PTEN Negatively Regulates MAPK Signaling during Caenorhabditis elegans Vulval Development

PLoS Genetics

Volumn 8, Issue 8, 2012, Pages

  Nakdimon, Itay ^a   Walser, Michael ^a   Fröhli, Erika ^a   Hajnal, Alex ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR DAUER FORMATION 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN DAF 18; PROTEIN KINASE B; RAS PROTEIN; TRANSCRIPTION FACTOR DAF 16; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL COMMUNICATION; CELL FATE; CONTROLLED STUDY; DAF 18 GENE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC EPISTASIS; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; NONHUMAN; PROTEIN EXPRESSION; RNA INTERFERENCE; SEXUAL DEVELOPMENT; STEM CELL; TISSUE INDUCTION; TUMOR SUPPRESSOR GENE; VULVA;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MODELS, BIOLOGICAL; MUTATION; NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS P21(RAS); PTEN PHOSPHOHYDROLASE; RECEPTOR, INSULIN; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VULVA; WNT PROTEINS;

CAENORHABDITIS ELEGANS;

EID: 84866150948     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002881     Document Type: Article

References (42)

1. Li J, Yen C, Liaw D, Podsypanina K, Bose S, et al. (1997) PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275: 1943-1947.
2. Blumenthal GM, Dennis PA, (2008) PTEN hamartoma tumor syndromes. Eur J Hum Genet 16: 1289-1300 doi:10.1038/ejhg.2008.162.
3. Liaw D, Marsh DJ, Li J, Dahia PL, Wang SI, et al. (1997) Germline mutations of the PTEN gene in Cowden disease, an inherited breast and thyroid cancer syndrome. Nat Genet 16: 64-67 doi:10.1038/ng0597-64.
4. Myers M, Pass I, Batty I, Van der Kaay J, Stolarov J, et al. (1998) The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc Natl Acad Sci USA 95: 13513-13518.
5. Dey N, Crosswell HE, De P, Parsons R, Peng Q, et al. (2008) The protein phosphatase activity of PTEN regulates SRC family kinases and controls glioma migration. Cancer Res 68: 1862-1871 doi:10.1158/0008-5472.CAN-07-1182.
6. Cai X-M, Tao B-B, Wang L-Y, Liang Y-L, Jin J-W, et al. (2005) Protein phosphatase activity of PTEN inhibited the invasion of glioma cells with epidermal growth factor receptor mutation type III expression. Int J Cancer 117: 905-912 doi:10.1002/ijc.21251.
7. Myers MP, Stolarov JP, Eng C, Li J, Wang SI, et al. (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc Natl Acad Sci USA 94: 9052-9057.
8. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, et al. (1998) Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science 280: 1614-1617.
9. Gildea J, Herlevsen M, Harding M, Gulding K, Moskaluk C, et al. (2004) PTEN can inhibit in vitro organotypic and in vivo orthotopic invasion of human bladder cancer cells even in the absence of its lipid phosphatase activity. Oncogene 23: 6788-6797 doi:10.1038/sj.onc.1207599.
10. Gu J, Tamura M, Pankov R, Danen EH, Takino T, et al. (1999) Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J Cell Biol 146: 389-403.
11. Hu PJ, (2007) Dauer. Worm Book pp. 1-19 doi:10.1895/wormbook.1.144.1.
12. Christensen R, la Torre-Ubieta de L, Bonni A, Colón-Ramos DA, (2011) A conserved PTEN/FOXO pathway regulates neuronal morphology during C. elegans development. Development 138: 5257-5267 doi:10.1242/dev.069062.
13. Fukuyama M, Rougvie A, Rothman J, (2006) C. elegans DAF-18/PTEN mediates nutrient-dependent arrest of cell cycle and growth in the germline. Curr Biol 16: 773-779 doi:10.1016/j.cub.2006.02.073.
14. Mihaylova V, Borland C, Manjarrez L, Stern M, Sun H, (1999) The PTEN tumor suppressor homolog in Caenorhabditis elegans regulates longevity and dauer formation in an insulin receptor-like signaling pathway. Proc Natl Acad Sci USA 96: 7427-7432.
15. Solari F, Bourbon-Piffaut A, Masse I, Payrastre B, Chan A, et al. (2005) The human tumour suppressor PTEN regulates longevity and dauer formation in Caenorhabditis elegans. Oncogene 24: 20-27 doi:10.1038/sj.onc.1207978.
16. 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.
