, Griffitts JS, Feitelson JS, Aroian RV (2000) Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155: 1693-1699.
7. Wei JZ, Hale K, Carta L, Platzer E, Wong C, et al. (2003) Bacillus thuringiensis crystal proteins that target nematodes. Proc Natl Acad Sci U S A 100: 2760-2765.
8. Cappello M, Bungiro RD, Harrison LM, Bischof LJ, Griffitts JS, et al. (2006) A purified Bacillus thuringiensis crystal protein with therapeutic activity against the hookworm parasite Ancylostoma ceylanicum. Proc Natl Acad Sci U S A 103: 15154-15159.
9. Huffman DL, Bischof LJ, Griffitts JS, Aroian RV (2004) Pore worms: using Caenorhabditis elegans to study how bacterial toxins interact with their target host. Int J Med Microbiol 293: 599-607.
10. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, et al. (2004) Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 101: 10995-11000.
11. Bischof LJ, Kao CY, Los FC, Gonzalez MR, Shen Z, et al. (2008) Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog 4: e1000176.
12. Bellier A, Chen CS, Kao CY, Cinar HN, Aroian RV (2009) Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans. PLoS Pathog 5: e1000689.
13. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65: 493-507.
14. Finch CE, Ruvkun G (2001) The genetics of aging. Annu Rev Genomics Hum Genet 2: 435-462.
15. Kenyon C (2005) The plasticity of aging: insights from long-lived mutants. Cell 120: 449-460.
16. Baumeister R, Schaffitzel E, Hertweck M (2006) Endocrine signaling in Caenorhabditis elegans controls stress response and longevity. J Endocrinol 190: 191-202.
17. 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.
18. Kurz CL, Tan MW (2004) Regulation of aging and innate immunity in C. elegans. Aging Cell 3: 185-193.
19. Bischof LJ, Huffman DL, Aroian RV (2006) Assays for toxicity studies in C. elegans with Bt crystal proteins. Methods Mol Biol 351: 139-154.
20. Lin K, Hsin H, Libina N, Kenyon C (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28: 139-145.
21. Kerry S, TeKippe M, Gaddis NC, Aballay A (2006) GATA transcription factor required for immunity to bacterial and fungal pathogens. PLoS One 1: e77.
22. 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.
23. Singh V, Aballay A (2009) Regulation of DAF-16-mediated Innate Immunity in Caenorhabditis elegans. J Biol Chem 284: 35580-35587.
24. Lin K, Dorman JB, Rodan A, Kenyon C (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319-1322.
25. Mukhopadhyay A, Tissenbaum HA (2007) Reproduction and longevity: secrets revealed by C. elegans. Trends Cell Biol 17: 65-71.
26. Evans EA, Chen WC, Tan MW (2008) The DAF-2 insulin-like signaling pathway independently regulates aging and immunity in C. elegans. Aging Cell 7: 879-893.
27. 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.
28. Li S, Armstrong CM, Bertin N, Ge H, Milstein S, et al. (2004) A map of the interactome network of the metazoan C. elegans. Science 303: 540-543.
29. Huang K, Johnson KD, Petcherski AG, Vandergon T, Mosser EA, et al. (2000) A HECT domain ubiquitin ligase closely related to the mammalian protein WWP1 is essential for Caenorhabditis elegans embryogenesis. Gene 252: 137-145.
30. Kagan RM, Clarke S (1995) Protein L-isoaspartyl methyltransferase from the nematode Caenorhabditis elegans: genomic structure and substrate specificity. Biochemistry 34: 10794-10806.
31. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237.
32. 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.
33. Carrano AC, Liu Z, Dillin A, Hunter T (2009) A conserved ubiquitination pathway determines longevity in response to diet restriction. Nature 460: 396-399.
34. 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.
35. Wiles TJ, Dhakal BK, Eto DS, Mulvey MA (2008) Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins. Mol Biol Cell 19: 1427-1438.
36. Hu PJ, Xu J, Ruvkun G (2006) Two membrane-associated tyrosine phosphatase homologs potentiate C. elegans AKT-1/PKB signaling. PLoS Genet 2: e99.
37. Zhang Y, Xu J, Puscau C, Kim Y, Wang X, et al. (2008) Caenorhabditis elegans EAK-3 inhibits dauer arrest via nonautonomous regulation of nuclear DAF-16/FoxO activity. Dev Biol 315: 290-302.
38. Gami MS, Iser WB, Hanselman KB, Wolkow CA (2006) Activated AKT/PKB signaling in C. elegans uncouples temporally distinct outputs of DAF-2/insulin-like signaling. BMC Dev Biol 6: 45.
39. Gomez TA, Banfield KL, Trogler DM, Clarke SG (2007) The L-isoaspartyl-O-methyltransferase in Caenorhabditis elegans larval longevity and autophagy. Dev Biol 303: 493-500.
40. Banfield KL, Gomez TA, Lee W, Clarke S, Larsen PL (2008) Protein-repair and hormone-signaling pathways specify dauer and adult longevity and dauer development in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 63: 798-808.
41. Mukhopadhyay A, Oh SW, Tissenbaum HA (2006) Worming pathways to and from DAF-16/FOXO. Exp Gerontol 41: 928-934.
42. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
43. Dillin A, Crawford DK, Kenyon C (2002) Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298: 830-834.
44. Bellier A, Chen CS, Kao CY, Cinar HN, Aroian RV (2009) Activation of the C. elegans hypoxic response confers protection against pore-forming toxins. PLoS Pathog, manuscript in press.
45. Zarse K, Schulz TJ, Birringer M, Ristow M (2007) Impaired respiration is positively correlated with decreased life span in Caenorhabditis elegans models of Friedreich Ataxia. FASEB J 21: 1271-1275.
46. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408-2413.
47. Finney DJ (1980) Probit analysis. Cambridge, England: Cambridge University Press xv, 333 p.