DAF-16 target identification in C. elegans: past, present and future

Biogerontology

Volumn 16, Issue 2, 2015, Pages 221-234

  Tullet, Jennifer M A ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF KENT   (United Kingdom)

Author keywords

Ageing; C. elegans; DAF 16; Insulin IGF 1 like signalling; mRNA profiling; Proteomics

Indexed keywords

INSULIN; MESSENGER RNA; PROTEOME; SOMATOMEDIN C; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTOME; CAENORHABDITIS ELEGANS PROTEIN; DAF-16 PROTEIN, C ELEGANS; FORKHEAD TRANSCRIPTION FACTOR;

AGING; CAENORHABDITIS ELEGANS; FUNCTIONAL GENOMICS; GENE CONTROL; LIFESPAN; LONGEVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; ANIMAL; METABOLISM; PHYSIOLOGY;

AGING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; INSULIN; INSULIN-LIKE GROWTH FACTOR I;

EID: 84925081605     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-014-9527-y     Document Type: Review

References (89)

1. Alic N, Tullet JM, Niccoli T, Broughton S, Hoddinott MP, Slack C, Gems D, Partridge L (2014) Cell-nonautonomous effects of dFOXO/DAF-16 in aging. Cell Rep 6(4):608–616
2. Anselmi CV, Malovini A, Roncarati R, Novelli V, Villa F, Condorelli G, Bellazzi R, Puca AA (2009) Association of the FOXO3A locus with extreme longevity in a southern Italian centenarian study. Rejuvenation Res 12:95–104
3. Apfeld J, O’Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18:3004–3009
4. Ayyadevara S, Alla R, Thaden JJ, Shmookler Reis RJ (2008) Remarkable longevity and stress resistance of nematode PI3K-null mutants. Aging Cell 7:13–22
5. Brignull HR, Moore FE, Tang SJ, Morimoto RI (2006) Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. J Neurosci 26:7597–7606
6. Budovskaya YV, Wu K, Southworth LK, Jiang M, Tedesco P, Johnson TE, Kim SK (2008) An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 134:291–303
7. Chen D, Li PW, Goldstein BA, Cai W, Thomas EL, Chen F, Hubbard AE, Melov S, Kapahi P (2013) Germline signaling mediates the synergistically prolonged longevity produced by double mutations in daf-2 and rsks-1 in C. elegans. Cell Rep 5:1600–1610
8. Chikina MD, Huttenhower C, Murphy CT, Troyanskaya OG (2009) Global prediction of tissue-specific gene expression and context-dependent gene networks in Caenorhabditis elegans. PLoS Comput Biol 5:e1000417
9. Ching TT, Paal AB, Mehta A, Zhong L, Hsu AL (2010) drr-2 encodes an eIF4H that acts downstream of TOR in diet-restriction-induced longevity of C. elegans. Aging Cell 9:545–557
10. Cohen E, Bieschke J, Perciavalle RM, Kelly JW, Dillin A (2006) Opposing activities protect against age-onset proteotoxicity. Science 313:1604–1610
11. Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D, Estepa G, Adame A, Pham HM, Holzenberger M, Kelly JW et al (2009) Reduced IGF-1 signaling delays age-associated proteotoxicity in mice. Cell 139:1157–1169
12. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, Kenyon C (2010) Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8:e1000450
13. DePina AS, Iser WB, Park SS, Maudsley S, Wilson MA, Wolkow CA (2011) Regulation of Caenorhabditis elegans vitellogenesis by DAF-2/IIS through separable transcriptional and posttranscriptional mechanisms. BMC Physiol 11:11
14. Depuydt G, Xie F, Petyuk VA, Shanmugam N, Smolders A, Dhondt I, Brewer HM, Camp DG, Smith RD, Braeckman BP (2013) Reduced insulin/IGF-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans. Mol Cell Proteomics, MCP
15. Dong MQ, Venable JD, Au N, Xu T, Park SK, Cociorva D, Johnson JR, Dillin A, Yates JR 3rd (2007) Quantitative mass spectrometry identifies insulin signaling targets in C. elegans. Science 317:660–663
16. Flachsbart F, Caliebe A, Kleindorp R, Blanche H, von Eller-Eberstein H, Nikolaus S, Schreiber S, Nebel A (2009) Association of FOXO3A variation with human longevity confirmed in German centenarians. Proc Natl Acad Sci USA 106:2700–2705
17. Fontana L, Partridge L, Longo VD (2010) Extending healthy life span–from yeast to humans. Science 328:321–326
