Cell-Nonautonomous Signaling of FOXO/DAF-16 to the Stem Cells of

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In Caenorhabditis elegans (C. elegans), the promotion of longevity by the transcription factor DAF-16 requires reduced insulin/IGF receptor (IIR) signaling or the ablation of the germline, although the reason for the negative impact of germ cells is unknown. FOXO/DAF-16 activity inhibits germline proliferation in both daf-2 mutants and gld-1 tumors. In contrast to its function as a germline tumor suppressor, we now provide evidence that somatic DAF-16 in the presence of IIR signaling can also result in tumorigenic activity, which counteracts robust lifespan extension. In contrast to the cell-autonomous IIR signaling, which is required for larval germline proliferation, activation of DAF-16 in the hypodermis results in hyperplasia of the germline and disruption of the surrounding basement membrane. SHC-1 adaptor protein and AKT-1 kinase antagonize, whereas AKT-2 and SGK-1 kinases promote, this cell-nonautonomous DAF-16 function. Our data suggest that a functional balance of DAF-16 activities in different tissues determines longevity and reveals a novel, cell-nonautonomous role of FOXO/DAF-16 to affect stem cells.

Vyšlo v časopise: Cell-Nonautonomous Signaling of FOXO/DAF-16 to the Stem Cells of. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002836
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002836

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Zdroje

1. FuZ, TindallDJ (2008) FOXOs, cancer and regulation of apoptosis. Oncogene 27: 2312–2319.

2. BrunetA, BonniA, ZigmondMJ, LinMZ, JuoP, et al. (1999) Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857–868.

3. ParadisS, AilionM, TokerA, ThomasJH, RuvkunG (1999) A PDK1 homolog is necessary and sufficient to transduce AGE-1 PI3 kinase signals that regulate diapause in Caenorhabditis elegans. Genes Dev 13: 1438–1452.

4. ParadisS, RuvkunG (1998) Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Genes Dev 12: 2488–2498.

5. BerdichevskyA, ViswanathanM, HorvitzHR, GuarenteL (2006) C. elegans SIR-2.1 interacts with 14-3-3 proteins to activate DAF-16 and extend life span. Cell 125: 1165–1177.

6. CalnanDR, BrunetA (2008) The FoxO code. Oncogene 27: 2276–2288.

7. HertweckM, GobelC, BaumeisterR (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.

8. LehtinenMK, YuanZ, BoagPR, YangY, VillenJ, et al. (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987–1001.

9. OhSW, MukhopadhyayA, SvrzikapaN, JiangF, DavisRJ, et al. (2005) JNK regulates lifespan in Caenorhabditis elegans by modulating nuclear translocation of forkhead transcription factor/DAF-16. Proc Natl Acad Sci U S A 102: 4494–4499.

10. RamaswamyS, NakamuraN, SansalI, BergeronL, SellersWR (2002) A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR. Cancer Cell 2: 81–91.

11. ModurV, NagarajanR, EversBM, MilbrandtJ (2002) FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem 277: 47928–47937.

12. PaikJH, KolliparaR, ChuG, JiH, XiaoY, et al. (2007) FoxOs are lineage-restricted redundant tumor suppressors and regulate endothelial cell homeostasis. Cell 128: 309–323.

13. SuntersA, MadureiraPA, PomeranzKM, AubertM, BrosensJJ, et al. (2006) Paclitaxel-induced nuclear translocation of FOXO3a in breast cancer cells is mediated by c-Jun NH2-terminal kinase and Akt. Cancer Res 66: 212–220.

14. TothovaZ, KolliparaR, HuntlyBJ, LeeBH, CastrillonDH, et al. (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 128: 325–339.

15. NakaK, HoshiiT, MuraguchiT, TadokoroY, OoshioT, et al. (2010) TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463: 676–680.

16. LinK, DormanJB, RodanA, KenyonC (1997) daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278: 1319–1322.

17. LinK, HsinH, LibinaN, KenyonC (2001) Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nat Genet 28: 139–145.

18. HondaY, HondaS (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.

19. MichaelsonD, KortaDZ, CapuaY, HubbardEJ (2010) Insulin signaling promotes germline proliferation in C. elegans. Development 137: 671–680.

20. LuoS, KleemannGA, AshrafJM, ShawWM, MurphyCT (2010) TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143: 299–312.

