Interplay of dFOXO and Two ETS-Family Transcription Factors Determines Lifespan in Drosophila melanogaster

PLoS Genetics

Volumn 10, Issue 9, 2014, Pages

  Alic, Nazif ^a   Giannakou, Maria E ^a,d   Papatheodorou, Irene ^a,b   Hoddinott, Matthew P ^a,c   Andrews, T Daniel ^b   Bolukbasi, Ekin ^a,c,e   Partridge, Linda ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e Biology and Environment   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; ODORANT BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AOP; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR PNT; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXO PROTEIN, DROSOPHILA; PROTEIN BINDING;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FAT BODY; FEMALE; GENE CONTROL; GENE INTERACTION; GENETIC CONSERVATION; LIFESPAN; LIPID METABOLISM; LONGEVITY; METABOLIC REGULATION; NONHUMAN; ORTHOLOGY; PROTEIN BINDING; PROTEIN SECRETION; TRANSCRIPTION REGULATION; ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; LIFE EXPECTANCY; METABOLISM; PHYSIOLOGY;

ANIMALS; BINDING SITES; CLUSTER ANALYSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FAT BODY; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LIFE EXPECTANCY; LIPID METABOLISM; ORGAN SPECIFICITY; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84907587680     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004619     Document Type: Article

References (87)

