Robustness and Epistasis in the C. elegans Vulval Signaling Network Revealed by Pathway Dosage Modulation

Developmental Cell

Volumn 24, Issue 1, 2013, Pages 64-75

  Barkoulas, Michalis ^a,b,c   van Zon, Jeroen S ^d,e   Milloz, Josselin ^b,f   van Oudenaarden, Alexander ^d   Félix, Marie Anne ^a,b,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e FOM INSTITUTE AMOLF   (Netherlands)

^f HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; EPIDERMAL GROWTH FACTOR; LIN 3 PROTEIN; NOTCH RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL FATE; CONTROLLED STUDY; EPISTASIS; EUKARYOTE; FEASIBILITY STUDY; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DOSAGE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENETIC VARIABILITY; MOLECULE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VULVA;

ANIMALS; BODY PATTERNING; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL DIFFERENTIATION; CELL LINEAGE; EMBRYONIC INDUCTION; EPIDERMAL GROWTH FACTOR; EPISTASIS, GENETIC; FEMALE; GENE DOSAGE; IN SITU HYBRIDIZATION, FLUORESCENCE; MEMBRANE PROTEINS; ORGAN SPECIFICITY; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VULVA;

CAENORHABDITIS ELEGANS; EUKARYOTA;

EID: 84872415180     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.12.001     Document Type: Article

References (61)

