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

PLoS Genetics

Volumn 8, Issue 8, 2012, Pages

  Qi, Wenjing ^a   Huang, Xu ^a   Neumann Haefelin, Elke ^a   Schulze, Ekkehard ^a   Baumeister, Ralf ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FLOXURIDINE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE B 1; PROTEIN KINASE B BETA; PROTEIN SHC; PROTEIN SHC 1; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; SOMATOMEDIN RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR DAF 16; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CARCINOGENIC ACTIVITY; CELL HYPERPLASIA; CELL PROLIFERATION; CONTROLLED STUDY; DAF 16 GENE; DAF 18 GENE; DAF 2 GENE; EMBRYO; FEMALE; GENE; GENE EXPRESSION; GENE SILENCING; GERM LINE; GONAD DEVELOPMENT; INTRACELLULAR SIGNALING; LARVA; LIFE EXTENSION; LONGEVITY; LOSS OF FUNCTION MUTATION; MALE; MEMBRANE DAMAGE; NONAUTONOMOUS SIGNALING; NONHUMAN; PHENOTYPE; PLEIOTROPY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA INTERFERENCE; SHC 1 GENE; STEM CELL; SUBCUTANEOUS TISSUE; TEMPERATURE SENSITIVE MUTANT; TRANSGENE; TRANSGENIC ANIMAL; UPREGULATION;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; HUMANS; LONGEVITY; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTORS, SOMATOMEDIN; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION FACTORS;

CAENORHABDITIS ELEGANS;

EID: 84866165842     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002836     Document Type: Article

References (47)

1. Fu Z, Tindall DJ, (2008) FOXOs, cancer and regulation of apoptosis. Oncogene 27: 2312-2319.
2. 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.
3. Paradis S, Ailion M, Toker A, Thomas JH, Ruvkun G, (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. 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. Genes Dev 12: 2488-2498.
5. Berdichevsky A, Viswanathan M, Horvitz HR, Guarente L, (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. Calnan DR, Brunet A, (2008) The FoxO code. Oncogene 27: 2276-2288.
7. Hertweck M, Gobel C, Baumeister R, (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. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, et al. (2006) A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 125: 987-1001.
9. Oh SW, Mukhopadhyay A, Svrzikapa N, Jiang F, Davis RJ, 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. Ramaswamy S, Nakamura N, Sansal I, Bergeron L, Sellers WR, (2002) A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR. Cancer Cell 2: 81-91.
11. Modur V, Nagarajan R, Evers BM, Milbrandt J, (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. 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.
13. Sunters A, Madureira PA, Pomeranz KM, Aubert M, Brosens JJ, 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. 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.
15. Naka K, Hoshii T, Muraguchi T, Tadokoro Y, Ooshio T, et al. (2010) TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463: 676-680.
16. Lin K, Dorman JB, Rodan A, Kenyon C, (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. 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.
18. 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.
19. Michaelson D, Korta DZ, Capua Y, Hubbard EJ, (2010) Insulin signaling promotes germline proliferation in C. elegans. Development 137: 671-680.
20. Luo S, Kleemann GA, Ashraf JM, Shaw WM, Murphy CT, (2010) TGF-beta and insulin signaling regulate reproductive aging via oocyte and germline quality maintenance. Cell 143: 299-312.
21. 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.
22. Arantes-Oliveira N, Apfeld J, Dillin A, Kenyon C, (2002) Regulation of life-span by germ-line stem cells in Caenorhabditis elegans. Science 295: 502-505.
23. Hsin H, Kenyon C, (1999) Signals from the reproductive system regulate the lifespan of C. elegans. Nature 399: 362-366.
24. Ghazi A, Henis-Korenblit S, Kenyon C, (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. Berman JR, Kenyon C, (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-Haefelin E, Qi W, Finkbeiner E, Walz G, Baumeister R, 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. Mizuno T, Fujiki K, Sasakawa A, Hisamoto N, Matsumoto K, (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. Luzi L, Confalonieri S, Di Fiore PP, Pelicci PG, (2000) Evolution of Shc functions from nematode to human. Curr Opin Genet Dev 10: 668-674.
29. 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.
30. Austin J, Kimble J, (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. Aitlhadj L, Sturzenbaum SR, (2010) The use of FUdR can cause prolonged longevity in mutant nematodes. Mech Ageing Dev 131: 364-365.
32. Mitchell DH, Stiles JW, Santelli J, Sanadi DR, (1979) Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol 34: 28-36.
33. Sherwood DR, Butler JA, Kramer JM, Sternberg PW, (2005) FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 121: 951-962.
34. Gems D, Sutton AJ, Sundermeyer ML, Albert PS, King KV, 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. Curran SP, Wu X, Riedel CG, Ruvkun G, (2009) A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 459: 1079-1084.
36. Lee RY, Hench J, Ruvkun G, (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. Kwon ES, Narasimhan SD, Yen K, Tissenbaum HA, (2010) A new DAF-16 isoform regulates longevity. Nature 466: 498-502.
38. Tullet JM, Hertweck M, An JH, Baker J, Hwang JY, et al. (2008) Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 132: 1025-1038.
39. Francis R, Barton MK, Kimble J, Schedl T, (1995) gld-1, a tumor suppressor gene required for oocyte development in Caenorhabditis elegans. Genetics 139: 579-606.
40. Trzebiatowska A, Topf U, Sauder U, Drabikowski K, Chiquet-Ehrismann R, (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. Kelly WG, Xu S, Montgomery MK, Fire A, (1997) Distinct requirements for somatic and germline expression of a generally expressed Caernorhabditis elegans gene. Genetics 146: 227-238.
42. Libina N, Berman JR, Kenyon C, (2003) Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan. Cell 115: 489-502.
43. Alam H, Williams TW, Dumas KJ, Guo C, Yoshina S, et al. (2010) EAK-7 controls development and life span by regulating nuclear DAF-16/FoxO activity. Cell Metab 12: 30-41.
44. Dansen TB, Burgering BM, (2008) Unravelling the tumor-suppressive functions of FOXO proteins. Trends Cell Biol 18: 421-429.
45. Sykes SM, Lane SW, Bullinger L, Kalaitzidis D, Yusuf R, et al. (2011) AKT/FOXO Signaling Enforces Reversible Differentiation Blockade in Myeloid Leukemias. Cell 146: 697-708.
46. Pinkston-Gosse J, Kenyon C, (2007) DAF-16/FOXO targets genes that regulate tumor growth in Caenorhabditis elegans. Nat Genet 39: 1403-1409.
47. Storz P, Doppler H, Copland JA, Simpson KJ, Toker A, (2009) FOXO3a promotes tumor cell invasion through the induction of matrix metalloproteinases. Mol Cell Biol 29: 4906-4917.