The Evolutionarily Conserved Longevity Determinants HCF-1 and SIR-2.1/SIRT1 Collaborate to Regulate DAF-16/FOXO

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The conserved DAF-16/FOXO transcription factors and SIR-2.1/SIRT1 deacetylases are critical for diverse biological processes, particularly longevity and stress response; and complex regulation of DAF-16/FOXO by SIR-2.1/SIRT1 is central to appropriate biological outcomes. Caenorhabditis elegans Host Cell Factor 1 (HCF-1) is a longevity determinant previously shown to act as a co-repressor of DAF-16. We report here that HCF-1 represents an integral player in the regulatory loop linking SIR-2.1/SIRT1 and DAF-16/FOXO in both worms and mammals. Genetic analyses showed that hcf-1 acts downstream of sir-2.1 to influence lifespan and oxidative stress response in C. elegans. Gene expression profiling revealed a striking 80% overlap between the DAF-16 target genes responsive to hcf-1 mutation and sir-2.1 overexpression. Subsequent GO-term analyses of HCF-1 and SIR-2.1-coregulated DAF-16 targets suggested that HCF-1 and SIR-2.1 together regulate specific aspects of DAF-16-mediated transcription particularly important for aging and stress responses. Analogous to its role in regulating DAF-16/SIR-2.1 target genes in C. elegans, the mammalian HCF-1 also repressed the expression of several FOXO/SIRT1 target genes. Protein–protein association studies demonstrated that SIR-2.1/SIRT1 and HCF-1 form protein complexes in worms and mammalian cells, highlighting the conservation of their regulatory relationship. Our findings uncover a conserved interaction between the key longevity determinants SIR-2.1/SIRT1 and HCF-1, and they provide new insights into the complex regulation of FOXO proteins.

Vyšlo v časopise: The Evolutionarily Conserved Longevity Determinants HCF-1 and SIR-2.1/SIRT1 Collaborate to Regulate DAF-16/FOXO. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002235
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002235

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1. KenyonCJ 2010 The genetics of ageing. Nature 464 504 512

2. BurgeringBMKopsGJ 2002 Cell cycle and death control: long live Forkheads. Trends Biochem Sci 27 352 360

3. LinKDormanJBRodanAKenyonC 1997 daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278 1319 1322

4. GiannakouMEGossMJungerMAHafenELeeversSJ 2004 Long-lived Drosophila with overexpressed dFOXO in adult fat body. Science 305 361

5. HwangboDSGershmanBTuMPPalmerMTatarM 2004 Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429 562 566

6. KappelerLDe Magalhaes FilhoCDupontJLeneuvePCerveraP 2008 Brain IGF-1 receptors control mammalian growth and lifespan through a neuroendocrine mechanism. PLoS Biol 6 e254 doi:10.1371/journal.pbio.0060254

7. YuanRTsaihSWPetkovaSBMarin de EvsikovaCXingS 2009 Aging in inbred strains of mice: study design and interim report on median lifespans and circulating IGF1 levels. Aging Cell 8 277 287

8. LiYWangWJCaoHLuJWuC 2009 Genetic association of FOXO1A and FOXO3A with longevity trait in Han Chinese populations. Hum Mol Genet 18 4897 4904

9. WillcoxBJDonlonTAHeQChenRGroveJS 2008 FOXO3A genotype is strongly associated with human longevity. Proc Natl Acad Sci U S A 105 13987 13992

10. ArdenKC 2008 FOXO animal models reveal a variety of diverse roles for FOXO transcription factors. Oncogene 27 2345 2350

11. KenyonCChangJGenschERudnerATabtiangR 1993 A C. elegans mutant that lives twice as long as wild type. Nature 366 461 464

12. WangMCO'RourkeEJRuvkunG 2008 Fat metabolism links germline stem cells and longevity in C. elegans. Science 322 957 960

13. Halaschek-WienerJKhattraJSMcKaySPouzyrevAStottJM 2005 Analysis of long-lived C. elegans daf-2 mutants using serial analysis of gene expression. Genome Res 15 603 615

14. LeeSSKennedySTolonenACRuvkunG 2003 DAF-16 target genes that control C. elegans life-span and metabolism. Science 300 644 647

15. McElweeJBubbKThomasJH 2003 Transcriptional outputs of the Caenorhabditis elegans forkhead protein DAF-16. Aging Cell 2 111 121