1. Ambros V. Cell cycle-dependent sequencing of cell fate decisions in Caenorhabditis elegans vulva precursor cells. Development 1999, 126:1947-1956.
2. Ansel J., Bottin H., Rodriguez-Beltran C., Damon C., Nagarajan M., Fehrmann S., François J., Yvert G. Cell-to-cell stochastic variation in gene expression is a complex genetic trait. PLoS Genet. 2008, 4:e1000049.
3. Barkai N., Leibler S. Robustness in simple biochemical networks. Nature 1997, 387:913-917.
4. Berset T., Hoier E.F., Battu G., Canevascini S., Hajnal A. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science 2001, 291:1055-1058.
5. Braendle C., Félix M.-A. Plasticity and errors of a robust developmental system in different environments. Dev. Cell 2008, 15:714-724.
6. Chen N., Greenwald I. The lateral signal for LIN-12/Notch in C. elegans vulval development comprises redundant secreted and transmembrane DSL proteins. Dev. Cell 2004, 6:183-192.
7. Corson F., Siggia E.D. Geometry, epistasis, and developmental patterning. Proc. Natl. Acad. Sci. USA 2012, 109:5568-5575.
8. Csete M.E., Doyle J.C. Reverse engineering of biological complexity. Science 2002, 295:1664-1669.
9. Eldar A., Dorfman R., Weiss D., Ashe H., Shilo B.Z., Barkai N. Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 2002, 419:304-308.
10. Félix M.-A. Cryptic quantitative evolution of the vulva intercellular signaling network in Caenorhabditis. Curr. Biol. 2007, 17:103-114.
11. Félix M.A. Caenorhabditis elegans vulval cell fate patterning. Phys. Biol. 2012, 9:045001.
12. Félix M.A., Barkoulas M. Robustness and flexibility in nematode vulva development. Trends Genet. 2012, 28:185-195.
13. Ferguson E.L., Horvitz H.R. Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 1985, 110:17-72.
14. Ferguson E.L., Sternberg P.W., Horvitz H.R. A genetic pathway for the specification of the vulval cell lineages of Caenorhabditis elegans. Nature 1987, 326:259-267.
15. Frøkjaer-Jensen C., Davis M.W., Hopkins C.E., Newman B.J., Thummel J.M., Olesen S.P., Grunnet M., Jorgensen E.M. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 2008, 40:1375-1383.
16. Giurumescu C.A., Sternberg P.W., Asthagiri A.R. Intercellular coupling amplifies fate segregation during Caenorhabditis elegans vulval development. Proc. Natl. Acad. Sci. USA 2006, 103:1331-1336.
17. Giurumescu C.A., Sternberg P.W., Asthagiri A.R. Predicting phenotypic diversity and the underlying quantitative molecular transitions. PLoS Comput. Biol. 2009, 5:e1000354.
18. Greenwald I.S., Sternberg P.W., Horvitz H.R. The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 1983, 34:435-444.
19. Gregor T., Wieschaus E.F., McGregor A.P., Bialek W., Tank D.W. Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 2007, 130:141-152.
20. Griffiths A., Miller J., Suzuki D., Lewontin R., Gelbart W. An Introduction to Genetic Analysis 2000, W.H. Freeman, New York. Seventh Edition.
21. Gutiérrez J. A developmental systems perspective on epistasis: computational exploration of mutational interactions in model developmental regulatory networks. PLoS ONE 2009, 4:e6823.
22. Han M., Aroian R.V., Sternberg P.W. The let-60 locus controls the switch between vulval and nonvulval cell fates in Caenorhabditis elegans. Genetics 1990, 126:899-913.
23. Hill R.J., Sternberg P.W. The gene lin-3 encodes an inductive signal for vulval development in C. elegans. Nature 1992, 358:470-476.
24. Hoyos E., Kim K., Milloz J., Barkoulas M., Pénigault J.B., Munro E., Félix M.A. Quantitative variation in autocrine signaling and pathway crosstalk in the Caenorhabditis vulval network. Curr. Biol. 2011, 21:527-538.
25. Hwang B.J., Sternberg P.W. A cell-specific enhancer that specifies lin-3 expression in the C. elegans anchor cell for vulval development. Development 2004, 131:143-151.
26. Katz W.S., Hill R.J., Clandinin T.R., Sternberg P.W. Different levels of the C. elegans growth factor LIN-3 promote distinct vulval precursor fates. Cell 1995, 82:297-307.
27. Kenyon C. A perfect vulva every time: gradients and signaling cascades in C. elegans. Cell 1995, 82:171-174.
28. Kiontke K., Barrière A., Kolotuev I., Podbilewicz B., Sommer R.J., Fitch D.H.A., Félix M.-A. Trends, stasis, and drift in the evolution of nematode vulva development. Curr. Biol. 2007, 17:1925-1937.
29. Kitano H. Biological robustness. Nat. Rev. Genet. 2004, 5:826-837.
30. Kitano H. A robustness-based approach to systems-oriented drug design. Nat. Rev. Drug Discov. 2007, 6:202-210.
