RNAi screen of DAF-16/FOXO target genes in C. Elegans links pathogenesis and dauer formation

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Jensen, Victor L ^a,b   Simonsen, Karina T ^c   Lee, Yu Hui ^b   Park, Donha ^a   Riddle, Donald L ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; CAENORHABDITIS ELEGANS PROTEIN; DAF 16 PROTEIN, C ELEGANS; DAF 7 PROTEIN, C ELEGANS; DAF-16 PROTEIN, C ELEGANS; DAF-7 PROTEIN, C ELEGANS; GREEN FLUORESCENT PROTEIN; INSULIN; SOMATOMEDIN C RECEPTOR; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; CELL ADHESION; CONTROLLED STUDY; EPITHELIUM CELL; GENE FUNCTION; GENE SYNTHESIS; GENE TARGETING; GENETIC SCREENING; INNATE IMMUNITY; MOLECULAR CLONING; NONHUMAN; RNA INTERFERENCE; STAPHYLOCOCCUS AUREUS; SYNDAF GENE; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; GENETICS; LARVA; METABOLISM; PHENOTYPE; PHYSIOLOGY; SECRETION;

CAENORHABDITIS ELEGANS; STAPHYLOCOCCUS AUREUS;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENETIC TESTING; GREEN FLUORESCENT PROTEINS; IMMUNITY, INNATE; INSULIN; LARVA; MODELS, GENETIC; PHENOTYPE; RECEPTOR, IGF TYPE 1; RNA INTERFERENCE; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 79251488788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015902     Document Type: Article

References (71)

1. Cassada RC, Russell RL (1975) The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46: 326-42.
2. Riddle DL, Swanson MM, Albert PS (1981) Interacting genes in nematode dauer larva formation. Nature 290: 668-671.
3. Tewari M, Hu PJ, Ahn JS, Ayivi-Guedehoussou N, Vidalain PO, et al. (2004) Systematic interactome mapping and genetic perturbation analysis of a C. elegans TGF-beta signaling network. Mol Cell 13: 469-82.
4. Hu PJ, Xu J, Ruvkun G (2006) Two membrane-associated tyrosine phosphatase homologs potentiate C. elegans AKT-1/PKB signaling. PLoS Genet 2: e99.
5. Liu T, Zimmerman KK, Patterson GI (2004) Regulation of signaling genes by TGFbeta during entry into dauer diapause in C. elegans. BMC Dev Biol 4: 11.
6. Jensen VL, Gallo M, Riddle DL (2006) Targets of DAF-16 involved in Caenorhabditis elegans adult longevity and dauer formation. Exp Gerontol 41: 922-927.
7. Patterson GI, Koweek A, Wong A, Liu Y, Ruvkun G (1997) The DAF-3 Smad protein antagonizes TGF-beta-related receptor signaling in the Caenorhabditis elegans dauer pathway. Gene Dev 11: 2679-2690.
8. 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. doi:10.1038/40194.
9. Antebi A, Yeh WH, Tait D, Hedgecock EM, Riddle DL (2000) Daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Gene Dev 14: 1512-1527.
10. Thomas JH, Birnby DA, Vowels JJ (1993) Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 134: 1105-17.
11. Ailion M, Thomas JH (2003) Isolation and characterization of hightemperature-induced dauer formation mutants in Caenorhabditis elegans. Genetics 165: 127-44.
12. Speese S, Petrie M, Schuske K, Ailion M, Ann K, et al. (2007) UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans. J Neurosci 27: 6150-62.
13. Ailion M, Inoue T, Weaver CI, Holdcraft RW, Thomas JH (1999) Neurosecretory control of aging in Caenorhabditis elegans. Proc Natl Acad Sci 96: 7394-7.
14. Alcedo J, Kenyon C (2004) Regulation of C. elegans longevity by specific gustatory and olfactory neurons. Neuron 41: 45-55.