21. PinkstonJM, GariganD, HansenM, KenyonC (2006) Mutations that increase the life span of C. elegans inhibit tumor growth. Science 313: 971–975.

22. Arantes-OliveiraN, ApfeldJ, DillinA, KenyonC (2002) Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295: 502–505.

23. HsinH, KenyonC (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399: 362–366.

24. GhaziA, Henis-KorenblitS, KenyonC (2009) A transcription elongation factor that links signals from the reproductive system to lifespan extension in Caenorhabditis elegans. PLoS Genet 5: e1000639 doi:10.1371/journal.pgen.1000639..

25. BermanJR, KenyonC (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.

26. Neumann-HaefelinE, QiW, FinkbeinerE, WalzG, BaumeisterR, et al. (2008) SHC-1/p52Shc targets the insulin/IGF-1 and JNK signaling pathways to modulate life span and stress response in C. elegans. Genes Dev 22: 2721–2735.

27. MizunoT, FujikiK, SasakawaA, HisamotoN, MatsumotoK (2008) Role of the Caenorhabditis elegans Shc adaptor protein in the c-Jun N-terminal kinase signaling pathway. Mol Cell Biol 28: 7041–7049.

28. LuziL, ConfalonieriS, Di FiorePP, PelicciPG (2000) Evolution of Shc functions from nematode to human. Curr Opin Genet Dev 10: 668–674.

29. HendersonST, JohnsonTE (2001) daf-16 integrates developmental and environmental inputs to mediate aging in the nematode Caenorhabditis elegans. Curr Biol 11: 1975–1980.

30. AustinJ, KimbleJ (1987) glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51: 589–599.

31. AitlhadjL, SturzenbaumSR (2010) The use of FUdR can cause prolonged longevity in mutant nematodes. Mech Ageing Dev 131: 364–365.

32. MitchellDH, StilesJW, SantelliJ, SanadiDR (1979) Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol 34: 28–36.

33. SherwoodDR, ButlerJA, KramerJM, SternbergPW (2005) FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 121: 951–962.

34. GemsD, SuttonAJ, SundermeyerML, AlbertPS, KingKV, et al. (1998) Two pleiotropic classes of daf-2 mutation affect larval arrest, adult behavior, reproduction and longevity in Caenorhabditis elegans. Genetics 150: 129–155.

35. CurranSP, WuX, RiedelCG, RuvkunG (2009) A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459: 1079–1084.

36. LeeRY, HenchJ, RuvkunG (2001) Regulation of C. elegans DAF-16 and its human ortholog FKHRL1 by the daf-2 insulin-like signaling pathway. Curr Biol 11: 1950–1957.

37. KwonES, NarasimhanSD, YenK, TissenbaumHA (2010) A new DAF-16 isoform regulates longevity. Nature 466: 498–502.

38. TulletJM, HertweckM, AnJH, BakerJ, HwangJY, et al. (2008) Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132: 1025–1038.

39. FrancisR, BartonMK, KimbleJ, SchedlT (1995) gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579–606.

40. TrzebiatowskaA, TopfU, SauderU, DrabikowskiK, Chiquet-EhrismannR (2008) Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol Biol Cell 19: 3898–3908.

41. KellyWG, XuS, MontgomeryMK, FireA (1997) Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146: 227–238.

42. LibinaN, BermanJR, KenyonC (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489–502.

43. AlamH, WilliamsTW, DumasKJ, GuoC, YoshinaS, et al. (2010) EAK-7 controls development and life span by regulating nuclear DAF-16/FoxO activity. Cell Metab 12: 30–41.

44. DansenTB, BurgeringBM (2008) Unravelling the tumor-suppressive functions of FOXO proteins. Trends Cell Biol 18: 421–429.

45. SykesSM, LaneSW, BullingerL, KalaitzidisD, YusufR, et al. (2011) AKT/FOXO Signaling Enforces Reversible Differentiation Blockade in Myeloid Leukemias. Cell 146: 697–708.

46. Pinkston-GosseJ, KenyonC (2007) DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 39: 1403–1409.

47. StorzP, DopplerH, CoplandJA, SimpsonKJ, TokerA (2009) FOXO3a promotes tumor cell invasion through the induction of matrix metalloproteinases. Mol Cell Biol 29: 4906–4917.