18. Friedman DB, Johnson TE (1988) Three mutants that extend both mean and maximum life span of the nematode, Caenorhabditis elegans, define the age-1 gene. J Gerontol 43:B102–B109
19. Frokjaer-Jensen C (2013) Exciting prospects for precise engineering of Caenorhabditis elegans genomes with CRISPR/Cas9. Genetics 195:635–642
20. Garigan D, Hsu AL, Fraser AG, Kamath RS, Ahringer J, Kenyon C (2002) Genetic analysis of tissue aging in Caenorhabditis elegans: a role for heat-shock factor and bacterial proliferation. Genetics 161:1101–1112
21. Gems D, de la Guardia Y (2013) Alternative perspectives on aging in caenorhabditis elegans: reactive oxygen species or hyperfunction? Antioxid Redox Signal 19:321–329
22. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, Edgley ML, Larsen PL, Riddle DL (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150:129–155
23. Gems D, Pletcher S, Partridge L (2002) Interpreting interactions between treatments that slow aging. Aging Cell 1:1–9
24. Golden TR, Melov S (2004) Microarray analysis of gene expression with age in individual nematodes. Aging Cell 3:111–124
25. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, Blanchard D, Gygi SP, Brunet A (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17:1646–1656
26. Halaschek-Wiener J, Khattra JS, McKay S, Pouzyrev A, Stott JM, Yang GS, Holt RA, Jones SJ, Marra MA, Brooks-Wilson AR et al (2005) Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome Res 15:603–615
27. Hansen M, Hsu AL, Dillin A, Kenyon C (2005) New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet 1:119–128
28. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, Kenyon C (2007) Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6:95–110
29. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, Kenyon C (2008) A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet 4:e24
30. Hashimshony T, Wagner F, Sher N, Yanai I (2012) CEL-Seq: single-cell RNA-Seq by multiplexed linear amplification. Cell Rep 2:666–673
31. Henderson ST, Johnson TE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11:1975–1980
32. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, Paupard MC, Hall DH, Driscoll M (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419:808–814
33. Hsu AL, Murphy CT, Kenyon C (2003) Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300:1142–1145
34. Johnson DW, Llop JR, Farrell SF, Yuan J, Stolzenburg LR, Samuelson AV (2014) The Caenorhabditis elegans Myc-Mondo/Mad complexes integrate diverse longevity signals. PLoS Genet 10:e1004278
35. Kapahi P, Chen D, Rogers AN, Katewa SD, Li PW, Thomas EL, Kockel L (2010) With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab 11:453–465
36. Kauffman AL, Ashraf JM, Corces-Zimmerman MR, Landis JN, Murphy CT (2010) Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLoS Biol 8:e1000372
37. Kennedy BK, Pennypacker JK (2013) Drugs that modulate aging: the promising yet difficult path ahead. Transl Res 163(5):456–465
38. Kenyon CJ (2010) The genetics of ageing. Nature 464:504–512
39. 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
40. Kimura KD, Tissenbaum HA, Liu Y, Ruvkun G (1997) daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277:942–946
41. Larsen PL, Albert PS, Riddle DL (1995) Genes that regulate both development and longevity in Caenorhabditis elegans. Genetics 139:1567–1583
42. Lee SS, Kennedy S, Tolonen AC, Ruvkun G (2003) DAF-16 target genes that control C. elegans life-span and metabolism. Science 300:644–647
43. Li Y, Wang WJ, Cao H, Lu J, Wu C, Hu FY, Guo J, Zhao L, Yang F, Zhang YX et al (2009) Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum Mol Genet 18:4897–4904
44. Li X, Matilainen O, Jin CY, Glover-Cutter KM, Holmberg CI, Blackwell TK (2011) Specific SKN-1/Nrf stress responses to perturbations in translation elongation and proteasome activity. PLoS Genet 7:e1002119