15. Golden JW, Riddle DL (1984) The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Dev Biol 102: 368-78.
16. Bell LR, Stone S, Yochem J, Shaw JE, Herman RK (2006) The molecular identities of the Caenorhabditis elegans intraflagellar transport genes dyf-6, daf-10 and osm-1. Genetics 173: 1275-86.
17. Swoboda P, Adler HT, Thomas JH (2000) The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 5: 411-21.
18. Kennedy S, Wang D, Ruvkun G (2004) A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427: 645-9.
19. Ohkura K, Suzuki N, Ishihara T, Katsura I (2003) SDF-9, a protein tyrosine phosphatase-like molecule, regulates the L3/dauer developmental decision through hormonal signaling in C. elegans. Development 130: 3237-48.
20. Jensen VL, Albert PS, Riddle DL (2007) Caenorhabditis elegans SDF-9 enhances insulin/insulin-like signaling through interaction with DAF-2. Genetics 177: 661-6.
21. 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.
22. 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.
23. McElwee J, Bubb K, Thomas JH (2003) Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2: 111-21.
24. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, et al. (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424: 277-83.
25. 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. Gene Dev 12: 2488-2498.
26. Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, et al. (2006) Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 38: 251-7.
27. Bork P, Beckmann G (1993) The CUB domain. A widespread module in developmentally regulated proteins. J Mol Biol 231: 539-545. doi:10.1006/jmbi.1993.1305.
28. Thomas JH (2006) Analysis of homologous gene clusters in Caenorhabditis elegans reveals striking regional cluster domains. Genetics 172: 127-43.
29. Shivers RP, Youngman MJ, Kim DH (2008) Transcriptional responses to pathogens in Caenorhabditis elegans. Curr Opin Microbiol 11: 251-6.
30. Nandakumar M, Tan MW (2008) Gamma-linolenic and stearidonic acids are required for basal immunity in Caenorhabditis elegans through their effects on p38 MAP kinase activity. PLoS genet 4: e1000273.
31. Lee SS, Kennedy S, Tolonen AC, Ruvkun G (2003) DAF-16 target genes that control C. elegans life-span and metabolism. Science 300: 644-7.
32. Robertson HM (2000) The large srh family of chemoreceptor genes in Caenorhabditis nematodes reveals processes of genome evolution involving largeduplications and deletions and intron gains and losses. Genome Res 10: 192-203.
33. Davalli AM, Biancardi E, Pollo A, Socci C, Pontiroli AE, et al. (1996) Dihydropyridine-sensitive and -insensitive voltage-operated calcium channels participate in the control of glucose-induced insulin release from human pancreatic beta cells. J Endocrinol 150: 195-203.
34. Suzuki Y, Han M (2006) Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Gene Dev 20: 423-8.
35. Shostak Y, Van Gilst MR, Antebi A, Yamamoto KR (2004) Identification of C. elegans DAF-12-binding sites, response elements, and target genes. Gene Dev 18: 2529-44.
36. Pinkston-Gosse J, Kenyon C (2007) DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 39: 1403-9.
37. Rogers A, Antoshechkin I, Bieri T, Blasiar D, Bastiani C, et al. (2008) WormBase 2007. Nucleic Acids Res 36: D612-7.
38. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, et al. (2006) P38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2: e183.
39. 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 103: 14086-91.
40. Bolz DD, Tenor JL, Aballay A (2010) A conserved PMK-1/p38 MAPK is required in Caenorhabditis elegans tissue-specific immune response to Yersinia pestis infection. J Biol Chem 285: 10832-10840. doi:10.1074/jbc.M109.091629.
41. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol 12: 1317-9.
42. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, et al. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12: 1209-14.
43. Asano A, Asano K, Sasaki H, Furuse M, Tsukita S (2003) Claudins in Caenorhabditis elegans: their distribution and barrier function in the epithelium. Curr Biol 13: 1042-6.
44. 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 96: 715-20.