16. MurphyCTMcCarrollSABargmannCIFraserAKamathRS 2003 Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature 424 277 283

17. LinKHsinHLibinaNKenyonC 2001 Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28 139 145

18. BerdichevskyAViswanathanMHorvitzHRGuarenteL 2006 C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125 1165 1177

19. BermanJRKenyonC 2006 Germ-cell loss extends C. elegans life span through regulation of DAF-16 by kri-1 and lipophilic-hormone signaling. Cell 124 1055 1068

20. EssersMAde Vries-SmitsLMBarkerNPoldermanPEBurgeringBM 2005 Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308 1181 1184

21. LiJEbataADongYRizkiGIwataT 2008 Caenorhabditis elegans HCF-1 functions in longevity maintenance as a DAF-16 regulator. PLoS Biol 6 e233 doi:10.1371/journal.pbio.0060233

22. WolffSMaHBurchDMacielGAHunterT 2006 SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 124 1039 1053

23. LehtinenMKYuanZBoagPRYangYVillenJ 2006 A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125 987 1001

24. TissenbaumHAGuarenteL 2001 Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans. Nature 410 227 230

25. WangYOhSWDeplanckeBLuoJWalhoutAJ 2006 C. elegans 14-3-3 proteins regulate life span and interact with SIR-2.1 and DAF-16/FOXO. Mech Ageing Dev 127 741 747

26. KaeberleinMMcVeyMGuarenteL 1999 The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev 13 2570 2580

27. RoginaBHelfandSL 2004 Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc Natl Acad Sci U S A 101 15998 16003

28. BrunetASweeneyLBSturgillJFChuaKFGreerPL 2004 Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 2011 2015

29. DaitokuHHattaMMatsuzakiHArataniSOhshimaT 2004 Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A 101 10042 10047

30. MottaMCDivechaNLemieuxMKamelCChenD 2004 Mammalian SIRT1 represses forkhead transcription factors. Cell 116 551 563

31. YangYHouHHallerEMNicosiaSVBaiW 2005 Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 24 1021 1032

32. LeeSHerrW 2001 Stabilization but not the transcriptional activity of herpes simplex virus VP16-induced complexes is evolutionarily conserved among HCF family members. J Virol 75 12402 12411

33. GersterTRoederRG 1988 A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins. Proc Natl Acad Sci U S A 85 6347 6351

34. GuntherMLaithierMBrisonO 2000 A set of proteins interacting with transcription factor Sp1 identified in a two-hybrid screening. Mol Cell Biochem 210 131 142

35. LuRMisraV 2000 Zhangfei: a second cellular protein interacts with herpes simplex virus accessory factor HCF in a manner similar to Luman and VP16. Nucleic Acids Res 28 2446 2454

36. LuRYangPO'HarePMisraV 1997 Luman, a new member of the CREB/ATF family, binds to herpes simplex virus VP16-associated host cellular factor. Mol Cell Biol 17 5117 5126

37. PilusoDBilanPCaponeJP 2002 Host cell factor-1 interacts with and antagonizes transactivation by the cell cycle regulatory factor Miz-1. J Biol Chem 277 46799 46808

38. TyagiSChabesALWysockaJHerrW 2007 E2F activation of S phase promoters via association with HCF-1 and the MLL family of histone H3K4 methyltransferases. Mol Cell 27 107 119

39. WysockaJMyersMPLahertyCDEisenmanRNHerrW 2003 Human Sin3 deacetylase and trithorax-related Set1/Ash2 histone H3-K4 methyltransferase are tethered together selectively by the cell-proliferation factor HCF-1. Genes Dev 17 896 911

40. JulienEHerrW 2004 A switch in mitotic histone H4 lysine 20 methylation status is linked to M phase defects upon loss of HCF-1. Mol Cell 14 713 725

41. TyagiSHerrW 2009 E2F1 mediates DNA damage and apoptosis through HCF-1 and the MLL family of histone methyltransferases. EMBO J 28 3185 3195

42. WangYTissenbaumHA 2006 Overlapping and distinct functions for a Caenorhabditis elegans SIR2 and DAF-16/FOXO. Mech Ageing Dev 127 48 56

43. ViswanathanMKimSKBerdichevskyAGuarenteL 2005 A role for SIR-2.1 regulation of ER stress response genes in determining C. elegans life span. Dev Cell 9 605 615

44. HassanHMFridovichI 1979 Intracellular production of superoxide radical and of hydrogen peroxide by redox active compounds. Arch Biochem Biophys 196 385 395