31. Komatsu H., Chao M.Y., Larkins-Ford J., Corkins M.E., Somers G.A., Tucey T., Dionne H.M., White J.Q., Wani K., Boxem M., Hart A.C. OSM-11 facilitates LIN-12 Notch signaling during Caenorhabditis elegans vulval development. PLoS Biol. 2008, 6:e196.
32. Krejcí A., Bernard F., Housden B.E., Collins S., Bray S.J. Direct response to Notch activation: signaling crosstalk and incoherent logic. Sci. Signal. 2009, 2:ra1.
33. Levy S.F., Siegal M.L. Network hubs buffer environmental variation in Saccharomyces cerevisiae. PLoS Biol. 2008, 6:e264.
34. Li J., Greenwald I. LIN-14 inhibition of LIN-12 contributes to precision and timing of C. elegans vulval fate patterning. Curr. Biol. 2010, 20:1875-1879.
35. Ma W., Lai L., Ouyang Q., Tang C. Robustness and modular design of the Drosophila segment polarity network. Mol. Syst. Biol. 2006, 2:70.
36. Masel J., Siegal M.L. Robustness: mechanisms and consequences. Trends Genet. 2009, 25:395-403.
37. Meir E., von Dassow G., Munro E., Odell G.M. Robustness, flexibility, and the role of lateral inhibition in the neurogenic network. Curr. Biol. 2002, 12:778-786.
38. Milloz J., Duveau F., Nuez I., Félix M.-A. Intraspecific evolution of the intercellular signaling network underlying a robust developmental system. Genes Dev. 2008, 22:3064-3075.
39. Moriya H., Shimizu-Yoshida Y., Kitano H. In vivo robustness analysis of cell division cycle genes in Saccharomyces cerevisiae. PLoS Genet. 2006, 2:e111.
40. Pénigault J.B., Félix M.A. High sensitivity of C. elegans vulval precursor cells to the dose of posterior Wnts. Dev. Biol. 2011, 357:428-438.
41. Phillips P.C. Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 2008, 9:855-867.
42. Qadota H., Inoue M., Hikita T., Köppen M., Hardin J.D., Amano M., Moerman D.G., Kaibuchi K. Establishment of a tissue-specific RNAi system in C. elegans. Gene 2007, 400:166-173.
43. Raj A., van den Bogaard P., Rifkin S.A., van Oudenaarden A., Tyagi S. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 2008, 5:877-879.
44. Raj A., Rifkin S.A., Andersen E., van Oudenaarden A. Variability in gene expression underlies incomplete penetrance. Nature 2010, 463:913-918.
45. Saffer A.M., Kim D.H., van Oudenaarden A., Horvitz H.R. The Caenorhabditis elegans synthetic multivulva genes prevent ras pathway activation by tightly repressing global ectopic expression of lin-3 EGF. PLoS Genet. 2011, 7:e1002418.
46. Shaye D.D., Greenwald I. Endocytosis-mediated downregulation of LIN-12/Notch upon Ras activation in Caenorhabditis elegans. Nature 2002, 420:686-690.
47. Siegal M.L., Bergman A. Waddington's canalization revisited: developmental stability and evolution. Proc. Natl. Acad. Sci. USA 2002, 99:10528-10532.
48. Simmer F., Tijsterman M., Parrish S., Koushika S.P., Nonet M.L., Fire A., Ahringer J., Plasterk R.H. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 2002, 12:1317-1319.
49. Simske J.S., Kim S.K. Sequential signalling during Caenorhabditis elegans vulval induction. Nature 1995, 375:142-146.
50. Sternberg P.W. Lateral inhibition during vulval induction in Caenorhabditis elegans. Nature 1988, 335:551-554.
51. Sternberg, P.W. (2005). Vulval development. In Wormbook, The C. elegans Research Community, ed., , http://www.wormbook.org.
52. Sternberg P.W., Horvitz H.R. The combined action of two intercellular signaling pathways specifies three cell fates during vulval induction in C. elegans. Cell 1989, 58:679-693.
53. Sternberg P.W., Han M. Genetics of RAS signaling in C. elegans. Trends Genet. 1998, 14:466-472.
54. Struhl G., Fitzgerald K., Greenwald I. Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 1993, 74:331-345.
55. Sundaram M., Greenwald I. Genetic and phenotypic studies of hypomorphic lin-12 mutants in Caenorhabditis elegans. Genetics 1993, 135:755-763.
56. Tan P.B., Lackner M.R., Kim S.K. MAP kinase signaling specificity mediated by the LIN-1 Ets/LIN-31 WH transcription factor complex during C. elegans vulval induction. Cell 1998, 93:569-580.
57. von Dassow G., Meir E., Munro E.M., Odell G.M. The segment polarity network is a robust developmental module. Nature 2000, 406:188-192.
58. Wagner A. Robustness and Evolvability in Living Systems 2005, Princeton University Press, Princeton, NJ.
59. Wang M., Sternberg P.W. Competence and commitment of Caenorhabditis elegans vulval precursor cells. Dev. Biol. 1999, 212:12-24.
60. Yoo A.S., Bais C., Greenwald I. Crosstalk between the EGFR and LIN-12/Notch pathways in C. elegans vulval development. Science 2004, 303:663-666.
61. Zand T.P., Reiner D.J., Der C.J. Ras effector switching promotes divergent cell fates in C. elegans vulval patterning. Dev. Cell 2011, 20:84-96.