17. Cahill CM, Tzivion G, Nasrin N, Ogg S, Dore J, et al. (2001) Phosphatidylinositol 3-kinase signaling inhibits DAF-16 DNA binding and function via 14-3-3-dependent and 14-3-3-independent pathways. J Biol Chem 276: 13402-13410 doi:10.1074/jbc.M010042200.
18. Brisbin S, Liu J, Boudreau J, Peng J, Evangelista M, et al. (2009) A role for C. elegans Eph RTK signaling in PTEN regulation. Dev Cell 17: 459-469 doi:10.1016/j.devcel.2009.08.009.
19. Suzuki Y, Han M, (2006) Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Genes Dev 20: 423-428 doi:10.1101/gad.1378906.
20. Sternberg PW, (2005) Vulval development. Worm Book pp. 1-28 doi:10.1895/wormbook.1.6.1.
21. Battu G, Hoier E, Hajnal A, (2003) The C. elegans G-protein-coupled receptor SRA-13 inhibits RAS/MAPK signalling during olfaction and vulval development. Development 130: 2567-2577.
22. Zou W, Lu Q, Zhao D, Li W, Mapes J, et al. (2009) Caenorhabditis elegans myotubularin MTM-1 negatively regulates the engulfment of apoptotic cells. PLoS Genet 5: e1000679 doi:10.1371/journal.pgen.1000679.
23. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421: 268-272 doi:10.1038/nature01279.
24. Kinchen JM, Doukoumetzidis K, Almendinger J, Stergiou L, Tosello-Trampont A, et al. (2008) A pathway for phagosome maturation during engulfment of apoptotic cells. Nat Cell Biol 10: 556-566 doi:10.1038/ncb1718.
25. Burdine RD, Branda CS, Stern MJ, (1998) EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 125: 1083-1093.
26. Berset T, Hoier E, Battu G, Canevascini S, Hajnal A, (2001) Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 291: 1055-1058 doi:10.1126/science.1055642.
27. Lackner MR, Kim SK, (1998) Genetic analysis of the Caenorhabditis elegans MAP kinase gene mpk-1. Genetics 150: 103-117.
28. Chang C, Hopper N, Sternberg P, (2000) Caenorhabditis elegans SOS-1 is necessary for multiple RAS-mediated developmental signals. EMBO J 19: 3283-3294 doi:10.1093/emboj/19.13.3283.
29. Tan PB, Lackner MR, Kim SK, (1998) MAP kinase signaling specificity mediated by the LIN-1 Ets/LIN-31 WH transcription factor complex during C. elegans vulval induction. Cell 93: 569-580.
30. Sasaoka T, Kobayashi M, (2000) The functional significance of Shc in insulin signaling as a substrate of the insulin receptor. Endocr J 47: 373-381.
31. Sasaoka T, Draznin B, Leitner JW, Langlois WJ, Olefsky JM, (1994) Shc is the predominant signaling molecule coupling insulin receptors to activation of guanine nucleotide releasing factor and p21ras-GTP formation. J Biol Chem 269: 10734-10738.
32. Nanji M, Hopper N, Gems D, (2005) LET-60 RAS modulates effects of insulin/IGF-1 signaling on development and aging in Caenorhabditis elegans. Aging Cell 4: 235-245 doi:10.1111/j.1474-9726.2005.00166.x.
33. Cui M, Chen J, Myers TR, Hwang BJ, Sternberg PW, et al. (2006) SynMuv Genes Redundantly Inhibit lin-3/EGF Expression to Prevent Inappropriate Vulval Induction in C. elegans. Dev Cell 10: 667-672 doi:10.1016/j.devcel.2006.04.001.
34. Planchon SM, Waite KA, Eng C, (2008) The nuclear affairs of PTEN. J Cell Sci 121: 249-253 doi:10.1242/jcs.022459.
35. Weng LP, Brown JL, Eng C, (2001) PTEN coordinates G(1) arrest by down-regulating cyclin D1 via its protein phosphatase activity and up-regulating p27 via its lipid phosphatase activity in a breast cancer model. Hum Mol Genet 10: 599-604.
36. Hong Y, Roy R, Ambros V, (1998) Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125: 3585-3597.
37. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
38. Hobert O, (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Bio Techniques 32: 728-730.
39. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970.
40. Sternberg PW, Horvitz HR, (1986) Pattern formation during vulval development in C. elegans. Cell 44: 761-772.
41. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237 doi:10.1038/nature01278.
42. Abramoff MD, Magalhães PJ, Ram SJ, (2004) Image processing with ImageJ. Biophotonics international 11: 36-42.