45. Liang V, Ullrich M, Lam H, Chew YL, Banister S, Song X, Zaw T, Kassiou M, Gotz J, Nicholas HR (2014) Altered proteostasis in aging and heat shock response in C. elegans revealed by analysis of the global and de novo synthesized proteome. Cell Mol Life Sci
46. Libina N, Berman JR, Kenyon C (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115:489–502
47. 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
48. Luo S, Murphy CT (2011) Caenorhabditis elegans reproductive aging: regulation and underlying mechanisms. Genesis 49:53–65
49. McColl G, Rogers AN, Alavez S, Hubbard AE, Melov S, Link CD, Bush AI, Kapahi P, Lithgow GJ (2010) Insulin-like signaling determines survival during stress via posttranscriptional mechanisms in C. elegans. Cell Metab 12:260–272
50. McElwee J, Bubb K, Thomas JH (2003) Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2:111–121
51. McElwee JJ, Schuster E, Blanc E, Thomas JH, Gems D (2004) Shared transcriptional signature in Caenorhabditis elegans Dauer larvae and long-lived daf-2 mutants implicates detoxification system in longevity assurance. J Biol Chem 279:44533–44543
52. McElwee JJ, Schuster E, Blanc E, Piper MD, Thomas JH, Patel DS, Selman C, Withers DJ, Thornton JM, Partridge L et al (2007) Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol 8:R132
53. McGee MD, Weber D, Day N, Vitelli C, Crippen D, Herndon LA, Hall DH, Melov S (2011) Loss of intestinal nuclei and intestinal integrity in aging C. elegans. Aging Cell 10:699–710
54. Melendez A, Talloczy Z, Seaman M, Eskelinen EL, Hall DH, Levine B (2003) Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301:1387–1391
55. 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
56. Morley JF, Brignull HR, Weyers JJ, Morimoto RI (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc Natl Acad Sci USA 99:10417–10422
57. Murphy CT (2006) The search for DAF-16/FOXO transcriptional targets: approaches and discoveries. Exp Gerontol 41:910–921
58. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, Li H, Kenyon C (2003) Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424:277–283
59. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, Janette J, Chen C, Alves P, Preston E et al (2011) Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Res 21:245–254
60. Ogg S, Paradis S, Gottlieb S, Patterson GI, Lee L, Tissenbaum HA, Ruvkun G (1997) The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389:994–999
61. Oh SW, Mukhopadhyay A, Dixit BL, Raha T, Green MR, Tissenbaum HA (2006) Identification of direct DAF-16 targets controlling longevity, metabolism and diapause by chromatin immunoprecipitation. Nat Genet 38:251–257
62. Pan KZ, Palter JE, Rogers AN, Olsen A, Chen D, Lithgow GJ, Kapahi P (2007) Inhibition of mRNA translation extends lifespan in Caenorhabditis elegans. Aging Cell 6:111–119
63. Pawlikowska L, Hu D, Huntsman S, Sung A, Chu C, Chen J, Joyner AH, Schork NJ, Hsueh WC, Reiner AP et al (2009) Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 8:460–472
64. Pinkston JM, Garigan D, Hansen M, Kenyon C (2006) Mutations that increase the life span of C. elegans inhibit tumor growth. Science 313:971–975
65. Pinkston-Gosse J, Kenyon C (2007) DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 39:1403–1409
66. Qi W, Huang X, Neumann-Haefelin E, Schulze E, Baumeister R (2012) Cell-nonautonomous signaling of FOXO/DAF-16 to the stem cells of Caenorhabditis elegans. PLoS Genet 8:e1002836
67. Reis-Rodrigues P, Czerwieniec G, Peters TW, Evani US, Alavez S, Gaman EA, Vantipalli M, Mooney SD, Gibson BW, Lithgow GJ et al (2012) Proteomic analysis of age-dependent changes in protein solubility identifies genes that modulate lifespan. Aging Cell 11:120–127
68. Riesen M, Feyst I, Rattanavirotkul N, Ezcurra M, Tullet JM, Papatheodorou Y, Ziehm M, Au C, Gilliat AF, Hellberg J et al (2014) MDL-1, a growth- and tumor-suppressor, slows aging and prevents germline hyperplasia and hypertrophy in C. elegans. Aging 6(2):98–117