45. MathewsWRGuidoDMFisherMAJaeschkeH 1994 Lipid peroxidation as molecular mechanism of liver cell injury during reperfusion after ischemia. Free Radic Biol Med 16 763 770

46. WangWShakesDC 1997 Expression patterns and transcript processing of ftt-1 and ftt-2, two C. elegans 14-3-3 homologues. J Mol Biol 268 619 630

47. LiJTewariMVidalMLeeSS 2007 The 14-3-3 protein FTT-2 regulates DAF-16 in Caenorhabditis elegans. Dev Biol 301 82 91

48. TusherVGTibshiraniRChuG 2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121

49. ShawWMLuoSLandisJAshrafJMurphyCT 2007 The C. elegans TGF-beta Dauer pathway regulates longevity via insulin signaling. Curr Biol 17 1635 1645

50. DennisGJrShermanBTHosackDAYangJGaoW 2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4 P3

51. McElweeJJSchusterEBlancEPiperMDThomasJH 2007 Evolutionary conservation of regulated longevity assurance mechanisms. Genome Biol 8 R132

52. XuCLiCYKongAN 2005 Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28 249 268

53. FuruyamaTNakazawaTNakanoIMoriN 2000 Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J 349 629 634

54. CurranSPWuXRiedelCGRuvkunG 2009 A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459 1079 1084

55. LiuXBrutlagDLLiuJS 2001 BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 127 138

56. Thomas-ChollierMSandOTuratsinzeJVJankyRDefranceM 2008 RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36 W119 127

57. BudovskayaYVWuKSouthworthLKJiangMTedescoP 2008 An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 134 291 303

58. JulienEHerrW 2003 Proteolytic processing is necessary to separate and ensure proper cell growth and cytokinesis functions of HCF-1. EMBO J 22 2360 2369

59. WysockaJHerrW 2003 The herpes simplex virus VP16-induced complex: the makings of a regulatory switch. Trends Biochem Sci 28 294 304

60. JohnsonKMMahajanSSWilsonAC 1999 Herpes simplex virus transactivator VP16 discriminates between HCF-1 and a novel family member, HCF-2. J Virol 73 3930 3940

61. van der HorstABurgeringBM 2007 Stressing the role of FoxO proteins in lifespan and disease. Nat Rev Mol Cell Biol 8 440 450

62. RimannIHajnalA 2007 Regulation of anchor cell invasion and uterine cell fates by the egl-43 Evi-1 proto-oncogene in Caenorhabditis elegans. Dev Biol 308 187 195

63. PuigserverPRheeJDonovanJWalkeyCJYoonJC 2003 Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423 550 555

64. RodgersJTLerinCHaasWGygiSPSpiegelmanBM 2005 Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 113 118

65. NemotoSFergussonMMFinkelT 2005 SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J Biol Chem 280 16456 16460

66. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

67. BreslowNEClaytonDG 1993 Approximate Inference in Generalized Linear Mixed Models. Journal of the American Statistical Association 88 9 25

68. TroemelERChuSWReinkeVLeeSSAusubelFM 2006 p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2 e183 doi:10.1371/journal.pgen.0020183

69. PleissJAWhitworthGBBergkesselMGuthrieC 2007 Transcript specificity in yeast pre-mRNA splicing revealed by mutations in core spliceosomal components. PLoS Biol 5 e90 doi:10.1371/journal.pbio.0050090

70. EisenMBSpellmanPTBrownPOBotsteinD 1998 Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95 14863 14868

71. Huang daWShermanBTLempickiRA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4 44 57

72. CrooksGEHonGChandoniaJMBrennerSE 2004 WebLogo: a sequence logo generator. Genome Res 14 1188 1190

73. GuptaSStamatoyannopoulosJABaileyTLNobleWS 2007 Quantifying similarity between motifs. Genome Biol 8 R24

74. CheesemanIMNiessenSAndersonSHyndmanFYatesJR3rd 2004 A conserved protein network controls assembly of the outer kinetochore and its ability to sustain tension. Genes Dev 18 2255 2268

75. TabbDLMcDonaldWHYatesJR3rd 2002 DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1 21 26

76. KristieTMSharpPA 1993 Purification of the cellular C1 factor required for the stable recognition of the Oct-1 homeodomain by the herpes simplex virus alpha-trans-induction factor (VP16). J Biol Chem 268 6525 6534