The caenorhabditis elegans synthetic multivulva genes prevent ras pathway activation by tightly repressing global ectopic expression of lin-3 EGF

PLoS Genetics

Volumn 7, Issue 12, 2011, Pages

  Saffer, Adam M ^a   Kim, Dong Hyun ^a   van Oudenaarden, Alexander ^a   Horvitz, H Robert ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; MESSENGER RNA; RAS PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; LIN 3 PROTEIN, C ELEGANS; LIN-3 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CELL FATE; CONTROLLED STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE REPRESSION; GENOTYPE; GERM LINE; GROWTH CURVE; LIN 3 GENE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PROTOZOAL GENETICS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SYNTHETIC MULTIVULVA GENE; ANIMAL; FEMALE; GENETICS; GERM CELL; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHENOTYPE; PROMOTER REGION; RNA INTERFERENCE; TRANSCRIPTION INITIATION; VULVA;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EPIDERMAL GROWTH FACTOR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; MAP KINASE SIGNALING SYSTEM; MUTATION; PHENOTYPE; PROMOTER REGIONS, GENETIC; RAS PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; VULVA;

EID: 84855259890     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002418     Document Type: Article

References (52)

1. Normanno N, De Luca A, Bianco C, Strizzi L, Mancino M, et al. (2006) Epidermal growth factor receptor (EGFR) signaling in cancer. Gene 366: 2-16.
2. Massague J, (1990) Transforming growth factor-alpha. A model for membrane-anchored growth factors. J Biol Chem 265: 21393-21396.
3. Yotsumoto F, Yagi H, Suzuki SO, Oki E, Tsujioka H, et al. (2008) Validation of HB-EGF and amphiregulin as targets for human cancer therapy. Biochem Biophys Res Commun 365: 555-561.
4. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, et al. (1990) TGF alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 61: 1137-1146.
5. Sandgren EP, Luetteke NC, Palmiter RD, Brinster RL, Lee DC, (1990) Overexpression of TGF alpha in transgenic mice: induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61: 1121-1135.
6. Downward J, (2003) Targeting RAS signalling pathways in cancer therapy. Nat Rev Cancer 3: 11-22.
7. Aroian RV, Koga M, Mendel JE, Ohshima Y, Sternberg PW, (1990) The let-23 gene necessary for Caenorhabditis elegans vulval induction encodes a tyrosine kinase of the EGF receptor subfamily. Nature 348: 693-699.
8. Beitel GJ, Clark SG, Horvitz HR, (1990) Caenorhabditis elegans ras gene let-60 acts as a switch in the pathway of vulval induction. Nature 348: 503-509.
9. Han M, Sternberg PW, (1990) let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. Cell 63: 921-931.
10. Hill RJ, Sternberg PW, (1992) The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature 358: 470-476.
11. Sternberg PW, Horvitz HR, (1986) Pattern formation during vulval development in C. elegans. Cell 44: 761-772.
12. Kimble J, (1981) Alterations in cell lineage following laser ablation of cells in the somatic gonad of Caenorhabditis elegans. Dev Biol 87: 286-300.
13. Katz WS, Lesa GM, Yannoukakos D, Clandinin TR, Schlessinger J, et al. (1996) A point mutation in the extracellular domain activates LET-23, the Caenorhabditis elegans epidermal growth factor receptor homolog. Mol Cell Biol 16: 529-537.
14. Ferguson EL, Horvitz HR, (1989) The multivulva phenotype of certain Caenorhabditis elegans mutants results from defects in two functionally redundant pathways. Genetics 123: 109-121.
15. Andersen EC, Saffer AM, Horvitz HR, (2008) Multiple levels of redundant processes inhibit Caenorhabditis elegans vulval cell fates. Genetics 179: 2001-2012.
16. Lu X, Horvitz HR, (1998) lin-35 and lin-53, two genes that antagonize a C. elegans Ras pathway, encode proteins similar to Rb and its binding protein RbAp48. Cell 95: 981-991.
17. Ceol CJ, Horvitz HR, (2001) dpl-1 DP and efl-1 E2F act with lin-35 Rb to antagonize Ras signaling in C. elegans vulval development. Mol Cell 7: 461-473.
18. Solari F, Ahringer J, (2000) NURD-complex genes antagonise Ras-induced vulval development in Caenorhabditis elegans. Curr Biol 10: 223-226.
19. Unhavaithaya Y, Shin TH, Miliaras N, Lee J, Oyama T, et al. (2002) MEP-1 and a homolog of the NURD complex component Mi-2 act together to maintain germline-soma distinctions in C. elegans. Cell 111: 991-1002.
20. Andersen EC, Horvitz HR, (2007) Two C. elegans histone methyltransferases repress lin-3 EGF transcription to inhibit vulval development. Development 134: 2991-2999.