1. Giannakou ME, Goss M, Junger MA, Hafen E, Leevers SJ, et al. (2004) Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305: 361.
2. Hwangbo DS, Gershman B, Tu MP, Palmer M, Tatar M, (2004) Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429: 562–566.
3. Demontis F, Perrimon N, (2010) FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 143: 813–825.
4. Alic N, Tullet J, Niccoli T, Broughton S, Hoddinott MP, et al. (2014) Cell-nonautonomous effects of dFOXO/DAF-16 in ageing. Cell Rep 6: 608–616.
5. 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.
6. Slack C, Giannakou ME, Foley A, Goss M, Partridge L, (2011) dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10: 735–748.
7. Postnikoff SD, Malo ME, Wong B, Harkness TA, (2012) The yeast forkhead transcription factors fkh1 and fkh2 regulate lifespan and stress response together with the anaphase-promoting complex. PLoS Genet 8: e1002583.
8. Kuningas M, Magi R, Westendorp RG, Slagboom PE, Remm M, et al. (2007) Haplotypes in the human Foxo1a and Foxo3a genes; impact on disease and mortality at old age. Eur J Hum Genet 15: 294–301.
9. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, et al. (2008) FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A 105: 13987–13992.
10. Flachsbart F, Caliebe A, Kleindorp R, Blanche H, von Eller-Eberstein H, et al. (2009) Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc Natl Acad Sci U S A 106: 2700–2705.
11. Anselmi CV, Malovini A, Roncarati R, Novelli V, Villa F, et al. (2009) Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study. Rejuvenation Res 12: 95–104.
12. Pawlikowska L, Hu D, Huntsman S, Sung A, Chu C, et al. (2009) Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 8: 460–472.
13. Eijkelenboom A, Burgering BM, (2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14: 83–97.
14. 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: 277–283.
15. McElwee JJ, Schuster E, Blanc E, Piper MD, Thomas JH, et al. (2007) Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol 8: R132.
16. 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.
17. Alic N, Andrews TD, Giannakou ME, Papatheodorou I, Slack C, et al. (2011) Genome-wide dFOXO targets and topology of the transcriptomic response to stress and insulin signalling. Mol Syst Biol 7: 502.
18. Bai H, Ping K, Hernandez AM, Tatar M, (2013) Activin Signaling Targeted by Insulin/dFOXO Regulates Aging and Muscle Proteostasis in Drosophila. PLoS Genet 9 (11) e1003941.
19. Webb AE, Pollina EA, Vierbuchen T, Urban N, Ucar D, et al. (2013) FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep 4: 477–491.
20. Eijkelenboom A, Mokry M, de Wit E, Smits LM, Polderman PE, et al. (2013) Genome-wide analysis of FOXO3 mediated transcription regulation through RNA polymerase II profiling. Mol Syst Biol 9: 638.
21. Puig O, Tjian R, (2005) Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev 19: 2435–2446.
22. van der Vos KE, Coffer PJ, (2008) FOXO-binding partners: it takes two to tango. Oncogene 27: 2289–2299.
23. Bouchard C, Marquardt J, Bras A, Medema RH, Eilers M, (2004) Myc-induced proliferation and transformation require Akt-mediated phosphorylation of FoxO proteins. EMBO J 23: 2830–2840.
24. Nemoto S, Fergusson MM, Finkel T, (2004) Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science 306: 2105–2108.
25. 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.
26. Seoane J, Le HV, Shen L, Anderson SA, Massague J, (2004) Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 117: 211–223.
27. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, et al. (2005) Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181–1184.
28. Teleman AA, Hietakangas V, Sayadian AC, Cohen SM, (2008) Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7: 21–32.
29. Paik JH, Kollipara R, Chu G, Ji H, Xiao Y, et al. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128: 309–323.
30. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, et al. (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325–339.
31. Poirier L, Shane A, Zheng J, Seroude L, (2008) Characterization of the Drosophila gene-switch system in aging studies: a cautionary tale. Aging Cell 7: 758–770.
32. Giannakou ME, Goss M, Jacobson J, Vinti G, Leevers SJ, et al. (2007) Dynamics of the action of dFOXO on adult mortality in Drosophila. Aging Cell 6: 429–438.
33. Giannakou ME, Goss M, Partridge L, (2008) Role of dFOXO in lifespan extension by dietary restriction in Drosophila melanogaster: not required, but its activity modulates the response. Aging Cell 7: 187–198.
34. Min KJ, Yamamoto R, Buch S, Pankratz M, Tatar M, (2008) Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7: 199–206.
35. Libina N, Berman JR, Kenyon C, (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489–502.
36. Bluher M, Kahn BB, Kahn CR, (2003) Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 299: 572–574.
37. Puig O, Marr MT, Ruhf ML, Tjian R, (2003) Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17: 2006–2020.
38. Junger MA, Rintelen F, Stocker H, Wasserman JD, Vegh M, et al. (2003) The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2: 20.
39. Karpac J, Biteau B, Jasper H, (2013) Misregulation of an adaptive metabolic response contributes to the age-related disruption of lipid homeostasis in Drosophila. Cell Rep 4: 1250–1261.
40. Breslin T, Eden P, Krogh M, (2004) Comparing functional annotation analyses with Catmap. BMC Bioinformatics 5: 193.
41. Bahadorani S, Cho J, Lo T, Contreras H, Lawal HO, et al. (2010) Neuronal expression of a single-subunit yeast NADH-ubiquinone oxidoreductase (Ndi1) extends Drosophila lifespan. Aging Cell 9: 191–202.
42. Sanz A, Soikkeli M, Portero-Otin M, Wilson A, Kemppainen E, et al. (2010) Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc Natl Acad Sci U S A 107: 9105–9110.
43. Casas-Tinto S, Marr MT, 2ndAndreu P, Puig O, (2007) Characterization of the Drosophila insulin receptor promoter. Biochim Biophys Acta 1769: 236–243.