45. Couillault C, Ewbank JJ (2002) Diverse bacteria are pathogens of Caenorhabditis elegans. Infect Immun 70: 4705-7.
46. Sifri CD, Begun J, Ausubel FM, Calderwood SB (2003) Caenorhabditis elegans as a Model Host for Staphylococcus aureus Pathogenesis. Infect Immun 71: 2208-2217. doi:10.1128/IAI.71.4.2208-2217.2003.
47. Zhang Y, Lu H, Bargmann CI (2005) Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438: 179-184. doi:10.1038/nature04216.
48. Perens EA, Shaham S (2005) C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev Cell 8: 893-906. doi:10.1016/j.devcel.2005.03.009.
49. Albert PS, Brown SJ, Riddle DL (1981) Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol 198: 435-451. doi:10.1002/cne.901980305.
50. Butcher RA, Ragains JR, Li W, Ruvkun G, Clardy J, et al. (2009) Biosynthesis of the Caenorhabditis elegans dauer pheromone. Proc Natl Acad Sci 106: 1875-1879. doi:10.1073/pnas.0810338106.
51. Golden JW, Riddle DL (1985) A gene affecting production of the Caenorhabditis elegans dauer-inducing pheromone. Mol Gen Genet 198: 534-536.
52. Ailion M, Thomas JH (2000) Dauer Formation Induced by High Temperatures in Caenorhabditis elegans. Genetics 156: 1047-1067.
53. Ren P, Lim C, Johnsen R, Albert PS, Pilgrim D, et al. (1996) Control of C. elegans Larval Development by Neuronal Expression of a TGF-beta Homolog. Science 274: 1389-1391. doi:10.1126/science.274.5291.1389.
54. Narbonne P, Roy R (2006) Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133: 611-9.
55. Sonnichsen B, Koski LB, Walsh A, Marschall P, Neumann B, et al. (2005) Fullgenome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434: 462-9.
56. Wong D, Bazopoulou D, Pujol N, Tavernarakis N, Ewbank JJ (2007) Genomewide investigation reveals pathogen-specific and shared signatures in the response of Caenorhabditis elegans to infection. Genome Biol 8: R194.
57. Darby C (2005) Interactions with microbial pathogens. WormBook. pp 1-15.
58. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, et al. (2002) Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161: 1101-12.
59. Ren M, Feng H, Fu Y, Land M, Rubin CS (2009) Protein Kinase D Is an Essential Regulator of C. elegans Innate Immunity. Immunity 30: 521-532. doi:10.1016/j.immuni.2009.03.007.
60. Larsen PL, Albert PS, Riddle DL (1995) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139: 1567-83.
61. 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. doi:10.1038/366461a0.
62. Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, et al. (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454: 1115-1118. doi:10.1038/nature07168.
63. Matsuura T, Sato T, Shingai R (2005) Interactions between Caenorhabditis elegans Individuals during Chemotactic Response. Zool Sci 22: 1095-1103. doi:10.2108/zsj.22.1095.
64. Hu PJ (2007) Dauer. WormBook. pp 1-19. doi:10.1895/wormbook.1.144.1.
65. Pradel E, Zhang Y, Pujol N, Matsuyama T, Bargmann CI, et al. (2007) Detection and avoidance of a natural product from the pathogenic bacterium Serratia marcescens by Caenorhabditis elegans. Proc Natl Acad Sci 104: 2295-2300. doi:10.1073/pnas.0610281104.
66. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218: 384-387.
67. Kiesecker JM, Skelly DK, Beard KH, Preisser E (1999) Behavioral reduction of infection risk. Proc Natl Acad Sci 96: 9165-9168.
68. 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: 231-7.
69. Smedley D, Haider S, Ballester B, Holland R, London D, et al. (2009) BioMart-biological queries made easy. BMC Genomics 10: 22. doi:10.1186/1471-2164-10-22.
70. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
71. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.