21. Poulin G, Dong Y, Fraser AG, Hopper NA, Ahringer J, (2005) Chromatin regulation and sumoylation in the inhibition of Ras-induced vulval development in Caenorhabditis elegans. Embo J 24: 2613-2623.
22. Couteau F, Guerry F, Muller F, Palladino F, (2002) A heterochromatin protein 1 homologue in Caenorhabditis elegans acts in germline and vulval development. EMBO Rep 3: 235-241.
23. Huang LS, Tzou P, Sternberg PW, (1994) The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Mol Biol Cell 5: 395-411.
24. Clark SG, Lu X, Horvitz HR, (1994) The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137: 987-997.
25. Davison EM, Saffer AM, Huang LS, Demodena J, Sternberg PW, et al. (2011) The LIN-15A and LIN-56 Transcriptional Regulators Interact to Negatively Regulate EGF/Ras Signaling in Caenorhabditis elegans Vulval Cell-Fate Determination. Genetics 187: 803-815.
26. Davison EM, Harrison MM, Walhout AJ, Vidal M, Horvitz HR, (2005) lin-8, which antagonizes Caenorhabditis elegans Ras-mediated vulval induction, encodes a novel nuclear protein that interacts with the LIN-35 Rb protein. Genetics 171: 1017-1031.
27. 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.
28. Ferguson EL, Sternberg PW, Horvitz HR, (1987) A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature 326: 259-267.
29. Hedgecock EM, Herman RK, (1995) The ncl-1 gene and genetic mosaics of Caenorhabditis elegans. Genetics 141: 989-1006.
30. Herman RK, Hedgecock EM, (1990) Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis. Nature 348: 169-171.
31. Myers TR, Greenwald I, (2005) lin-35 Rb acts in the major hypodermis to oppose ras-mediated vulval induction in C. elegans. Dev Cell 8: 117-123.
32. Schott S, Ramos F, Coustham V, Palladino F, (2009) HPL-2/HP1 prevents inappropriate vulval induction in Caenorhabditis elegans by acting in both HYP7 and vulval precursor cells. Genetics 181: 797-801.
33. Ceol CJ, Horvitz HR, (2004) A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev Cell 6: 563-576.
34. Siegfried KR, Kidd AR 3rd, Chesney MA, Kimble J, (2004) The sys-1 and sys-3 genes cooperate with Wnt signaling to establish the proximal-distal axis of the Caenorhabditis elegans gonad. Genetics 166: 171-186.
35. Han M, Aroian RV, Sternberg PW, (1990) The let-60 locus controls the switch between vulval and nonvulval cell fates in Caenorhabditis elegans. Genetics 126: 899-913.
36. Ferguson EL, Horvitz HR, (1985) Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110: 17-72.
37. Liu J, Tzou P, Hill RJ, Sternberg PW, (1999) Structural requirements for the tissue-specific and tissue-general functions of the Caenorhabditis elegans epidermal growth factor LIN-3. Genetics 153: 1257-1269.
38. Katz WS, Hill RJ, Clandinin TR, Sternberg PW, (1995) Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell 82: 297-307.
39. Chang C, Newman AP, Sternberg PW, (1999) Reciprocal EGF signaling back to the uterus from the induced C. elegans vulva coordinates morphogenesis of epithelia. Curr Biol 9: 237-246.
40. Hwang BJ, Sternberg PW, (2004) A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development. Development 131: 143-151.
41. Hsieh J, Liu J, Kostas SA, Chang C, Sternberg PW, et al. (1999) The RING finger/B-box factor TAM-1 and a retinoblastoma-like protein LIN-35 modulate context-dependent gene silencing in Caenorhabditis elegans. Genes Dev 13: 2958-2970.
42. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S, (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877-879.
43. Thompson BE, Lamont LB, Kimble J, (2006) Germ-line induction of the Caenorhabditis elegans vulva. Proc Natl Acad Sci U S A 103: 620-625.
44. Wang D, Kennedy S, Conte D Jr, Kim JK, Gabel HW, et al. (2005) Somatic misexpression of germline P granules and enhanced RNA interference in retinoblastoma pathway mutants. Nature 436: 593-597.
45. Petrella LN, Wang W, Spike CA, Rechtsteiner A, Reinke V, et al. (2011) synMuv B proteins antagonize germline fate in the intestine and ensure C. elegans survival. Development 138: 1069-1079.
46. 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.
47. Jiang LI, Sternberg PW, (1998) Interactions of EGF, Wnt and HOM-C genes specify the P12 neuroectoblast fate in C. elegans. Development 125: 2337-2347.
48. Thomas JH, Stern MJ, Horvitz HR, (1990) Cell interactions coordinate the development of the C. elegans egg-laying system. Cell 62: 1041-1052.
49. Hu M, Polyak K, (2008) Microenvironmental regulation of cancer development. Curr Opin Genet Dev 18: 27-34.
50. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
51. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH, (2001) Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28: 160-164.
52. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.