69. Robida-Stubbs S, Glover-Cutter K, Lamming DW, Mizunuma M, Narasimhan SD, Neumann-Haefelin E, Sabatini DM, Blackwell TK (2012) TOR signaling and rapamycin influence longevity by regulating SKN-1/Nrf and DAF-16/FoxO. Cell Metab 15:713–724
70. Schuster E, McElwee JJ, Tullet JM, Doonan R, Matthijssens F, Reece-Hoyes JS, Hope IA, Vanfleteren JR, Thornton JM, Gems D (2010) DamID in C. elegans reveals longevity-associated targets of DAF-16/FoxO. Mol Syst Biol 6:399
71. Soerensen M, Dato S, Christensen K, McGue M, Stevnsner T, Bohr VA, Christiansen L (2010) Replication of an association of variation in the FOXO3A gene with human longevity using both case-control and longitudinal data. Aging Cell 9:1010–1017
72. Stanfel MN, Shamieh LS, Kaeberlein M, Kennedy BK (2009) The TOR pathway comes of age. Biochim Biophys Acta 1790:1067–1074
73. Stein GM, Murphy CT (2012) The intersection of aging, longevity pathways, and learning and memory in C. elegans. Front Genet 3:259
74. Stout GJ, Stigter EC, Essers PB, Mulder KW, Kolkman A, Snijders DS, van den Broek NJ, Betist MC, Korswagen HC, Macinnes AW et al (2013) Insulin/IGF-1-mediated longevity is marked by reduced protein metabolism. Mol Syst Biol 9:679
75. Suh Y, Atzmon G, Cho MO, Hwang D, Liu B, Leahy DJ, Barzilai N, Cohen P (2008) Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci USA 105:3438–3442
76. Tank EM, Rodgers KE, Kenyon C (2011) Spontaneous age-related neurite branching in Caenorhabditis elegans. J Neurosci 31:9279–9288
77. Tepper RG, Ashraf J, Kaletsky R, Kleemann G, Murphy CT, Bussemaker HJ (2013) PQM-1 complements DAF-16 as a key transcriptional regulator of DAF-2-mediated development and longevity. Cell 154:676–690
78. Toth ML, Melentijevic I, Shah L, Bhatia A, Lu K, Talwar A, Naji H, Ibanez-Ventoso C, Ghose P, Jevince A et al (2012) Neurite sprouting and synapse deterioration in the aging Caenorhabditis elegans nervous system. J Neurosci 32:8778–8790
79. Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2:e183
80. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, Liu S, Oliveira RP, Baumeister R, Blackwell TK (2008) Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132:1025–1038
81. Tullet JM, Araiz C, Sanders MJ, Au C, Benedetto A, Papatheodorou I, Clark E, Schmeisser K, Jones D, Schuster EF et al (2014) DAF-16/FoxO directly regulates an atypical AMP-activated protein kinase gamma isoform to mediate the effects of insulin/IGF-1 signaling on aging in caenorhabditis elegans. PLoS Genet 10:e1004109
82. van Steensel B, Henikoff S (2000) Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat Biotechnol 18:424–428
83. Vellai T, Takacs-Vellai K, Zhang Y, Kovacs AL, Orosz L, Muller F (2003) Genetics: influence of TOR kinase on lifespan in C. elegans. Nature 426:620
84. Von Stetina SE, Watson JD, Fox RM, Olszewski KL, Spencer WC, Roy PJ, Miller DM 3rd (2007) Cell-specific microarray profiling experiments reveal a comprehensive picture of gene expression in the C. elegans nervous system. Genome Biol 8:R135
85. Wang J, Robida-Stubbs S, Tullet JM, Rual JF, Vidal M, Blackwell TK (2010) RNAi screening implicates a SKN-1-dependent transcriptional response in stress resistance and longevity deriving from translation inhibition. PLoS Genet 6:e1001048
86. Wilhelm M, Schlegl J, Hahne H, Moghaddas Gholami A, Lieberenz M, Savitski MM, Ziegler E, Butzmann L, Gessulat S, Marx H et al (2014) Mass-spectrometry-based draft of the human proteome. Nature 509:582–587
87. Willcox BJ, Donlon TA, He Q, Chen R, Grove JS, Yano K, Masaki KH, Willcox DC, Rodriguez B, Curb JD (2008) FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci USA 105:13987–13992
88. Wolkow CA, Kimura KD, Lee MS, Ruvkun G (2000) Regulation of C. elegans life-span by insulinlike signaling in the nervous system. Science 290:147–150
89. Zhang P, Judy M, Lee SJ, Kenyon C (2013) Direct and indirect gene regulation by a life-extending FOXO protein in C. elegans: roles for GATA factors and lipid gene regulators. Cell Metab 17:85–100