44. Roukens MG, Alloul-Ramdhani M, Moghadasi S, Op den Brouw M, Baker DA, (2008) Downregulation of vertebrate Tel (ETV6) and Drosophila Yan is facilitated by an evolutionarily conserved mechanism of F-box-mediated ubiquitination. Mol Cell Biol 28: 4394–4406.
45. Roukens MG, Alloul-Ramdhani M, Baan B, Kobayashi K, Peterson-Maduro J, et al. (2010) Control of endothelial sprouting by a Tel-CtBP complex. Nat Cell Biol 12: 933–942.
46. Hock H, Meade E, Medeiros S, Schindler JW, Valk PJ, et al. (2004) Tel/Etv6 is an essential and selective regulator of adult hematopoietic stem cell survival. Genes Dev 18: 2336–2341.
47. Lai ZC, Rubin GM, (1992) Negative control of photoreceptor development in Drosophila by the product of the yan gene, an ETS domain protein. Cell 70: 609–620.
48. Rebay I, Rubin GM, (1995) Yan functions as a general inhibitor of differentiation and is negatively regulated by activation of the Ras1/MAPK pathway. Cell 81: 857–866.
49. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407.
50. Cox DR, (1972) Regression models and life-tables. J R Stat Soc Ser B Stat Methodol 34: 187–220.
51. O'Neill EM, Rebay I, Tjian R, Rubin GM, (1994) The activities of two Ets-related transcription factors required for Drosophila eye development are modulated by the Ras/MAPK pathway. Cell 78: 137–147.
52. Brunner D, Ducker K, Oellers N, Hafen E, Scholz H, et al. (1994) The ETS domain protein pointed-P2 is a target of MAP kinase in the sevenless signal transduction pathway. Nature 370: 386–389.
53. Halfon MS, Carmena A, Gisselbrecht S, Sackerson CM, Jimenez F, et al. (2000) Ras pathway specificity is determined by the integration of multiple signal-activated and tissue-restricted transcription factors. Cell 103: 63–74.
54. Rera M, Bahadorani S, Cho J, Koehler CL, Ulgherait M, et al. (2011) Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab 14: 623–634.
55. Buchon N, Osman D, David FP, Fang HY, Boquete JP, et al. (2013) Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep 3: 1725–1738.
56. Marianes A, Spradling AC, (2013) Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2: e00886.
57. Negre N, Brown CD, Ma L, Bristow CA, Miller SW, et al. (2011) A cis-regulatory map of the Drosophila genome. Nature 471: 527–531.
58. Webber JL, Zhang J, Cote L, Vivekanand P, Ni X, et al. (2013) The relationship between long-range chromatin occupancy and polymerization of the Drosophila ETS family transcriptional repressor Yan. Genetics 193: 633–649.
59. Rera M, Clark RI, Walker DW, (2012) Intestinal barrier dysfunction links metabolic and inflammatory markers of aging to death in Drosophila. Proc Natl Acad Sci U S A 109: 21528–21533.
60. Zhang W, Thompson BJ, Hietakangas V, Cohen SM, (2011) MAPK/ERK signaling regulates insulin sensitivity to control glucose metabolism in Drosophila. PLoS Genet 7: e1002429.
61. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857–868.
62. Rothemund S, Liou YC, Davies PL, Krause E, Sonnichsen FD, (1999) A new class of hexahelical insect proteins revealed as putative carriers of small hydrophobic ligands. Structure 7: 1325–1332.
63. Graham LA, Davies PL, (2002) The odorant-binding proteins of Drosophila melanogaster: annotation and characterization of a divergent gene family. Gene 292: 43–55.
64. Gronke S, Clarke D-F, Broughton S, Andrews TD, Partridge L, (2010) Molecular evolution and functional characterisation of Drosophila insulin-like peptides. PLoS Genet 6: e1000857.
65. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci U S A 102: 3105–3110.
66. Lemmon MA, Schlessinger J, (2010) Cell signaling by receptor tyrosine kinases. Cell 141: 1117–1134.
67. Rogge R, Green PJ, Urano J, Horn-Saban S, Mlodzik M, et al. (1995) The role of yan in mediating the choice between cell division and differentiation. Development 121: 3947–3958.
68. Fontana L, Partridge L, Longo VD, (2010) Extending healthy life span–from yeast to humans. Science 328: 321–326.
69. Gudbjartsson DF, Walters GB, Thorleifsson G, Stefansson H, Halldorsson BV, et al. (2008) Many sequence variants affecting diversity of adult human height. Nat Genet 40: 609–615.
70. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, et al. (2010) Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467: 832–838.
71. Fujii S, Amrein H, (2002) Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J 21: 5353–5363.
72. Roignant JY, Carre C, Mugat B, Szymczak D, Lepesant JA, et al. (2003) Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9: 299–308.
73. Bass TM, Grandison RC, Wong R, Martinez P, Partridge L, et al. (2007) Optimization of dietary restriction protocols in Drosophila. J Gerontol A Biol Sci Med Sci 62: 1071–1081.
74. Alic N, Hoddinott MP, Vinti G, Partridge L, (2011) Lifespan extension by increased expression of the Drosophila homologue of the IGFBP7 tumour suppressor. Aging Cell 10: 137–147.
75. Broughton S, Alic N, Slack C, Bass T, Ikeya T, et al. (2008) Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS One 3: e3721.
76. Choksi SP, Southall TD, Bossing T, Edoff K, de Wit E, et al. (2006) Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell 11: 775–789.
77. Smyth GK, Speed T, (2003) Normalization of cDNA microarray data. Methods 31: 265–273.
78. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
79. Toedling J, Skylar O, Krueger T, Fischer JJ, Sperling S, et al. (2007) Ringo–an R/Bioconductor package for analyzing ChIP-chip readouts. BMC Bioinformatics 8: 221.
80. Zacher B, Kuan PF, Tresch A, (2010) Starr: Simple Tiling ARRay analysis of Affymetrix ChIP-chip data. BMC Bioinformatics 11: 194.
81. Bickel P, Boley N, Brown J, Huang H, Zhang N, (2010) Subsampling Methods for Genomic Inference. Ann Appl Stat 4: 1660–1697.
82. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–193.
83. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
84. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249–264.
85. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Stat Methodol 57: 289–300.
86. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.
87. Mussel C, Hopfensitz M, Kestler HA, (2010) BoolNet–an R package for generation, reconstruction and analysis of Boolean networks. Bioinformatics 26: 1378–1380.